https://doi.org/10.1093/plcell/koac303 THE PLANT CELL 2023: 35: 24–66
Climate change challenges, plant science solutions
Nancy A. Eckardt,1,* Elizabeth A. Ainsworth,2 Rajeev N. Bahuguna,3 Martin R. Broadley,4,5
Wolfgang Busch,6 Nicholas C. Carpita,7 Gabriel Castrillo,4,8 Joanne Chory,6,9 Lee R. DeHaan,10
Carlos M. Duarte,11 Amelia Henry,12 S.V. Krishna Jagadish,13 Jane A. Langdale,14 Andrew D.B. Leakey,15
James C. Liao,16 Kuan-Jen Lu,16 Maureen C. McCann,7 John K. McKay,17 Damaris A. Odeny,18
Eder Jorge de Oliveira,19 J. Damien Platten,12 Ismail Rabbi,20 Ellen Youngsoo Rim,21 Pamela C. Ronald,21,22
David E. Salt,4,8 Alexandra M. Shigenaga,21 Ertao Wang,23 Marnin Wolfe24 and Xiaowei Zhang23
1 Senior Features Editor, The Plant Cell, American Society of Plant Biologists, USA
2 USDA ARS Global Change and Photosynthesis Research Unit, Urbana, Illinois 61801, USA
3 Centre for Advanced Studies on Climate Change, Dr Rajendra Prasad Central Agricultural University, Samastipur 848125, Bihar, India
4 School of Biosciences, University of Nottingham, Nottingham, NG7 2RD, UK
5 Rothamsted Research, West Common, Harpenden, Hertfordshire, AL5 2JQ, UK
6 Plant Molecular and Cellular Biology Laboratory, Salk Institute for Biological Studies, La Jolla, California 92037, USA
7 Biosciences Center, National Renewable Energy Laboratory, Golden, Colorado 80401, USA
8 Future Food Beacon of Excellence, University of Nottingham, Nottingham, NG7 2RD, UK
9 Howard Hughes Medical Institute, Salk Institute for Biological Studies, La Jolla, California 92037, USA
10 The Land Institute, Salina, Kansas, USA
11 Red Sea Research Center (RSRC) and Computational Bioscience Research Center, King Abdullah University of Science and Technology (KAUST),
Thuwal, 23955-6900, Saudi Arabia
12 International Rice Research Institute, Rice Breeding Innovations Platform, Los Ban~os, Laguna 4031, Philippines
13 Department of Plant and Soil Science, Texas Tech University, Lubbock, Texas 79410, USA
14 Department of Biology, University of Oxford, Oxford, OX1 3RB, UK
15 Department of Plant Biology, Department of Crop Sciences, and Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Illinois
61801, USA
16 Institute of Biological Chemistry, Academia Sinica, Taipei 11528, Taiwan
17 Department of Agricultural Biology, Colorado State University, Fort Collins, Colorado 80523, USA
18 The International Crops Research Institute for the Semi-Arid Tropics–Eastern and Southern Africa, Gigiri 39063-00623, Nairobi, Kenya
19 Embrapa Mandioca e Fruticultura, Rua da Embrapa, Cruz das Almas, BA, Brazil
20 International Institute of Tropical Agriculture (IITA), PMB 5320 Ibadan, Oyo, Nigeria
21 Department of Plant Pathology and the Genome Center, University of California, Davis, California 95616, USA
22 Innovative Genomics Institute, Berkeley, California 94704, USA
23 National Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology,
Chinese Academy of Sciences, Shanghai 200032, China
24 Auburn University, Dept. of Crop Soil and Environmental Sciences, College of Agriculture, Auburn, Alabama 36849, USA
*Author for correspondence: neckardt@aspb.org
Authors are listed alphabetically (with the exception of the lead author/coordinating editor). All authors contributed to writing and revising the article.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the
Instructions for Authors (https://academic.oup.com/plcell) is: Nancy A. Eckardt (neckardt@aspb.org).
Received June 21, 2022. Accepted September 29, 2022. Advance access publication October 12, 2022
VC The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. Open Access
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution,
and reproduction in any medium, provided the original work is properly cited.
PerspectiveDownloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 25
Abstract
Climate change is a defining challenge of the 21st century, and this decade is a critical time for action to mitigate the
worst effects on human populations and ecosystems. Plant science can play an important role in developing crops with en-
hanced resilience to harsh conditions (e.g. heat, drought, salt stress, flooding, disease outbreaks) and engineering efficient
carbon-capturing and carbon-sequestering plants. Here, we present examples of research being conducted in these areas
and discuss challenges and open questions as a call to action for the plant science community.
Introduction possibilities, stimulate further research, and motivate plant
scientists at any stage of their careers to become involved in
Climate change is caused by an accumulation of greenhouse
work aimed at mitigating climate change and enhancing
gases (GHGs) (e.g. CO2, methane) in the atmosphere leading
food and energy security. Mitigating the climate change cri-
to increased planetary heat-trapping and global warming.
sis will require all hands on deck.
The IPCC Sixth assessment report (IPCC, 2022) strongly sug-
gests that limiting global warming to 1.5C above pre- How can more carbon be retained in soil and
industrial levels will be needed to avoid severe climate biomass?
change effects. This will require halving global CO2 emissions
by 2030 and cutting them to net zero by 2050, as well as re- Carbon sequestration in annual cropping systems
moving an additional 2–10 billion metric tons (Gt) of CO2 (By John K. McKay)
each year. In some locations, warming may benefit certain Annual cropping systems present opportunities for carbon
crops, and, over time, the optimal growing regions may shift sequestration that have yet to be exploited. In addition to
farther away from the equator. However, the effects of cli- the need to reduce GHG emissions, active atmospheric CO2
mate change are not limited to increasing temperatures and removal strategies, also called Negative Emissions
heatwaves in many parts of the world but include changes Technologies (NETs), are needed to attain net CO2 reduc-
in rainfall, more severe and frequent storms, increased tions and avoid the most damaging climate change out-
drought, and increased threat of wildfires. All of these effects comes (National Academies of Sciences, Engineering, and
are anticipated to adversely affect crop yields and food secu- Medicine, 2019). Atmospheric CO2 removal technologies
rity worldwide within the next 20 years (Zhao et al., 2017; Li need to be implemented now and increase to levels on the
et al. 2019; Jägermeyr et al., 2021). As the impact of climate order of 10 Gt CO2 per year by 2050, and 20 Gt CO2 per
change on crop systems intensifies, the need to develop year by 2100 (National Academies of Sciences, Engineering,
stress-resilient crops to combat food insecurity rises. and Medicine, 2019).
In this article, we explore several ways in which plant sci- Among NET for CO2 removal, soil carbon sequestration is
entists are working on solutions related to carbon sequestra- the least expensive and most ready to scale in the next dec-
tion to help achieve net zero CO2 emissions and crop ades (National Academies of Sciences, Engineering, and
improvements to protect and enhance yields for increased Medicine, 2019). Current US cropping systems use genetics
food security. The first section outlines challenges and that were not designed to minimize GHG emissions nor to
approaches for enhancing the carbon sequestration capacity maximize carbon sequestration, yet heritable genetic varia-
of crops (annual and perennial) and seagrasses, followed by tion for these traits exists in many crops. In addition, agricul-
a section on improving photosynthesis. A third section tural soils experienced well-documented decreases in soil
addresses engineering climate resilience in crops (resistance carbon over the last century (Davidson and Ackerman,
or tolerance to abiotic and biotic stresses). The final section 1993) and are capable of sequestering all of the CO2 cur-
describes the vision of a sustainable global bioeconomy rently in the atmosphere (Ciais et al., 2013). Here, I review
rooted in plant biology. We acknowledge that there are the challenges with attempts to achieve soil carbon seques-
other areas, not covered here, in which plant science can tration in current annual cropping systems, both with the
play a role in mitigating adverse climate change effects, in- way in which the maize (Zea mays)–soy (Glycine max) rota-
cluding bioenergy, forestry, and ecosystem conservation. tion was designed and the science to date on how manage-
Solutions in all of these areas are needed in the very near fu- ment might lead to predictable increases in soil carbon. I
ture, and in the longer term. We do not provide an in- then focus on genetic changes that are needed to create
depth review of these topics. Rather, the examples provided carbon-negative crops, including optimal combinations of
here illustrate a few of the many avenues of research being traits that can be addressed in breeding programs.
conducted by plant scientists around the world. A compan- The major, unaddressed problem for sustainability and
ion review by Verslues et al. (2023) addresses unresolved GHG emissions in annual cropping systems is excess nitro-
questions in plant abiotic stress. We hope that these stories gen (N) in the form of synthetic fertilizer (Northrup et al.,
help to inform the plant science community of the 2021), which leaches into groundwater, rivers, and oceans
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
26 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
and into the atmosphere as N2O, a GHG with an effect size (Oryza sativa), breeding during the Green Revolution led
300 that of CO2 (Albritton et al., 2001). An obvious ex- to the fixation of mutations that reduce NUE (OsTCP19;
ample is ethanol production from maize, where N is respon- Liu et al., 2021b) and root growth (Dro1; Arai-Sanoh
sible for 480% of GHG emissions overall (Kim et al., 2014). et al., 2014) in the elite breeding lines.
For the parts of the world where the Green Revolution was It is worth considering the traits of an ideal annual crop
successfully deployed (Evenson and Gollin, 2003), a major for carbon-negative supply chains for food, feed, fiber, and
consequence is the exclusive use of crop genotypes that re- fuel. As mentioned, genetic changes to lower N require-
quire high N inputs. To fix this N problem, we need to im- ments and create deeper, more massive root systems can
prove N use efficiency (NUE) and greatly reduce N input. make annual biomass feedstock production carbon negative
Increasing NUE is feasible (Hirel et al., 2007; Northrup et al., (Paustian et al., 2016a). Another key trait for carbon seques-
2021) and can be achieved in part by removing a small tration is population density, where increasing the number
number of large-effect mutations that were selected to high of individuals per hectare leads to more root systems and
frequency in elite germplasm in the Green Revolution greater carbon input. Crop species that were not part of the
(Moyers et al., 2018). Getting farmers to reduce N input is a Green Revolution have promise in this respect (Amaducci
much greater challenge. First, overfertilizing every other year et al., 2008). For example, industrial hemp (Cannabis sativa)
is a well-established management practice of the maize-soy was never bred for high N inputs, can be grown at popula-
rotation that encompasses 73 million hectares of farmland tion densities of 500,000 plants per hectare, and has greater
in the USA. Although soybean is an N-fixing species, in root biomass below 50 cm than other major crops
modern cropping systems high-yielding soy crops require (Amaducci et al., 2008). Root carbon composition is also a
hundreds of kilograms of N per hectare (Salvagiotti et al., genetic target, as some forms of carbon may be more recal-
2008). Although fertilizer has recently increased in price, so citrant to degradation and therefore longer lived in soils.
have crop commodity prices, and thus farmers remain in- The idea of engineering roots to create more recalcitrant
centivized to maximize N inputs. In the USA, the maize–soy forms of carbon, such as suberin, is discussed below by
rotation is highly subsidized by federal funds in the form of Busch and Chory. Suberin is one example; another is lignin,
direct payment to farmers as well as mandates on using eth-
which is a parameter in models of soil carbon (Parton,
anol from fermentation of maize grain and biodiesel from
1996). We found large heritable variation in percent lignin in
transesterification of soy lipids.
maize roots (Figure 1) and are testing the prediction that
Most efforts in using annual cropping systems for soil car-
genotypes with greater root lignin will lead to greater quan-
bon sequestration have focused on changes in management
tity and durability of soil carbon.
that were originally designed for soil health (Ogle et al.,
Root exudates, a diverse set of simple carbon molecules
2019), such as reduced tillage, greater residue retention, and
that are released passively or actively into the soil, also con-
cover crops that are designed to increase the amount of
tribute to soil organic carbon (SOC). Little is known regard-
above-ground plant biomass left in the field per unit area
ing the degree to which root exudates are controlled by
per year (McClelland et al., 2021). Most of the published
studies on the effect of management on soil carbon are lim- genetics versus the environment. Even less is known about
ited to the top 30 cm of soil, which is where most of the the genetic control of the abundance and composition of
carbon inputs are expected (Ogle et al., 2019). However, this root exudates, even in model species. This is due in part to
top 30 cm is also the least durable soil carbon and can re- the difficulty of measuring the relevant phenotypes in agri-
spire back into CO2 in a few years. Getting soil carbon culturally relevant environments. On the soil modeling side,
inputs deeper into the soil is needed to achieve greater and recent progress has been made in separating biomass and
more durable carbon sequestration in agricultural systems exudate inputs to soil carbon, where exudates are predicted
(Paustian et al., 2016a, 2016b, 2019) and will require genetic to lead to increases in mineral-associated organic matter,
changes in crops. which in turn is predicted to have a longer residence time
Genetic changes in annual cropping systems are needed than other soil carbon fractions (Zhang et al., 2021b).
both to reduce inputs (Northrup et al., 2021) and achieve Finally, the soil and root microbiome, which is influenced by
carbon sequestration levels of tons per hectare per year root exudates and plant genotype (Peiffer et al., 2013;
(Paustian et al., 2016a). Some changes can be achieved by Wagner et al., 2020; Favela et al., 2021), influences the car-
selecting against large-effect mutations that went to high bon retention properties of soils, although data on effect
frequency during the Green Revolution. Prior to the sizes are lacking (Naylor et al., 2020). Ectomycorrhizae are
Green Revolution, putting large amounts of synthetic N thought to be key drivers of SOC accumulation in forests
on agricultural fields reduced yield, as tall crops heavy (Soudzilovskaia et al., 2019) and could be exploited in crop-
with grain were highly prone to lodging. In many cases se- ping systems. Manipulating the soil and root microbiome of
lection during the Green Revolution was based on recur- cropping systems at scale will be much more difficult than
rent backcrossing to dwarf lines and involved small obtaining seed from new crop genotypes but is a possible
effective population sizes and low levels of effective re- tool for engineering annual cropping systems for enhanced
combination (Moyers et al., 2018). For example, in rice carbon sequestration.
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 27
the amount of the natural product suberin in roots. Suberin
is a lipophilic complex polyester that is composed of very
long-chain fatty acids and polyaromatic compounds. Suberin
may be a good source for stable SOC due to its intrinsic bio-
chemical stability (Lorenz et al., 2007) and its interaction
with soil minerals and occlusion in topsoil microaggregates
(Kell, 2012; Lin and Simpson, 2016). We note that there are
numerous other plant traits that promise to be useful for
enhancing the capacity of plants to sequester carbon in the
soil (see some additional examples in the previous section
by McKay).
There are several significant challenges to utilizing crops
for carbon sequestration. Genetic trait enhancement is a
lengthy process and its adoption by the public will be chal-
lenging. Establishing a link between root traits and carbon
Figure 1 Quantitative variation in lignin content in maize root sys-
tems from a field study of 358 maize inbred lines. A description of the accumulation and permanence in agricultural soils will re-
experiment can be found in Woods et al. (2022). quire substantial experimental efforts. Carbon accumulation
and persistence are also dependent on soil type, climate
Harnessing plants: A global initiative to enhance parameters, and agricultural practices such as the use of
plant-based carbon sequestration cover crops and no-till farming (Schmidt et al., 2018).
(By Wolfgang Busch and Joanne Chory) Although there is good potential for plant-based carbon se-
questration in the surface soil layer (up to 1.85 Gt C/year in
We consider solutions for carbon sequestration based on
the top 30 cm of global cropland soils alone; Zomer et al.,
plants’ abilities to draw down CO2 from the atmosphere via
photosynthesis and convert it to biomass. Earth’s soils con- 2017), an enhanced rooting depth and altered biochemical
tain a large amount of carbon, estimated at approximately makeup of roots could yield a much larger sequestration ca-
2,300 Gt carbon to 3-m depth, which constitutes about pacity. Finally, time is pressing—every year that goes by
three times the current atmospheric pool of CO without significant carbon drawdown will negatively impact
2
(Schlesinger and Bernhardt, 2020). The main source of SOC billions of humans and decrease the biodiversity of our
is plant material (e.g. aboveground plant biomass, roots, and planet.
root exudates), which can be stored in the soil or respired The Salk Harnessing Plants Initiative is working to identify
back into the atmosphere. It is estimated that cropland and genetic and molecular mechanisms to increase root biomass,
grazing land soils (about 5 billion hectares globally) have an root depth, and suberin root content. We use examples of
enormous capacity for storing carbon (Sanderman et al., this research to highlight considerations for plant-based car-
2017). Combined with existing agricultural infrastructure, bon sequestration that we have identified during this work.
this capacity provides an opportunity to leverage genetics to Each of the target traits comes with specific challenges and
improve traits related to plant-mediated carbon opportunities. For instance, increased root mass will elevate
sequestration. the carbon input into soils and can improve the ability of
Several plant traits are good candidates for facilitating roots to forage for nutrients and water. However, increasing
plant carbon sequestration (Figure 2). Root biomass is one, root mass beyond a certain level might come at the expense
as it is estimated that a given mass of root inputs contrib- of yield. Nevertheless, the relationship between root biomass
utes about five times more SOC than the equivalent mass and yield is not necessarily a zero-sum game as enhanced
of aboveground litter (Jackson et al., 2017). However, traits water and nutrient uptake of a bigger root system can sup-
associated with mechanisms that increase recalcitrance of port a larger shoot. This might be particularly relevant under
SOC to breakdown by soil microorganisms (SOC protection) drought or nutrient-limited conditions. An example of the
will also be required to increase residence time in soils. lack of a strict tradeoff of root biomass and yield in major
Mechanisms of SOC protection include a complex interplay crops is the lack of correlation of yield and root biomass in
between the chemical makeup of SOC, physical occlusion of maize as well as soybean in a multi-location, multi-year
SOC within soil aggregates, formation of stable organo- study (Ordón~ez et al., 2020). Increasing root depth promises
mineral complexes, and water-film connectivity between to increase the lifetime of the average carbon molecule de-
SOC and microbes (Schmidt et al., 2011; Lehmann et al., posited by roots in the soil, provide roots access to deeper
2020). More than half of the global SOC is found in deep soil layers that can contain more moisture, and facilitate the
soil layers (Jobbágy and Jackson, 2000), and the mean resi- capture of nitrate that leaches deeper into the soil during
dence time of SOC increases with depth, implying lower de- the growing season. However, surface roots are still impor-
composability of root-derived carbon in deeper soil layers tant for foraging immobile nutrients such as phosphorus.
(Gill et al., 1999; Prieto et al., 2016). Root biochemistry also Therefore, achieving an optimal balance between shallow
influences decomposability, and a prime candidate trait is roots and deep roots will be important. As an effective
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
28 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Figure 2 Toward an ideal carbon-capturing crop plant. A, The ideal plant should accumulate suberin in the cell wall of its root cells and form a
vast and deep root system. To realize this goal, the existing literature and experimental evidence are curated to look for candidate genes affecting
root system architecture and root mass. This information is combined with root-specific promoters and suberin biosynthetic genes. B, The ideal
plant is created by capitalizing on both classical (breeding) and more recent (genome editing, genetic engineering) approaches to introduce favor-
able alleles and genes that will increase root biomass and transgenes that will increase the deposition of suberin in the root. In addition to trap-
ping more carbon, these ideal plants will replenish carbon-depleted soils with degradation-recalcitrant carbon polymers (indicated by the darker
color of the soil on the right). Figure credit: P. Salomé.
apoplastic barrier, suberin in specific areas of the root could To quantitatively link these root traits to carbon charac-
provide enhanced flood and drought resilience and might teristics in the soil, we are working with soil scientists to
enhance root growth in deeper, more anoxic layers of the better estimate the soil carbon impact of crop varieties that
soil. Extensive variation for each of these traits between and have different root mass, depth, and suberin content. We
within species indicates that there are genetic mechanisms aim to test the effects of genetic alterations via gene editing
that can be leveraged to improve them. or gene engineering approaches in crops over the next few
Our work in enhancing these traits is being conducted in years. Recent advances in high-throughput phenotyping, se-
parallel with model plants via forward and reverse genetic quencing, and functional single-cell genomics now provide a
approaches, as well as in diversity collections of major row way to leverage genes, gene constructs, and genetic variants
crops and cover crops to identify crop-specific targets using within and between species. We aim to have the proof of
genome-wide association studies (GWASs). While we are in- concepts for enhanced crop traits within the next 3 years to
terested in trait changes that will work in the field and then partner with both NGOs and agriculture companies to
maintain crop productivity, it is not feasible to measure all enhance varieties that are of interest to farmers.
these root traits in the field at high throughput. We there- There are numerous other opportunities for plant biolo-
fore rely on initial screening approaches in the laboratory or gists to contribute to climate change mitigation efforts,
the greenhouse to measure and engineer root traits, subse- ranging from work on traits that will reduce agricultural
quently moving to in-soil or field-testing with a subset of N2O or methane emissions to creating carbon
lines that display distinctive traits. We focus on root mass in sequestration-friendly microbiota or mycorrhizal associa-
relation to depth, as the engineering or breeding goal is to tions. As a community, we should think of and work toward
direct as much root mass as possible to a deeper depth, and promising plant biology-based solutions.
on enhancing the accumulation of suberin. Suberin is a
highly effective apoplastic diffusion barrier and producing it Rapid de novo domestication of perennial crops
everywhere in the root would be detrimental to plant (By Lee R. DeHaan)
health. Therefore, we focus on specific root tissues that al- Most agricultural soils have lost 50%–70% of the SOC that
ready produce suberin such as the periderm or the exoder- they had previously accumulated under native plant com-
mis, which are outer layers in mature root systems. We are munities; therefore, raising the carbon levels in historically
targeting such tissues as suberin sinks by using tissue- tilled agricultural soils offers the potential to partially miti-
specific promoters to drive suberin production, as well as gate climate change by capturing 30–60 Gt of organic car-
utilizing genes involved in the formation of these tissues to bon (Lal, 2003). The restoration of SOC in agricultural soils
produce additional tissue layers. would not only mitigate climate change through
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 29
sequestration but would also contribute to adaptation to quality (Audu et al., 2022) is being developed through wide
climate change by developing soils with greater nutrient hybridization (Hayes et al., 2018). A direct domestication
holding capacity, resistance to erosion from extreme rain program is underway to develop the perennial sunflower rel-
events, increased water infiltration, and water storage to sta- ative Silphium integrifolium into a dual-purpose forage and
bilize productivity in the face of erratic rainfall (Blanco- grain crop (Van Tassel et al., 2017). Various perennial legu-
Canqui et al., 2013). minous species are also being considered for their suitability
Although planting long-lived perennial plants on degraded for use as perennial grains (Schlautman et al., 2018).
agricultural soils would be one of the most effective ways to Perennial flax (Linum) species are being evaluated for direct
rapidly restore soil carbon levels, this approach is limited be- domestication as perennial oilseeds (Tork et al., 2019).
cause the herbaceous perennials currently available for use Direct domestication of the cool season perennial grass
in agriculture (mainly forage crops) produce biomass that is species intermediate wheatgrass (Thinopyrum intermedium;
unsuitable for direct human consumption (Paustian et al., Figure 3) was initiated in the 1980s, and now the harvested
2016a). Therefore, efforts are underway to develop new crop grain is being produced and sold in North America under
plants that would have extensive long-lived root systems the trade name Kernza (DeHaan and Ismail, 2017). With its
and would achieve carbon sequestration levels similar to pe- extensive root system (Sprunger et al., 2019), the crop has
rennial biofuels (Crews and Rumsey, 2017; Dheri et al., 2022) potential for carbon storage belowground (De Oliveira et al.,
while simultaneously producing abundant human-edible 2020) and to accumulate microbial necromass (Peixoto
protein, starch, and oils through mechanically harvestable et al., 2020). However, genetic improvement for grain yield is
grain (Glover et al., 2010). needed, since selected populations still have a yield potential
Efforts to develop perennial grain crops began decades of less than half that of bread wheat (Triticum aestivum) in
ago, but recent advances in genetics and breeding are accel- the same region (Culman et al., 2013). In addition to the
erating the timeline and the first successful perennial grains currently limited genetic potential for grain yield, the crop
are now entering fields and markets. A perennial rice breed- faces many challenges. New crops always struggle with the
ing program was initiated in 1996, targeting the roughly 19 need to coordinate supply chain development in concert
million hectares of upland rice grown worldwide where for- with expanding acreage. Novel perennial grains also intro-
est land is often cleared and degraded (Sacks et al., 2003). duce a new array of challenges for farmers and agronomists,
Annual rice (Oryza sativa ssp. indica) and the rhizomatous such as controlling pests and diseases and managing for sus-
perennial relative Oryza longistaminata were hybridized, and tained yield over many years. With intermediate wheatgrass,
a breeding program has produced lines for flooded paddies the decline in yield that occurs in aging stands is an ongoing
that persist through eight harvests with yields and quality challenge (Pinto et al., 2021).
traits on par with modern rice cultivars (Huang et al., 2018; Recent developments in plant biology, genetics, and
Hu et al., 2022). Perennial paddy rice is expected to reduce breeding have opened the door to breeding new crops with
GHG emissions and water consumption relative to annual carbon-storing perennial root systems and abundant grain
rice (Oda et al., 2019). The development of perennial rice for production at a time scale that can proceed at the pace of
upland conditions also remains possible in the near term. commercial enterprise development (Runck et al., 2014).
Perennial grain sorghum is being developed through wide Low-cost genome sequencing and innovative genome as-
hybridization of annual grain sorghum (Sorghum bicolor) sembly approaches are allowing the rapid generation of ref-
with perennial species (Figure 3). Progress for yield and sur- erence sequences even for large-genome perennial species.
vival has been made by selecting among progeny of crosses Genomic information is now leveraged to perform genomic
between S. bicolor and the tetraploid perennial Sorghum selection (Meuwissen et al., 2001) which can greatly acceler-
halepense, and evaluation under tropical conditions suggests ate the breeding of perennial crops. Whereas traditional
no barrier to high-yielding perennial varieties in warmer breeding of a perennial crop might require 5 or more years
regions (Cox et al., 2018b). Recently, diploid perennial grain per generation, involving field evaluation of multiple years
sorghum lines have been derived from diploid  tetraploid followed by intermating of selected individuals, genomic se-
crosses (Cox et al., 2018a) and from crosses between S. bi- lection uses a genomic prediction model based on the per-
color and the perennial diploid species Sorghum propinquum formance of plants grown from multiple generations over
(Foster et al., 2020). Working at the diploid level is expected many years. Applying genomic models to genetic marker
to expedite the development of perennial grain sorghum by data from seedlings of intermediate wheatgrass has accu-
simplifying crosses between perennial germplasm and locally rately predicted mature plant performance (Crain et al.,
adapted S. bicolor varieties. Now, marker-assisted selection is 2021). Speed breeding (Watson et al., 2018) paired with ge-
being initiated to accelerate progress in breeding for traits nomic selection has the potential to further accelerate pe-
related to perenniality and productivity (Cox et al., 2018b). rennial crop improvement by increasing the number of
A wide array of perennial grain crops could likely be devel- generations that can be completed per year. Genomic selec-
oped either by direct domestication of wild perennial spe- tion with speed breeding is currently being implemented
cies or wide hybridization between crops and related with intermediate wheatgrass to complete two full cycles of
perennials. Perennial wheat with potential to improve soil selection per year, compared to one cycle every 3 years with
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
30 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Figure 3 Examples of wide hybridization and direct domestication to develop perennial grains. The wild perennial Sorghum halepense (A) was hy-
bridized with the domestic species Sorghum bicolor (B) and selective breeding of the progeny produced lines with intermediate head and seed
size (C) and the ability to regrow from underground rhizomes (D). In an example of direct domestication, the mostly wild grass Thinopyrum inter-
medium can be harvested with conventional equipment (E) and cleaned to obtain a human-edible grain (F) that has properties similar to wheat,
as seen in this loaf made with an 80/20 blend of wheat and Th. intermedium flour (G). Domesticated Th. intermedium types now possess domesti-
cation traits, such as shatter resistance (H, at right).
classical approaches. Although these methods hold great of “orphan” perennial grain species is another approach wor-
promise, they remain to be validated across the many re- thy of investigation. Pigeonpea (Cajanus cajan) is an N-fixing
peated cycles of selection necessary to produce a highly pro- semi-perennial shrub that is grown in Asia and southern
ductive domestic crop. Africa. Although types that can be grown for several seasons
The application of genome editing techniques to the do- without replanting have been used in erosion control and
mestication of wild species creates exciting possibilities to are still grown by some farmers, annual pigeonpea is now
compress the development timeline for new crops (Zsögön the dominant form. A recent study in Malawi indicated that
et al., 2018). For instance, by comparing the genome se- farmers are less likely to adopt erratically performing peren-
quence of the perennial Thinopyrum intermedium with re- nial pigeonpea due to social pressures and lack of trust in
lated domestic grains, targets for genome editing to obtain the technology (Grabowski et al., 2019). Expanded acreage
domestic phenotypes have been identified and a roadmap of soil-conserving perennial pigeonpea may depend on the
for rapid domestication established (DeHaan et al., 2020). development of improved management techniques spread
Although new crop development is the primary approach through peer learning, and new cultivars that enable consis-
being used to produce new perennial grains, the rediscovery tent production.
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 31
The basic genetic and physiological control of the peren- research may provide additional insights on their role.
nial growth habit has only recently been the subject of ex- Further efforts in resolving carbon concentration mecha-
perimentation and remains poorly understood (Park et al., nisms and the role of the microbiome, specifically the root
2017). This lack of understanding has thus far hindered the component, offer promise to contribute to developments in
development of perennial grain crops. With a clear under- carbon capture technologies and to increase the efficiency
standing of the pathways involved, rapid conversion of exist- of seagrass restoration, respectively.
ing annual crops into perennials could be possible.
Combined approaches of wide hybridization, genome edit- What do we know?
ing, mutagenesis, and transgenics could be used to achieve The high productivity of seagrass meadows even under low
perennial growth in high-yielding cultivars. Because the need light conditions (Duarte and Chiscano, 1999) supplies much
for carbon sequestration in soils is urgent, these approaches of the carbon sequestered in seagrass meadows (Kennedy
could be implemented in parallel, following the approach et al., 2010). The keys to the high productivity of seagrass
used to develop COVID vaccines (Ball, 2020) to develop an meadows are efficient light use (Enrıquez et al., 1994), low
array of high-yielding perennial crops in the coming years. nutrient requirements (Duarte, 1990), and carbon concen-
trating mechanisms that allow seagrasses to use both CO2
The promise of seagrasses for carbon capture and and HCO3 to support their high photosynthetic rates
storage (Larkum et al., 2006). The analysis of the full genome se-
(By Carlos M. Duarte) quence of the seagrass Zostera marina pointed to a number
Seagrasses are a group of about 74 angiosperm species that of evolutionary adaptations required for these species to col-
complete their life cycle in the marine environment, where onize the ocean from freshwater angiosperm ancestors
they form lush meadows that rank amongst the world’s (Olsen et al., 2016). Some of these adaptations help explain
most productive ecosystems (Duarte and Chiscano, 1999; their high carbon removal, including the loss of volatiles,
Hemminga and Duarte, 2000). Seagrass meadows are consistent with the loss of stomata through which they are
strongly autotrophic, producing more organic matter than emitted for airborne communication and plant defense,
consumed in the ecosystem (Duarte et al., 2010) and acting, which reduces losses of carbon and the probability of infec-
therefore, as sinks for CO2, much of which is buried in sea- tions, as stomata are a main entry point for pests and
grass soils (Duarte et al., 2005, 2013a; Fourqurean et al., pathogens in terrestrial plants (Olsen et al., 2016).
2012). The role of seagrasses as intense carbon sinks in the The seagrass genome also revealed new combinations of
biosphere is supported by their high photosynthetic effi- structural traits related to the cell wall, enabling the synthe-
ciency, low nutrient requirements, adaptations that mini- sis of cutin-cuticular waxes, suberin–lignin near the plasma
mize carbon losses, and their capacity to cope with anoxic, membrane, and macroalgal-like sulfated polysaccharides
sulfide-rich sediments. Indeed, whereas seagrasses occupy an (Olsen et al., 2016), recently confirmed by direct analyses of
estimated 0.08% of the ocean seafloor, they contribute an the seagrass cell walls, which revealed the presence of
estimated 12.7% of all organic carbon annually buried in the fucose-containing sulfated polysaccharides, apiogalacturonan
ocean seafloor (Duarte et al., 2005). Yet at least one-third of and lignin (particularly in roots and rhizomes; Pfeifer et al.,
the historical global area occupied by seagrasses has been 2022). This composition, together with low N and phospho-
lost, leading to the loss of this carbon sink and the risk of rus content, renders seagrass tissues highly recalcitrant to
remineralization and subsequent CO2 emission of the car- microbial degradation (Enrıquez et al., 1993), helping to ex-
bon stocks accumulated in their soils over millennia. Hence, plain high seagrass-derived lignin concentrations in seagrass
seagrass meadows represent a key component of the so- soils (Nakakuni et al., 2021) and the high organic carbon
called “blue carbon” strategies aimed at avoiding losses and preservation supporting high carbon sequestration rates.
restoring coastal vegetated habitats to contribute to climate The full genome sequence conducted to date excluded en-
change mitigation, through carbon capture and storage, and dophytic prokaryotes (Olsen et al., 2016), which also have
climate change adaptation through the coastal protection important contributions, as exemplified by the recent dis-
seagrasses offer (Duarte et al., 2013a; Macreadie et al., 2021). covery of a symbiosis with an N-fixing, root-endophytic bac-
A range of tools within plant sciences, from genomics and teria, which helps explain the high productivity of seagrass
metabolomics to microbiome investigations are providing in oligotrophic environments (Mohr et al., 2021).
important insights into the underpinnings of the remarkable Seagrass morphology is a basic underpinning of their role
carbon capture capacity of seagrass. Whereas the role of sea- in carbon removal. They are able to form dense canopies,
grasses in carbon capture and storage has been addressed exceeding 15 m2 of leaf surface per m2 of ground covered
largely through the quantification of stocks (Fourqurean (Romero et al., 2006), and their rhizomes and roots also
et al., 2012) and burial rates (Duarte et al., 2005, 2013a), sea- form a dense web in the sediments, with 0.18–3 m2 of rhi-
grass traits related to carbon capture and storage have been zome per squaremeter and 0.47–1 m2 of roots per square-
poorly addressed. Here, I discuss the fundamental plant meter of soil (Duarte et al., 1998). The dense web of
traits that render seagrasses so efficient in carbon removal seagrass leaves acts as a filter that retains particles entrained
and identify a number of promising areas where further in the flow and dissipates wave and turbulent energy,
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
32 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
enhancing the deposition and retention of particles in their Known unknowns
soils (Hendriks et al., 2008). Meanwhile, the dense web of Carbon concentrating mechanisms that allow seagrasses to
rhizomes and roots in the sediments injects a significant support their high photosynthetic rates and circumvent
fraction of seagrass net production (2.8%–48.6% of total net boundary-layer rate-limiting effects are not fully resolved
production; Duarte et al., 1998) into the soil and provides (Larkum et al., 2006). Seagrass carbon metabolism remains
physical cohesion, thereby reinforcing the soils against the poorly understood and seems to neither fully conform to C4
erosive force of storms and extreme-energy events, such as nor Crassulacean acid metabolism (Larkum et al., 2006).
tsunamis (Chatenoux and Peduzzi, 2007; Sasa et al., 2012). Genomic analyses conducted to date have focused on the
Rhizome growth and meristematic dominance are the seagrass genome and ignored the rich community of endo-
keys to the exponential clonal growth of seagrasses, which is phytes. There is a growing number of analyses of the sea-
a major driver of the efficiency of seagrass restoration proj- grass microbiome, including bacteria and fungi (Tarquinio
ects in restoring seagrass carbon removal (Duarte et al., et al., 2019; Garcias-Bonet et al., 2021; Torta et al., 2022), but
2013b), as demonstrated in assessments of the carbon re- they remain mostly descriptive and functional analyses are
moval benefits of seagrass restoration (Marbà et al., 2015; limited, despite evidence that endophytes may play a major
Oreska et al., 2020). Seagrass restoration traditionally was role in supporting nutrient metabolism (Mohr et al., 2021)
small in scale and relatively expensive and inefficient, largely and detoxification (Crump et al., 2018). For instance, re-
due to small planting units (van Katwijk et al., 2016). cently discovered cable bacteria in seagrass roots could alle-
However, observations from hundreds of restoration projects viate critical sulfide toxicity and promote nutrient uptake by
(van Katwijk et al., 2016) have led to major recent successes, mobilizing soil iron and phosphorous with acidification asso-
such as the cost-effective restoration of 36 km2 of Zostera ciated with electrogenic sulfide oxidation, and by stimulating
marina meadows in Virginia’s coastal waters, with major car- dissimilatory nitrate reduction to ammonium and even fix-
bon removal benefits (Orth et al., 2020), as well as the long- ing N2 (Scholz et al., 2021).
term success of Posidonia australis restoration in SW
Opportunities around unknown unknowns
Australia, again coupled with important carbon removal
benefits (Marbà et al., 2015). Hence, seagrass restoration has Overall, limited progress has been made in applying modern
a significant scope to contribute to climate action concepts and tools of plant science to further our understand-
(Macreadie et al., 2021). There is ample scope for plant sci- ing of seagrass carbon removal, where an ecological focus pre-
ence to contribute to enhancing the success of seagrass res- vails. This is not surprising given that seagrasses represent only
toration, through, for instance, the use of probiotic 0.02% of angiosperm species and have little scope to emerge
applications (Peixoto et al., 2022) or selective breeding of as model organisms. Yet, the strong selection pressure required
seagrasses used for restoration to enhance their resistance, for angiosperms to cope with life in the marine environment
and thereby restoration success, in areas experiencing ma- and anoxic, sulfide-rich sediments is likely to have generated
rine heat waves (Zabin et al., 2022). novel mechanisms that can open new pathways in biotechnol-
Lack of oxygen in seagrass soils, where oxygen penetration ogy. Understanding the carbon concentration mechanism of
is limited to the top few mm of seagrass soils, slows down seagrass can open the door for hybrid photosynthesis technol-
microbial degradation and the bioturbation activity of ben- ogies for carbon removal (Kornienko et al., 2018), while resolv-
ing the functional role of their microbiome can help improve
thic fauna, thereby improving the efficiency of carbon burial.
the outcomes of seagrass restoration. The limited effort of
Anoxic sediments support sulfate-reducing bacteria, produc-
plant science on seagrass research to date suggests the exis-
ing sulfide that is toxic to seagrass. However, seagrasses pro-
tence of “unknown unknowns” and, therefore, a potential for
tect themselves from toxic sulfide intrusions by releasing
new discoveries that can lead to applications in carbon re-
oxygen through their roots, transported from photosyntheti-
moval, conservation ecology and, more broadly, plant science.
cally produced oxygen in their leaves to their roots and rhi-
zomes (Borum et al., 2006), thereby maintaining a protective Can we improve photosynthesis?
oxidized layer a few millimeters thick around their roots and
rhizomes (Brodersen et al., 2015). Oxygen transport from Photosynthesis: A key target for improving crop
photosynthetic production sites to roots is enabled by the productivity, sustainability, and resilience in the
development of a lacunae system that provides gaseous con- face of climate change
nectivity between leaves, rhizomes, and roots (Borum et al., (By Elizabeth A. Ainsworth and Andrew D.B. Leakey)
2006). While continuous within organs, they are interrupted Photosynthesis heavily influences crop productivity, resource
between organs by diaphragms one cell thick, perforated by use efficiency, and sensitivity to stresses. Therefore, strategic
interstitial pores (0.5–1.0 lm), which provide protection engineering of photosynthetic metabolism and the morpho-
from flooding while allowing gas flow (Roberts et al., 1984). logical features of leaves that control carbon and water
In addition, the below-ground tissues of seagrasses exhibit fluxes can: (1) increase the food, fuel, fiber, and feed pro-
physiological adaptations which allow them to rely tempo- duced by crops; while (2) reducing demand for water and
rarily on anaerobic fermentative metabolism (Borum et al., improving agricultural GHG balance; and (3) making crops
2006). more resilient to future climatic and atmospheric conditions.
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 33
Detailed models of photosynthetic metabolism (Zhu et al., recycles 2P-glycolate at the expense of ATP and NADH
2012; Bellasio, 2019) and crop function can identify engi- (Walker et al., 2016). A number of genetic engineering strat-
neering strategies (Kromdijk et al., 2016; Leakey et al., 2019; egies have successfully demonstrated that photorespiration
Wu et al., 2019). Synthetic biology is also opening doors for can be partially bypassed, resulting in improved photosyn-
novel photosynthetic systems to be custom designed to thetic carbon assimilation (Kebeish et al., 2007; Carvalho
new environments (Zhu et al., 2020, and discussed below by et al., 2012; South et al., 2019). Recently, transgenic tobacco
Lu and Liao). Here, we discuss engineering for greater photo- (Nicotiana tabacum) was developed to recycle 2P-glycolate
synthesis under near-future elevated atmospheric CO2 con- in the chloroplast via overexpression of plant malate syn-
centrations and temperatures, plus improved thase and Chlamydomonas (C. reinhardtii) glycolate dehy-
photosynthetic water use efficiency (WUE) and NUE. drogenase and simultaneous RNAi to downregulate a
Despite a general effect of higher atmospheric CO2 en- glycolate–glycerate transporter (South et al., 2019). When
hancing photosynthesis in C3 plants, global warming is these plants were grown in the field at elevated tempera-
expected to have profoundly negative consequences for crop tures ( + 5C), they showed greater resilience to heat stress
photosynthesis and productivity by the middle to end of this compared to wild-type (Cavanagh et al., 2022), providing
century (Slattery and Ort, 2019). Rising temperatures also in- strong proof-of-concept for this strategy.
crease vapor pressure deficit (Ficklin and Novick, 2017), Growth at elevated CO2 (550–600 ppb, which is in the
which may increase irrigation demand in the future and limit range of predicted average atmospheric CO2 concentrations
the potential yield of current crop genotypes grown under by 2050) generally enhances yields of C3 crops in major tem-
standard management practices (Ort and Long, 2014; perate growing regions (Ainsworth and Long, 2021). This pri-
DeLucia et al., 2019). Photosynthesis is a temperature- marily results from enhanced photosynthetic CO2 fixation
dependent process, with rates increasing to an optimum, driven by greater Rubisco carboxylation rates combined
then decreasing once that temperature optimum is exceeded with inhibition of Rubisco oxygenation rates (Stitt, 1991).
(Moore et al., 2021). This temperature dependency reflects Even if C3 plants acclimate to elevated CO2 in the long term
the biochemical processes that determine rate limitations, by downregulating investment in Rubisco content and elec-
namely Rubisco activity (and the balance between photosyn- tron transport capacity, photosynthesis is generally stimu-
thetic carbon assimilation and photorespiration) and lated along with NUE (Leakey et al., 2009). Field experiments
ribulose-1,5-bisphosphate regeneration. While in vitro with transgenic plants overexpressing Calvin–Benson–
Rubisco carboxylation rates increase beyond 50C, de- Bassham (CBB) cycle enzymes further enhanced the benefits
creased discrimination by Rubisco for oxygen and increased of elevated CO2 on carbon gain and yield by increasing pho-
solubility of oxygen relative to CO2 with rising temperatures tosynthetic electron transport capacity (Rosenthal et al.,
inhibit net photosynthetic carbon assimilation in temperate 2011; Köhler et al., 2017). If coupled with breeding or engi-
C3 crops at temperatures exceeding 30C, due to increased neering to maintain high sink capacity, which is a prerequi-
photorespiration (Moore et al., 2021). Rubisco activase is a site to maximizing the potential of photosynthetic
key target for improving photosynthesis at elevated tempera- enhancements in elevated CO2 (Ainsworth and Long, 2021),
tures because of the thermolability of the enzyme (Salvucchi this provides a widely applicable pathway to a greater CO2-
and Crafts-Brandner, 2004) and the observation that acti- fertilization effect on yield.
vases from species or genotypes adapted to warmer climates Greater atmospheric CO2 also causes stomatal closure,
are more thermostable (Scafaro et al., 2016). resulting in lower transpiration and greater WUE (Leakey
Work in Arabidopsis thaliana suggested that simply over- et al., 2009, 2019). This can reduce drought-induced stress
expressing a thermostable Rubisco activase could improve and yield loss (Fitzgerald et al., 2016). However, interactions
photosynthesis and growth in high temperature conditions with abscisic acid signaling, canopy micrometeorology, and
(Kurek et al., 2007), but that result was not translated to N fixation can also cause the CO2-fertilization effect on yield
crops where overexpression of Rubisco activase resulted in to be lost under hot and dry conditions (Gray et al., 2016).
lower Rubisco content (Fukayama et al., 2012, 2018). Studies There is also significant uncertainty about which of these
in rice discovered that over-expression of both Rubisco and responses will occur in tropical locations where water avail-
Rubisco activase were required for enhanced photosynthesis ability, high temperatures, and soil fertility might be most
at both optimal and high temperatures (Qu et al., 2021; limiting (Leakey et al., 2012). A possible target to improve
Suganami et al., 2021). A highly thermostable Rubisco acti- yield in times and places of drought is to reduce the
vase identified in the Crassulacean acid metabolism plant amount of water lost through stomata to the atmosphere
Agave tequilana (Shivhare and Mueller-Cajar, 2017) and relative to photosynthetic CO2 uptake, that is increasing
greater understanding of the mechanisms of thermostability WUE by reducing stomatal density or accelerating stomatal
in different Rubisco activase isoforms (Scafaro et al., 2019; closing speed (Leakey et al., 2019). Modeling suggests that
Degen et al., 2020) provide potential guides for further im- prioritizing reductions in water use over increases in carbon
proving thermotolerance in crops. gain when trying to enhance WUE may lead to better yield
Another target for improving photosynthesis at elevated outcomes in many growing environments for both C3 and
temperatures is reducing photorespiration, the process that C4 species, especially as atmospheric CO2 concentrations
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
34 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
continue to rise (Leakey et al., 2019; Wu et al., 2019). studies (South et al., 2019). When GO was replaced with
Successful pursuit of this strategy would increase productiv- Chlamydomonas glycolate dehydrogenase (GDH), which
ity while making currently marginal land viable for produc- produces NADH instead of H2O2, transgenic tobacco
tion, reduce freshwater use for irrigation, and make crops showed higher carbon assimilation rates, resistance to pho-
more resilient to climate change. torespiration stress, and a significant increase in biomass in
Crop productivity today is highly dependent on fertilizer the field tests (South et al., 2019). Under high temperatures
application, which has negative environmental effects ( + 5C), this pathway decreased yield loss by 11%–21%
through nitrate run-off and release of the potent GHG ni- (Cavanagh et al., 2022).
trous oxide. The need for N inputs is strongly linked to the
high N cost of photosynthetic proteins. However, there may Conversion of two glycolate (C2) to one glycerate (C3) with
be potential to re-invest N in different photosynthetic com- CO2 release in chloroplasts (Figure 4B). The synthetic path-
ponents to increase carbon gain and improve NUE (Evans way originated from E. coli, consisting of dehydrogenase
and Clarke, 2019). (GDH), glyoxylate carboligase (GCL), and tartronic semialde-
hyde reductase (TSR). Unlike the first approach, this syn-
Enhancing plant CO thetic pathway preserves 75% of carbon from two glyoxylate
2 fixation through synthetic
biology to produce one glycerate, which is returned to the CBB cy-
(By Kuan-Jen Lu and James C. Liao) cle (Kebeish et al., 2007). The remaining carbon is CO2 pro-
duced via GCL. Expressing the above genes in Arabidopsis
Synthetic biology encompasses engineering natural or non-
chloroplasts increased the growth rate and biomass yield.
natural enzymes or pathways into plants to accomplish a
This synthetic pathway was shown to benefit crop plants
designated purpose. In addition to the approaches discussed
such as Camelina sativa and potato (Solanum tuberosum) in
above, here we discuss attempts using synthetic biology to
greenhouse and growth chamber conditions (Nolke et al.,
enhance CO2 fixation, focusing on recycling photorespiration
2014; Dalal et al., 2015).
products and CO2-fixation pathways (Figure 4).
Fixation of an additional CO2 to compensate for the carbon
Recycling photorespiration products
loss by GCL (Figure 4C). The synthetic malyl-CoA glycerate
Plant photorespiration produces a nonproductive product, (MCG) cycle also uses GCL, and TSR to convert two glyoxy-
2P-glycolate, through the oxygenase activity of Rubisco. 2P- lates to glycerate, which is then converted to phosphoenol-
glycolate is converted to glycerate in peroxisomes and to phyruvate (PEP). The oxygen-insensitive PEP carboxylase
CO2 in mitochondria in a process requiring ATP and (PPC) then carboxylates CO2 and PEP to OAA (C4), fol-
NADPH with CO2 and ammonium released (Walker et al., lowed by splitting OAA to acetyl-CoA and glyoxylate (Yu
2016). Current synthetic pathways for reducing photorespir- et al., 2018b). The glyoxylate is then recycled in the GCL re-
atory CO2 loss involve the following types: action. The net result is the conversion of glyoxylate (or gly-
colate) to a productive biosynthetic product, acetyl-CoA,
Breakdown of one glycolate (a C2 compound) to two CO2 in
without carbon loss. The MCG cycle has been accomplished
chloroplasts without ATP or NADPH consumption (Figure
in Synechococcus elongatus PCC7942, a photoautotrophic cy-
4A). The released CO2 can be reassimilated by Rubisco, and
anobacterium (Yu et al., 2018b). Compared to the wild-type,
no ammonium would be released. For example, an engi-
the strain expressing the MCG cycle fixed higher amounts of
neered “GOC” pathway in rice consists of a glycolate oxidase
CO
(OsGLO3), an oxalate oxidase (OsOXO3), and a catalase 2 to produce more acetyl-CoA and its derived compound
ketoisocaproate, an intermediate in leucine biosynthesis.
(OsCATC) overexpressed in rice chloroplasts (Shen et al.,
2019). Glycolate is converted to oxalate, which is completely Fixation of an additional CO2 to glycolate after activation
oxidized to two CO2 by OsOXO3. OsCATC is required for (Figure 4D). An elegant tartronyl-CoA (TaCo) pathway was
decomposing H2O2, preventing plants from oxidative stress. demonstrated recently, in which glycolate is activated to
Rice plants engineered with the GOC pathway showed a glycoly-CoA, which is then caboxylated to tartronyl-CoA
22% increase in photosynthesis, but increases in yield were and then to glycerate. This approach requires a new-to-
inconsistent and dependent on the season in field tests nature enzyme, glycolyl-CoA carboxylase, which was devel-
(Shen et al., 2019). An earlier example overexpressed a ma- oped by rational design and high-throughput screening
late synthase (MS) from pumpkin (Cucurbita pepo), a cata- (Scheffen et al., 2021).
lase (CAT) from Escherichia coli, and a peroxisomal glycolate
oxidase (GO) in Arabidopsis chloroplasts (Maier et al., 2012). Rubisco-independent, synthetic CO2 fixation pathways
In this manner, glycolate is completely oxidized to CO2 via Six Rubisco-independent CO2-fixation pathways in microor-
both the heterologous and endogenous enzymes. The trans- ganisms have been identified in nature (Berg, 2011), and a
genic Arabidopsis had a greater rosette number and size number of theoretical synthetic pathways have been
with higher biomass under the ambient CO2, short-day con- designed in silico based on reported enzyme activities and
ditions. However, introduction of the above three genes in thermodynamics (Bar-Even, 2018). The first step in imple-
tobacco did not result in increased biomass in greenhouse menting synthetic pathways is to demonstrate the pathway
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 35
Figure 4 Synthetic biology approaches for recycling photorespiration and CO2-fixation pathways. A and B, Photorespiration engineered for break-
down of one glycolate to two CO2 molecules (A) or conversion of two glycolate to one glycerate plus one CO2 molecule (B). The CO2 released in
the chloroplast is recycled back to the CBB cycle for carbon reassimilation (Maier et al., 2012; Shen et al., 2019; South et al., 2019). C, The MCG-cy-
cle engineered to convert glycolate to acetyl-CoA without carbon loss (Yu et al., 2018b). D, Creation of a new enzyme, such as glycolyl-CoA car-
boxylase, to achieve glycolate recycling to produce glycerate with input of ATP and an additional CO2 molecule (Scheffen et al., 2021). E, Rubisco-
independent CETCH and rPS-MCG synthetic CO2-fixation pathways (Luo et al., 2022).
feasibility in a cell-free system. This in vitro demonstration export any of its intermediates as a product, such as acetyl-
requires in-depth processes in solving problems in co-factor CoA (C2), pyruvate (C3), and malate (C4). This self-
regeneration, enzyme stability, and pathway control. replenishing characteristic is also seen in almost all naturally
Through these processes, incompatibility of enzyme reac- evolved cycles. Since the output C2, C3, or C4 intermediates
tions, kinetic barrier, and thermodynamic limitations can be are essential for cell growth, it is potentially malleable for
identified. To date, two Rubisco-independent synthetic CO2- in vivo engineering. Introduction of the CETCH cycle or the
fixing pathways, CETCH and reductive pyruvate synthesis rPS–MCG cycle in a plant would require the activity of
(rPS)–MCG (Figure 4E), have been demonstrated, and many heterologous enzymes, along with co-enzyme B12,
achieved similar or increased CO2 fixation rates in vitro which is absent in plants. Hence, enzyme design, pathway
compared with the CBB cycle in vivo (Schwander et al., evaluation in prokaryotes, plant-associated microbiome engi-
2016; Luo et al., 2022). The CETCH pathway consists of 17 neering, and various genome editing strategies have been
enzymes from different organisms (Schwander et al., 2016). proposed to facilitate this process (Erb et al., 2017; Gupta
An oxygen-insensitive carboxylase/reductase (CCR) from et al., 2021; Ke et al., 2021).
Methylorubrum extorqens was chosen as the carboxylase to
fix CO2 in the CETCH cycle because of its high carboxylase Engineering carbon dioxide-responsive C3 crops to
activity and broad substrate range. The carboxylation sub- sustain higher productivity under a CO2-rich,
strate acrylyl-CoA and crotonyl-CoA in CETCH were regen- warmer climate
erated to complete the cycle for continuous fixation of CO2. (By Rajeev N. Bahuguna and S. V. Krishna Jagadish)
The fixed carbon is converted to glyoxylate as the output. C4 plant species are overrepresented in agriculture systems
The rPS–MCG cycle consists of two parts (Luo et al., and have substantially higher productivity compared to C3
2022). The first utilizes the MCG cycle described above. In crops mainly due to higher photosynthetic efficiency (Rao
the second part, rPS converts acetyl-CoA to pyruvate et al., 2012; Sales et al., 2021). Yet a number of C3 crops are
through a series of reactions that takes two acetyl-CoA to important food sources for millions of people globally, in-
make a crotonyl-CoA, which is carboxylated by CCR to pro- cluding cereals such as wheat, rice, barley (Hordeum vulgare),
duce a C5 compound. The C5 compound is split into a C3 oats (Avena sativa), and many vegetable and tree crops.
(pyruvate) and C2 (acetyl-CoA) through a series of carbon Therefore, efforts to increase the photosynthetic efficiency
rearrangement reactions that complete the cycle. The rPS– and productivity of C3 crops are underway to help meet the
MCG cycle exhibits a self-replenishing feature as it can increasing global food demand (Cui 2021). The high CO2
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
36 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
saturation point for photosynthesis of C3 plants (intercellu- on RN have been reported, ranging from direct inhibition of
lar CO2 levels 600 mmol mol–1) makes them more respon- respiration to no significant impact or even an increase un-
sive to elevated CO2 than C4 plants, which are saturated for der long-term exposure to elevated CO2 (Griffin et al., 1996;
CO2 under current atmospheric CO2 levels (Loladze, 2014; Gonzalez-Meler et al., 1996, 2004; Ziska and Bunce, 1998;
Dingkuhn et al., 2020; Kundu et al., 2022). Thus, C3 crops Drake et al., 1999; Baker et al., 2000; Davey et al., 2004; Ayub
provide a unique opportunity to harvest more carbon from et al., 2014). However, none of these studies considered the
a CO2-rich environment and convert it to biomass and yield genetic background for CO2 responsiveness, which could be
(Broberg et al., 2019; Ainsworth and Long, 2021). a major determinant of the effect of elevated CO2 on RN,
In contrast to the positive effect of CO2 on C3 photosyn- and carbon balance dynamics in C3 crops (Figure 5).
thesis, the global rise in temperature is a major factor limit- Despite the well-documented photosynthetic enhance-
ing the yield of major cereal crops (Lobell and Gourdji, 2012; ment of C3 crops under elevated CO2 (Leakey et al., 2009),
Teixeira et al., 2013; Zhao et al., 2017). A rise in night tem- active selection in C3 crops for CO2 responsiveness has not
perature has been shown to have a large impact on the pro- been given adequate attention (Ziska et al., 2012; Dingkuhn
ductivity of C3 crops such as rice (Peng et al., 2004; Welch et al., 2020). The complexity of field-based CO2 enrichment
et al., 2010) and wheat (Hein et al., 2020, 2022; Impa et al., facilities and space constraints for screening and characteriz-
2021). Recent studies suggest that high night temperature ing a large number of genotypes remain major bottlenecks
(HNT) is related to physiological changes such as an in- for identifying potential CO2-responsive genotypes. Recently,
creased rate of night respiration (RN) and a reduced rate of Shimono et al. (2014) and Kikuchi et al. (2017) demon-
starch accumulation in developing grains in rice (Bahuguna strated that altering planting density provides a means of
et al., 2017; Shi et al., 2017), wheat (Narayanan et al., 2016a, assessing phenotypic plasticity in rice genotypes under en-
2016b; Impa et al., 2020), and barley (Garcıa et al., 2015, hanced resource availability (e.g. space, light, nutrients).
2016). Hence, the positive effect of CO2 on C3 photosynthe- Interestingly, genotypes responsive to higher available
sis and augmented rate of night respiration under HNT resources under low planting density responded similarly
have opposing effects on carbon-balance dynamics under under an elevated CO2 environment (Shimono et al., 2014).
CO2-rich, warmer environments (Song et al., 2014; Dusenge Subsequently, in a series of field experiments, Bahuguna
et al., 2019). While the sensitivity of RN to a rise in tempera- et al. (2022) assessed the variable phenotypic plasticity of
ture is well documented (Atkin and Tjoelker, 2003), variable 194 diverse rice genotypes by measuring parameters related
effects of the long- and short-term impact of elevated CO2 to photosynthesis, biomass, and yield under different
Figure 5 Schematic diagram showing average annual atmospheric [CO2] level for 2021 and the effect of rising night temperature (Tmin) on rice
productivity by enhanced respiration: photosynthesis ratio (RN/A) resulting in augmented release of carbon at the cost of biomass and yield in
conventional genotypes. On the contrary, introgression of CO2-responsiveness trait in C3 crops facilitates enhanced carbon sequestration and allo-
cation of additional carbon into biomass, and compensating Tmin-induced carbon losses. LCR, least CO2-responsive; HCR, high CO2-responsive.
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 37
planting densities. A wide genetic variability observed for four-carbon reaction product subsequently transported to
the phenotypic plasticity under a resource-rich environment inner bundle sheath cells for decarboxylation and re-fixation
showed a strong relationship (R2 = 0.71) with CO2 respon- by Rubisco in the Calvin cycle (Figure 6). Given the special-
siveness under realistic CO2 conditions using a field-based ized leaf anatomy and compartmentalization of metabolic
free air CO2 enrichment facility. Further, the high CO2-re- reactions required for C4 function, evolution of the pathway
sponsive (HCR) genotypes showed significantly higher rates must have involved functional modification of multiple
of photosynthesis (A) and lower rates of RN resulting in a genes, including those encoding enzymes, metabolite trans-
lower RN/A ratio as compared to the least CO2-responsive porters, and regulators of cell-type patterning. Despite this
(LCR) genotypes. Interestingly, elevated CO2 was identified apparent complexity, the C4 photosynthetic pathway
as the major driver influencing carbon-balance dynamics evolved over 60 times independently and is represented in
and the phenotypic response of HCR genotypes resulting in diverse families of flowering plants (Sage, 2016). The adap-
higher biomass and yield under elevated CO2 + HNT condi- tive success of the C4 photosynthetic strategy is demon-
tions, whereas the LCR genotype was severely affected by strated by the fact that just 2% of plant species utilize the
HNT despite exposure to elevated CO2. pathway but C4 plants are responsible for 25% of terres-
This study demonstrated that the impact of HNT on grain trial primary productivity (Still et al., 2003).
yield, total biomass, and grain weight was compensated by
elevated CO2, but this response was mainly confined to the Why C4 rice?
HCR genotypes (Bahuguna et al., 2022). Thus, LCR or con- In addition to strategies that aim to improve the efficiency
ventional genotypes are expected to lose biomass and yield of the C3 photosynthetic pathway (discussed above, and see
under an elevated CO2, warmer climate due to augmented Ort et al., 2015; Johnson, 2022) or to introduce Crassulacean
respiratory carbon losses, whereas HCR genotypes could ac- acid metabolism into C3 plants (Schiller and Bräutigam,
cumulate more carbon per unit area and maintain their bio- 2021), the enhanced efficiency of C4 photosynthesis provides
mass and yield by compensating for carbon losses under a potential engineering opportunity for improved yield and
HNT (Figure 5). In addition, the ability to fix additional car- resilience against abiotic stresses in C3 crops. Although the
bon with a lower respiration-to-photosynthesis ratio in HCR C4 pathway utilizes two extra ATP molecules per CO2 fixed
genotypes provides an opportunity to sequester a substan- than the C3 pathway, in warm and dry environments where
tial amount of carbon into biomass. There is, however, a dissolved oxygen conditions are relatively high, these energy
need for prediction models for simulated carbon fluxes at costs are offset by those not spent on photorespiration (3.5
temporal and spatial scales to assess the carbon sequestra- ATP per O2 fixed). In general, C4 plants also use less water
tion potential of CO2-responsive C3 crops. In conclusion, the (Kocacinar et al., 2008) and N (Evans and von Caemmerer,
introgression of a ‘CO2-responsiveness’ trait into elite rice va- 2000) per CO2 fixed and have substantially faster growth
rieties and other C3 crops could help sustain and enhance rates (Monteith 1978). Physiological models that incorporate
crop yield in a warmer environment. these factors predict that if C4 traits could be introduced
into C3 plants, enhanced radiation, N, and WUEs could gen-
The C4 rice project erate substantial yield increases, particularly in warm envi-
(By Jane Langdale) ronments where crops are rainfed and fertilizer applications
In the majority of photosynthetic organisms, both in water are limited (Mitchell and Sheehy, 2006).
and on land, CO2 is fixed by Rubisco into the three-carbon Importantly, the level of atmospheric CO2 at which C4
compound 3-phospho-glycerate, the first intermediate of outcompetes C3 is dependent on temperature; C4 is favored
the CBB cycle. The efficiency of this C3 photosynthetic path- below 550 ppm CO2 at 35C, 450 ppm at 30C, and 350
way is compromised because Rubisco also reacts with oxy- ppm at 25C (Ehleringer et al., 1997). Although future pre-
gen, forming 2-phospho-glycolate, which has to be dictions of atmospheric CO2 levels differ depending on fossil
detoxified in the energetically costly photorespiratory path- fuel usage scenarios, with current levels at 419 ppm and an-
way (Walker et al., 2016). Because of this energetically waste- nual increases of 2–3 ppm over the last decade (https://gml.
ful competitive reaction, the decrease in atmospheric CO2 noaa.gov/ccgg/trends/gl_gr.html), the status quo would re-
levels that occurred during the Oligocene (Pearson et al., sult in atmospheric CO2 levels of 500 ppm by 2050. C4
2009) would have been accompanied by photosynthetic in- plants could thus outperform C3 plants where temperatures
efficiencies at a global scale. exceeded 33oC, which given climate warming predictions
The reported drop from 800 to 400 ppm atmospheric could be much of the global agricultural landscape for at
CO2 during this period is thought to have driven, at least in least part of the year. Leaving predictions aside, long-term
part, the evolution of the C4 photosynthetic pathway that field experiments at elevated ( + 180 ppm) CO2 demon-
concentrates CO2 at the site of Rubisco and thus minimizes strated that the biomass of C3 but not C4 grasses was en-
photorespiration (Sage, 2016). In the C4 pathway, CO2 is ini- hanced over the first 12 years of the project but then C4
tially fixed by phosphoenolpyruvate carboxylase (PEPCase), outperformed C3 in the following 8 years (Reich et al., 2018).
which is oxygen insensitive. This carboxylation reaction This switch was correlated with net N mineralization rates
occurs in the outer mesophyll cells of the leaf, with the in the soil, which were initially enhanced by elevated CO2 in
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
38 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Figure 6 Schematics of C3 CBB and NADP-ME C4 Cycles. A, CBB C3 cycle. B, NADP-ME C4 cycle. C, Transverse leaf sections and corresponding
schematics of C3 rice (left) and C4 maize (right). Bars = 30 lm. Adapted from Langdale (2011), Figures 1 and 3.
C3 plots but were later depressed. Despite the difficulties in of the genes encoding metabolite transporters (reviewed in
predicting exactly how plants will respond to global change, Langdale, 2011), but regulators of C4 leaf anatomy had not
C4 engineering is thus a plausible strategy, albeit one with been identified. The strategy to introduce C4 traits into rice
significant challenges. was thus three-pronged: (1) introduce compartmentalized
C4 metabolism into existing bundle sheath cells and the
Strategy mesophyll cells immediately adjacent to them by expressing
The C3 species rice is an obvious target for C4 engineering maize genes in specific cell-types of rice; (2) activate chloro-
because it is one of the world’s top three staple crops and plast development and photosynthesis in existing bundle
in many parts of Asia it is the major source of calorie intake. sheath cells by expressing a known regulator of chloroplast
With predicted population increases, the one hectare of development in maize (the Golden2 [ZmG2] gene; Hall
land that provided enough rice to feed 27 people in Asia in et al., 1998); and (3) identify regulators of C4 leaf anatomy
2007 will need to support at least 43 people by 2050—a in maize with a view to future manipulation in rice. The
60% increase in demand (Zeigler, 2007). Successful conver- ultimate goal was to combine the metabolic prototypes
sion of a C3 plant into one that utilizes the C4 pathway generated in the first two strands with the anatomical
requires that leaf anatomy be modified to reduce the num- prototype.
ber of mesophyll cells between veins to the extent that Much of the first decade of the project was spent devel-
there is an approximate 1:1 ratio of mesophyll:bundle sheath oping tools in rice to enable this strategy, for example ro-
cells in the leaf; that chloroplast development is activated in bust transformation pipelines, cell-type-specific promoters,
the normally achlorophyllous bundle sheath cells; and that and modular cloning technology. Ongoing research contin-
C4 pathway enzymes and metabolite transporters are com- ues to characterize potential regulators of C4 leaf anatomy
partmentalized and functional in either the mesophyll or and to evaluate whether manipulation in rice can modify
bundle sheath cells. cell-type patterning in the leaf (Wang et al., 2013a, 2017a;
When the C4 Rice Project (www.c4rice.com) was initiated, Schuler et al., 2018; Hughes et al., 2019; Hughes and
genes encoding all of the enzymes of the C4 pathway had Langdale, 2020, 2022)—but much more discovery research is
been identified in maize and other C4 species, as had some needed before an anatomical prototype can be designed
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 39
and engineered (Sedelnikova et al., 2018). Recent work has, introgression of single genes/QTLs. With a few exceptions
however, made progress toward engineering C4 metabolic (i.e. Sub1 varieties for submergence such as Swarna-sub1
prototypes. [Mackill et al., 2012] and drought-tolerant DRR dhan 42
[IR64 qDTY2.2 + qDTY4.1; Swamy et al. 2013]) the majority
Progress of recently released stress-tolerant varieties were convention-
Maize genes encoding C4 pathway enzymes have been ally bred (i.e. by crossing and selecting over several
expressed in specific cell types of both an elite cultivar of generations).
indica rice (IR64) and a model cultivar of japonica rice The use of genes and QTLs through marker-assisted selec-
(Kitaake), and in both cases the pathway is partly functional. tion could shorten the breeding process. Although hundreds
Specifically, primary carboxylation by PEPCase is seen in me- of stress-tolerance genes, QTLs, and physiological mecha-
sophyll cells, but subsequent decarboxylation in bundle nisms have been identified, only a small number of these re-
sheath cells has yet to be detected (Lin et al., 2020; search outputs have been used in breeding (Wissuwa et al.,
Ermakova et al., 2021). Creating a fully functional cycle will 2016; Cobb et al., 2019; Platten et al., 2019) and the fre-
require a better understanding of metabolite flux within and quency of known abiotic stress QTLs in the current elite
between the two cell types, which may require the develop- breeding material remains low (Juma et al., 2021). There is
ment of more sensitive detection methods. In a second ad- thus a need to bridge the gap between upstream science
vance, chloroplast development has been activated in the and breeding for adaptation to climate change so that valu-
normally achlorophyllous bundle sheath cells of rice, able traits/genes/QTLs are more actively utilized in breeding
through constitutive expression of ZmG2 (Wang et al., pipelines.
2017b). No fitness penalty was observed in greenhouse- Modern breeding strategies have shifted to a paradigm of
grown lines expressing ZmG2, in either IR64 or Kitaake back- population improvement based on elite x elite crossing
grounds (Wang et al., 2017b) and although only evaluated (Juma et al., 2021) within core panels, which for stress-prone
in the nonelite Kitaake background, field-grown lines overex- areas have been selected from the most stress-tolerant geno-
pressing ZmG2 exhibited up to 30% yield increases (Li et al., types available (i.e. Khanna et al., 2022). This strategy
2020). These examples validate the overall engineering strat- presents significant opportunities for upstream plant biolo-
egy but there is still a long way to go before a full transition gists to contribute to breeding efforts. With a defined list of
to C4 can be achieved in any C3 species. genetic backgrounds (many of which have already been se-
Can we develop climate-resilient crops? quenced; see, for example, Mansueto et al., 2017) to which
potential stress tolerance traits/genes/QTLs can be com-
The trait development pipeline: Bridging the gap pared, those that best complement the elite breeding pool
between upstream science and breeding for can be prioritized. However, although traditional varieties
adaptation to climate change are the most promising source of stress tolerance, they also
(By J. Damien Platten and Amelia Henry) typically possess detrimental traits that make them unsuit-
Improving the adaptability of crops is a key strategy to miti- able for use in elite  elite crossing. A defined protocol is
gate the effects of climate change on productivity (Aggarwal needed to deliver useful traits/genes/QTLs from traditional
et al., 2019). We focus on rice breeding in this section; how- varieties into elite backgrounds and into the breeding pool.
ever, the pipeline we describe (Figure 7) could easily be ex- In seeking to bridge the gap between upstream plant sci-
tended to other crops, taking into consideration the ence and breeding for stress tolerance, an understanding of
challenges and parameters unique to each species. For ex- breeding program needs is critical. In the briefest terms, reli-
ample, the platform is being adopted across the CGIAR ability is key: a gene/QTL must reliably improve the target
partnership for global food security (https://www.cgiar.org/) trait, in relevant elite genomic backgrounds and in relevant
for other mandate crops. In rice breeding, abiotic stress tol- environments (field locations). Therefore, the growth stages,
erance was not a selection target during the Green genetic backgrounds, and environmental conditions relevant
Revolution, and some evidence suggests that stress tolerance to breeding programs should be reflected in the study sys-
was even selected against due to tight linkage between tems used in upstream research. One example is in the vali-
stress tolerance loci and loci conferring unfavorable agro- dation of candidate genes for stress tolerance: this is
nomic traits (Vikram et al., 2015). Subsequently, a range of frequently done in the background of japonica rice due to
breeding approaches has been taken to improve stress toler- the established transformation protocols. However, the rice
ance, including introgression of quantitative trait loci (QTLs) type preferred in most stress-prone rice-growing regions is
for stress tolerance traits as well as direct selection for grain indica, which grows better than temperate japonica rice in
yield under stress using traditional varieties as the sources of field trials in the tropics. Use of the relevant genetic back-
stress tolerance. Characterization of stress-tolerant varieties ground is important because stress tolerance alleles are of-
has revealed that combinations of physiological traits have ten absent in japonica genomes and thus their level of stress
been affected by selection for yield under stress (Anantha tolerance is more easily improved, exaggerating apparent ef-
et al., 2016; Kumar et al., 2021), which may explain some of fect size. Other recommendations for increasing the likeli-
the difficulty in developing superior varieties through hood of upstream research outputs being taken up by
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
40 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Figure 7 The Trait Development Pipeline for delivery of valuable stress tolerance traits/genes/QTLs from upstream research into the elite breeding
pool for improvement of crop productivity under climate change. The Trait Development Pipeline is organized into six stages: 1) guidelines for
prioritizing traits (assessment), 2) defining standards for phenotyping protocols, 3) identifying donors and QTL (including refining marker quality
metrics), 4) introgressing and 5) validating traits/genes/QTLs into elite genetic backgrounds to develop the elite donor lines that are 6) handed to
the breeding program for crossing. Those elite donor lines will then be systematically crossed and tested in target environments where climate
change is increasingly affecting the degree of abiotic stress affecting crop production. Created with BioRender.com
breeding are to take additional steps such as validation of most recently identified traits/genes/QTLs to incorporate
identified QTLs in relevant elite genomic backgrounds and into the breeding program, while at the same time effec-
to link with researchers who can evaluate the material under tively connecting with local breeders who can conduct wide-
field conditions. spread testing and who understand the needs of farmers in
On the other side of the gap, downstream science must stress-prone regions. This “bridge building” among scientific
make released varieties and advanced breeding lines more disciplines is critical to the development of more efficient
accessible to upstream scientists. Familiarity with this mate- pipelines that bring novel improvements to crops for cli-
rial is important because in some cases, key genes have been mate change-affected farmers.
identified and advocated as promising breeding targets with- To strengthen linkages between upstream and down-
out the recognition that they are already present in the stream development efforts, a framework has been devel-
breeding pool. Furthermore, the availability of improved ma- oped that organizes and codifies trait development efforts.
terial to upstream researchers will help to ensure that target This “Trait Development Pipeline” developed at the
loci are effective in those genetic backgrounds. Downstream International Rice Research Institute (Figure 7) applies stage
science also must stay up to date and gain access to the gate systems widely used in industry (Covarrubias-Pazaran
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 41
et al., 2022) to assess trait development progress against de- improvement. Breeders have traditionally used CWRs as
fined advancement criteria. The organization by stages ena- sources of superior traits, including key traits for enhancing
bles external review of the progress at each stage and adaptation to climate change (Dempewolf et al. 2014). The
provides decision points on whether to proceed, giving an main breeding objectives for climate change adaptation in-
opportunity to discontinue efforts that are not likely to clude resilience to abiotic stresses (drought, heat, salinity,
make an impact in breeding programs. and flooding/waterlogging) and biotic stresses brought
The current Trait Development Pipeline is organized into about as a result of the increase in atmospheric CO2 and el-
six stages that link a variety of research disciplines, and the evated average temperatures. Here, we provide examples of
pipeline provides a structure that gives a framework for recent progress in the use of CWRs in managing these
teamwork between these areas. The pipeline starts with an stresses and highlight specific areas where work is needed.
assessment of the trait of interest in the context of priority Table 1 provides a summary of the use of CWRs in breeding
traits needed by farmers and consumers that are not already for tolerance to abiotic stresses.
present in the elite breeding pool (see “Product concepts”
and “Market segments”; Covarrubias-Pazaran et al., 2022). A Drought stress
set of criteria regarding the availability and reliability of phe- Despite the complexity of drought stress (Ilyas et al., 2021),
notyping protocols for the trait, potential donor genotypes, CWRs have been reported that are more efficient than crop
mapping populations, QTLs, and markers determine ad- relatives in drought-related physiological processes such as
vancement to subsequent stages in the Trait Development higher WUE, higher CO2 assimilation, deeper root systems,
Pipeline. The pipeline is dynamic and subject to modifica- more efficient regulatory networks, leaf curling, and stomatal
tion over time based on researcher feedback and as techni- closure, as well as showing an abundance of allelic diversity
ques and technologies change. The outputs of the Trait within candidate genes. For example, higher WUE, higher car-
Development Pipeline are validated donor lines containing bon assimilation, and greater carboxylation efficiency were
new traits/genes/QTLs in a fully elite background. These reported in wild lettuce (Lactuca serriola; Eriksen et al., 2020),
“elite donor lines” can be used in the elite  elite crossing and Moenga et al. (2020) reported novel divergent drought
work to improve the most advanced breeding lines which tolerance mechanisms in wild chickpea (Cicer reticulatum)
will be evaluated in multilocation trials, evaluated by local that would be a great resource for improving cultivated
researchers, and considered for release as varieties for dis- chickpea (Cicer arietinum). Drought-related transcription fac-
semination to farmers. In this way, the outputs of trait/ tors of the Asr (abscisic acid, stress, ripening) family have a
gene/QTL discovery realize an ongoing impact across the high level of diversity in CWRs (Cortés et al. 2012) that might
breeding pool rather than improving just a single variety. be further exploited to improve cultivated crops. Most
Such sustained improvement through mainstream breeding drought studies to date in CWRs have focused on major
programs will facilitate the deployment of new technologies crops, and there is tremendous scope to undertake similar
to as many climate-change-affected crop production market studies in minor and under-researched crops.
segments as possible.
Application of the pipeline to known genes and QTLs Heat stress
helps to identify gaps in knowledge and products available, Heat stress is one of the greatest concerns for crop produc-
and addressing these gaps is already enabling the rapid in- tion considering the increasing effects of climate change.
troduction of a wide variety of genes contributing to disease The wild wheat relatives Triticum monococcum, T. dicoc-
resistance, heat, drought, cold, and salinity tolerance into coides, and Aegilops speltoides ssp. liqustica and CWR-
mainstream rice breeding efforts. Breeding programs are derived wheat genotypes were among the most heat toler-
thus able to respond in a far more agile manner to changing ant when tested alongside elite wheat genotypes (Peng
climate and market demands. As these genes are deployed et al., 2013; El Haddad et al., 2021). Similar observations have
into elite backgrounds, it becomes easier for small breeding been made in wild rice, Oryza meridionalis Ng. and O. aus-
programs to also leverage their value; the “heavy lifting” of traliensis, in which heat tolerance was associated with a
eliminating highly unfavorable genomic backgrounds, break- more stable activation of Rubisco (Scafaro et al., 2016).
ing linkage drag, and developing coupling-phase linkages has Overexpressing a thermostable variant of Rubisco activase
been done, so only minimal or no additional effort is re- from CWR significantly improved yield in domesticated rice
quired to move the new genes to other elite breeding pro- (Oryza sativa L.; Scafaro et al., 2018). More studies on the
grams. Thus, the value of new genes is no longer exclusively physiological and molecular basis of heat tolerance in wild
available to large, well-resourced programs. versus domesticated species are needed to enhance the de-
ployment of novel heat tolerant alleles in crop improvement.
Enhancing climate resilience through the use of
crop wild relatives Salinity tolerance
(By Damaris A. Odeny) Halophytic plants adapt to salinity through three distinct
Crop wild relatives (CWRs) are wild species that are closely mechanisms, all of which have been identified in various
related to domesticated crops and can be used for crop CWRs: osmotic stress tolerance, Na + or Cl– exclusion, and
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
42 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Table 1. Examples of wild relatives used to enhance abiotic stress tolerance in cultivated crops
Crop More resilient wild species Trait of interest Reference
Wheat Aegilops cylindrica Drought Pour-Aboughadareh et al. (2017)
Ae. crassa
Ae. caudata
Triticum urartu
T. monococcum Heat Khanna-Chopra and Viswanathan (1999);
T. dicoccoides Peng et al. (2013); El Haddad et al. (2021)
Ae. speltoides ssp. liqustica
T. ararticum
Ae. speltoides Salinity Ahmadi et al. (2018)
Ae. caudata
Ae. cylindrica
T. boeoticum
Sorghum Sorghum macrospermum Drought Cowan et al. (2020)
S. brachypodum Ochieng et al. (2020)
S. arundinaceum
S. sudanense
S. purpureosericeum
Banana Musa balbisiana; Drought Eyland et al. (2022)
M. acuminata ssp. errans
Rice Oryza rufipogon Salinity Tin et al. (2021)
O. nivara; O. coarctata Zhang and Xie (2014)
O. nivara; O. rufipogon Flooding Niroula et al. (2012)
O. meridionalis Ng. Heat Scafaro et al. (2012); Scafaro et al. (2016);
O. australiensis Scafaro et al. (2018)
Maize Zea nicaraguensis Flooding Mano et al. (2006);
Z. luxurians Mano et al. (2005);
Z. mays ssp. huehuetenangensis
Z. diploperennis Drought Shaibu et al. (2021)
Tomato Solanum cheesmaniae; Salinity Dehan and Tal (1978); Shalata and Tal (1998);
S. pennellii Mittova et al. (2002); Frary et al. (2010);
S. galapagense Pailles et al. (2020)
S. pimpinellifolium Heat Driedonks (2018)
Tepary bean Wild Phaseolus acutifolius Drought Buitrago-Bitar et al. (2021)
Adzuki bean Vigna nakashimae; V. riukiensis Salinity Yoshida et al. (2016)
Eggplant Solanum insanum Salinity Brenes et al. 2020)
Chickpea Cicer reticulatum Drought Moenga et al. (2020)
Sugarcane Saccharum spontaneum Salinity Kasirajan et al. (2021)
tolerance of tissue to accumulated Na + or Cl–. Wild rela- can be used to enhance flooding tolerance in elite SUB1
tives of adzuki bean, Vigna nakashimae and V. riukiensis, genotypes, which are not always tolerant to anaerobic con-
prevented Na + accumulation in roots and stems, and toler- ditions during germination. Wild species with tolerance to
ated accumulated Na + , respectively (Yoshida et al., 2016). A waterlogging/stagnant flooding have been reported to pos-
wild relative of tomato, Solanum pennellii, showed greater sess unique alleles for aerenchyma formation (Zhang et al.,
induction of antioxidant activity than cultivated tomato 2017), or to provide a stronger barrier to radial oxygen loss
(Solanum lycopersicum L.) under salt stress (Frary et al., (Pedersen et al., 2021). The availability of these different
2010). Salinity tolerance has also been reported in Oryza gla- sources of flooding/waterlogging resistance in CWRs pro-
berrima (Platten et al., 2013), Hordeum spontaneum (Kiani- vides an opportunity to introgress the beneficial alleles into
Pouya et al., 2020), and in Aegilops spp. (Zamani Babgohari elite varieties, especially where genomics-assisted introgres-
et al., 2013). sion and selection is possible.
Flooding tolerance CWRs as sources of resistance/tolerance to biotic stress
Flooding tolerance has been mainly studied in rice leading Introgression of disease resistance genes into cultivated crop
to the identification of the SUB1 locus (Mackill et al., 2012). species is perhaps the most beneficial use of CWRs in crop
Additional submergence-tolerant alleles (SUB1A-1) were improvement to date. Major genes have been introgressed
identified from wild rice species O. nivara and O. rufipogon, from CWRs for resistance to late blight (Phytophthora infes-
together with a likely presence of other submergence mech- tans) in potato (Solanum tuberosum L.; Ghislain et al., 2019),
anisms in other wild rice accessions (Niroula et al., 2012). blast disease (Magnaporthe oryzae) resistance in rice (Yoshida
Two anaerobic germination QTLs (qAGP1 and qAGP3) from and Miyashita, 2009) and several other key pathogens in
O. nivara introgression lines (Liu et al., 2021a) potentially wheat (Rani et al., 2020) and tomato (Sharlach et al., 2013),
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 43
just to mention a few. Pest resistance also benefited from pathogen pressure (Venkatesh and Kang, 2019). Similarly,
CWRs (Therezan et al., 2021), among the most recent being the impact of increased atmospheric CO2 in relation to
the introduction of fall armyworm (Spodoptera frugiperda) re- plant–pathogen interactions remains unsettled. For example,
sistance from wild relatives of maize (Singh et al., 2022). high CO2 concentrations led to increased susceptibility of
Climate change-related warmer average temperatures and al- wheat to fungal infection (Váry et al., 2015), whereas soy-
tered weather patterns are contributing to altered patterns in bean (Glycine max) exhibited either enhanced or reduced
the occurrence of crop pests and pathogens and the emer- susceptibility to infection, depending on the pathogen stud-
gence of new pests and pathogens around the globe, as ex- ied (Eastburn et al., 2010). Deeper insight into the complex
plored in more detail in the section by Rim et al. below. More interplay among abiotic and biotic stresses will inform ongo-
studies will be needed to focus on the introgression of quanti- ing work to mitigate crop damage caused by extreme cli-
tative resistance from wild to cultivated species to improve mate conditions or pathogens.
the durability of resistance to various diseases and pests. One mitigation strategy is the application of beneficial
microbes that enhance plant health and immunity. For in-
De novo domestication for resilience to climate change
stance, Actinobacteria in the genus Streptomyces are enriched
Despite several wild relatives having remarkable tolerance to in the root microbiome of plants under drought stress
biotic and abiotic stresses, successful introgression of these (Naylor et al., 2017). Application of Streptomyces strains to
traits into elite backgrounds has been difficult due to linkage seeds improved wheat growth and yield in drought field con-
drag (Nevo and Chen, 2010) and the complexity of most ditions (Yandigeri et al., 2012). Beneficial strains of
traits. De novo domestication, the incorporation of domesti-
Trichoderma fungus heightened plant immunity and antago-
cated genes into the nondomesticated species to develop
nized pathogenic fungi (Tyskiewicz et al., 2022). Soil applica-
new crops (Razzaq et al., 2021), presents a novel opportu-
tion of Trichoderma reduced fungal infection in soybeans,
nity for immediate utilization of the novel resilience alleles
tomatoes, peanuts (Arachis hypogaea), and other crops (Zin
in CWRs. The availability of vast genomic and phenomic
and Badaluddin, 2020). Inoculation with Trichoderma has
resources allow for machine learning (Niazian and Niedbała,
also been shown to enhance tolerance to abiotic stresses
2020) and more precise genome editing (Hua et al., 2019).
An excellent example of de novo domestication has been such as drought and salinity (Zhang et al., 2016; Scudeletti
reported in Solanum pimpinellifolium (Zsögön et al., 2018). et al., 2021). Biocontrol strategies present an opportunity to
There are now several countries that have exempted enhance resilience to environmental stress and disease pres-
genome-edited plants from genetically modified organism sure, while reducing the use of chemical pesticides or fertil-
regulations, making it possible to utilize de novo domesti- izers that can further damage the environment.
cated plants as soon as they are generated. Another strategy well-aligned with sustainable agriculture
practices is the introduction of genetic improvements that
Development of disease-resistant crops for a protect crops against pathogens and confer resilience to abi-
changing climate otic stress in a heritable manner. There are numerous exam-
(By Ellen Youngsoo Rim, Alexandra M. Shigenaga, Pamela ples of genetic alterations in crops leading to resistance to
C. Ronald) specific pathogens, many of which were achieved through
the introduction of immune receptors (Ercoli et al., 2022).
Plant reactions to a single stress differs from those of plants
Immune receptors are activated by direct or indirect interac-
exposed to combined abiotic and biotic stresses, with a shift
in signaling pathways and transcriptomic responses (Atkinson tion with microbial molecules to elicit host defense
and Urwin, 2012; Prasch and Sonnewald, 2013; Sharma et al., responses. Advances in genome sequencing and analysis
2013). Thus, understanding how plants respond to pathogen have accelerated the discovery of immune receptors and
stress under nonoptimal environmental conditions is essential other beneficial genetic traits in cultivated crop varieties and
for the development of resilient crops in a changing climate their wild relatives (Ercoli et al., 2022; Zsögön et al., 2022;
(Chaloner et al., 2021; Velásquez et al., 2018). and discussed in the section above by Odeny). For instance,
Diverse plant–pathogen interactions have been shown to a previously unknown variant of the immune receptor FLS2
be affected by adverse environmental conditions, leading to was identified in the genome of a wild grape species (Vitis
increased host susceptibility, or in some cases, increased riparia; Fürst et al., 2020). The introduction of the new FLS2
host resistance (Velásquez et al., 2018). Various plant species variant conferred resistance to Agrobacterium tumefaciens in
become more susceptible to fungal, viral, or bacterial patho- tobacco, offering a potential strategy to control crown gall
gens in response to elevated temperatures (Cohen and disease, which affects many crops including nut trees and
Leach, 2020; Velásquez et al., 2018). For example, exposure grapevines. Once identified, desirable genetic traits can be
to elevated temperature combined with drought stress led introduced into crops through methods such as marker-
to greater susceptibility to Turnip mosaic virus due to down- assisted breeding or genetic engineering. The use of gene-
regulated defense response gene expression (Prasch and stacking to introduce multiple protective genes into a single
Sonnewald, 2013). However, there are examples where high background will likely be an important consideration in en-
temperatures led to enhanced host resistance against gineering climate resilience (Figure 8).
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
44 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Figure 8 Development of crops with enhanced resilience to abiotic and biotic stress. Crops are exposed to a variety of stresses. Abiotic stresses
will intensify as the following climate conditions change: water availability, precipitation, temperatures, and atmospheric CO2 levels. Biotic stres-
sors that plants encounter will vary, but may consist of: bacteria, fungi, oomycetes, nematodes, viruses, and insect pests. As climate change alters
environmental conditions and plant-pathogen interactions, strategies to develop more climate-ready and disease-resistant crop varieties include
breeding or genome engineering approaches with stacking disease resistance genes, stacking climate tolerance and disease resistance genes, and/
or addition of beneficial microbes (see text for examples).
Genome engineering tools such as CRISPR–Cas9 and tran- effects of overactive defenses. For instance, growth penalties
scription activator-like effector nucleases allow greater con- associated with powdery mildew resistance in wheat were
trol over the sequence and genomic location of these reversed upon ectopic activation of genes encoding sugar
genetic changes. Crop engineering is an especially promising transporters through a mechanism yet to be elucidated (Li
avenue for mitigating vector-borne plant diseases, which are et al., 2022). In another example, necrosis associated with
anticipated to rise as higher temperatures expand the geo- broad spectrum potato virus resistance was eliminated
graphical distribution and survival of insect pests (Perilla- through mutating the regulatory region of the resistance-
Henao and Casteel, 2016; Huang et al., 2020; Skendzic et al., conferring immune receptor (Harris et al., 2013).
2021). For instance, introduction of proteins that target the Alternatively, protective genes can be designed to be
insect vector or the pathogen itself can confer host resis- expressed under specific conditions. High temperatures in-
tance. Expression of antimicrobial proteins that bind the crease susceptibility of the model plant Arabidopsis to the
membrane of Xylella fastidiosa, the causative agent of bacterial pathogen Pseudomonas syringae pv. tomato
Pierce’s Disease, decreased disease incidence in grapevines DC3000 (Pst; Wang et al., 2009; Huot et al., 2017). Disease re-
(Vitis vinifera; Dandekar et al., 2019). Such genetic strategies sistance genes expressed under a heat-inducible promoter
may lead to more effective and sustainable management of protected against Pst infection after exposure to high tem-
vector-borne diseases, which have relied heavily on chemical perature without pleiotropic growth defects (Leng et al.,
insecticides. 2021). Another challenge is that pathogens can overcome
Introduction of beneficial traits, however, have mainly fo- resistant traits by developing novel virulence strategies or by
cused on the development of crop varieties with resistance evolving mechanisms to evade detection by existing im-
to a single stress. Major hurdles remain in engineering crops mune receptors. Gene stacking might be used to delay or
with combined stress tolerance (Steinwand and Ronald, prevent the evolution of resistance-breaking pathogens un-
2020). For one, enhanced stress tolerance is often accompa- der diverse climate stresses.
nied by fitness costs, such as reduced plant growth and A promising avenue to simultaneously reduce crop loss to
yields (Velásquez et al., 2018; Venkatesh and Kang, 2019). pathogen and environmental stress is introducing disease re-
Additional genetic interventions can reduce detrimental sistance in the context of climate resilience (Rivero et al.,
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 45
2022; Figure 8). Identification of resistance genes that are improve plant access to nutrients, particularly phosphorus
more effective under abiotic stress, such as increased temper- and N. Two major groups are arbuscular mycorrhizal fungi
ature, is one approach (Chen et al., 2018; Dossa et al., 2020). (AMF), which colonize host roots and are widely distributed
For example, stacking the rice disease resistance genes Xa4 in plants, and ectomycorrhizae, mainly associated with trees
and Xa7 provided enhanced resistance to Xanthomonas ory- and shrubs (Genre et al., 2020). The soil region influenced
zae pv. oryzae (Xoo), the causal agent of bacterial blight dis- by mycorrhizal roots is called the mycorrhizosphere
ease, under high temperature conditions (Dossa et al., 2020). (Priyadharsini et al., 2016), where mycorrhizal fungi sequester
Alternatively, disease resistance genes can be introduced into carbon and form aggregate particles in soil that have a ma-
crop varieties that already sustain high resilience to abiotic jor impact on the composition of microbial and plant com-
stress. The introduction of six genes associated with resistance munities (Priyadharsini et al., 2016; Wang et al., 2021).
to the fungal pathogen Magnaporthe oryzae, the causal agent Under a warmer climate, mycorrhizal fungi can increase car-
of rice blast disease, into a rice variety with elevated drought bon sequestration by influencing the root/shoot ratio (Zhou
tolerance resulted in plants that are both resistant to blast in- et al., 2022). Ectomycorrhizal fungi can significantly affect
fection and tolerant of drought stress in the field (Carrillo the carbon sequestration capacity of certain soils, for exam-
et al., 2021). Another approach is stacking genes, through ple in boreal forests (Clemmensen et al., 2015; Genre et al.,
breeding or genome engineering, to confer both abiotic stress 2020). Colonization by AMF can mitigate adverse effects of
tolerance and disease resistance. For example, submergence drought and salt stress by improving nutrient uptake, mini-
(Sub1) and salt (Saltol) tolerance genes were stacked with mizing oxidative damage, and increasing osmotic adjustment
eight pathogen and pest resistance genes in an elite rice line (Hameed et al., 2014; Klinsukon et al., 2021).
(Das and Rao, 2015); this line showed resistance to M. oryzae, Several challenges restrict the application of AMF in agri-
Xoo and gall midge, as well as tolerance of submergence and culture as a biofertilizer. Plants vary widely in response to in-
salinity. In some cases, genes can act as regulatory hubs to dividual mycorrhizal fungi (Klironomos, 2003), and results of
control abiotic and biotic signaling pathways and are particu- research focusing on one or few AMF species under con-
larly valuable candidates to target for crop engineering trolled conditions may not translate to field conditions. In
(Husaini, 2022). For example, the rice transcription factor addition, many aspects of the signaling and nutrient ex-
MADS26 orchestrates abiotic and biotic stress responses. change pathways are shared between mycorrhizal fungi and
Downregulation of MADS26 led to enhanced resistance to M. biotrophic pathogens (Wang et al., 2012; Zhang et al., 2015;
oryzae and Xoo as well as drought tolerance in the field Jacott et al., 2017; Jiang et al., 2017; Zhang et al., 2021a).
(Khong et al., 2015). The effectiveness of each of these strate- Thus, it is critical to dissect how plants distinguish between
gies to develop resilience to multiple types of stress will vary AMF- and pathogen-influenced agronomic traits and engage
depending on the crop, pathogen, and environmental condi- productively with symbiotic microorganisms while simulta-
tions. Research on various strategies and their evaluation un- neously restricting pathogens.
der field conditions will be crucial to combat the negative Mycorrhizal fungi strongly influence host plant phospho-
effects of climate change on agricultural systems. rus acquisition. Interestingly, the phosphate starvation re-
sponse was found to be a core regulator in both a direct
Mycorrhizal and rhizobial symbioses under climate phosphate uptake pathway via root hairs and epidermis and
change challenges an indirect phosphate uptake pathway via mycorrhizal sym-
(By Xiaowei Zhang, Ertao Wang) biosis (Shi et al., 2021), suggesting the possibility of develop-
N cycling strongly influences climate change as it is closely ing crops that use phosphorus and N more efficiently by
correlated to the production of CO2, N2O, and CH4. coordination of the direct phosphate uptake pathway and
Currently, crop productivity is highly dependent on fertilizer mycorrhizal pathway in future.
application, particularly N, which has negative environmen-
tal effects through nitrate run-off and release of the potent N fixation in legumes and nonlegumes
GHG nitrous oxide. The development of high-yielding, dis- Biological N fixation is the process by which nitrogenase (an
ease-resistant crops can be aided significantly by improving enzyme found only in certain prokaryotes known as diazo-
associations with symbiotic microorganisms that enhance trophs) converts dinitrogen gas from the atmosphere into
nutrient assimilation in the host plant. Here, we summarize ammonia and is the main path for the formation of com-
the potential application of engineered mycorrhizal and rhi- bined N in nature. Three forms of N fixation are found in
zobial symbioses in developing self-fertilizing crops and nature: free-living, associative, and symbiotic (Soumare et al.,
maintaining sustainable agriculture in the era of global cli- 2020). In associative N fixation, N-fixing microorganisms liv-
mate change (Figure 9). ing on the surfaces or in the interstitial spaces of the plant
host use photosynthetic products from the plant as carbon
Mycorrhizal symbiosis sources to fix N for their own use and provide the excess
Plant roots are associated with diverse microbes, including fixed N to the host (Soumare et al., 2020). In symbiotic N
bacteria, fungi, and viruses collectively called the rhizosphere fixation, N-fixing bacteria colonize the cells of plant organs
microbiome. Among them, mycorrhizal fungi are known to such as root nodules and supply N to support host growth
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
46 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Figure 9 Mycorrhizal symbiosis and N self-fertilizing crops. A, Positive effects of mycorrhizal symbiosis. The mycorrhizal hyphal network forms a
mycorrhizosphere (light brown) which can enlarge the plant nutrient absorption area and supply a convenient zone for root-related microbes.
Benefits from mycorrhizal symbiosis include increased tolerance or resistance to abiotic or biotic stresses. B, Three steps to develop N self-fertiliz-
ing cereal crops to enhance climate change resilience. (1) Increasing associative N fixation. The mucilage (light green) is rich in carbohydrates and
harbors abundant diazotrophic microbiota (pink). Engineered cereal plants (such as maize) have the ability to produce rhizophine, which can be
perceived by engineered diazotrophs (orange). (2) Transferring symbiotic N fixation to cereal plants. Cereal crops are engineered for symbiotic N
fixation by expressing the chimeric receptors perceiving rhizobia signals and overexpressing key symbiotic regulators (CSSP genes, CRE1, etc.) and
nodule development genes (SCR-SHR, LBD16, etc.) to form nodule-like structures. (3) Autonomous N fixation in cereal crops. The ideal plant
which could assimilate N2 into ammonium is created by overexpressing rhizobial N fixation genes in plant cells.
and development, in systems such as Rhizobium/legume, Three mechanisms have been proposed to develop N self-
Frankia/alder, and Cyanobacteria/Australian cycads fertilizing cereal crops to enhance climate change resilience
(Pankievicz et al., 2019; Soumare et al., 2020). The rhizo- (Figure 9B):
bium–legume symbiosis is the most important N fixation 1. Increasing associative N fixation. Diazotrophs are present
system in terrestrial communities. in the carbon-enriched mucilage in maize aerial roots and
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 47
were found to contribute 29%–82% of the N nutrition of et al., 2013b). Transgenic Arabidopsis expressing a nine-nif
Sierra Mixe maize in a 5-year field experiment (Van Deynze gene cassette (nifBHDKENXhesAnifV) showed moderate ni-
et al., 2018). Engineering the cereal host and/or the diazo- trogenase activity and resulted in higher biomass and chlo-
trophs to enhance this association is therefore a promising rophyll compared to control plants grown in low-N or N-
avenue to increase biologically fixed N in crops. free medium (Yao et al., 2021). If the results of this study
It has been shown that the engineered expression in can be validated, this will provide the possibility to construct
Medicago truncatula and barley (Hordeum vulgare) of rhizo- cereal crops capable of autonomous N fixation in the future.
pine, a small molecule compound synthesized by a few rhizo-
bia, could be sensed by engineered bacteria Azorhizobium Enhancing climate resilience in the hardy staple
caulinodans ORS571 with a 103-fold increase in perception crop cassava
sensitivity (Geddes et al., 2019; Haskett et al., 2022). This pro- (By Marnin Wolfe, Eder Jorge de Oliveira, and Ismail Rabbi)
vides the possibility of increasing N fixation from endophytic Cassava (Manihot esculenta) is a staple root crop grown on
and free-living bacteria associated with crop plants, although
more than 28 million hectares and crucial to the food secu-
the in situ nitrogenase activity was suboptimal. Further experi-
rity of almost half a billion people. Cassava is uniquely posi-
ments should explore optimizing the expression levels of rhi-
tioned as one of the most climate change resilient crops
zopine biosynthetic genes to reduce fitness costs in host
due to its ability to tolerate prolonged droughts, often ex-
plants due to excessive gene expression.
ceeding 5 months. The cultivation of cassava has continued
2. Transferring symbiotic N fixation to cereal plants. The asso- to increase in tropical regions, where climate change
ciation of legumes with N-fixing bacteria requires several impacts will be particularly adverse (El-Sharkawy, 1993; Parry
molecular processes common to the mycorrhizal associa- and Rosenzweig, 1993; de Oliveira Aparecido et al., 2020). In
tions that are more widespread in plants, showing that the this section, we overview the innovations that have recently
evolution of the Rhizobium–legume symbiosis utilized many accelerated cassava genetic improvement, the challenges
existing processes that facilitate mycorrhizal interactions that drought and heat are expected to pose in coming deca-
(Roy et al., 2020; Wang et al., 2022). This close relationship des, and address prospects to improve climate resilience
provides a possibility to engineer symbiotic N fixation into through interdisciplinary innovations.
non-legume cereal crops by synthetic biology (Mus et al.,
2016). Some progress has been made toward this goal: (i) The NextGen cassava breeding project: A decade of
The overexpression of chimeric receptors, for which the ex- innovation
tracellular domains of the rice Myc factor receptors MYC Cassava is a clonally propagated crop domesticated in South
FACTOR RECEPTOR1 (OsMYR1) and CHITIN ELICITOR America that continues to radiate throughout the tropics.
RECEPTOR KINASE1 (OsCERK1) were replaced with those Phenotypic recurrent selection has been the mainstay of cas-
from the M. truncatula Nod factor receptors NOD FACTOR sava breeding in much of its history. As a result of its 12- to
PERCEPTION (MtNFP) and RECEPTOR-LIKE KINASE3 24-month growth cycle, low multiplication rate and low-
(MtLYK3), respectively, triggers calcium spiking in response seed set, phenotypic selection requires 4–6 years between
to a low concentration Nod factor treatment in rice (He crosses, a major bottleneck for genetic improvement
et al., 2019). (ii) The overexpression of several symbiotic reg- (Ceballos et al., 2015). Cassava has emerged as a model for
ulators induces spontaneous root-nodule-like structures the adoption of new breeding technologies among root and
(Soyano et al., 2013; Tirichine et al., 2007; Yang et al., 2022). tuber crops, including the incorporation of improved experi-
(iii) The key development genes in M. truncatula SHORT mental designs and phenotyping, as well marker-assisted se-
ROOT (MtSHR), SCARECROW (MtSCR), and LLOB-DOMAIN lection (Mbanjo et al., 2021).
PROTEIN16 (MtLBD16) specify cortical cell fate with the abil- In 2012, the Next-Generation Cassava (NGC) Breeding
ity to de-differentiate to form nodule primordia in response Project initiated a multi-disciplinary effort to accelerate ge-
to symbiotic signals (Schiessl et al., 2019; Soyano et al., 2019;
netic improvement, notably using genomic selection at
Dong et al., 2021). This constitutes a genetic toolkit to gen-
breeding programs in Africa and Latin America. NGC part-
erate nodule-like structures to accommodate N-fixing rhizo-
ners in Africa include the International Institute of Tropical
bia, that is by engineering the expression of these key
Agriculture and the National Root Crops Research Institute
regulators of nodule organogenesis in cereal crops. However,
in Nigeria; the West Africa Center for Crop Improvement in
creating the micro-aerobic conditions necessary for rhizobia
Ghana; the National Crops Resources Research Institute,
in the nodule organs of cereal crops to perform N fixation is
still a black box. Uganda, and Makerere University in Uganda; and the
Tanzania Agricultural Research Institute in Tanzania. In
3. Autonomous N fixation in cereal crops. An ideal approach South America, collaborators include EMBRAPA in Brazil
for self-fertilizing cereal crops would be to make them fix N and the International Center for Tropical Agriculture in
autonomously. A detailed study showed that the smallest N Colombia. In the USA, collaborators are Cornell University,
fixation operon consists of 9 genes, nifB, nifH, nifD, nifK, nifE, the Boyce Thompson Institute at Cornell, the University of
nifN, nifX, hesA, and nifV in Paenibacillus WLY78 (Wang Hawaii, and the USDA-ARS in Ithaca, NY. The details of
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
48 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
partners and funding found at https://www.nextgencassava. The complexity of drought-tolerance genetic architecture
org. suggests that genomic selection, augmented by genome
Instead of requiring phenotyping breeding lines over many editing and cutting-edge phenomics, will be necessary for
years before selecting new parents, genomic selection ena- the rapid development of climate-resilient cassava varieties.
bles breeders to predict performance based on genome- Currently, final yield is the basis for selection for drought tol-
wide genetic markers, even at the seedling stage erance (Khadka et al., 2020). However, yield is affected by
(Figure 10A). Genotyping of all germplasm and targeted many factors into drought and is only measurable after 10–
phenotyping of representative subsets make breeding value 12 months. Earlier stage, nondestructive evaluation of physi-
prediction in early stages possible, increasing selection inten- ological drought responses and root bulking is needed.
sity and reducing selection cycle time (Heffner et al., 2009). Remote sensing of photosynthetic performance using drones
The transition from phenotypic to genomic selection has with hyperspectral imaging (Verma et al., 1993; Banerjee et
gained momentum in cassava through the NGC, and while al., 2020) and root yield using ground penetrating radar is
breeding cycle times are 50% shorter, selection intensity and now possible (Agbona et al., 2021). High-throughput pheno-
accuracy are higher (Wolfe et al., 2017), and the rate of im- typing plus genomic prediction and GWAS-based discovery
provement is demonstrably increased relative to previous are powerful tools for climate-resilience breeding (Juliana
decades (Figure 10B). et al., 2019; Jha et al., 2020). Pilot tests have been conducted
Several additional innovations came to cassava under on cassava for association with above and below-ground
NGC, including: (1) GWAS enabling the cataloging and vali- traits (Selvaraj et al., 2020).
dation of trait-linked single-nucleotide polymorphisms used Genome editing and metabolic engineering are promising
for marker-assisted selection (Wolfe et al., 2017; Zhang et al., supplements to exploiting existing natural diversity.
2018; Rabbi et al., 2020); (2) Cassavabase.org, an open-access, Transformation of cassava to express isopentenyl transferase
breeding database for efficient management of phenotype resulted in increased water retention and leaf retention un-
and genotype data (Morales et al., 2022); and (3) use of der water stress (Zhang et al., 2010). The overexpression of
plant growth regulators for improved flowering and seed set transcription factors like DEHYDRATION-RESPONSIVE
(Hyde et al., 2020). Genomic resources developed during the ELEMENT BINDING PROTEIN (DREB), ABA-RESPONSIVE
last decade, including reference genomes (Lyons et al., 2021) ELEMENT BINDING PROTEIN1 (AREB1), and ABA-
and HapMap (Ramu et al., 2017; Kuon et al., 2019) have laid RESPONSIVE ELEMENT BINDING FACTOR2 (ABF2) were
a foundation for trait-discovery research. These technologies also shown to increase drought tolerance in some species
collectively will enable breeders worldwide to tackle the (Rivero et al., 2007). In Arabidopsis, CRISPR/Cas9 was used
food-security challenges posed by climate change. to modify the OPEN STOMATA2 (OST2) gene resulting in
greater drought tolerance through enhanced stomatal re-
Climate resilient cassava breeding: Innovations for the sponse (Osakabe et al., 2016). Engineering multiple traits
next decade such as improving light reaction efficiency, reducing photo-
Although cassava is considered a drought-tolerant species respiration, improving sucrose synthesis to increase sucrose
(Okogbenin et al., 2013), there is still a large gap between loading and stimulate cambium activity could improve
the yield obtained by farmers in semi-arid regions (9.5 starch synthesis and metabolite transport into storage roots
t.ha–1) and yield observed under experimental water deficit and increase sink capacity (Obata et al., 2020; Sonnewald
(23.6 t.ha–1) with improved genotypes (de Oliveira et al., et al., 2020). In cassava, there are no published studies on
2015). Fortunately, there is enormous genetic variability to the use of genome editing to mitigate drought response,
tap for drought tolerance for future genetic improvement but several studies have demonstrated the feasibility of using
(de Oliveira et al., 2017; Figure 10C). Most cassava field test- CRISPR/Cas9 for virus resistance (Gomez et al., 2019) and re-
ing by breeders is done in both high-rainfall and drought- ducing cyanogenic compounds (Gomez et al., 2021).
prone environments. Over the annual cropping cycle, geno- Climate change will disproportionately impact already
types are routinely exposed to 3–5 months of drought and food insecure regions of the world (Easterling and Apps,
higher temperatures during which they are evaluated for 2005). Cassava, already a hardy crop, can help to attenuate
leaf retention, greenness, and damage by dry season pests some of those negative impacts. For example, cassava
such as green mites (Ezenwaka et al., 2018). Advanced test- planted under free-air CO2 enrichment has been shown to
ing is usually done in multienvironment trials, including low positively respond with increased yield and higher WUE
rainfall, heat-stressed environments (Hershey, 1984). (Rosenthal et al., 2012; Ruiz-Vera et al., 2020). Given suffi-
Although genetic control of drought tolerance in cassava, as cient investment, the role of cassava as a food-security and
measured by yield under drought, is complex with strong industrial crop will continue to expand and serve as a buffer
genotype-by-environment interaction (de Oliveira et al., to future climate change-related food insecurity. We have
2015), a recent GWAS identified candidate genes with described ways in which cassava is a “climate-smart”
known association to drought tolerance and markers useful crop and an important staple for millions in the tropics.
for breeding (dos Santos Silva et al., 2021). Now is the time to continue the modernization in cassava
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 49
Figure 10 Genomic selection (GS) in a cassava breeding program. A, Each breeding cycle begins with a crossing block trial where seeds are gener-
ated. The first evaluation, a seedling nursery (SDN) usually involves 410K plants, but cassava does not produce storage roots when planted from
seed and no yield data is collected. After 12 months, seedlings are cloned (5–10 cuttings/plant) into their first single-row, unreplicated clonal eval-
uation trial (CET) followed by at least three stages of yield trials (preliminary [PYT], advanced [AYT], and uniform [UYT]). All lines entering CET
are genotyped genome-wide; sometimes this is done during the seedling nursery. As a result, genomic prediction enables selection of new parents
for crossing even as early as the SDN (dashed red arrow). B, GS has resulted in demonstrable acceleration in the rate of genetic improvement since
initiation in 2012. Results shown are from the IITA GS population. The genomically predicted performance of GS-era (purple) and historical (yel-
low) clones relative to a multi-trait selection index (y-axis) is plotted against the year when each clone was first generated (x-axis). C, Field trial
showing variability for one of the major future challenges to cassava: drought. The top image shows plants 3 months after planting, under irriga-
tion at Petrolina (Pernambuco, Brazil). The bottom image shows plants 3 months later under water deficit.
breeding and biotechnology to benefit the most vulnerable 2019), showed similar decreases in mineral nutrients. A
populations. more comprehensive set of FACE experiments were
reported across three countries, with multiple sites and
The carbon nutrient penalty: Will it matter? crops (Myers et al., 2014, Dietterich et al., 2015), which con-
(By Gabriel Castrillo, Martin R. Broadley, and David E. Salt) firmed decreases in Zn and Fe concentration of 5%–10% for
Hidden hunger, the lack of sufficient dietary micronutrients C3 grains and legumes at the elevated CO2 concentrations
including iron (Fe) and zinc (Zn), is a major problem for a predicted for 2050 (546–586 ppm). A large meta-analysis
significant portion of the world’s human population representing numerous FACE and non-FACE experiments
(Kumssa et al., 2015; Lenaerts and Demont, 2021). also identified similar reductions in Zn, and in other dietary
Experiments with plants cultivated in growth chambers mineral nutrients such as calcium (Ca) and magnesium (Mg;
have suggested that elevated atmospheric CO2 is associated Loladze, 2014). This carbon nutrient penalty was projected to
with a decline in mineral nutrients in a number of crops, for cause a decrease in the global availability of dietary Fe and
example, decreased Fe and Zn concentrations in wheat, bar- Zn of between 2.5% and 3.6% by 2050 (Beach et al., 2019);
ley, and rice (Manderscheid et al., 1995; Fangmeier et al., producing the forecast that many countries that currently
1997; Seneweera and Conroy, 1997; la Puente de et al., 2000; have high levels of hidden hunger will continue to do so.
Pleijel et al., 2000). Free-air CO2 enrichment (FACE) experi- A better understanding of the impact of elevated CO2 on
ments with plants grown under standard field management mineral nutrient concentrations in crops requires concomi-
practices, with various crops including soybean, sorghum tant consideration of elevated temperature, as they go hand
(Sorghum bicolor), potatoes, wheat, barley, and rice (Prior in hand. Combined FACE and temperature (T-FACE) experi-
et al., 2008; Högy and Fangmeier, 2009; Högy et al., 2009; ments have begun to address the possible impact of ele-
Erbs et al., 2010; Fernando et al., 2014a, 2014b; Ujiie et al., vated temperatures on the carbon nutrient penalty. In
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
50 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
soybean, elevated CO2 caused a decrease in seed Fe and Zn et al., 2019), and wheat (Gardiner et al., 2018). The applica-
concentrations (as previously observed), while elevated tem- tion of genome-wide association mapping to this variation
perature had the opposite effect; but the combined effect of has led to the identification of genes controlling variation in
elevated temperature and CO2 restored seed Fe and Zn con- numerous elements (Baxter et al., 2010; Chao et al., 2012,
centrations (Köhler et al., 2019). A similar compensating ef- 2014; Forsberg et al., 2015; Yang et al., 2018). Ecological stud-
fect of elevated temperature on the carbon nutrient penalty ies are starting to reveal the adaptive benefit of this variation
was also observed in rice and wheat (Guo et al., 2022). for coastal populations (Busoms et al., 2018, 2021).
Under uniform global temperature increases, the carbon nu- Soil microbiota contributes to the biogeochemical cycling
trient penalty may therefore be expected to disappear. of elements, soil regeneration, and plant and animal growth
However, rising global temperatures will not be uniform and productivity (Custódio et al., 2022). In experiments with
across the globe, with different regions experiencing different Arabidopsis, the root microbiome was shown to control dif-
levels of warming. Predicting if elevated temperatures will ferentiation of the endodermis, a diffusion barrier that
balance nutrient loss due to elevated CO2 may be more affects mineral nutrient homeostasis, through the repression
complex and uncertain. of responses to the phytohormone abscisic acid in the root
Improved access to diverse diets, comprising more (Salas-González et al., 2021). However, these mechanisms
nutrient-dense foods, can play a role in alleviating hidden have not been evaluated under future elevated CO2 scenar-
hunger. However, access to micronutrient-adequate diets is ios. Elevated CO2 in the short term increases metabolic ac-
unlikely for many people in the coming decades, for socio- tivity and microbial biomass in the soil, with a concomitant
economic reasons (Nelson et al., 2018). Geographical con- promotion of plant growth and root exudation, conditions
straints to micronutrient availability in many food systems, that reduce soil N content (Chen et al., 2014; Xiong et al.,
reported from recent GeoNutrition surveys, further com- 2015; Yu et al., 2018a). Thus, in the long-term, elevated CO2
pound this challenge (Gashu et al., 2021). Interventions to is predicted to have a negative impact on the soil carbon cy-
alleviate hidden hunger include supplements, food fortifica- cle, promoting the depletion of easily decomposed carbon
tion, and biofortification of staple crops through breeding and increasing the degradation of mineralized SOC with a
and agronomy. Zn-biofortified wheat varieties released in net increase in atmospheric CO2 (Yang et al., 2019a).
India and Pakistan (Zia et al., 2020; Govindan et al., 2022), Elevated CO2 influences microbial enzymatic activities for
and Zn-biofortified hybrid maize varieties in Guatemala and phosphorus and N cycling but this effect changes depending
Colombia (Maqbool and Beshir, 2019) can increase grain Zn on the ecosystem (Naylor et al., 2020). We need to under-
concentration by more than the anticipated decreases due stand microbiome stability in diverse ecological contexts,
to elevated CO2. The continued development of crops that considering spatial resolution, microbial connectivity, and
can reliably accumulate sufficient quantities of mineral multi-kingdom composition. This will allow us to feed cur-
nutrients against a backdrop of climate change is an impor- rent models with realistic experimental data to predict the
tant part of this solution. The use of micronutrient fertilizers impact of climate changes on soil microbial populations and
(Joy et al., 2017) and “regenerative” agricultural interventions their interactions with plants, helping us to develop
(Manzeke-Kangara et al., 2021) can also play a role in reduc- microbial-based strategies to alleviate climate change
ing hidden hunger. impacts on soil and food production.
Our understanding of mineral nutrient homeostasis in
plants is extensive, with over 176 genes identified to date Can we achieve a biomass-based
(Whitt et al., 2020), but far from complete. Of these known bioeconomy?
genes, over 80 are characterized as ion transporters, many of
which were investigated based on their predicted function (By Maureen C. McCann and Nicholas C. Carpita)
as transmembrane proteins. High-throughput elemental Gross domestic product, a measure of economic prosperity,
analysis of plant material, also known as ionomics (Salt is tightly correlated with energy consumption. Fossil fuels
et al., 2008), has proved to be a powerful forward genetic accounted for 80% of global energy resources in 2020. Coal
screening tool that allows the discovery of genes involved in and gas can eventually be displaced by renewable energy
mineral nutrient homeostasis and the study of natural ge- from wind and solar, geothermal and hydroelectric, and nu-
netic variation in the system (Huang and Salt, 2016). This clear energy (U.S. Department of Energy, 2015). Oil, however,
approach highlights the critical importance of the Casparian provides both liquid transportation fuels and raw materials
strip in the endodermal cell wall in controlling mineral nu- for the petrochemical industry. As addressing climate change
trient homeostasis (Hosmani et al., 2013; Pfister et al., 2014; becomes increasingly urgent, we now need to shift from oil
Kamiya et al., 2015; Reyt et al., 2020, 2021; Alcock et al., derived from long-dead organisms to living organisms that
2021). Ionomics has also revealed a global pattern of natural can provide chemicals, fuels, and materials (Carpita and
variation in the leaf and seed ionome of Arabidopsis McCann, 2020). In this section, we imagine a biomass-based,
(Campos et al., 2021), and in rice (Pinson et al., 2015), barley circular bioeconomy, enabled by recombinant DNA technol-
(Houston et al., 2020), soybean (Ziegler et al., 2018), common ogies, with the potential to decouple our prosperity from
bean (Phaseolus vulgaris; Nazir et al., 2022), peanut (Zhang fossil fuel consumption (National Academies of Science,
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 51
Engineering, and Medicine, 2020). To succeed, this bioecon- The diversity of plant metabolism, natural and engineered,
omy must be fully rooted in plant biology. also provides a foundation for engineering biology to create
Natural and engineered oil-accumulating plants and economic value. Living plant cells synthesize between
microalgae, such as cyanobacteria, are an important source 100,000 and 1 million kinds of molecules (Fang et al., 2019).
of liquid hydrocarbons for use as fuel components. To ad- Making natural or synthetic products directly in plants can
dress how plants can displace a significant proportion of oil take advantage of orders-of-magnitude greater metabolic
consumption also requires use of the sugars and aromatics complexity and potential product yields than can be
derived from plant cell walls (McCann and Carpita, 2015). achieved in microbial chassis organisms. Efficient production
Electric and hybrid vehicles powered by renewable energy of target compounds in plants will require a systems-level
sources are becoming viable long-term options for light understanding of metabolism and constraints, including
ground transportation (U.S. Department of Energy, 2015). tradeoffs between carbon fluxes and cellular energy
However, air, marine, and heavy-duty modes of transporta- balances.
tion, which contribute one-third of US transportation GHG The structural complexity of plant cell wall components
emissions, will remain dependent upon energy-dense, liquid- can provide oligomeric and polymeric substrates for materi-
hydrocarbon fuels for decades because of slow fleet turn- als such as thermosets, thermoplastics, composites, cellulose
over: aircraft, for example, have a service lifetime of 25–30 nanocrystals, and nanofibers. Thermoset materials include
years. Advanced biofuels, fully compatible with existing epoxy, silicone, and polyurethane. Lignin- and carbohydrate-
engines and transportation infrastructure, can include liquid derived monomers have been incorporated into polymers to
hydrocarbons produced by chemical or enzymatic catalytic create new bio-based materials with improved performance
conversion of biomass-derived sugars and aromatics (Huber characteristics compared to fossil fuel-derived thermoset
et al., 2003; Wang et al., 2014). materials (Zhao and Abu-Omar, 2015; Jiang et al., 2018;
Plant-based biofuels also offer the potential for the pro- Chen et al., 2019). Poplar fibers have also been directly in-
duction of valuable chemical co-products. Decades of re- corporated into composites with polylactic acid as a replace-
search have overcome the technological barriers to the ment for conventional carbon nanofibers that reinforce
production of cellulose-derived glucose and, more recently, polymers for large-scale 3D printing applications (Zhao
lignin-derived aromatics. As a result of new deconstruction et al., 2019). In contrast to thermosets, thermoplastics can
be melted, and some of their monomers may be recycled.
technologies that preserve aromatic ring structures (Bozell
The entire pathway to polyhydroxybutyrate was engineered
et al., 2011; Labbé et al., 2012; Parsell et al., 2013; Socha
in cotton over 25 years ago (John and Keller, 1996), and
et al., 2014), lignin is no longer a major source of biomass
more recently in the bioenergy crop switchgrass (Panicum
recalcitrance. Catalytic depolymerization of lignin has been
virgatum) (Somleva et al., 2008). Routes for the biological
achieved without decomposition of cellulose or xylan, en-
synthesis of polyhydroxyurethane have been envisioned
abling the concept of the “lignin-first” biorefinery, where aro-
(Nohra et al., 2013). When pulped wood particles are
matic fuel substrates are removed before cellulose and other
treated with acids, cellulose nanocrystals, and cellulose nano-
carbohydrates are processed (Ragauskas et al., 2014;
fibers are recovered, derivatives of which are used for several
Schutyser et al., 2015; Key and Bozell, 2016; Yang et al., kinds of synthetic materials as replacements for plastics
2019b). To produce hydrocarbon fuels, deoxygenation reac- (Moon et al., 2011; Zhu et al., 2016).
tions must proceed to full chemical reduction, but for Maximizing the recovery of biomass carbon into fuels and
chemical products, reactions must necessarily be highly se- co-products requires flexible design capabilities to produce
lective to preserve desirable functional chemical groups. The cell wall architectures that can be easily and completely
petroleum industry produces a handful of platform chemi- deconstructed for current and future conversion processes
cals from oil, including ethylene, propylene, C4-olefins, ben- (McCann and Carpita, 2015). As robust cell wall architec-
zene, toluene, and xylene, that are oxygenated to make tens tures are integral to plant growth and development, genetic
of thousands of chemicals (Wang et al., 2014; Parsell et al., variants that are tailored with regard to biomass quality for
2015). Plants synthesize highly oxygenated polymers, and conversion processes must not be compromised for yield or
the chemical moieties in these structures hold tremendous sustainability traits in field performance. Major knowledge
value as useful building blocks for chemical co-products. gaps include how biosynthetic products are integrated into
Pathways that employ lignin-derived aromatics as substrates composite structures, how their individual structural com-
to replace commodity chemicals have been envisioned using plexities contribute to molecular- to macro-scale architec-
either enzymatic or chemical catalysis (Wellisch et al., 2010; tures, and how cell wall architectures might be redesigned
Zakzeski et al., 2010). Controlled fractionation of biomass for production of high-value products (Carpita and
with downstream catalytic upgrading provides several value- McCann, 2020).
added streams for the major biomass components: xylans to Material use is tightly coupled to energy use, GHG emis-
furfural (Vinueza et al., 2015), lignin to aromatics and dicar- sions, land and water use, and waste flows. About one-third
boxylic acids (Zeng et al., 2015), and cellulose to hydroxyme- of global GHG emissions comes from industrial manufactur-
thylfurfural (Hewetson et al., 2016). ing. To decarbonize this economic sector will require
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
52 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
changing the means of manufacture as well as the nature of soil science. Improved communication and collaboration
material inputs (Chui et al., 2020). We might imagine how across disciplines and between academia and industry can
to build simplified production systems with the components also be viewed as a low-tech effort that can have a strong
of plant cells or make biohybrid materials outside an intact impact. Identifying and seeking out potential collaborators
organism. We might imagine designing plants to synthesize who can link the research to impactful pathways should be
homopolymers, heteropolymers and composite materials, a primary goal early in the planning stages of research proj-
displacing structural concrete and steel with new materials ects for maximum benefit. Socio-economic and political per-
like superwood (Chen et al., 2020), or developing new-to- spectives will also be crucial in determining which
nature materials with advantageous properties. approaches will be adopted and how quickly they will be
Food security is a paramount concern and there are land implemented. Networking, discussion, and collaboration in
use issues to consider in raising crops for nonfood versus the socio-political arena and with industry, governmental,
food production. Nonfood cash crops, such as—tradition- and nongovernmental organizations may also be crucial.
ally—cotton (Gossypium hirsutum), tobacco, hemp, hops
(Humulus lupulus), and biofuel feedstocks, to name just a
few, can be of considerable value to growers and mitigate fi- Implementation
nancial risk. The diversification of food and nonfood plant Many current practices have substantial potential for miti-
products within a single cropping system, or a single crop, gating CO2 emissions, including reducing food and agricul-
coupled with principles of sustainability and climate change tural waste, shifting to plant-based diets, reducing
resilience, could thus be an advantage toward achieving deforestation coupled with afforestation/reforestation, and
both food and energy security. The decarbonization of agri- restoring coastal wetlands. Some technological solutions also
culture could include the use of bioenergy crops to displace have potential in the shorter term, including direct air cap-
fossil fuels as a source of hydrogen for ammonia production ture, biochar, enhanced rock weathering, and bioenergy
(Gencer et al., 2020) as well as displacement of fossil fuels combined with carbon capture and storage. To date, none
for harvesting and drying. of these options has been implemented globally due to cost,
In the USA, an annual sustainable resource of over 1.6 bil- timeline, inefficiency, lack of scalability, or an uncertain and
lion tons of lignocellulosic biomass could be considered a evolving carbon price and market. Estimates for the poten-
strategic carbon reserve (U.S. Department of Energy, 2016). tial of available technologies vary widely and will depend on
This quantity of biomass represents double the entire an- the ability of nations to realize effective measures (Roe et al.,
nual output of the US agricultural system—grains, fruits, 2019). We have explored ways that plant science can help
vegetables, hay, and pasture grasses. To double or triple the to tip the balance toward enhanced climate change mitiga-
capacity of the current agricultural system for a biomass- tion and crop resilience. The section on enhancing carbon
based bioeconomy, additional acres must be brought into
capture and sequestration in annual cropping systems
production, all crops must be high-yielding, and growers
speaks to our immediate needs for carbon capture on a
must benefit from diversification of plant products.
massive scale and the possibility that plant scientists can
Conclusions achieve a meaningful impact in this arena.
Some of the goals of examples discussed may require years
We presented examples of some plant biology-based solu-
to realize fully, such as engineering C4 photosynthesis into
tions that we believe show promise toward enhancing ter-
rice, symbiotic N fixation into cereals, and crops that pro-
restrial carbon sequestration and engineering climate
duce a variety of synthetic products. Although time is press-
resilient crops. Although we addressed several disparate
ing, this does not make them unworthy of attention. First,
topics, a few overarching conclusions emerge.
aspects of these longer-term goals may provide significant
Innovation benefits in the short term, and second, the need for carbon
Some of the ideas described here may seem far-fetched to capture and enhancing crop resilience and food security will
today’s readers, but we believe that for our planet to remain continue in the future. The need is urgent for every plant bi-
inhabitable and sustainable, many of the ideas proposed ologist to consider today how their research can contribute
here—or others like them—will need to be realized, and we to addressing climate change, ensuring food security, and
will need plant scientists to help achieve them. achieving a sustainable biomass-based bioeconomy.
Collaboration
By definition, efforts to mitigate global climate change must Acknowledgments
be large scale. Plant scientists contributing meaningfully in We thank two anonymous reviewers and the editors for
this arena most likely will be those who seek out effective their helpful comments. Wolfgang Busch and Joanne Chory
collaboration—not only with other plant scientists but also are grateful for the work of colleagues in the Harnessing
with those in other disciplines, including for example agron- Plants Initiative (HPI): Julie Law, Joe Noel, Todd Michael, and
omy, bioinformatics, data science, engineering, forestry, and all other HPI team members.
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 53
Funding Amaducci S, Zatta A, Raffanini M, Venturi G (2008)
Characterisation of hemp (Cannabis sativa L.) roots under different
Collaborative research in the J.K. McKay (Colorado State growing conditions. Plant Soil 313: 227
University) and C. Topp (Donald Danforth Plant Science Anantha MS, Patel D, Quintana M, Swain P, Dwivedi JL, Torres
Center) labs is funded by U.S. Department of Energy RO, Verulkar SB, Variar M, Mandal NP, Kumar A, et al. (2016)
Advanced Research Projects Agency-Energy award DE- Trait combinations that improve rice yield under drought:
Sahbhagi Dhan and new drought-tolerant varieties in South Asia.
AR0000826 (variation in NUE and root growth responses to Crop Sci 56: 408–421
N in rice breeding lines) and by funding from Wells Fargo Arai-Sanoh Y, Takai T, Yoshinaga S, Nakano H, Kojima M,
IN2 (carbon sequestration potential of hemp crops grown Sakakibara H, Kondo M, Uga Y (2014) Deep rooting conferred by
for grain and fiber). The work of HPI is funded by gifts from DEEPER ROOTING 1 enhances rice yield in paddy fields. Scient
the TED Audacious Program, the Bezos Earth Fund, the Hess Rep 4: 5563
Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dy-
Corporation, SEMPRA Energy and others. The NextGen namic response of plant respiration to temperature. Trends Plant
Cassava Breeding project is funded by the UK’s Foreign, Sci 8: 343–351
Commonwealth & Development Office (FCDO) and the Bill Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and
and Melinda Gates Foundation (Grant INV-007637). abiotic stresses: from genes to the field. J Exp Bot 63: 3523–3543
Research on improving photosynthetic water use efficiency Audu V, Ruf T, Vogt-Kaute W, Emmerling C (2022) Changes in mi-
crobial biomass and activity support ecological intensification of
by the A.D.B. Leakey group is funded by the Office of
marginal land through cultivation of perennial wheat in organic
Biological and Environmental Research in the U.S. agriculture. Biol Agric Hortic. doi: 10.1080/01448765.2022.2040589
Department of Energy, Office of Science (DE-SC0018277 and Ayub G, Zaragoza-Castells J, Griffin KL, Atkin OK (2014) Leaf res-
DE-SC0018420). The C4 Rice project is funded by a grant piration in darkness and in the light under pre-industrial, current
from the Bill & Melinda Gates Foundation to the University and elevated atmospheric CO2 concentrations. Plant Sci 226:
of Oxford (INV-002970). Work in the P.C. Ronald lab is 120–130
Bahuguna RN, Chaturvedi AK, Pal M, Viswanathan C, Jagadish
funded by gifts from the CHAN ZUCKERBERG INITIATIVE SK, Pareek A (2022) Carbon dioxide responsiveness mitigates rice
and grants from the National Science Foundation (2027795 yield loss under high night temperature. Plant Physiol 188:
to P.C.R.), the United States Department of Agriculture, the 285–300
National Institutes of Health (GM122968 and GM55962 to Bahuguna RN, Solis CA, Shi W, Jagadish SVK (2017) Post-flowering
P.C.R.), and the Joint BioEnergy Institute funded by the US night respiration and altered sink activity account for high night
temperature-induced grain yield and quality loss in rice (Oryza sat-
Department of Energy (No. DE-AC02-05CH11231 to J.C.M
iva L.). Physiol Plant 159: 59–73
and P.C.R.). Baker JFT, Allen LRA Jr, Boote KNJ Pickering NB (2000) Direct
Conflict of interest statement. None declared. effects of atmospheric carbon dioxide concentration on whole can-
opy dark respiration of rice. Global Change Biol 6: 275–286
Banerjee BP, Joshi S, Thoday-Kennedy E, Pasam RK, Tibbits J,
Hayden M, Spangenberg G, Kant S (2020) High-throughput phe-
References notyping using digital and hyperspectral imaging-derived bio-
Agbona A, Teare B, Ruiz-Guzman H, Dobreva ID, Everett ME, markers for genotypic nitrogen response. J Exp Bot 71: 4604–4615
Adams T, Montesinos-Lopez OA, Kulakow PA, Hays DB (2021) Ball P (2020) The lightning-fast quest for COVID vaccines—and
Prediction of root biomass in cassava based on ground penetrating what it means for other diseases. Nature 589: 16–18
radar phenomics. Remote Sens 13: 4908 Bar-Even A (2018) Daring metabolic designs for enhanced plant car-
Aggarwal P, Vyas S, Thornton P, Campbell BM (2019) How much bon fixation. Plant Sci 273: 71–83
does climate change add to the challenge of feeding the planet Baxter I, Brazelton JN, Yu D, Huang YS, Lahner B, Yakubova E, Li
this century? Environ Res Lett 14: 043001 Y, Bergelson J, Borevitz JO, Nordborg M, et al. (2010) A coastal
Ahmadi J, Pour-Aboughadareh A, Fabriki-Ourang S, Mehrabi AA, cline in sodium accumulation in Arabidopsis thaliana is driven by
Siddique KH (2018) Screening wild progenitors of wheat for salin- natural variation of the sodium transporter AtHKT1;1. PLoS Genet
ity stress at early stages of plant growth: insight into potential 6: e1001193
sources of variability for salinity adaptation in wheat. Crop Pasture Beach RH, Sulser TB, Crimmins A, Cenacchi N, Cole J, Fukagawa
Sci 69: 649–658 NK, Mason-D’Croz D, Myers S, Sarofim MC, Smith M, et al.
Ainsworth EA, Long SP (2021) 30 years of free-air carbon dioxide (2019) Combining the effects of increased atmospheric carbon di-
enrichment (FACE): What have we learned about future crop pro- oxide on protein, iron, and zinc availability and projected climate
ductivity and its potential for adaptation? Global Change Biol 27: change on global diets: a modelling study. Lancet Planet Health 3:
27–49 e307–e317
Albritton DL, Meira Filho LG, Cubasch U, Dai X, Ding Y, Griggs Bellasio C (2019) A generalised dynamic model of leaf-level C3 pho-
DJ, Hewitson B, Houghton JT, Isaksen I, Karl T et al. (2001) tosynthesis combining light and dark reactions with stomatal be-
Technical Summary. In Houghton JT, Ding Y, Griggs DJ, Noguer M, haviour. Photosyn Res 141: 99–118
van der Linden PJ, Dai X, Maskell K, Johnson CA, eds, Climate Berg IA (2011) Ecological aspects of the distribution of different au-
Change 2001: The scientific basis. Contribution of working group I totrophic CO2 fixation pathways. Appl Environ Microbiol 77:
to the third assessment report of the intergovernmental panel on 1925–1936
climate change, Cambridge University Press, Cambridge, United Blanco-Canqui H, Shapiro CA, Wortmann CS, Drijber RA, Mamo
Kingdom and New York, NY, USA, pp. 881 M, Shaver TM, Ferguson RB (2013) Soil organic carbon: the value
Alcock TD, Thomas CL, Ó Lochlainn S, Pongrac P, Wilson M, to soil properties. J Soil Water Conserv 68: 129A–134A
Moore C, Reyt G, Vogel-Mikus K, Kelemen M, Hayden R, et al. Borum J, Sand-Jensen K, Binzer T, Pedersen O, Greve TM (2006)
(2021) Magnesium and calcium overaccumulate in the leaves of a Oxygen movement in seagrasses. In Seagrasses: Biology, Ecology
schengen3 mutant of Brassica rapa. Plant Physiol 186: 1616–1631 and Conservation. Springer, Dordrecht, pp 255–270
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
54 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Bozell JJ, Black SK, Myers M, Cahill D, Miller WP, Park S (2011) relationships of natural and engineered wood. Nat Rev Mater 5:
Solvent fractionation of renewable woody feedstocks: Organosolv 642–666
generation of biorefinery process streams for the production of Chen C-H, Tung S-H, Jeng R-J, Abu-Omar MA, Lin C-H (2019) A
biobased chemicals. Biomass Bioenerg 35: 4197–4208 facile strategy to achieve fully bio-based epoxy thermosets from
Brenes M, Solana A, Boscaiu M, Fita A, Vicente O, Calatayud Á, eugenol. Green Chem 21: 4475–4488
Prohens J, Plazas M (2020) Physiological and biochemical Chen S, Zhang W, Bolus S, Rouse MN, Dubcovsky J (2018)
responses to salt stress in cultivated eggplant (Solanum melongena Identification and characterization of wheat stem rust resistance
L.) and in S. insanum L., a close wild relative. Agronomy 10: 651 gene Sr21 effective against the Ug99 race group at high tempera-
Broberg MC, Högy P, Fen Z, Pleijel H (2019) Effects of elevated ture. PLoS Genet 14: e1007287
CO2 on wheat yield: non-linear response and relation to site pro- Chui M, Evers M, Manyika J, Zheng A, Nisbet T (2020) The Bio
ductivity. Agronomy 9: 243 Revolution: innovations transforming economies, societies, and our
Brodersen KE, Nielsen DA, Ralph PJ, Kühl M (2015) Oxic micro- lives. Report of the McKinsey Global Institute. McKinsey & Co.,
shield and local p H enhancement protects Z ostera muelleri from San Francisco. www.mckinsey.com/mgi
sediment derived hydrogen sulphide. New Phytol 205: 1264–1276 Ciais P, Sabine C, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra
Buitrago-Bitar MA, Cortés AJ, López-Hernández F, London~o- A, DeFries R, Galloway J, Heimann M, et al. (2013) Carbon and
Caicedo JM, Mun~oz-Florez JE, Mun~oz LC, Blair MW (2021) other biogeochemical cycles. In TF Stocker, D Qin, G-K Plattner, M
Allelic diversity at abiotic stress responsive genes in relationship to Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex, PM Midgley
ecological drought indices for cultivated tepary bean, Phaseolus (eds) Climate Change 2013: The Physical Science Basis.
acutifolius A. Gray, and its wild relatives. Genes 12: 556 Contribution of Working Group I to the Fifth Assessment Report
Busoms S, Paajanen P, Marburger S, Bray S, Huang XY, of the Intergovernmental Panel on Climate Change. Cambridge
Poschenrieder C, Yant L, Salt DE (2018) Fluctuating selection on University Press, Cambridge, UK and New York, NY, pp 465–470
migrant adaptive sodium transporter alleles in coastal Arabidopsis Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA,
thaliana. Proc Natl Acad Sci USA 115: E12443–E12452 Lindahl BD (2015) Carbon sequestration is related to mycorrhizal
Busoms S, Terés J, Yant L, Poschenrieder C, Salt DE (2021) fungal community shifts during long-term succession in boreal for-
Adaptation to coastal soils through pleiotropic boosting of ion ests. New Phytol 205: 1525–1536
and stress hormone concentrations in wild Arabidopsis thaliana. Cobb JN, Biswas PS, Platten JD (2019) Back to the future: revisiting
New Phytol 232: 208–220 MAS as a tool for modern plant breeding. Theor Appl Genet 132:
Campos ACAL, van Dijk WFA, Ramakrishna P, Giles T, Korte P,
647–667
Douglas A, Smith P, Salt DE (2021) 1,135 ionomes reveal the Cohen SP, Leach JE (2020) High temperature-induced plant disease
global pattern of leaf and seed mineral nutrient and trace element
susceptibility: more than the sum of its parts. Curr Opin Plant Biol
diversity in Arabidopsis thaliana. Plant J 106: 536–554
56: 235–241
Carpita NC, McCann MC (2020) Redesigning plant cell walls for the
Cortés AJ, Chavarro MC, Madrin~án S, This D, Blair MW (2012)
biomass-based bioeconomy. J Biol Chem 295: 15144–15157
Molecular ecology and selection in the drought-related Asr gene
Carrillo MGC, Martin F, Variar M, Bhatt JC, Perez-Quintero AL,
polymorphisms in wild and cultivated common bean (Phaseolus
Leung H, Leach JE, Vera Cruz CM (2021) Accumulating candidate
vulgaris L.). BMC Genet 13: 58
genes for broad-spectrum resistance to rice blast in a
Covarrubias-Pazaran G, Gebeyehu Z, Gemenet D, Werner C,
drought-tolerant rice cultivar. Sci Rep 11: 21502
Carvalho J, Madgwick P, Powers S, Keys A, Lea P, Parry M (2012) Labroo M, Sirak S, Coaldrake P, Rabbi I, Kayondo SI, Parkes E,
An engineered pathway for glyoxylate metabolism in tobacco et al. (2022) Breeding schemes: what are they, how to formalize
plants aimed to avoid the release of ammonia in photorespiration. them, and how to improve them? Front Plant Sci 12
BMC Biotech 11: 111 Cowan MF, Blomstedt CK, Norton SL, Henry RJ, Møller BL,
Cavanagh AP, South PF, Bernacchi CJ, Ort DR (2022) Alternative Gleadow R (2020) Crop wild relatives as a genetic resource for
pathway to photorespiration protects growth and productivity at generating low-cyanide, drought-tolerant Sorghum. Environ Exp
elevated temperatures in a model crop. Plant Biotech J 20: Bot 169: 103884
711–721 Cox S, Nabukalu P, Paterson AH, Kong W, Auckland S, Rainville
Ceballos H, Kawuki RS, Gracen VE, Yencho GC, Hershey CH L, Cox S, Wang S (2018a) High proportion of diploid hybrids pro-
(2015) Conventional breeding, marker-assisted selection, genomic duced by interspecific diploid3 tetraploid Sorghum hybridization.
selection and inbreeding in clonally propagated crops: a case study Genet Resour Crop Evol 65: 387–390
for cassava. Theor Appl Genet 128: 1647–1667 Cox S, Nabukalu P, Paterson AH, Kong W, Nakasagga S (2018b)
Chaloner TM, Gurr SJ, Bebber DP (2021) Plant pathogen infection Development of perennial grain sorghum. Sustainability 10: 172
risk tracks global crop yields under climate change. Nat Clim Crain J, DeHaan L, Poland J (2021) Genomic prediction enables
Change 11: 710–715 rapid selection of high-performing genets in an intermediate
Chao DY, Chen Y, Chen J, Shi S, Chen Z, Wang C, Danku JM, wheatgrass breeding program. Plant Genome 14: e20080
Zhao FJ, Salt DE (2014) Genome-wide association mapping identi- Crews TE, Rumsey BE (2017) What agriculture can learn from native
fies a new arsenate reductase enzyme critical for limiting arsenic ecosystems in building soil organic matter: a review. Sustainability
accumulation in plants. PLoS Biol 12: e1002009 9: 578
Chao DY, Silva A, Baxter I, Huang YS, Nordborg M, Danku J, Crump BC, Wojahn JM, Tomas F, Mueller RS (2018)
Lahner B, Yakubova E, Salt DE (2012) Genome-wide association Metatranscriptomics and amplicon sequencing reveal mutualisms
studies identify heavy metal ATPase3 as the primary determinant in seagrass microbiomes. Front Microbiol 9: 388
of natural variation in leaf cadmium in Arabidopsis thaliana. PLoS Cui H (2021) Challenges and approaches to crop improvement
Genet 8: e1002923 through C3-to-C4 engineering. Front Plant Sci. doi:
Chatenoux B, Peduzzi P (2007) Impacts from the 2004 Indian 10.3389/fpls.2021.715391 (First published September 14, 2021)
Ocean Tsunami: analysing the potential protecting role of environ- Culman SW, Snapp SS, Ollenburger M, Basso B, DeHaan LR
mental features. Natural Hazards 40: 289–304 (2013) Soil and water quality rapidly responds to the perennial
Chen YP, Liu Q, Liu YJ, Jia FA, He XH (2014) Responses of soil micro- grain Kernza wheatgrass. Agron J 105: 735–744
bial activity to cadmium pollution and elevated CO2. Sci Rep 4: 4287 Custódio V, Gonin M, Stabl G, Bakhoum N, Oliveira MM, Gutjahr
Chen C, Kuang Y, Zhu S, Burgert I, Keplinger T, Gong A, Li T, C, Castrillo G (2022) Sculpting the soil microbiota. Plant J 109:
Berglung L, Eichorn SJ, Hu L (2020) Structure-property–function 508–522
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 55
Dalal J, Lopez H, Vasani NB, Hu Z, Swift JE, Yalamanchili R, dos Santos Silva PP, Sousa MBe, de Oliveira EJ, Morgante CV, de
Dvora M, Lin X, Xie D, Qu R, et al. (2015) A photorespiratory by- Oliveira CRS, Vieira SL, Borel JC (2021) Genome-wide association
pass increases plant growth and seed yield in biofuel crop study of drought tolerance in cassava. Euphytica 217: 60
Camelina sativa. Biotechnol Biofuels 8: 175 Dossa GS, Quibod I, Atienza-Grande G, Oliva R, Maiss E, Vera
Dandekar AM, Jacobson A, Ibán~ez AM, Gouran H, Dolan DL, Cruz C, Wydra K (2020) Rice pyramided line IRBB67 (Xa4/Xa7)
Agüero CB, Uratsu SL, Just R, Zaini PA (2019) Trans-graft protec- homeostasis under combined stress of high temperature and bac-
tion against Pierce’s disease mediated by transgenic grapevine terial blight. Sci Rep 10: 683
rootstocks. Front Plant Sci 10: 84 Drake BG, Azcon-Bieto J, Berry J, Bunce J, Dijkstra P, Farrar J,
Das G, Rao GJN (2015) Molecular marker assisted gene stacking for Gifford RM, Gonzalez-Meler MA, Koch G, Lambers H, et al.
biotic and abiotic stress resistance genes in an elite rice cultivar. (1999) Does elevated atmospheric CO2 concentration inhibit mito-
Front Plant Sci 6: 698 chondrial respiration in green plants? Plant Cell Environ 22:
Davey PA, Hunt S, Hymus GJ, DeLucia EH, Drake BG, Karnosky 649–657
DF, Long SP (2004) Respiratory oxygen uptake is not decreased by Driedonks NJ (2018) From flower to fruit in the heat-Reproductive
an instantaneous elevation of [CO2], but is increased with thermotolerance in tomato and its wild relatives. Doctoral disserta-
long-term growth in the field at elevated [CO2]. Plant Physiol 134: tion, Radboud University Nijmegen, Netherlands.
520–527 Duarte CM (1990) Seagrass nutrient content. Marine Ecol Prog Ser
Davidson EA, Ackerman IL (1993) Changes in soil carbon invento- 6: 201–207
ries following cultivation of previously untilled soils. Duarte CM, Chiscano CL (1999) Seagrass biomass and production: a
Biogeochemistry 20: 161–193 reassessment. Aquatic Bot 65: 159–174
de Oliveira Aparecido LE, da Silva Cabral de Moraes JR, de Duarte CM, Losada IJ, Hendriks IE, Mazarrasa I, Marbà N (2013a)
Meneses KC, Lorençone PA, Lorençone JA, de Olanda Souza The role of coastal plant communities for climate change mitiga-
GH, Torsoni GB (2020) Agricultural zoning as tool for expansion tion and adaptation. Nat Climate Change 3: 961–968
of cassava in climate change scenarios. Theor Appl Climatol 142: Duarte CM, Marbà N, Gacia E, Fourqurean JW, Beggins J, Barrón
1085–1095 C, Apostolaki ET (2010) Seagrass community metabolism: assess-
de Oliveira EJ, de Tarso Aidar T, Morgante CV, Chaves de Melo ing the carbon sink capacity of seagrass meadows. Global
Chaves AR, Cruz JL, Coelho Filho MA (2015) Genetic parameters Biogeochem Cycles 24: GB4032
for drought-tolerance in cassava. Pesqui Agropecu Bras 50: Duarte CM, Merino M, Agawin NS, Uri J, Fortes MD, Gallegos ME,
233–241 Marbà N, Hemminga MA (1998) Root production and below-
de Oliveira EJ, Morgante CV, de Tarso Aidar S, de Melo Chaves ground seagrass biomass. Marine Ecol Prog Ser 171: 97–108
AR, Antonio RP, Cruz JL, Filho MAC (2017) Evaluation of cassava Duarte CM, Middelburg JJ, Caraco N (2005) Major role of marine
germplasm for drought tolerance under field conditions. Euphytica vegetation on the oceanic carbon cycle. Biogeosciences 2: 1–8
213: 188 Duarte CM, Sintes T, Marbà N (2013b) Assessing the CO 2 capture
De Oliveira G, Brunsell NA, Crews TE, DeHaan LR, Vico G (2020) potential of seagrass restoration projects. J Appl Ecol 50:
Carbon and water relations in perennial Kernza (Thinopyrum 1341–1349
intermedium): an overview. Plant Sci 295: 110279 Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism
Degen GE, Worrall D, Carmo-Silva E (2020) An isoleucine residue and climate change: elevated CO 2 and temperature impacts on
acts as a thermal and regulatory switch in wheat Rubisco activase. photosynthesis, photorespiration and respiration. New Phytol 221:
Plant J 103: 742–751 32–49
DeHaan L, Larson S, López-Marqués RL, Wenkel S, Gao C, Eastburn DM, Degennaro MM, Delucia EH, Dermody O, Mcelrone
Palmgren M (2020) Roadmap for accelerated domestication of an AJ (2010) Elevated atmospheric carbon dioxide and ozone alter
emerging perennial grain crop. Trends Plant Sci 25: 525–537 soybean diseases at SoyFACE. Global Change Biol 16: 320–330
DeHaan LR, Ismail BP (2017) Perennial cereals provide ecosystem Easterling W, Apps M (2005) Assessing the consequences of climate
benefits. Cereal Foods World 62: 278–281 change for food and forest resources: a view from the IPCC. In J
Dehan K, Tal M (1978) Salt tolerance in the wild relatives of the cul- Salinger, MVK Sivakumar, RP Motha, eds,Increasing Climate
tivated tomato: responses of Solanum pennellii to high salinity. Variability and Change: Reducing the Vulnerability of Agriculture
Irrig Sci 1: 71–76 and Forestry. Springer Netherlands, Dordrecht, pp 165–189
DeLucia EH, Chen S, Guan K, Peng B, Li Y, Gomez-Casanovas N, Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, at-
Kantola IB, Bernacchi CJ, Huang Y, Long SP, et al. (2019) Are mospheric CO2 and climate. Oecologia 112: 285–299
we approaching a water ceiling to maize yields in the United El Haddad N, Kabbaj H, Zaı̈m M, El Hassouni K, Sall AT, Azouz
States? Ecosphere 10: e02773 M, Ortiz R, Baum M, Amri A, Gamba F, et al. (2021) Crop wild
Dempewolf H, Eastwood RJ, Guarino L, Khoury CK, Müller JV, relatives in durum wheat breeding: drift or thrift? Crop Sci 61:
Toll J (2014) Adapting agriculture to climate change: a global ini- 37–54
tiative to collect, conserve, and use crop wild relatives. Agroecol El-Sharkawy MA (1993) Drought-tolerant cassava for Africa, Asia,
Sustain Food Syst 38: 369–377 and Latin America. Bioscience 43: 441–451
Dheri GS, Lal R, Moonilall NI (2022) Soil carbon stocks and water Enrıquez S, Agustı S, Duarte CM (1994) Light absorption by marine
stable aggregates under annual and perennial biofuel crops in cen- macrophytes. Oecologia 98: 121–129
tral Ohio. Agric Ecosyst Environ 324: 107715 Enrıquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decom-
Dietterich LH, Zanobetti A, Kloog I, Huybers P, Leakey AD, position rates among photosynthetic organisms: the importance of
Bloom AJ, Carlisle E, Fernando N, Fitzgerald G, Hasegawa T, et detritus C: N: P content. Oecologia 94: 457–471
al. (2015) Impacts of elevated atmospheric CO2 on nutrient con- Erb TJ, Jones PR, Bar-Even A (2017) Synthetic metabolism: meta-
tent of important food crops. Sci Data 2: 150036 bolic engineering meets enzyme design. Curr Opin Chem Biol 37:
Dingkuhn M, Luquet D, Fabre D, Muller B, Yin X, Paul MJ (2020) 56–62
The case for improving crop carbon sink strength or plasticity for Erbs M, Manderscheid R, Jansen G, Seddig S, Pacholski A, Hans-
a CO2-rich future. Curr Opin Plant Biol 56: 259–272 Joachim Weigel H-J (2010) Effects of free-air CO2 enrichment and
Dong WT, Zhu YY, Chang HZ, Wang CH, Yang J, Shi J, Gao J, nitrogen supply on grain quality parameters and elemental compo-
Yang W, Lan L, Wang Y, et al. (2021) An SHR-SCR module speci- sition of wheat and barley grown in a crop rotation. Agric Ecosyst
fies legume cortical cell fate to enable nodulation. Nature 589: 586 Environ 136: 59–68
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
56 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Ercoli MF, Luu DD, Rim EY, Shigenaga A, Teixeira de Araujo A, Frary A, Göl D, Keleş D, Ökmen B, Pınar H, Şıgva HÖ,
Chern M, Jain R, Joe A, Ruan R, Stewart V, et al. (2022) Plant Yemenicioglu A, Doganlar S (2010) Salt tolerance in Solanum
immunity: rice XA21-mediated resistance to bacterial infection. pennellii: antioxidant response and related QTL. BMC Plant Biol
Proc Natl Acad Sci USA 119: e2121568119 10: 58
Eriksen RL, Adhikari ND, Mou B (2020) Comparative photosynthe- Fukayama H, Ueguchi C, Nishikawa K, Katoh N, Ishikawa C,
sis physiology of cultivated and wild lettuce under control and Masumoto C, Hatanaka T, Misoo S (2012) Overexpression of
low-water stress. Crop Sci 60: 2511–2526 Rubisco activase decreases the photosynthetic CO2 assimilation
Ermakova M, Arrivault S, Giuliani R, Danila F, Alonso- rate by reducing Rubisco content in rice leaves. Plant Cell Physiol
Cantabrana H, Vlad D, Ishihara H, Feil R, Guenther M, Borghi 53: 976–986
GL, et al. (2021) Installation of C4 photosynthetic pathway Fukayama H, Mizumoto A, Ueguchi C, Katsunuma J, Morita R,
enzymes in rice using a single construct. Plant Biotechnol J 19: Sasayama D, Hatanaka T, Azuma T (2018) Expression level of
575–588 Rubisco activase negatively correlates with Rubisco content in
Evans JR, Clarke VC (2019) The nitrogen cost of photosynthesis. J transgenic rice. Photosyn Res 137: 465–474
Exp Bot 70: 7–15 Fürst U, Zeng Y, Albert M, Witte AK, Fliegmann J, Felix G (2020)
Evans JR, von Caemmerer S (2000) Would C4 rice produce more Perception of Agrobacterium tumefaciens flagellin by FLS2XL con-
biomass than C3 rice? In JE Sheehy, PL Mitchell, B Hardy, eds, fers resistance to crown gall disease. Nat Plants 6: 22–27
Redesigning Rice Photosynthesis to Increase Yield (IRRI), Elsevier Garcıa GA, Dreccer MF, Miralles DJ, Serrago RA (2015) High night
Science BV, Amsterdam, pp 53–71 temperatures during grain number determination reduce wheat
Evenson RE, Gollin D (2003) Assessing the impact of the Green and barley grain yield: a field study. Global Change Biol 21:
Revolution, 1960 to 2000. Science 300: 758–762 4153–4164
Eyland D, Luchaire N, Cabrera-Bosquet L, Parent B, Janssens SB, Garcıa GA, Serrago RA, Dreccer MF, Miralles DJ (2016)
Swennen R, Welcker C, Tardieu F, Carpentier SC (2022) Post-anthesis warm nights reduce grain weight in field-grown
High-throughput phenotyping reveals differential transpiration be- wheat and barley. Field Crops Res 195: 50–59
haviour within the banana wild relatives highlighting diversity in Garcias-Bonet N, Eguıluz VM, Dıaz-Rúa R, Duarte CM (2021)
drought tolerance. Plant Cell Environ. doi: 10.1111/pce.14310 (First Host-association as major driver of microbiome structure and
published March 16, 2022) composition in Red Sea seagrass ecosystems. Environ Microbiol 23:
Ezenwaka L, Carpio DP, Jannink J-L, Rabbi I, Danquah E, Asante I, 2021–2034
Danquah A, Blay E, Egesi C (2018) Genome-wide association Gardiner LJ, Joynson R, Omony J, Rusholme-Pilcher R, Olohan L,
study of resistance to cassava green mite pest and related traits in Lang D, Bai C, Hawkesford M, Salt D, Spannagl M, et al. (2018)
cassava. Crop Sci 58: 1907–1918 Hidden variation in polyploid wheat drives local adaptation.
Fang C, Fernie AR, Luo J (2019) Exploring the diversity of plant me- Genome Res 28: 1319–1332
tabolism. Trends Plant Sci 24: 83–98 Gashu D, Nalivata PC, Amede T, Ander EL, Bailey EH, Botoman L,
Fangmeier A, Grüters U, Högy P, Vermehren B, Jäger H-J (1997) Chagumaira C, Gameda S, Haefele SM, Hailu K, et al. (2021)
Effects of elevated CO2, nitrogen supply and tropospheric ozone The nutritional quality of cereals varies geospatially in Ethiopia and
on spring wheat-II. Nutrients (N, P, K, S, Ca, Mg, Fe, Mn, Zn). Malawi. Nature 594: 71–76
Environ Pollut 96: 43–59 Geddes BA, Paramasivan P, Joffrin A, Thompson AL, Christensen
Favela A, Bohn MO, Kent AD (2021) Maize germplasm chronose- K, Jorrin B, Brett P, Conway SJ, Oldroyd GED, Poole PS (2019)
quence shows crop breeding history impacts recruitment of the Engineering transkingdom signalling in plants to control gene ex-
rhizosphere microbiome. ISME J 15: 2454–2464 pression in rhizosphere bacteria. Nat Commun 10: 3430.
Fernando N, Panozzo J, Tausz M, Norton RM, Neumann N, Gencer E, Burniske GR, Doering OC, Tyner W, Agrawal R, Delgass
Fitzgerald GJ, Myers S, Nicolas ME, Seneweer S (2014a) WN, Ejeta G, McCann MC, Carpita NC (2020) Sustainable pro-
Intra-specific variation of wheat grain quality in response to ele- duction of ammonia fertilizers from biomass. Biofuels Bioprod
vated [CO2] at two sowing times under rain-fed and irrigation Biorefining. doi: 10.1002/bbb.2101 (First published May 10, 2020)
treatments. J Cereal Sci 59: 137–144 Genre A, Lanfranco L, Perotto S, Bonfante P (2020) Unique and
Fernando N, Panozzo J, Tausz M, Norton RM, Neumann N, common traits in mycorrhizal symbioses. Nat Rev Microbiol 18:
Fitzgerald GJ, Seneweer S (2014b) Elevated CO2 alters grain qual- 649–660
ity of two bread wheat cultivars grown under different environ- Ghislain M, Byarugaba AA, Magembe E, Njoroge A, Rivera C, Román
mental conditions. Agric Ecosyst Environ 185: 24–33 ML, Tovar JC, Gamboa S, Forbes GA, Kreuze JF, et al. (2019)
Ficklin DL, Novick KA (2017) Historic and projected changes in va- Stacking three late blight resistance genes from wild species directly
por pressure deficit suggest a continental-scale drying of the into African highland potato varieties confers complete field resistance
United States atmosphere. J Geophys Res Atmos 122: 2061–2079 to local blight races. Plant Biotechnol J 17: 1119–1129
Fitzgerald GJ, Tausz M, O’Leary G, Mollah MR, Tausz-Posch S, Gill R, Burke IC, Milchunas DG, Lauenroth WK (1999) Relationship
Seneweera S, Mock I, Low M, Partington DL, McNeill D, et al. between root biomass and soil organic matter pools in the short-
(2016) Elevated atmospheric [CO2] can dramatically increase grass steppe of eastern Colorado. Ecosystems 2: 226–236
wheat yields in semi-arid environments and buffer against heat Glover JD, Reganold JP, Bell LW, Borevitz J, Brummer EC, Buckler
waves. Global Change Biol 22: 2269–2284 ES, Cox CM, Cox TS, Crews TE, Culman SW, et al. (2010)
Forsberg SK, Andreatta ME, Huang XY, Danku J, Salt DE, Increased food and ecosystem security via perennial grains. Science
Carlborg Ö (2015) The multi-allelic genetic architecture of a 328: 1638–1639
variance-heterogeneity locus for molybdenum concentration in Gomez MA, Berkoff KC, Gill BK, Iavarone AT, Lieberman SE, Ma
leaves acts as a source of unexplained additive genetic variance. JM, Schultink A, Wyman SK, Chauhan RD, Taylor NJ, et al.
PLoS Genet 11: e1005648 (2021) CRISPR-Cas9-mediated knockout of CYP79D1 and CYP79D2
Foster TL, Baldi HD, Shen X, Burson BL, Klein RR, Murray SC, in cassava attenuates toxic cyanogen production. bioRxiv:
Jessup RW (2020) Development of novel perennial Sorghum bi- 2021.10.08.462827
color 3 S. propinquum hybrids. Crop Sci 60: 863–872 Gomez MA, Lin ZD, Moll T, Chauhan RD, Hayden L, Renninger K,
Fourqurean JW, Duarte CM, Kennedy H, Marbà N, Holmer M, Beyene G, Taylor NJ, Carrington JC, Staskawicz BJ, et al. (2019)
Mateo MA, Apostolaki ET, Kendrick GA, Krause-Jensen D, Simultaneous CRISPR/Cas9-mediated editing of cassava eIF4E iso-
McGlathery KJ, et al. (2012) Seagrass ecosystems as a globally sig- forms nCBP-1 and nCBP-2 reduces cassava brown streak disease
nificant carbon stock. Nat Geosci 5: 505–509 symptom severity and incidence. Plant Biotechnol J 17: 421–434
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 57
Gonzalez-Meler MA, Ribas-Carbo M, Siedow JN, Drake BG (1996) Hershey CH (1984) Breeding cassava for adaptation to stress condi-
Direct inhibition of plant mitochondrial respiration by elevated tions: development of a methodology. In Symposium of the
CO2. Plant Physiol 112: 1349–1355 International Society for Tropical Root Crops, Lima, Peru
Gonzalez-Meler MA, Taneva LINA, Trueman RJ (2004) Plant respi- Hewetson B, Zhang X, Mosier NS (2016) Enhanced acid-catalyzed
ration and elevated atmospheric CO2 concentration: cellular biomass conversion to hydroxymethylfurfural following cellulose
responses and global significance. Annals Bot 94: 647–656 solvent-and organic solvent-based lignocellulosic fractionation pre-
Govindan V, Singh RP, Juliana P, Mondal S, Bentley AR (2022) treatment. Energy Fuels 30: 9975–9977
Mainstreaming grain zinc and iron concentrations in CIMMYT Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of im-
wheat germplasm. J Cereal Sci 105: 103473 proving nitrogen use efficiency in crop plants: towards a more cen-
Grabowski P, Olabisi LS, Adebiyi J, Waldman K, Richardson R, tral role for genetic variability and quantitative genetics within
Rusinamhodzi L, Snapp S (2019) Assessing adoption potential in integrated approaches. J Exp Bot 58: 2369–2387
a risky environment: the case of perennial pigeonpea. Agric Syst Högy P, Fangmeier A (2009) Atmospheric CO2 enrichment affects
171: 89–99 potatoes: 2. Tuber quality traits. Eur J Agron 30: 85–94
Gray SB, Siebers M, Locke AM, Rosenthal D, Strellner R, Paul RE, Högy P, Wieser H, Köhler P, Schwadorf K, Breuer J, Franzaring J,
Klein SP, McGrath JM, Dermody O, Ainsworth EA, et al. (2016) Muntifering R, Fangmeier A (2009) Effects of elevated CO2 on
Intensifying drought eliminates the expected benefits of elevated grain yield and quality of wheat: results from a 3-year free-air CO2
[CO2] for soybean. Nat Plants 2: 16132 enrichment experiment. Plant Biol 11: 60–69.
Griffin KL, Ball JT, Strain BR (1996) Direct and indirect effects of el- Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot
evated CO2 on whole-shoot respiration in ponderosa pine seed- ML, Salt DE (2013) Dirigent domain-containing protein is part of
lings. Tree Physiol 16: 33–41 the machinery required for formation of the lignin-based
Guo X, Huang B, Zhang H, Cai C, Li G, Li H, Zhang Y, Struik PC, Casparian strip in the root. Proc Natl Acad Sci USA 110:
Liu Z, Dong M, et al. (2022) T-FACE studies reveal that increased 14498–14503
temperature exerts an effect opposite to that of elevated CO2 on Houston K, Qiu J, Wege S, Hrmova M, Oakey H, Qu Y, Smith P,
nutrient concentration and bioavailability in rice and wheat grains. Situmorang A, Macaulay M, Flis P, et al. (2020) Barley sodium
Food Energy Secur 11: e336 content is regulated by natural variants of the Na + transporter
Gupta D, Sharma G, Saraswat P, Ranjan R (2021) Synthetic biology HvHKT1;5. Commun Biol 3: 258
in plants, a boon for coming decades. Mol Biotechnol 63: Hu F, Zhang S, Huang G, Zhang Y, Lv X, Wan K, Liang J, Dao J,
1138–1154 Wu S, Zhang L, et al. (2022) Perennial rice improves farmer liveli-
Hall LN, Rossini L, Cribb L, Langdale JA (1998) GOLDEN 2: a novel hood and ecosystem security. Preprint posted to Research Square
transcriptional regulator of cellular differentiation in the maize leaf. February 2, 2022, doi: 10.21203/rs.3.rs-1302277/v1
Plant Cell 10: 925–936 Hua K, Zhang J, Botella JR, Ma C, Kong F, Liu B, Zhu J-K (2019)
Hameed A, Wu Q-S, Abd-Allah EF, Hashem A, Kumar A, Ahmad Perspectives on the application of genome-editing technologies in
Lone H, Ahmad P (2014) Role of AM fungi in alleviating drought crop breeding. Mol Plant 12: 1047–1059
stress in plants. In M Miransari (ed) Use of Microbes for the Huang W, Reyes-Caldas P, Mann M, Seifbarghi S, Kahn A,
Alleviation of Soil Stresses. Springer, New York, NY, pp 55–75 Almeida RPP, Béven L, Heck M, Hogenhout SA, Coaker G
Harris CJ, Slootweg EJ, Goverse A, Baulcombe DC (2013) Stepwise (2020) Bacterial vector-borne plant diseases: unanswered questions
artificial evolution of a plant disease resistance gene. Proc Natl and future directions. Mol Plant 13: 1379–1393
Acad Sci USA 110: 21189–21194 Huang XY, Salt DE (2016) Plant ionomics: from elemental profiling
Haskett TL, Paramasivan P, Mendes MD, Green P, Geddes BA, to environmental adaptation. Mol Plant 9: 787–797
Knights HE, Jorrin B, Ryu MH, Brett P, Voigt CA, et al. (2022) Huang G, Qin S, Zhang S, Cai X, Wu S, Dao J, Zhang J, Huang L,
Engineered plant control of associative nitrogen fixation. Proc Natl Harnpichitvitaya D, Wade LJ, et al. (2018) Performance, econom-
Acad Sci USA 119: e2117465119 ics and potential impact of perennial rice PR23 relative to annual
Hayes RC, Wang S, Newell MT, Turner K, Larsen J, Gazza L, rice cultivars at multiple locations in Yunnan Province of China.
Anderson JA, Bell LW, Cattani DJ, Frels K, et al. (2018) The per- Sustainability 10: 1086
formance of early-generation perennial winter cereals at 21 sites Huber GW, Shabaker JW, Dumesic JA (2003) Raney Ni–Sn catalyst
across four continents. Sustainability 10: 1124 for H production from biomass-derived hydrocarbons. Science 300:
He JM, Zhang C, Dai HL, Liu H, Zhang XW, Yang J, Chen X, Zhu 2075–2077
Y, Wang DP, Qi XF, et al. (2019) A LysM receptor heteromer Hughes TE, Langdale JA (2020) SCARECROW gene function is re-
mediates perception of arbuscular mycorrhizal symbiotic signal in quired for photosynthetic development in maize. Plant Direct 4:
rice. Mol Plant 12: 1561–1576 e00264
Heffner EL, Sorrells ME, Jannink J-L (2009) Genomic selection for Hughes TE, Langdale JA (2022) SCARECROW is deployed in distinct
crop improvement. Crop Sci 49: 1–12 contexts during rice and maize leaf development. Development
Hein NT, Bheemanahalli R, Wagner D, Vennapusa AR, 149: e200410
Bustamante C, Ostmeyer T, Pokharel M, Chiluwal A, Fu J, Hughes TE, Sedelnikova OV, Wu H, Becraft PW, Langdale JA
Srikanthan DS, et al. (2020) Improved cyber-physical system cap- (2019) Redundant SCARECROW genes pattern distinct cell layers
tured post-flowering high night temperature impact on yield and in roots and leaves of maize. Development 146: e177543
quality of field grown wheat. Scient Rep 10: 1–15 Huot B, Castroverde CDM, Velásquez AC, Hubbard E, Pulman JA,
Hein NT, Impa SM, Wagner D, Bheemanahalli R, Kumar R, Tiwari Yao J, Childs KL, Tsuda K, Montgomery BL, He SY (2017) Dual
M, Prasad PVV, Tilley M, Wu X, Neilsen M, et al. (2022) Grain impact of elevated temperature on plant defence and bacterial vir-
micronutrient composition and yield components in field-grown ulence in Arabidopsis. Nature Commun 8: 1808
wheat are negatively impacted by high night-time temperature. Husaini AM (2022) High-value pleiotropic genes for developing mul-
Cereal Chem. doi: 10.1002/cche.10523 tiple stress-tolerant biofortified crops for 21st-century challenges.
Hemminga MA, Duarte CM (2000) Seagrass Ecology. Cambridge Heredity. doi:10.1038/s41437-022-00500-w (First published
University Press, Cambridge, UK February 16, 2022)
Hendriks IE, Sintes T, Bouma TJ, Duarte CM (2008) Experimental Hyde PT, Guan X, Abreu V, Setter TL (2020) The anti-ethylene
assessment and modeling evaluation of the effects of the seagrass growth regulator silver thiosulfate (STS) increases flower produc-
Posidonia oceanica on flow and particle trapping. Marine Ecol tion and longevity in cassava (Manihot esculenta Crantz). Plant
Prog Ser 356: 163–173 Growth Regul 90: 441–453
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
58 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Ilyas M, Nisar M, Khan N, Hazrat A, Khan AH, Hayat K, Fahad S, Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J,
Khan A, Ullah A (2021) Drought tolerance strategies in plants: a Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peterhansel
mechanistic approach. J Plant Growth Regul 40: 926–944 C (2007) Chloroplastic photorespiratory bypass increases photo-
Impa SM, Raju B, Hein NT, Sandhu J, Prasad PV, Walia H, Jagadish synthesis and biomass production in Arabidopsis thaliana. Nat
SK (2021) High night temperature effects on wheat and rice: current Biotechnol 25: 593–599
status and way forward. Plant Cell Environ 44: 2049–2065 Kell DB (2012) Large-scale sequestration of atmospheric carbon via
Impa SM, Vennapusa AR, Bheemanahalli R, Sabela D, Boyle D, plant roots in natural and agricultural systems: why and how. Phil
Walia H, Jagadish SK (2020) High night temperature induced Trans R Soc B 367: 1589–1597
changes in grain starch metabolism alters starch, protein, and lipid Kennedy H, Beggins J, Duarte CM, Fourqurean JW, Holmer M,
accumulation in winter wheat. Plant Cell Environ 43: 431–447 Marbà N, Middelburg JJ (2010) Seagrass sediments as a global car-
IPCC (2022) Climate Change 2022: impacts, adaptation, and vulnera- bon sink: isotopic constraints. Global Biogeochem Cycles 24:
bility. In H-O Pörtner, DC Roberts, M Tignor, ES Poloczanska, K GB4026
Mintenbeck, A Alegrıa, M Craig, S. Langsdorf, S. Löschke, V. Möller, Key RE, Bozell JJ (2016) Progress toward lignin valorization via selec-
et al., eds, Contribution of Working Group II to the Sixth tive catalytic technologies and the tailoring of biosynthetic path-
Assessment Report of the Intergovernmental Panel on Climate ways. ACS Sustain Chem Eng 4: 5123–5135
Change. Cambridge University Press, Cambridge, UK and New Khadka K, Earl HJ, Raizada MN, Navabi A (2020) A
York, NY, USA, pp 3056 physio-morphological trait-based approach for breeding drought
Jackson RB, Lajtha K, Crow SE, Hugelius G, Kramer MG, Pin~eiro G tolerant wheat. Front Plant Sci 11: 715
(2017) The ecology of soil carbon: pools, vulnerabilities, and biotic Khanna A, Anumalla M, Catolos M, Bartholome J, Fritsche-Neto
and abiotic controls. Annu Rev Ecol Evol Syst 48: 419–445 R, Platten JD, Pisano DJ, Gulles A, Cruz MTS, Ramos J, et al.
Jacott CN, Murray JD, Ridout CJ (2017) Trade-offs in arbuscular (2022) Genetic trends estimation in IRRIs rice drought breeding
mycorrhizal symbiosis: disease resistance, growth responses and program and identification of high yielding drought-tolerant lines.
perspectives for crop breeding. Agronomy 7: 75 Rice 15: 14
Jägermeyr J, Müller C, Ruane AC, Elliott J, Balkovic J, Castillo O, Khanna-Chopra R, Viswanathan C (1999) Evaluation of heat stress
Faye B, Foster I, Folberth C, Franke JA, et al. (2021) Climate tolerance in irrigated environment of T. aestivum and related spe-
impacts on global agriculture emerge earlier in new generation of cies. I. Stability in yield and yield components. Euphytica 106:
climate and crop models. Nat Food 2: 873–885 169–180
Jha UC, Bohra A, Nayyar H (2020) Advances in “omics” approaches Khong GN, Pati PK, Richaud F, Parizot B, Bidzinski P, Mai CD,
to tackle drought stress in grain legumes. Plant Breed 139: 1–27 Bes M, Bourrie I, Meynard D, Beeckman T, et al. (2015)
Jiang YN, Wang WX, Xie QJ, Liu N, Liu LX, Wang D, Zhang X,
OsMADS26 negatively regulates resistance to pathogens and
Yang C, Chen X, Tang D, et al. (2017) Plants transfer lipids to
drought tolerance in rice. Plant Physiol 169: 2935–2949
sustain colonization by mutualistic mycorrhizal and parasitic fungi.
Kiani-Pouya A, Rasouli F, Rabbi B, Falakboland Z, Yong M, Chen
Science 356: 1172–1175.
ZH, Zhou M, Shabala S (2020) Stomatal traits as a determinant of
Jiang Y, Ding D, Zhao S, Zhu H, Kenttämaa HI, Abu-Omar MM
superior salinity tolerance in wild barley. J Plant Physiol 245:
(2018) Renewable thermosets based on lignin and carbohydrate
153108
derived monomers. Green Chem 20: 1131–1138
Kikuchi S, Bheemanahalli R, Jagadish SVK, Kumagai E, Masuya Y,
Jobbágy EG, Jackson RB (2000) The vertical distribution of soil or-
ganic carbon and its relation to climate and vegetation. Ecol Appl Kuroda E, Raghavan C, Dingkuhn M, Abe A, Shimono H (2017)
10: 423–436 Genome-wide association mapping for phenotypic plasticity in
John ME, Keller G (1996) Metabolic pathway engineering in cotton: rice. Plant Cell Environ 40: 1565–1575
biosynthesis of polydroxybutryate in fiber cells. Proc Natl Acad Sci Kim S, Dale BE, Keck P (2014) Energy requirements and greenhouse
USA 93: 12768–12773 gas emissions of maize production in the USA. Bioenerg Res 7:
Johnson SL (2022) A year at the forefront of engineering photosyn- 753–764
thesis. Biol Open 11: bio059335. Klinsukon C, Lumyong S, Kuyper TW, Boonlue S (2021)
Joy EJM, Ahmad W, Zia MH, Kumssa DB, Young SD, Ander EL, Colonization by arbuscular mycorrhizal fungi improves salinity tol-
Watts MJ, Stein AJ, Broadley MR (2017) Valuing increased zinc erance of eucalyptus (Eucalyptus camaldulensis) seedlings. Sci
(Zn) fertiliser-use in Pakistan. Plant Soil 411: 139–150 Rep-Uk 11: 4362
Juliana P, Montesinos-López OA, Crossa J, Mondal S, González Klironomos JN (2003) Variation in plant response to native and ex-
Pérez L, Poland J, Huerta-Espino J, Crespo-Herrera L, Govindan otic arbuscular mycorrhizal fungi. Ecology 84: 2292–2301
V, Dreisigacker S, et al. (2019) Integrating genomic-enabled pre- Kocacinar F, Mckown AD, Sage TL, Sage RF (2008) Photosynthetic
diction and high-throughput phenotyping in breeding for pathway influences xylem structure and function in Flaveria
climate-resilient bread wheat. Theor Appl Genet 132: 177–194 (Asteraceae). Plant Cell Environ 31: 1363–1376
Juma RU, Bartholomé J, Thathapalli Prakash P, Hussain W, Köhler IH, Huber SC, Bernacchi CJ, Baxter IR (2019) Increased
Platten JD, Lopena V, Verdeprado H, Murori R, Ndayiragije A, temperatures may safeguard the nutritional quality of crops under
Katiyar SK, et al. (2021) Identification of an elite core panel as a future elevated CO2 concentrations. Plant J 97: 872–886
key breeding resource to accelerate the rate of genetic improve- Köhler IH, Ruiz-Vera UM, VanLoocke A, Thomey ML, Clemente T,
ment for irrigated rice. Rice 14: 92 Long SP, Ort DR, Bernacchi CJ (2017) Expression of cyanobacte-
Kamiya T, Borghi M, Wang P, Danku JM, Kalmbach L, Hosmani rial FBP/SBPase in soybean prevents yield depression under future
PS, Naseer S, Fujiwara T, Geldner N, Salt DE (2015) The MYB36 climate conditions. J Exp Bot 68: 715–726
transcription factor orchestrates Casparian strip formation. Proc Kornienko N, Zhang JZ, Sakimoto KK, Yang P, Reisner E (2018)
Natl Acad Sci USA 112: 10533–10538 Interfacing nature’s catalytic machinery with synthetic materials
Kasirajan L, Valiyaparambth R, Velu J, Hari H, for semi-artificial photosynthesis. Nat Nanotechnol 13: 890–899
Srinivasavedantham V, Athaiappan S (2021) Gene expression Kromdijk J, Glowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK,
studies of Saccharum spontaneum, a wild relative of sugarcane in Long SP (2016) Improving photosynthesis and crop productivity
response to salinity stress. Biotechnol Appl Biochem 68: 288–296 by accelerating recovery from photoprotection. Science 354:
Ke J, Wang B, Yoshikuni Y (2021) Microbiome engineering: syn- 857–861
thetic biology of plant-associated microbiomes in sustainable agri- Kumar S, Tripathi S, Singh SP, Prasad A, Akter F, Syed MA, Badri
culture. Trends Biotechnol 39: 244–261 J, Das SP, Bhattarai R, Natividad MA, et al. (2021) Rice breeding
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 59
for yield under drought has selected for longer flag leaves and Lin LH, Simpson MJ (2016) Enhanced extractability of cutin- and
lower stomatal density. J Exp Bot 72: 4981–4992 suberin-derived organic matter with demineralization implies phys-
Kumssa DB, Joy EJ, Ander EL, Watts MJ, Young SD, Walker S, ical protection over chemical recalcitrance in soil. Organic
Broadley MR (2015) Dietary calcium and zinc deficiency risks are Geochem 97: 111–121
decreasing but remain prevalent. Sci Rep 5: 10974 Liu L, Li X, Liu S, Min J, Liu W, Pan X, Fang B, Hu M, Liu Z, Li Y,
Kundu P, Goel K, Zinta G (2022) Nutritional imbalance in plants et al. (2021a) Identification of QTLs associated with the anaerobic
under rising atmospheric CO2. In V Kumar, A Kumar Srivastava, P germination potential using a set of Oryza nivara introgression
Suprasanna, eds, Plant Nutrition and Food Security in the Era of lines. Genes Genom 43:399–406. https://doi.org/10.1007/s13258-
Climate Change. Elsevier Academic Press, Amsterdam, pp 513–536 021-01063-6
Kuon JE, Qi W, Schläpfer P, Hirsch-Hoffmann M, von Bieberstein Liu Y, Wang H, Jiang Z, Wang W, Xun R, Wang Q, Zhang Z, Li A,
PR, Patrignani A, Poveda L, Grob S, Keller M, Shimizu-Inatsugi R, Liang Y, Ou S, et al. (2021b) Genomic basis of geographical adap-
et al. (2019) Haplotype-resolved genomes of geminivirus-resistant tation to soil nitrogen in rice. Nature 590: 600–605
and geminivirus-susceptible African cassava cultivars. BMC Biol 17: Lobell DB, Gourdji SM (2012) The influence of climate change on
1–15 global crop productivity. Plant Physiol 160: 1686–1697
Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, Lassner MW, Loladze I (2014) Hidden shift of the ionome of plants exposed to el-
Zhu G (2007) Enhanced thermostability of Arabidopsis Rubisco evated CO2 depletes minerals at the base of human nutrition.
activase improves photosynthesis and growth rates under moder- eLife 3: e02245
ate heat stress. Plant Cell 19: 3230–3241 Lorenz K, Lal R, Preston CM, Nierop KGJ (2007) Strengthening the
la Puente de LS, Perez PP, Martinez-Carrasco R, Morcuende RM, soil organic carbon pool by increasing contributions from recalci-
del Molino IMM (2000) Action of elevated CO2 and high temper- trant aliphatic bio(macro)molecules. Geoderma 142: 1–10
atures on the mineral chemical composition of two varieties of Luo S, Lin PP, Nieh L-Y, Liao G-B, Tang P-W, Chen C, Liao JC
wheat. Agrochimica 44: 221–230 (2022) A cell-free self-replenishing CO2-fixing system. Nat Catalysis
Labbé N, Kline LM, Moens L, Kim K, Kim PC, Hayes DG (2012) 5: 154–162
Activation of lignocellulosic biomass by ionic liquid for biorefinery Lyons JB, Bredeson JV, Mansfeld BN, Bauchet GJ, Berry J, Boyher
fractionation. Bioresour Technol 104: 701–707 A, Mueller LA, Rokhsar DS, Bart RS (2021) Current status and
Lal R (2003) Global potential of soil carbon sequestration to mitigate impending progress for cassava structural genomics. Plant Mol
the greenhouse effect. Crit Rev Plant Sci 22: 151–184 Biol 109: 177–191
Langdale JA (2011) C4 cycles: past, present, and future research on Mackill DJ, Ismail AM, Singh US, Labios RV, Paris TR (2012)
C4 photosynthesis. Plant Cell 23: 3879–3892 Development and rapid adoption of submergence-tolerant (Sub1)
Larkum WD, Orth RJ, Duarte CM (2006) Seagrasses: biology, rice varieties. Adv Agron 115: 299–352
Ecology and Conservation. Springer, Dordrecht, The Netherlands Macreadie PI, Costa MD, Atwood TB, Friess DA, Kelleway JJ,
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort Kennedy H, Lovelock CE, Serrano O, Duarte CM (2021) Blue car-
DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and wa- bon as a natural climate solution. Nat Rev Earth Environ 2:
ter relations: six important lessons from FACE. J Exp Bot 60: 826–839
2859–2976 Maier A, Fahnenstich H, von Caemmerer S, Engqvist MK, Weber
Leakey ADB, Bishop KA, Ainsworth EA (2012) A multi-biome gap AP, Flugge UI, Maurino VG (2012) Transgenic Introduction of a
in understanding of crop and ecosystem responses to elevated glycolate oxidative cycle into A. thaliana chloroplasts leads to
CO2. Curr Opin Plant Biol 15: 228–236 growth improvement. Front Plant Sci 3: 38
Leakey ADB, Ferguson JN, Pignon CP, Wu A, Jin Z, Hammer GL, Manderscheid R, Bender J, Jäger H-J, Weigel HJ (1995) Effects of
Lobell DB (2019) Water use efficiency as a constraint and target season long CO2 enrichment on cereals. II. Nutrient concentra-
for improving the resilience and productivity of C3 and C4 crops. tions and grain quality. Agric Ecosyst Environ 54: 175–185
Ann Rev Plant Biol 70: 781–808 Mano YO, Muraki M, Fujimori M, Takamizo T, Kindiger B (2005)
Lehmann J, Hansel CM, Kaiser C, Kleber M, Maher K, Manzoni S, Identification of QTL controlling adventitious root formation dur-
Nunan N, Reichstein M, Schimel JP, Torn MS, et al. (2020) ing flooding conditions in teosinte (Zea mays ssp. huehuetenan-
Persistence of soil organic carbon caused by functional complexity. gensis) seedlings. Euphytica 142: 33–42
Nat Geosci 13: 529–534 Mano YO, Omori FU, Takamizo TA, Kindiger B, Bird RM, Loaisiga
Lenaerts B, Demont M (2021) The global burden of chronic and CH (2006) Variation for root aerenchyma formation in flooded
hidden hunger revisited: new panel data evidence spanning and non-flooded maize and teosinte seedlings. Plant Soil 281:
1990-2017. Glob Food Sec 28: 100480 269–279
Leng J, Tu W, Hou Y, Cui H (2021) Temperature-inducible trans- Mansueto L, Fuentes RR, Borja FN, Detras J, Abriol-Santos JM,
genic EDS1 and PAD4 in Arabidopsis confer an enhanced disease Chebotarov D, Sanciangco M, Palis K, Copetti D, Poliakov A, et
resistance at elevated temperature. Plants 10: 1258 al. (2017) Rice SNP-seek database update: new SNPs, indels, and
Li S, Lin D, Zhang Y, Deng M, Chen Y, Lv B, Li B, Lei Y, Wang Y, queries. Nucleic Acids Res 45: D1075–D1081
Zhao L, et al. (2022) Genome-edited powdery mildew resistance Manzeke-Kangara MG, Joy EJM, Mtambanengwe F, Chopera P,
in wheat without growth penalties. Nature 602: 455–460 Watts MJ, Broadley MR, Mapfumo P (2021) Good soil manage-
Li X, Wang P, Li J, Wei SB, Yan YY, Yang J, Zhao M, Langdale JA, ment can reduce dietary zinc deficiency in Zimbabwe. CAB Agric
Zhou WB (2020) Maize GOLDEN2-LIKE genes enhance biomass Biosci 2: 36
and grain yields in rice by improving photosynthesis and reducing Maqbool AM, Beshir A (2019) Zinc biofortification of maize (Zea
photoinhibition. Commun Biol 3: 151 mays L.): status and challenges. Plant Breed 138: 1–28
Li Y, Guan K, Schnitkey GD, DeLucia E, Peng B (2019) Excessive Marbà N, Arias-Ortiz A, Masqué P, Kendrick GA, Mazarrasa I,
rainfall leads to maize yield loss of a comparable magnitude to ex- Bastyan GR, Garcia-Orellana J, Duarte CM (2015) Impact of sea-
treme drought in the United States. Global Change Biol 25: grass loss and subsequent revegetation on carbon sequestration
2325–2337 and stocks. J Ecol 103: 296–302
Lin H, Arrivault S, Coe RA, Karki S, Covshoff S, Bagunu E, Lunn Mbanjo EGN, Rabbi IY, Ferguson ME, Kayondo SI, Eng NH,
JE, Stitt M, Furbank RT, Hibberd JM, et al. (2020) A partial C4 Tripathi L, Kulakow P, Egesi C (2021) Technological innovations
photosynthetic biochemical pathway in rice. Front Plant Sci 11: for improving cassava production in sub-saharan Africa. Front
e564463 Genet 11: 623736
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
60 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
McCann MC, Carpita NC (2015) Biomass recalcitrance: a Naylor D, DeGraaf S, Purdom E, Coleman-Derr D (2017) Drought
multi-scale, multi-factor and conversion-specific property. J Exp and host selection influence bacterial community dynamics in the
Bot 66: 4109–4118 grass root microbiome. ISME J 11: 2691–2704
McClelland SC, Paustian K, Schipanksi ME (2021) Management of Nazir M, Mahajan R, Mansoor S, Rasool S, Mir RA, Singh R,
cover crops in temperate climates influences soil organic carbon Thakral V, Kumar V, Sofi PA, El-Serehy HA, et al. (2022)
stocks - a meta-analysis. Ecol Appl 31: e02278 Identification of QTLs/candidate genes for seed mineral contents
Meuwissen TH, Hayes BJ, Goddard M (2001) Prediction of total ge- in common bean Phaseolus vulgaris L through genotyping-by-se-
netic value using genome-wide dense marker maps. Genetics 157: quencing. Front Genet 13: 750814
1819–1829 Nelson G, Bogard J, Lividini K, Arsenault J, Riley M, Sulser TB,
Mitchell PL, Sheehy JE (2006) Supercharging rice photosynthesis to Mason-D’Croz D, Power B, Gustafson D, Herrero M, et al.
increase yield. New Phytol 171: 688–693 (2018) Income growth and climate change effects on global nutri-
Mittova V, Guy M, Tal M, Volokita M (2002) Response of the culti- tion security to mid-century. Nat Sustain 1: 773–781
vated tomato and its wild salt-tolerant relative Lycopersicon pen- Nevo E, Chen G (2010) Drought and salt tolerances in wild relatives
nellii to salt-dependent oxidative stress: increased activities of for wheat and barley improvement. Plant Cell Environ 33: 670–685
antioxidant enzymes in root plastids. Free Radic Res 36: 195–202 Niazian M, Niedbała G (2020) Machine learning for plant breeding
Moenga SM, Gai Y, Carrasquilla-Garcia N, Perilla-Henao LM, and biotechnology. Agriculture 10: 436
Cook DR (2020) Gene co-expression analysis reveals transcriptome Niroula RK, Pucciariello C, Ho VT, Novi G, Fukao T, Perata P
divergence between wild and cultivated chickpea under drought (2012) SUB1A-dependent and -independent mechanisms are in-
stress. Plant J 104: 1195–1214 volved in the flooding tolerance of wild rice species. Plant J 72:
Mohr W, Lehnen N, Ahmerkamp S, Marchant HK, Graf JS, 282–293
Tschitschko B, Yilmaz P, Littmann S, Gruber-Vodicka H, Leisch Nohra B, Candy L, Blanco J-F, Guerin C, Raoul Y, Mouloungui Z
N, et al. (2021) Terrestrial-type nitrogen-fixing symbiosis between (2013) From petrochemical polyurethanes to biobased polyhydrox-
seagrass and a marine bacterium. Nature 600: 105–109 yurethanes. Macromolecules 46: 3771–3792
Monteith JL (1978) Reassessment of maximum growth-rates for C3 Nolke G, Houdelet M, Kreuzaler F, Peterhansel C, Schillberg S
and C4 crops. Exp Agric 14: 1–5 (2014) The expression of a recombinant glycolate dehydrogenase
Moon RJ, Martini A, Nairn J, Simonsen J, Youngblood J (2011) polyprotein in potato (Solanum tuberosum) plastids strongly
Cellulose nanomaterials review: structure, properties and nano- enhances photosynthesis and tuber yield. Plant Biotechnol J 12:
composites. Chem Soc Rev 40: 3941–3994 734–742
Moore CE, Meacham-Hensold K, Lemonnier P, Slattery RA, Northrup DL, Basso B, Wang MQ, Morgan CLS, Benfey PN (2021)
Benjamin C, Bernacchi CJ, Lawson T, Cavanagh AP (2021) The
Novel technologies for emission reduction complement conserva-
effect of increasing temperature on crop photosynthesis: from
tion agriculture to achieve negative emissions from row-crop pro-
enzymes to ecosystems. J Exp Bot 72: 2822–2844
duction. Proc Natl Acad Sci USA 118: e2022666118
Morales N, Ogbonna AC, Ellerbrock BJ, Bauchet GJ, Tantikanjana
Obata T, Klemens PAW, Rosado-Souza L, Schlereth A, Gisel A,
T, Tecle IY, Powell AF, Lyon D, Menda N, Simoes CC, et al.
Stavolone L, Zierer W, Morales N, Mueller LA, Zeeman SC, et
(2022) Breedbase: a digital ecosystem for modern plant breeding.
al. (2020) Metabolic profiles of six African cultivars of cassava
G3 12: kac078
Moyers BT, Morell PL, McKay JK (Manihot esculenta Crantz) highlight bottlenecks of root yield.
(2018) Genetic costs of domestica-
tion and improvement. J Heredity 109: 103–116 Plant J 102: 1202–1219
Mus F, Crook MB, Garcia K, Garcia Costas A, Geddes BA, Kouri Ochieng G, Ngugi K, Wamalwa LN, Manyasa E, Muchira N,
ED, Paramasivan P, Ryu MH, Oldroyd GED, Poole PS, et al. Nyamongo D, Odeny DA (2020) Novel sources of drought toler-
(2016) Symbiotic nitrogen fixation and the challenges to its exten- ance from landraces and wild sorghum relatives. Crop Sci 61:
sion to nonlegumes. Appl Environ Microbiol 82: 3698–3710 104–118
Myers SS, Zanobetti A, Kloog I, Huybers P, Leakey AD, Bloom AJ, Oda M, Nguyen HC, Huynh VT (2019) Evaluation of cropping
Carlisle E, Dietterich LH, Fitzgerald G, Hasegawa T, et al. (2014) method for perennial ratoon rice: Adaptation of SALIBU to
Increasing CO2 threatens human nutrition. Nature 510: 139–142 triple-cropping in Vietnam. F1000Res 8: 1825
Nakakuni M, Watanabe K, Kaminaka K, Mizuno Y, Takehara K, Ogle SM, Alsaker C, Baldock J, Bernoux M, Jay Breidt F,
Kuwae T, Yamamoto S (2021) Seagrass contributes substantially McConkey B, Regina K, Vazquez-Amabile GG (2019) Climate
to the sedimentary lignin pool in an estuarine seagrass meadow. and soil characteristics determine where no-till management can
Sci Total Environ 793: 148488 store carbon in soils and mitigate greenhouse gas emissions. Sci
Narayanan S, Prasad PV, Welti R (2016a) Wheat leaf lipids during Rep 9: 11665
heat stress: II. Lipids experiencing coordinated metabolism are Okogbenin E, Setter TL, Ferguson M, Mutegi R, Ceballos H,
detected by analysis of lipid co-occurrence. Plant Cell Environ 39: Olasanmi B, Fregene M (2013) Phenotypic approaches to drought
608–617 in cassava: review. Front Physiol 4: 93
Narayanan S, Tamura PJ, Roth MR, Prasad PV, Welti R (2016b) Olsen JL, Rouzé P, Verhelst B, Lin YC, Bayer T, Collen J, Dattolo
Wheat leaf lipids during heat stress: I. High day and night tempera- E, De Paoli E, Dittami S, Maumus F, et al. (2016) The genome of
tures result in major lipid alterations. Plant Cell Environ 39: the seagrass Zostera marina reveals angiosperm adaptation to the
787–803 sea. Nature 530: 331–335
National Academies of Sciences, Engineering, and Medicine Ordón~ez RA, Archontoulis SV, Martinez-Feria R, Hatfield JL,
(2019) Negative Emissions Technologies and Reliable Wright EE, Castellano MJ (2020) Root to shoot and carbon to ni-
Sequestration: A Research Agenda. The National Academies Press, trogen ratios of maize and soybean crops in the US Midwest. Eur J
Washington, DC Agron 120: 126130
National Academies of Science, Engineering, and Medicine (2020) Oreska MP, McGlathery KJ, Aoki LR, Berger AC, Berg P, Mullins L
Safeguarding the Bioeconomy. The National Academies Press, (2020) The greenhouse gas offset potential from seagrass restora-
Washington, DC tion. Scient Rep 10: 1–15
Naylor D, Sadler N, Bhattacharjee A, Graham EB, Anderton CR, Ort DR, Long SP (2014) Limits on yields in the corn belt. Science
McClure R, Lipton M, Hofmockel KS, Jansson JK (2020) Soil 344: 483–484
microbiomes under climate change and implications for carbon cy- Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R,
cling. Annu Rev Environ Resour 45: 29–59 Croce R, Hanson MR, Hibberd JM, Long SP, et al. (2015)
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 61
Redesigning photosynthesis to sustainably meet global food and Harnessing the microbiome to prevent global biodiversity loss. Nat
bioenergy demand. Proc Natl Acad Sci USA 112: 8529–8536 Microbiol 7: 1726–1735
Orth RJ, Lefcheck JS, McGlathery KS, Aoki L, Luckenbach MW, Peng J, Sun D, Peng Y, Nevo E (2013) Gene discovery in triticum
Moore KA, Oreska MP, Snyder R, Wilcox DJ, Lusk B (2020) dicoccoides, the direct progenitor of cultivated wheats. Cereal Res
Restoration of seagrass habitat leads to rapid recovery of coastal Commun 41: 1–22
ecosystem services. Sci Adv 6: eabc6434 Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X,
Osakabe Y, Watanabe T, Sugano SS, Ueta R, Ishihara R, Shinozaki Centeno GS, Khush GS Cassman KG (2004) Rice yields decline
K, Osakabe K (2016) Optimization of CRISPR/Cas9 genome edit- with higher night temperature from global warming. Proc Nat
ing to modify abiotic stress responses in plants. Scient Rep 6: Acad Sci USA 101: 9971–9975
26685 Perilla-Henao LM, Casteel CL (2016) Vector-borne bacterial plant
Pailles Y, Awlia M, Julkowska M, Passone L, Zemmouri K, Negr~ao pathogens: interactions with hemipteran insects and plants. Front
S, Schmöckel SM, Tester M (2020) Diverse traits contribute to sa- Plant Sci 7: 1163
linity tolerance of wild tomato seedlings from the Galapagos Pfeifer L, van Erven G, Sinclair EA, Duarte CM, Kabel MA, Classen
islands. Plant Physiol 182: 534–546 B (2022) Profiling the cell walls of seagrasses from A (Amphibolis)
Pankievicz VCS, Irving TB, Maia LGS, Ane JM (2019) Are we there to Z (Zostera). BMC Plant Biol 22: 1–18
yet? The long walk towards the development of efficient symbiotic Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y, Vermeer
associations between nitrogen-fixing bacteria and non-leguminous JE, Yamazaki M, Li G, Maurel C, Takano J, et al. (2014) A
crops. BMC Biol 17: 99 receptor-like kinase mutant with absent endodermal diffusion bar-
Park JY, Kim H, Lee I (2017) Comparative analysis of molecular and rier displays selective nutrient homeostasis defects. eLife 3: e03115
physiological traits between perennial Arabis alpina Pajares and an- Pinson SRM, Tarpley L, Yan W, Yeater K, Lahner B, Yakubova E,
nual Arabidopsis thaliana Sy-0. Scient Rep 7: 1–11 Huang X-Y, Zhang M, ML Guerinot, Salt DE (2015) Worldwide
Parry M, Rosenzweig C (1993) The potential effects of climate genetic diversity for mineral element concentrations in rice grain.
change on world food supply. In MB Jackson, CR Black, eds, Crop Sci 55: 1–18
Interacting Stresses on Plants in a Changing Climate. Springer Pinto P, DeHaan L, Picasso V (2021) Post-harvest management
Berlin Heidelberg, Berlin Heidelberg, pp 1–26 practices impact on light penetration and Kernza intermediate
Parsell TH, Owen BC, Klein I, Jarell TM, Marcum CL, Haupert LJ, wheatgrass yield components. Agronomy 11: 442
Amundson LM, Kenttämaa HI, Riberio F, Miller JT, et al. (2013) Platten JD, Cobb JN, Zantua RE (2019) Criteria for evaluating mo-
Cleavage and hydrodeoxygenation (HDO) of C–O bonds relevant lecular markers: comprehensive quality metrics to improve
to lignin conversion using Pd/Zn synergistic catalysis. Chem Sci 4: marker-assisted selection. PLoS One 14: e0210529
Platten JD, Egdane JA, Ismail AM (2013) Salinity tolerance, Na + ex-
806–813
clusion and allele mining of HKT1;5 in Oryza sativa and O. glaber-
Parsell T, Yohe S, Degenstein J, Jarrell T, Klein I, Gençer E,
rima: many sources, many genes, one mechanism? BMC Plant Biol
Hewetson B, Hurt M, Kim JI, Choudari H, et al. (2015) A syner-
13: 32
gistic biorefinery based on catalytic conversion of lignin prior to
Pleijel H, Gelang J, Sild E, Danielsson H, Younis S, Karlsson P-K,
cellulose starting from lignocellulosic biomass. Green Chem 17:
Wallin G, Skärby L, Selldén G (2000) Effects of elevated carbon
1492–1499
dioxide, ozone and water availability on spring wheat growth and
Parton W (1996) The CENTURY model. In DS Powlson, P Smith, JU
yield. Physiol Planta 108: 61–70
Smith (eds) Evaluation of Soil Organic Matter Models. Springer, Pour-Aboughadareh A, Ahmadi J, Mehrabi AA, Etminan A,
Berlin, pp 283–291 Moghaddam M, Siddique KHM (2017) Physiological responses to
Paustian K, Campbell N, Dorich C, Marx E, Swan A (2016a) drought stress in wild relatives of wheat: implications for wheat
Assessment of potential greenhouse gas mitigation from changes improvement. Acta Physiol Plant 39: 106
to crop root mass and architecture. Final report to ARPA-E, 34. Prasch CM, Sonnewald U (2013) Simultaneous application of heat,
https://arpa-e.energy.gov/sites/default/files/documents/files/Revised drought, and virus to arabidopsis plants reveals significant shifts in
_Final_Report_to_ARPA_Bounding_Analysis.pdf (April 18, 2022) signaling networks. Plant Physiol 162: 1849–1866
Paustian K, Larson E, Kent J, Marx E, Swan A (2019) Soil C seques- Prieto I, Stokes A, Roumet C (2016) Root functional parameters
tration as a biological negative emission strategy. Front Climate 1: predict fine root decomposability at the community level. J Ecol
8 104: 725–733.
Paustian K, Lehmann J, Ogle S, Reay D, Robertson GP, Smith P Prior SA, Runion GB, Rogers HH, Torbert HA (2008) Effects of at-
(2016b) Climate-smart soils. Nature 532: 49–57 mospheric CO2 enrichment on crop nutrient dynamics under
Pearson PN, Foster GL, Wade BS (2009) Atmospheric carbon diox- no-till conditions. J Plant Nutr 31: 758–773
ide through the Eocene–Oligocene climate transition. Nature 461: Priyadharsini P, Rojamala K, Koshila Ravi R, Muthuraja R,
1110–1113 Nagaraj K, Muthukumar T (2016) Mycorrhizosphere: the ex-
Pedersen O, Nakayama Y, Yasue H, Kurokawa Y, Takahashi H, tended rhizosphere and its significance. In DK Choudhary, A
Heidi Floytrup A, Omori F, Mano Y, David Colmer T, Nakazono Varma, N Tuteja, eds, Plant-Microbe Interaction: An Approach to
M (2021) Lateral roots, in addition to adventitious roots, form a Sustainable Agriculture. Springer, New York, pp 97–124
barrier to radial oxygen loss in Zea nicaraguensis and a chromo- Qu Y, Sakoda K, Fukayama H, Kondo E, Suzuki Y, Makino A,
some segment introgression line in maize. New Phytol 229: Terashima I, Yamori W (2021) Overexpression of both Rubisco
94–105 and Rubisco activase rescues rice photosynthesis and biomass un-
Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler der heat stress. Plant Cell Environ 44: 2308–2320
ES, Ley RE (2013) Diversity and heritability of the maize rhizo- Rabbi IY, Kayondo SI, Bauchet G, Yusuf M, Aghogho CI,
sphere microbiome under field conditions. Proc Natl Acad Sci USA Ogunpaimo K, Uwugiaren R, Smith IA, Peteti P, Agbona A,
110: 6548–6553 et al. (2020) Genome-wide association analysis reveals new insights
Peixoto L, Elsgaard L, Rasmussen J, Kuzyakov Y, Banfield CC, into the genetic architecture of defensive, agro-morphological and
Dippold MA, Olesen JE (2020) Decreased rhizodeposition, but in- quality-related traits in cassava. Plant Mol Biol 109: 195–213
creased microbial carbon stabilization with soil depth down to Ragauskas AJ, Beckham GT, Biddy MJ, Chandra R, Chen F, Davis
3.6 m. Soil Biol Biochem 150: 108008 MF, Davison BH, Dixon RA, Gilna P, Keller M, et al. (2014)
Peixoto RS, Voolstra CR, Sweet M, Duarte CM, Carvalho S, Villela Lignin valorization: improving lignin processing in the biorefinery.
H, Lunshof JE, Gram L, Woodhams DC, Walter J, et al. (2022) Science 344: 1246843
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
62 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Ramu P, Esuma W, Kawuki R, Rabbi IY, Egesi C, Bredeson JV, Sacks EJ, Roxas JP, Cruz MTS (2003) Developing perennial upland
Bart RS, Verma J, Buckler ES, Lu F (2017) Cassava haplotype rice II: field performance of S1 families from an intermated Oryza
map highlights fixation of deleterious mutations during clonal sativa/O. longistaminata population. Crop Sci 43: 129–134
propagation. Nat Genet 49: 959–963 Sage RF (2016) A portrait of the C4 photosynthetic family on the
Rani K, Raghu BR, Jha SK, Agarwal P, Mallick N, Niranjana M, 50th anniversary of its discovery: species number, evolutionary lin-
Sharma JB, Singh AK, Sharma NK, Rajkumar S, et al. (2020) A eages, and Hall of Fame. J Exp Bot 67: 4039–4056
novel leaf rust resistance gene introgressed from Aegilops markgra- Salas-González I, Reyt G, Flis P, Custódio V, Gopaulchan D,
fii maps on chromosome arm 2AS of wheat. Theoret Appl Genet Bakhoum N, Dew TP, Suresh K, Franke RB, Dangl JL, et al. (2021)
133: 2685–2694 Coordination between microbiota and root endodermis supports
Rao Z, Chen F, Zhang X, Xu Y, Xue Q, Zhang P (2012) Spatial and plant mineral nutrient homeostasis. Science 371: eabd0695
temporal variations of C3/C4 relative abundance in global terres- Sales CR, Wang Y, Evers JB, Kromdijk J (2021) Improving C4 photo-
trial ecosystem since the Last Glacial and its possible driving mech- synthesis to increase productivity under optimal and suboptimal
anisms. Chinese Sci Bull 57: 4024–4035 conditions. J Exp Bot 72: 5942–5960
Razzaq A, Saleem F, Wani SH, Abdelmohsen SA, Alyousef HA, Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the
Abdelbacki AM, Alkallas FH, Tamam N, Elansary HO (2021) plant ionome. Annu Rev Plant Biol 59: 709–733
De-novo domestication for improving salt tolerance in crops. Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A,
Frontiers Plant Sci 12: 1623 Dobermann A (2008) Nitrogen uptake, fixation and response to
Reich PB, Hobbie SE, Lee TD, Pastore MA (2018) Unexpected re- fertilizer N in soybeans: a review. Field Crops Res 108: 1–13
versal of C3 versus C4 grass response to elevated CO2 during a Salvucchi ME, Crafts-Brandner SJ (2004) Relationship between the
20-year field experiment. Science 360: 317–320 heat tolerance of photosynthesis and the thermal stability of
Reyt G, Chao Z, Flis P, Salas-González I, Castrillo G, Chao DY, Rubisco activase in plants from contrasting thermal environments.
Salt DE (2020) Uclacyanin proteins are required for lignified nano- Plant Physiol 134: 1460–1470
domain formation within casparian strips. Curr Biol 30: Sanderman J, Hengl T, Fiske GJ (2017) Soil carbon debt of
4103–4111.e6 12,000 years of human land use. Proc Natl Acad Sci USA 114:
Reyt G, Ramakrishna P, Salas-González I, Fujita S, Love A, 9575–9580
Tiemessen D, Lapierre C, Morreel K, Calvo-Polanco M, Flis P, Sasa S, Sawayama S, Sakamoto S, Tsujimoto R, Terauchi G, Yagi
et al. (2021) Two chemically distinct root lignin barriers control H, Komatsu T (2012) Did huge tsunami on 11 March 2011 impact
solute and water balance. Nat Commun 12: 2320 seagrass bed distributions in Shizugawa Bay, Sanriku Coast, Japan?
Rivero RM, Mittler R, Blumwald E, Zandalinas SI (2022) In Remote Sensing of the Marine Environment II (Vol. 8525, p.
Developing climate-resilient crops: improving plant tolerance to 85250X). International Society for Optics and Photonics
stress combination. Plant J 109: 373–389 Scafaro AP, Atwell BJ, Muylaert S, Reusel BV, Ruiz GA, Rie JV,
Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gallé A (2018) A thermotolerant variant of Rubisco activase from
Gepstein S, Blumwald E (2007) Delayed leaf senescence induces a wild relative improves growth and seed yield in rice under heat
extreme drought tolerance in a flowering plant. Proc Natl Acad Sci stress. Front Plant Sci 20: 1663
USA 104: 19631–19636 Scafaro AP, Bautsoens N, den Boer B, Van Rie J, Gallé A (2019) A
Roberts DG, McComb AJ, Kuo J (1984) The structure and continu- conserved sequence from heat-adapted species improves Rubisco
ity of the lacunar system of the seagrass Halophila ovalis (R. Br.) activase thermostability in wheat. Plant Physiol 181: 43–54
Hook f.(Hydrocharitaceae). Aquatic Bot 18: 377–388 Scafaro AP, Gallé A, Van Rie J, Carmo-Silva E, Salvucci ME,
Roe, S, Streck C, Obersteiner M, Frank S, Grisom B, Drouet L, Atwell BJ (2016) Heat tolerance in a wild Oryza species is attrib-
Fricko O, Gusti M, Harris N, Hasegawa T, et al. (2019) uted to maintenance of Rubisco activation by a thermally stable
Contribution of the land sector to a 1.5C world. Nat Climate Rubisco activase ortholog. New Phytol 211: 899–911
Change 9: 817–828 Scafaro AP, Yamori W, Carmo-Silva AE, Salvucci ME, von
Romero J, Lee KS, Pérez M, Mateo MA, Alcoverro T (2006) Caemmerer S, Atwell BJ (2012) Rubisco activity is associated with
Nutrient dynamics in seagrass ecosystems. In Seagrasses: Biology, photosynthetic thermotolerance in a wild rice (Oryza meridiona-
Ecology and Conservation. Springer, Dordrecht, pp 227–254 lis). Physiol Planta 146: 99–109
Rosenthal DM, Locke AM, Khozaei M, Raines CA, Long SP, Ort Scheffen M, Marchal DG, Beneyton T, Schuller SK, Klose M, Diehl
DR (2011) Over-expressing the C3 photosynthesis cycle enzyme C, Lehmann J, Pfister P, Carrillo M, He H, et al. (2021) A
sedoheptulose-1-7 bisphosphatase improves photosynthetic carbon new-to-nature carboxylation module to improve natural and syn-
gain and yield under fully open air CO2 fumigation (FACE). BMC thetic CO2 fixation. Nat Catalysis 4: 105–115
Plant Biol 11: 123 Schiessl K, Lilley JLS, Lee T, Tamvakis I, Kohlen W, Bailey PC,
Rosenthal DM, Slattery RA, Miller RE, Grennan AK, Cavagnaro Thomas A, Luptak J, Ramakrishnan K, Carpenter MD, et al.
TR, Fauquet CM, Gleadow RM, Ort DR (2012) Cassava (2019) NODULE INCEPTION recruits the lateral root developmen-
about-FACE: greater than expected yield stimulation of cassava tal program for symbiotic nodule organogenesis in Medicago trun-
(Manihot esculenta) by future CO2levels. Global Change Biol 18: catula. Curr Biol 29: 3657–3668.e5
2661–2675 Schiller K, Bräutigam A (2021) Engineering of crassulacean acid me-
Roy S, Liu W, Nandety RS, Crook A, Mysore KS, Pislariu CI, tabolism. Ann Rev Plant Biol 72: 77–103
Frugoli J, Dickstein R, Udvardi MK (2020) Celebrating 20 years of Schlautman B, Barriball S, Ciotir C, Herron S, Miller AJ (2018)
genetic discoveries in legume nodulation and symbiotic nitrogen Perennial grain legume domestication phase I: criteria for candi-
fixation. Plant Cell 32: 15–41 date species selection. Sustainability 10: 730
Ruiz-Vera UM, De Souza AP, Ament MR, Gleadow RM, Ort DR Schlesinger WH, Bernhardt ES (2020) Biogeochemistry: An Analysis
(2020) High sink-strength prevents photosynthetic of Global Change. Elsevier Science, Amsterdam
down-regulation in cassava grown at elevated CO2 concentration. J Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G,
Exp Bot 72: 542–560 Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning
Runck BC, Kantar MB, Jordan NR, Anderson JA, Wyse DL, DAC, et al. (2011) Persistence of soil organic matter as an ecosys-
Eckberg JO, Barnes RJ, Lehman CL, DeHaan LR, Stupar RM, et tem property. Nature 478: 49–56
al. (2014) The reflective plant breeding paradigm: a robust system Schmidt R, Gravuer K, Bossange AV, Mitchell J, Scow K (2018)
of germplasm development to support strategic diversification of Long-term use of cover crops and no-till shift soil microbial com-
agroecosystems. Crop Sci 54: 1939–1948 munity life strategies in agricultural soil. PLoS One 13: e0192953
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 63
Scholz VV, Martin BC, Meyer R, Schramm A, Fraser MW, Nielsen Singh GM, Xu J, Schaefer D, Day R, Wang Z, Zhang F (2022) Maize
LP, Kendrick GA, Risgaard-Petersen N, Burdorf LD, Marshall IP diversity for fall armyworm resistance in a warming world. Crop
(2021) Cable bacteria at oxygen-releasing roots of aquatic plants: a Sci 62: 1–9
widespread and diverse plant-microbe association. New Phytol Skendzic S, Zovko M, Zivkovic IP, Lesic V, Lemic D (2021) The im-
232: 2138–2151 pact of climate change on agricultural insect pests. Insects 12: 440
Schuler ML, Sedelnikova OV, Walker BJ, Westhoff P, Langdale JA Slattery RA, Ort DR (2019) Carbon assimilation in crops at high
(2018) SHORTROOT-mediated increase in stomatal density has temperatures. Plant Cell Environ 42: 2750–2758
no impact on photosynthetic efficiency. Plant Physiol 176: Socha AM, Parthasarathi P, Shi J, Pattathil S, Whyte D, Bergeron
757–772 M, George A, Tran K, Stavila V, Venkatachalam S, et al. (2014)
Schutyser W, Van den Bosch S, Renders T, De Boe T, Koelewijn Efficient biomass pretreatment using ionic liquids derived from lig-
SF, Dewaele A, Ennaert T, Verkindern O, Goderis B, Courtin nin and hemicellulose. Proc Natl Acad Sci USA 111: 12582–12587
CM, et al. (2015) Influence of bio-based solvents on the catalytic Somleva MN, Snell KD, Beaulieu JJ, Peoples OP, Garrison BR,
reductive fractionation of birch wood. Green Chem 17: 5035–5045 Patterson NA (2008) Production of polyhydroxybutyrate in
Schwander T, Schada von Borzyskowski L, Burgener S, Cortina switchgrass, a value-added co-product in an important lignocellu-
NS, Erb TJ (2016) A synthetic pathway for the fixation of carbon losic biomass crop. Plant Biotech J 6: 663–678
dioxide in vitro. Science 354: 900–904 Song Y, Yu J, Huang B (2014) Elevated CO2-mitigation of high tem-
Scudeletti D, Crusciol CAC, Bossolani JW, Moretti LG, Momesso perature stress associated with maintenance of positive carbon bal-
L, Servaz Tuban~a B, de Castro SGQ, De Oliveira EF, Hungria M, ance and carbohydrate accumulation in Kentucky bluegrass. PLoS
et al. (2021) Trichoderma asperellum inoculation as a tool for at- One 9: e89725
tenuating drought stress in sugarcane. Front Plant Sci 12: 645542 Sonnewald U, Fernie AR, Gruissem W, Schläpfer P, Anjanappa
Sedelnikova OV, Hughes TE, Langdale JA (2018) Understanding the RB, Chang S, Ludewig F, Rascher U, Muller O, van Doorn AM,
genetic basis of C4 Kranz anatomy with a view to engineering C3 et al. (2020) The Cassava Source-Sink project: opportunities and
crops. Annu Rev Genet 52: 249–270 challenges for crop improvement by metabolic engineering. Plant J
Selvaraj MG, Valderrama M, Guzman D, Valencia M, Ruiz H, 103: 1655–1665
Acharjee A (2020) Machine learning for high-throughput field Soudzilovskaia NA, van Bodegom PM, Terrer C, van’t Zelfde M,
phenotyping and image processing provides insight into the associ- McCallum I, Luke McCormack M, Fisher JB, Brundrett MC,
ation of above and below-ground traits in cassava (Manihot escu- César de Sá N, Tedersoo L (2019) Global mycorrhizal plant distri-
lenta Crantz). Plant Methods 16: 87 bution linked to terrestrial carbon stocks. Nat Commun 10: 5077
Seneweera SP, Conroy JP (1997) Growth, grain yield and quality of Soumare A, Diedhiou AG, Thuita M, Hafidi M, Ouhdouch Y,
rice (Oryza sativa L.) in response to elevated CO2 and phosphorus Gopalakrishnan S, Kouisni L (2020) Exploiting biological nitrogen
nutrition. Soil Sci Plant Nutr 43: 1131–1136 fixation: a route towards a sustainable agriculture. Plants (Basel) 9:
Shaibu AS, Badu-Apraku B, Ayo-Vaughan MA (2021) Enhancing 1011
drought tolerance and Striga hermonthica resistance in maize us- South PF, Cavanagh AP, Liu HW, Ort DR (2019) Synthetic glycolate
ing newly derived inbred lines from the wild maize relative, Zea metabolism pathways stimulate crop growth and productivity in
diploperennis. Agronomy 11: 177 the field. Science 363: 6422
Shalata A, Tal M (1998) The effect of salt stress on lipid peroxida- Soyano T, Kouchi H, Hirota A, Hayashi M (2013) NODULE
tion and antioxidants in the cultivated tomato and its wild INCEPTION directly targets NF-Y subunit genes to regulate essen-
salt-tolerant relative Lycopersicon pennellii. Physiol Plant 104: tial processes of root nodule development in Lotus japonicus. PloS
169–174 Genet 9: e1003352
Sharlach M, Dahlbeck D, Liu L, Chiu J, Jiménez-Gómez JM, Soyano T, Shimoda Y, Kawaguchi M, Hayashi M (2019) A shared
Kimura S, Koenig D, Maloof JN, Sinha N, Minsavage GV, et al. gene drives lateral root development and root nodule symbiosis
(2013) Fine genetic mapping of RXopJ4, a bacterial spot disease re- pathways in Lotus. Science 366: 1021–1023
sistance locus from Solanum pennellii LA716. Theor Appl Genet Sprunger CD, Culman SW, Peralta AL, DuPont ST, Lennon JT,
126: 601–609 Snapp SS (2019) Perennial grain crop roots and nitrogen manage-
Sharma R, De Vleesschauwer D, Sharma MK, Ronald PC (2013) ment shape soil food webs and soil carbon dynamics. Soil Biol
Recent advances in dissecting stress-regulatory crosstalk in rice. Biochem 137: 107573
Mol Plant 6: 250–260 Steinwand MA, Ronald PC (2020) Crop biotechnology and the fu-
Shen BR, Wang LM, Lin XL, Yao Z, Xu HW, Zhu CH, Teng HY, Cui ture of food. Nat Food 1: 273–283
LL, Liu EE, Zhang JJ, et al. (2019) Engineering a new chloroplastic Still CJ, Berry JA, Collatz GJ, DeFries RS (2003) Global distribution
photorespiratory bypass to increase photosynthetic efficiency and of C3 and C4 vegetation: carbon cycle implications. Global
productivity in rice. Mol Plant 12: 199–214 Biogeochem Cycles 17: 1–6
Shi W, Yin X, Struik PC, Solis C, Xie F, Schmidt RC, Huang M, Stitt M (1991) Rising CO2 levels and their potential significance for
Zou Y, Ye C, Jagadish SVK (2017) High day- and night-time tem- carbon flow in photosynthetic cells. Plant Cell Environ 14:
peratures affect grain growth dynamics in contrasting rice geno- 741–762
types. J Exp Bot 68: 5233–5245 Suganami M, Suzuki Y, Tazoe Y, Yamori W, Makino A (2021)
Shi JC, Zhao BY, Zheng S, Zhang XW, Wang XL, Dong W, Xie Q, Co-overproducing Rubisco and Rubisco activase enhances photo-
Wang G, Xiao Y, Chen F, et al. (2021) A phosphate starvation synthesis in the optimal temperature range in rice. Plant Physiol
response-centered network regulates mycorrhizal symbiosis. Cell 185: 108–119
184: 5527–5540.18. Swamy BPM, Ahmed HU, Henry A, Mauleon R, Dixit S, Vikram P,
Shimono H, Ozaki Y, Jagadish SVK, Sakai H, Usui Y, Hasegawa T, Tilatto R, Verulkar SB, Perraju P, Mandal NP, et al. (2013)
Kumagai E, Nakano H, Yoshinaga S (2014) Planting geometry as Genetic, physiological, and gene expression analyses reveal that
a pre-screening technique for identifying CO2 responsive rice multiple QTL enhance yield of rice mega-variety IR64 under
geno- types: a case study of panicle number. Physiol Plant 152: drought. PLoS One 8: e62795
520–528 Tarquinio F, Hyndes GA, Laverock B, Koenders A, Säwström C
Shivhare D, Mueller-Cajar O (2017) In vitro characterization of (2019) The seagrass holobiont: understanding seagrass-bacteria
thermostable CAM Rubisco activase reveals a Rubisco interacting interactions and their role in seagrass ecosystem functioning. FEMS
surface loop. Plant Physiol 174: 1505–1516 Microbiol Lett 366: p.fnz057.
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
64 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Teixeira EI, Fischer G, Van Velthuizen H, Walter C, Ewert F (2013) (2023) Burning questions for a warming and changing world: 15
Global hot-spots of heat stress on agricultural crops due to climate unknowns in plant abiotic stress. Plant Cell 35: 67–108
change. Agric Forest Meteorol 170: 206–215 Vikram P, Swamy BPM, Dixit S, Singh R, Singh BP, Miro B, Kohli
Therezan R, Kortbeek R, Vendemiatti E, Legarrea S, de Alencar A, Henry A, Singh NK, Kumar A (2015) Drought susceptibility of
SM, Schuurink RC, Bleeker P, Peres LEP (2021) Introgression of modern rice varieties: an effect of linkage of drought tolerance
the sesquiterpene biosynthesis from Solanum habrochaites to cul- with undesirable traits. Scient Rep 5: 14799
tivated tomato offers insights into trichome morphology and ar- Vinueza NR, Kim ES, Gallardo VA, Mosier NS, Abu-Omar MM,
thropod resistance. Planta 254: 11 https://doi.org/10.1007/s00425- Carpita NC, Kenttäma HI (2015) Tandem mass spectrometric
021-03651-y. characterization of the conversion of xylose to furfural. Biomass
Tin HQ, Loi NH, Bjornstad Å, Kilian B (2021) Participatory selec- Bioenerg 74: 1–5
tion of CWR-derived salt-tolerant rice lines adapted to the coastal Wagner MR, Roberts JH, Balint-Kurti P, Holland JB (2020)
zone of the Mekong Delta. Crop Sci 61: 277–288 Heterosis of leaf and rhizosphere microbiomes in field-grown
Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, maize. New Phytol 228: 1055–1069
Sato S, Asamizu E, Tabata S, Stougaard J (2007) A Walker BJ, VanLoocke A, Bernacchi CJ, Ort DR (2016) The costs of
gain-of-function mutation in a cytokinin receptor triggers sponta- photorespiration to food production now and in the future. Annu
neous root nodule organogenesis. Science 315: 104–107 Rev Plant Biol 67: 107–129
Tork DG, Anderson NO, Wyse DL, Betts KJ (2019) Domestication Wang D, Dong W, Murray J, Wang E (2022) Innovation and appro-
of perennial flax using an ideotype approach for oilseed, cut flower, priation in mycorrhizal and rhizobial symbioses. Plant Cell 34:
and garden performance. Agronomy 9: 707 1573–1599
Torta L, Burruano S, Giambra S, Conigliaro G, Piazza G, Mirabile Wang ET, Schornack S, Marsh JF, Gobbato E, Schwessinger B,
G, Pirrotta M, Calvo R, Bellissimo G, Calvo S, et al. (2022) Eastmond P, Schultze M, Kamoun S, Oldroyd GE (2012) A com-
Cultivable fungal endophytes in roots, rhizomes and leaves of mon signaling process that promotes mycorrhizal and oomycete
Posidonia oceanica (L.) Delile along the coast of Sicily, Italy. Plants colonization of plants. Curr Biol 22: 2242–2246
11: 1139 Wang L, Zhang L, Liu Z, Zhao D, Liu X, Zhang B, Xie J, Hong Y, Li
Tyskiewicz R, Nowak A, Ozimek E, Jaroszuk-Sciseł J (2022) P, Chen S, et al. (2013b) A minimal nitrogen fixation gene cluster
Trichoderma: the current status of its application in agriculture for from Paenibacillus sp. WLY78 enables expression of active nitroge-
the biocontrol of fungal phytopathogens and stimulation of plant nase in Escherichia coli. PLoS Genet 9: e1003865
growth. Int J Mol Sci 23: 2329 Wang P, Karki S, Biswal AK, Lin H-C, Dionora MJ, Rizal G, Yin X,
U.S. Department of Energy (2015) Quadrennial technology review. Schuler ML, Hughes T, Fouracre JP, et al. (2017a) Candidate reg-
An assessment of energy technologies and research opportunities. ulators of early leaf development in maize perturb hormone signal-
Office of Efficiency and Renewable Energy
ling and secondary cell wall formation when constitutively
U.S. Department of Energy (2016) Billion-ton report: advancing do-
expressed in rice. Scient Rep 7: 4535
mestic resources for a thriving bioeconomy. Office of Efficiency
Wang P, Kelly S, Fouracre JP, Langdale JA (2013a) Genome-wide
and Renewable Energy.
transcript analysis of early maize leaf development reveals gene
Ujiie K, Ishimaru K, Hirotsu N, Nagasaka S, Miyakoshi Y, Ota M,
cohorts associated with the differentiation of C4 Kranz anatomy.
Tokida T, Sakai H, Usui Y, Ono K, et al. (2019) How elevated
Plant J 75: 656–670
CO2 affects our nutrition in rice, and how we can deal with it.
Wang P, Khoshravesh R, Karki S, Tapia R, Balahadia CP,
PLoS One 14: e0212840
Van Deynze A, Zamora P, Delaux PM, Heitmann C, Jayaraman D, Bandyopadhyay A, Quick WP, Furbank RT, Sage TL, Langdale
Rajasekar S, Graham D, Maeda J, Gibson D, Schwartz KD, et al. JA (2017b) Re-creation of a key step in the evolutionary switch
(2018) Nitrogen fixation in a landrace of maize is supported by a from C3 to C4 leaf anatomy. Curr Biol 27: 3278–3287
mucilage-associated diazotrophic microbiota. PLoS Biol 16: Wang T, Nolte MW, Shanks BH (2014) Catalytic dehydration of C6
e2006352 carbohydrates for the production of hydroxymethylfurfural (HMF)
van Katwijk MM, Thorhaug A, Marbà N, Orth RJ, Duarte CM, as a versatile platform chemical. Green Chem 16: 548–572
Kendrick GA, Althuizen IH, Balestri E, Bernard G, Cambridge Wang XL, Feng H, Wang YY, Wang MX, Xie XG, Chang H, Wang
ML, et al. (2016) Global analysis of seagrass restoration: the impor- L, Qu J, Sun K, He W, et al. (2021) Mycorrhizal symbiosis modu-
tance of large-scale planting. J Appl Ecol 53: 567–578. lates the rhizosphere microbiota to promote rhizobia-legume sym-
Van Tassel DL, Albrecht KA, Bever JD, Boe AA, Brandvain Y, biosis. Mol Plant 14: 503–516
Crews TE, Gansberger M, Gerstberger P, González-Paleo L, Wang Y, Bao Z, Zhu Y, Hua J (2009) Analysis of temperature modu-
Hulke BS, et al. (2017) Accelerating Silphium domestication: an lation of plant defense against biotrophic microbes. Mol Plant
opportunity to develop new crop ideotypes and breeding strate- Microbe Interact 22: 498–506
gies informed by multiple disciplines. Crop Sci 57: 1274–1284 Watson A, Ghosh S, Williams MJ, Cuddy WS, Simmonds J, Rey
Váry Z, Mullins E, McElwain JC, Doohan FM (2015) The severity of MD, Asyraf Md Hatta M, Hinchliffe A, Steed A, Reynolds D, et
wheat diseases increases when plants and pathogens are acclima- al. (2018) Speed breeding is a powerful tool to accelerate crop re-
tized to elevated carbon dioxide. Global Change Biol 21: search and breeding. Nat Plants 4: 23–29
2661–2669 Welch JR, Vincent JR, Auffhammer M, Moya PF, Dobermann A,
Velásquez AC, Castroverde CDM, He SY (2018) Plant–pathogen Dawe D (2010) Rice yields in tropical/subtropical Asia exhibit large
warfare under changing climate conditions. Curr Biol 28: but opposing sensitivities to minimum and maximum tempera-
R619–R634 tures. Proc Natl Acad Sci USA 107: 14562–14567
Venkatesh J, Kang B-C (2019) Current views on Wellisch M, Jungmeier G, Karbowski A, Patel MK, Rogulska M
temperature-modulated R gene-mediated plant defense responses (2010) Biorefinery systems - potential contributors to sustainable
and tradeoffs between plant growth and immunity. Curr Opin innovation. Biofuels Bioprod Biorefin 4: 275–286
Plant Biol 50: 9–17 Whitt L, Ricachenevsky FK, Ziegler GZ, Clemens S, Walker E,
Verma SB, Sellers PJ, Walthall CL, Hall FG, Kim J, Goetz SJ (1993) Maathuis FJM, Kear P, Baxter I (2020) A curated list of genes
Photosynthesis and stomatal conductance related to reflectance that affect the plant ionome. Plant Direct 4: e00272
on the canopy scale. Remote Sens Environ 44: 103–116 Wissuwa M, Kretzschmar T, Rose TJ (2016) From promise to appli-
Verslues PE, Bailey-Serres J, Brodersen C, Buckley TN, Conti L, cation: root traits for enhanced nutrient capture in rice breeding. J
Christmann A, Dinneny JR, Grill E, Hayes S, Heckman RW Exp Bot 67: 3605–3615
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
Climate change challenges, plant science solutions THE PLANT CELL 2023: 35; 24–66 | 65
Wolfe MD, Del Carpio DP, Alabi O, Ezenwaka LC, Ikeogu UN, Zhang C, He J, Dai H, Wang G, Zhang X, Wang C, Shi J, Chen X,
Kayondo IS, Lozano R, Okeke UG, Ozimati AA, Williams E, Wang D, Wang E (2021a) Discriminating symbiosis and immunity
et al. (2017) Prospects for genomic selection in cassava breeding. signals by receptor competition in rice. Proc Natl Acad Sci
Plant Genome 10: 1–19 USA 118: e2023738118
Woods P, Lehner K, Hein K, Mullen JL, McKay JK (2022) Root pull- Zhang F, Xie J (2014) Genes and QTLs resistant to biotic and abiotic
ing force across drought in maize reveals genotype by environment stresses from wild rice and their applications in cultivar improve-
interactions and candidate genes. Front Plant Sci 13: 883209 ments. In W Yan, ed, Rice – Germplasm, Genetics and
Wu A, Hammer GL, Doherty A, von Caemmerer S, Farquhar GD Improvement, Vol 23. Intech Open, London, pp 59–78
(2019) Quantifying impacts of enhancing photosynthesis on crop Zhang H, Mittal N, Leamy LJ, Barazani O, Song B-H (2017) Back
yield. Nat Plants 5: 380–388 into the wild—Apply untapped genetic diversity of wild relatives
Xiong J, He Z, Shi S, Kent A, Deng Y, Wu L, Van Nostrand JD, for crop improvement. Evol Appl 10: 5–24
Zhou J (2015) Elevated CO2 shifts the functional structure and Zhang H, Wang ML, Schaefer R, Dang P, Jiang T, Chen C (2019)
metabolic potentials of soil microbial communities in a C4 agroe- GWAS and coexpression network reveal ionomic variation in culti-
cosystem. Sci Rep 5: 9316. vated peanut. J Agric Food Chem 67: 12026–12036
Yandigeri MS, Meena KK, Singh D, Malviya N, Singh DP, Solanki Zhang XW, Dong WT, Sun JH, Feng F, Deng YW, He ZH, Oldroyd
MK, Yadav, AK, Arora, DK (2012) Drought-tolerant endophytic GED, Wang E (2015) The receptor kinase CERK1 has dual
actinobacteria promote growth of wheat (Triticum aestivum) un- functions in symbiosis and immunity signalling. Plant J 81: 258–267
der water stress conditions. Plant Growth Regul 68: 411–420. Zhang P, Wang W-Q, Zhang G-L, Kaminek M, Dobrev P, Xu J,
Yang J, Lan LLY, Jin Y, Yu N, Wang D, Wang ET (2022) Gruissem W (2010) Senescence-inducible expression of isopen-
Mechanisms underlying legume-rhizobium symbioses. J Integr tenyl transferase extends leaf life, increases drought stress resis-
Plant Biol 64: 244–267 tance and alters cytokinin metabolism in cassava. J Integr Plant
Yang M, Lu K, Zhao FJ, Xie W, Ramakrishna P, Wang G, Du Q, Biol 52: 653–669
Liang L, Sun C, Zhao H, et al. (2018) Genome-wide association Zhang S, Chen X, Lu C, Ye J, Zou M, Lu K, Feng S, Pei J, Liu C,
studies reveal the genetic basis of ionomic variation in rice. Plant Zhou X, et al. (2018) Genome-wide association studies of 11 agro-
Cell 30: 2720–2740 nomic traits in Cassava (Manihot esculenta Crantz). Front Plant
Yang S, Zheng Q, Yuan M, Shi Z, Chiariello NR, Docherty KM, Sci 9: 503
Dong S, Field CB, Gu Y, Gutknecht J, et al. (2019a) Long-term el- Zhang S, Gan Y, Xu B (2016) Application of plant-growth-promoting
evated CO2 shifts composition of soil microbial communities in a fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat
Californian annual grassland, reducing growth and N utilization to salt stress through improvement of antioxidative defense system
and gene expression. Front Plant Sci 7: 1405
potentials. Sci Total Environ 652: 1474–1481
Zhang Y, Lavallee JM, Robertson AD, Even R, Ogle SM, Paustian
Yang H, Zhang X, Luo H, Liu B, Shiga TM, Li X, Kim JI, Rubinelli
K, Cotrufo MF (2021b) Simulating measurable ecosystem carbon
P, Overton JC, Subramanyam V, et al. (2019b) Overcoming cellu-
and nitrogen dynamics with the mechanistically defined MEMS 2.0
lose recalcitrance in woody biomass for the lignin-first biorefinery.
model. Biogeosciences 18: 3147–3171
Biotechnol Biofuels 12: 171
Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M,
Yao QH, Peng RH, Wang B, Tian YS, Zhu YM, Gao JJ, Liu ZJ,
Yao Y, Bassu S, Ciais P, et al. (2017) Temperature increase
Fu XY, Xu J, Han HJ, et al. (2021) Endowing Plants with the
reduces global yields of major crops in four independent estimates.
Capacity for Autogenic Nitrogen Fixation. Preprint posted to
Proc Natl Acad Sci USA 114: 9326–9331
Research Square on May 7, 2021, https://doi.org/10.21203/rs.3.rs- Zhao S, Abu-Omar MM (2015) Biobased epoxy nanocomposites de-
436726/v1 rived from lignin-based monomers. Biomacromolecules 16:
Yoshida K, Miyashita NT (2009) DNA polymorphism in the blast 2025–2031
disease resistance gene Pita of the wild rice Oryza rufipogon and Zhao X, Tekinalp H, Meng X, Ker D, Benson B, Yunqiao P,
its related species. Genes Genet Syst 84: 121–136 Ragauskas AJ, Wang Y, Li K, Webb E, et al. (2019) Poplar as bio-
Yoshida Y, Marubodee R, Ogiso-Tanaka E, Iseki K, Isemura T, fiber reinforcement in composites for large-scale 3D printing. ACS
Takahashi Y, Muto C, Naito K, Kaga A, Okuno K, et al. (2016) Appl Bio Mater 2: 4557–4570
Salt tolerance in wild relatives of adzuki bean, Vigna angularis Zhou LY, Zhou XH, He YH, Fu YL, Du ZG, Lu M, Sun XY, Li CH,
(Willd.) Ohwi et Ohashi. Genet Resour Crop Evol 63: 627–637 Lu CY, Liu RQ, et al. (2022) Global systematic review with
Yu H, Deng Y, He Z, Van Nostrand JD, Wang S, Jin D, Wang A, meta-analysis shows that warming effects on terrestrial plant bio-
Wu L, Wang D, Tai X, Zhou J (2018a) Elevated CO2 and warming mass allocation are influenced by precipitation and mycorrhizal as-
altered grassland microbial communities in soil top-layers. Front sociation. Nat Commun 13: 4914
Microbiol 9: 1790 Zhu H, Luo W, Ciesielski PN, Fang Z, Zhu JY, Hendriksson G,
Yu H, Li X, Duchoud F, Chuang DS, Liao JC (2018b) Augmenting Himmel ME, Hu L (2016) Wood-derived materials for green elec-
the Calvin-Benson-Bassham cycle by a synthetic tronics, biological devices, and energy applications. Chem Rev 116:
malyl-CoA-glycerate carbon fixation pathway. Nat Commun 9: 9305–9374
2008 Zhu X-G, Ort DR, Parry MAJ, von Caemmerer S (2020) A wish list
Zabin CJ, Jurgens LJ, Bible JM, Patten MV, Chang AL, Grosholz for synthetic biology in photosynthesis research. J Exp Bot 71:
ED, Boyer KE (2022) Increasing the resilience of ecological restora- 2219–2225
tion to extreme climatic events. Front Ecol Environ 5: 310–318 Zhu X-G, Wang Y, Ort DR, Long SP (2012) e-photosynthesis: a
Zakzeski J, Bruijnincx PCA, Jongerius AL, Weckhuysen BM (2010) comprehensive dynamic mechanistic model of C3 photosynthesis:
The catalytic valorization of lignin for the production of renewable from light capture to sucrose synthesis. Plant Cell Environ 36:
chemicals. Chem Rev 110: 3552–3599 1711–1727
Zamani Babgohari M, Niazi A, Moghadam AA, Deihimi T, Zia MH, Ahmed I, Bailey EH, Lark RM, Young SD, Lowe NM, Joy
Ebrahimie E (2013) Genome-wide analysis of key salinity-tolerance EJM, Wilson L, Zaman M, Broadley MR (2020) Site-specific fac-
transporter (HKT1; 5) in wheat and wild wheat relatives (A and D tors influence the field performance of a Zn-biofortified wheat va-
genomes). In Vitro Cellular Dev Biol-Plant 49: 97–106 riety. Front Sustain Food Syst 4: 135
Zeng J, Yoo CG, Wang F, Pan X, Vermerris W, Tong Z (2015) Ziegler RS (2007) Foreward. In JE Sheehy, PL Mitchell, B Hardy, eds,
Biomimetic Fenton-catalyzed lignin depolymerization to high-value Charting new pathways to C4 rice, International Rice Research
aromatics and dicarboxylic acids. ChemSusChem 8: 861–871 Institute, Los Ban~os, Phillipines, pp. 422
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023
66 | THE PLANT CELL 2023: 35; 24–66 Eckardt et al.
Ziegler G, Nelson R, Granada S, Krishnan HB, Gillman JD, Baxter production by active selection to rising atmospheric carbon diox-
I (2018) Genomewide association study of ionomic traits on di- ide. Proc R Soc B: Biol Sci 279: 4097–4105
verse soybean populations from germplasm collections. Plant Zomer RJ, Bossio DA, Sommer R, Verchot LV (2017) Global seques-
Direct 2: e00033 tration potential of increased organic carbon in cropland soils. Sci
Zin NA, Badaluddin NA (2020) Biological functions of Trichoderma Rep 7: 15554
spp. for agriculture applications. Ann Agric Sci 65: 168–178 Zsögön A, Cermák T, Naves E, Notini MM, Edel KH, Weinl S,
Ziska LH, Bunce JA (1998) The influence of increasing growth Freschi L, Voytas DF, Kudla J, Peres LEP (2018) De novo domes-
temperature and CO2 concentration on the ratio of respiration to tication of wild tomato using genome editing. Nat Biotechnol 36:
photosynthesis in soybean seedlings. Global Change Biol 4: 637–643 1211–1216
Ziska LH, Bunce JA, Shimono H, Gealy DR, Baker JT, Newton PC, Zsögön A, Peres LEP, Xiao Y, Yan J, Fernie AR (2022) Enhancing
Reynolds MP, Jagadish KS, Zhu C, Howden M, et al. (2012) Food crop diversity for food security in the face of climate uncertainty.
security and climate change: on the potential to adapt global crop Plant J 109: 402–414\\
Downloaded from https://academic.oup.com/plcell/article/35/1/24/6759373 by International Rice Research Institute user on 04 January 2023