www.nature.com/hdy
REVIEW ARTICLE OPEN
Progenitor species hold untapped diversity for potential
climate-responsive traits for use in wheat breeding and crop
improvement
Fiona J. Leigh 1, Tally I. C. Wright 1, Richard A. Horsnell 1, Sarah Dyer 1,2 and Alison R. Bentley 1,3✉
© The Author(s) 2022
Climate change will have numerous impacts on crop production worldwide necessitating a broadening of the germplasm base
required to source and incorporate novel traits. Major variation exists in crop progenitor species for seasonal adaptation,
photosynthetic characteristics, and root system architecture. Wheat is crucial for securing future food and nutrition security and its
evolutionary history and progenitor diversity offer opportunities to mine favourable functional variation in the primary gene pool.
Here we provide a review of the status of characterisation of wheat progenitor variation and the potential to use this knowledge to
inform the use of variation in other cereal crops. Although significant knowledge of progenitor variation has been generated, we
make recommendations for further work required to systematically characterise underlying genetics and physiological mechanisms
and propose steps for effective use in breeding. This will enable targeted exploitation of useful variation, supported by the growing
portfolio of genomics and accelerated breeding approaches. The knowledge and approaches generated are also likely to be useful
across wider crop improvement.
Heredity (2022) 128:291–303; https://doi.org/10.1038/s41437-022-00527-z
INTRODUCTION cultivars with enhanced resilience to environmental changes in
Modern crop breeding involving targeted crossing and selection order to secure future food security.
has led to the development of elite, high yielding cultivars. The
genetic components of yield have been improved through constant Expanding the wheat gene pool
selection for desirable traits, initially in landraces and early varieties Hexaploid wheat (Triticum aestivum) arose through a limited
and then through trait driven plant breeding (Fradgley et al. 2019). number of hybridisation events between a domesticated form of
In wheat, the positive impact of this is exemplified by the the tetraploid wild emmer wheat, Triticum turgidum ssp dicoc-
introduction of semi-dwarfing genes contributing to large increases coides (AABB) and Aegilops tauschii (DD) around 10,000 years ago
in yield potential during the so-called Green Revolution (Borlaug (McFadden and Sears 1946; Cox 1997; Petersen et al. 2006). An
1968). In addition to genetic improvement, agronomic potential is intermediate, hulled hexaploid is proposed by Kerber and
strongly influenced by the environment. Environmental adaptation, Rowland (1974) though this is not supported by the archae-
through direct breeding and selection, allows for optimisation of ological record (Feldman 2001). As bread wheat spread, the crop
yield within the seasonal constraints of a given region (Worland and became adapted to local conditions through selection and the
Snape 2001), control of biotic stresses including pests and diseases resulting distinct, locally adapted wheats are known as landraces
(either via crop management or the deployment of disease (Camacho Villa et al. 2005; Jones et al. 2012). Landraces of
resistance genes) and targeting of abiotic response, for example hexaploid wheat have long been used for wheat improvement
to available water (Reynolds et al. 2007), applied fertiliser and are a reservoir of readily available diversity that can be
(Swarbreck et al. 2019) and other production-limiting stresses. The introduced into breeding programmes with relative ease (Wingen
quest to optimise both genetic potential and environmental et al. 2014). Domestication and subsequent selection have created
response for a range of crop production regions around the world bottlenecks, reducing genetic diversity in all cultivated wheat
is being enhanced by the array of genetic and bioinformatics tools species derived from wild emmer wheat including pasta or durum
now available (Adamski et al. 2020). wheat (T. turgidum ssp. durum) and bread wheat (Tanksley and
Climate is the driver of environmental change with an impact McCouch 1997; Lopes et al. 2015). Some of this diversity may be
for crop production capacity (Rosenzweig et al. 2008). Global reintroduced to bread wheat by interrogating progenitor species
climate change creates an urgency for the development of for functional variation in target traits.
1The John Bingham Laboratory, NIAB, 93 Lawrence Weaver Road, Cambridge CB3 0LE, UK. 2Present address: European Molecular Biology Laboratory, European Bioinformatics
Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK. 3Present address: International Maize and Wheat Improvement Center (CIMMYT), Texcoco,
Mexico. Associate editor: Frank Hailer. ✉email: a.bentley@cgiar.org
Received: 30 December 2020 Revised: 13 March 2022 Accepted: 15 March 2022
Published online: 5 April 2022
1234567890();,:
F.J. Leigh et al.
292
Tetraploid (AABB) wild emmer wheat has a modern-day range tracking of these introgressions (Przewieslik-Allen et al. 2019; King
that spans the western Fertile Crescent, southeastern Turkey, and et al. 2017, 2019). Such marker systems are likely to facilitate
the mountainous regions of eastern Iraq and western Iran. enhanced and targeted deployment of diversity from wild
Tetraploid wheats related to wild emmer include emmer wheat relatives in breeding programmes in the future.
(T. turgidum ssp. dicoccum), a domesticated tetraploid wheat that Climate change is predicted to increase the frequency and
was widely cultivated prior to the adoption of hexaploid wheat intensity of abiotic stress events and their impacts on wheat
(Salamini et al. 2002), and durum wheat which is widely cultivated, productivity (Lopes et al. 2015). Here we review the potential for
predominantly within the Mediterranean Rim (Martínez-Moreno further detailed interrogation of adaptive and physiological
et al. 2020). Tetraploid wheats are readily crossable with hexaploid variation in wheat’s progenitor species. Work to date has focussed
wheat and allelic diversity from tetraploid donors or ‘tetraploid primarily on biotic stresses but there is evidence to support the
derived alleles’ can be introgressed via direct crossing and usefulness of progenitor species for introducing targeted variation
backcrossing (Ullah et al. 2018). for optimising responses to changing climates. Our review
The diploid progenitor species Ae. tauschii (DD) is part of the demonstrates that there is a gap in the systematic characterisation
large Aegilops genus (van Slageren 1994) that includes at least 10 of progenitor variation specifically for responses to abiotic stress
diploid and 12 polyploid species (Matsuoka et al. 2015). Many (up including seasonal adaptation, physiological response, and root
to 14; reviewed by Schneider et al. 2008) Aegilops species have system architecture (RSA). Further understanding the genetic and
been used in wheat crossing programmes although most species physiological basis of these responses will support future targeted
in the genus are challenging to introgress due to issues with use of progenitor variation for mobilisation into wheat breeding.
chromosome pairing. This limitation does not exist with Ae.
tauschii that is characterised as the specific wheat D-genome
donor (Kihara 1944, McFadden and Sears 1946) and it has been PROGENITOR SPECIES PROVIDE ADDITIONAL VARIATION FOR
frequently used for introgression into hexaploid wheat because FLOWERING TIME AND ADAPTIVE RESPONSE
there is little inhibition of meiotic chromosome pairing between If heat or drought stress occurs during grain filling, abortion of
D-genome chromosomes (Kishii 2019). The distribution of Ae. tillers and/or lower kernel weight reduces wheat yield (reviewed
tauschii centres on a region to the south of the Caspian Sea and by Fleury et al. 2010 and Ni et al. 2018). The manipulation of
into Azerbaijan. The species range spreads eastward, to Pakistan flowering time can shift grain production away from risk periods,
and western China, via the Kopet Dag Mountains of Turkmenistan, thereby providing an escape strategy. Research undertaken in
and westward, to central Syria, via the valleys of southeastern both Arabidopsis and agronomically important grasses (maize, rice
Turkey (van Slageren 1994). Although the genus and specific and wheat) over the past 20 years has revealed that floral
species have a wide geographical range, the genetic diversity of transition is controlled by complex overlapping genetic pathways
hexaploid wheat’s D-genome is severely limited because of the (reviewed by Cockram et al. 2007; Colasanti and Coneva 2009).
small number of polyploidisation events that gave rise to it (Giles Wheat is a long-day species in which floral initiation is accelerated
and Brown 2006). Collections and populations of Ae. tauschii have by exposure to lengthening days. Although the underlying
been used to identify useful genes for specific traits, many of genetics of flowering are complex (reviewed by Hyles et al.
which are disease-related (recently reviewed by Kishii 2019) 2020), manipulation of the major vernalisation and photoperiod
including resistance genes for foliar pathogens and insect pests response genes are widely used in wheat breeding programmes
(Gaurav et al. 2021). to provide adaption to agroeconomic environments (Bentley et al.
Whilst direct hexaploid × Ae. tauschii crossing has been 2011).
documented, Ae. tauschii is predominantly captured via the Adaption in terms of phenology is a powerful tool, particularly
creation of synthetic allohexaploids made by chromosome in marginal environments. Since the 1990s, 25% of reported global
doubling of triploid hybrids from an inter-specific AABB × DD wheat yield improvement has come from wheat grown in
cross (also called synthetic wheats or synthetic hexaploid wheats marginal environments due to breeding for wide adaption
(SHW); Dreisigacker et al. 2008; Mujeeb-Kazi et al. 2013). These can (Lantican et al. 2005). Marginal environments and the necessity
be used to introduce diversity from either or both the tetraploid or to mitigate climate-based yield impacts are likely to become more
diploid donor. Synthetic wheats have been used for breeding to prominent under a climate change scenario. Climate change is
increase diversity (Dreisigacker et al. 2008; Li et al. 2014a), for also likely to have impacts on crop production in temperate and
adaption (Li et al. 2014a), disease resistance (Ogbonnaya et al. cold regions of the world where flowering is a function of both
2008) and yield improvement (Jafarzadeh et al. 2016). The creation winter cold and spring heat (Yu et al. 2010). Temperate cereals
of octoploid (AABBDDDD) synthetics has also been reported grow across a wide range of semi-arid environments but show
(Chèvre et al. 1989), as have synthetic amphiploids created using marked reductions in productivity (Reynolds et al. 2010) and yield
introgressions with other wheat species such as Ae. crassa, Ae. (Lobell and Field 2007) at high temperatures. Increased tempera-
cylindrica and Ae. ventricosa (Mirzaghaderi et al. 2020). These tures in winter may delay fulfilment of vernalisation requirement
however have not typically been used for downstream breeding (a prolonged period of cold, non-freezing, temperatures required
applications due to the complexities of ploidy, recombination and for subsequent competence to flower) resulting in later flowering,
tracking introgression segments. although increased spring temperatures could mask or offset this
Ancestral wheat species such as Triticum urartu (the AA genome (Yu et al. 2010). In areas of high latitude and altitude the effect
donor of bread wheat) and members of the Aegilops tribe could be exacerbated, as plants in these regions are particularly
including Ae. speltioides (a relative of the BB genome donor) offer a sensitive to temperature cues. Vernalisation in wheat is controlled
wealth of diversity in agronomically important traits such as by the major Vrn-1 locus (Dubcovsky et al. 1998) with the
disease resistance (Rowland and Kerber 1974). Many of these additional Vrn-2 and Vrn-3 loci also contributing to variation
species do not cross readily with bread wheat due to the presence (Yoshida et al. 2010). Hexaploid wheat has three homoeologous
of Ph1 genes preventing recombination between chromosomes Vrn-1 loci (denoted -A1, -B1 and -D1) located on group 5
(Sears 1977). Instead, a wheat line carrying a mutant allele of ph1 chromosomes. Dominant alleles confer a spring growth habit
may be used to induce bread wheat and ancestor homoeologous meaning that a cold period is not required for induction of
recombination (Rey et al. 2017). The resulting lines carry large flowering.
introgressions and development of high-throughput single- Natural plant populations often have wide flowering time
nucleotide polymorphism (SNP)-based marker systems designed variation (Grazzani et al. 2003) and therefore progenitor species
to screen wild relative species has facilitated rapid validation and offer potential functional genetic variation for fine-tuning adaptive
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
293
response. In hexaploid wheat, the photoperiod response Ppd-1 in Vrn-D1 dominant alleles in hexaploid wheat, indicating that the
loci are a homoallelic series on group 2 chromosomes (Worland loss of vernalisation requirement in the progenitor and domes-
and Snape 2001; Beales et al. 2007; Bentley et al. 2011). In ticated forms of wheat occurred separately, but followed a similar
tetraploid (AABB) wheat Wilhelm et al. (2009) described two mutational event (Takumi et al. 2011). Understanding the
mutations of the Ppd-A1 gene leading to photoperiod insensitivity vernalisation response and the interactions between Vrn-1 and
(PI) and early flowering. These effects have also been confirmed in other genes (e.g., the floral repressors Vrn-2), particularly at high
hexaploid and SHW (Bentley et al. 2011). However, screening of temperatures will be important for future resilience breeding.
ancestral tetraploids (T. dicoccoides (n= 122) and T. dicoccum (n= Dixon et al. (2019) demonstrate that diverse material can
276)) for these mutant Ppd-A1a alleles revealed no variation, provide variants of many of these genes and that understanding
suggesting that these are photoperiod sensitive species, and that their interactions can potentially facilitate their use for incorporat-
insensitivity arose post-domestication, being first observed in T. ing resilience to temperature fluctuations. Overall, although
durum landrace accessions as well as in collections from southern significant variation has been reported for adaptive response in
Europe (Italy, Spain, France), North Africa and North America wheat progenitor species, gaps exist in deployment into breeding.
(Bentley et al. 2011). We propose that this is due to two main factors: the lack of
Diversity in flowering time has been further characterised by resolution available for genetic trait dissection in wild progenitors
several studies in tetraploids wheats (Nishimura et al. 2018; Wright and the confounding effects of genotype × environment. Many of
et al. 2020; Würschum et al. 2019). Alleles of the Ppd-A1 associated the alleles or QTLs described from progenitor species to date have
with early flowering (but distinct from the Ppd-A1a alleles not been genetically resolved and many co-locate in forward
described by Wilhelm et al. 2009) were detected in emmer wheat genetic studies. The availability of sequenced progenitor collec-
by Nishimura et al. (2018) who also identified an early heading tions (e.g., Gaurav et al. 2021) is likely to improve the resolution of
date QTL associated with Vrn-A3. This QTL was found to be a cis- novel alleles from progenitors, thereby enabling their rapid
element GATA box in Vrn-A3 (located on chromosome 7AS), which extraction and validation. This will also likely address the other
suppressed the late-flowering (photoperiod sensitive) Ppd-A1b current limitation in separating the confounding effects of
allele (Nishimura et al. 2018). A QTL controlling flowering time was environment and masking effects of interacting loci. Overlapping
also reported on 7B linked to Vrn-B3 in an emmer mapping flowering time pathways introduce functional redundancy,
population (Wright et al. 2020). Takenaka and Kawahara (2012) particularly in hexaploid wheat, and they are influenced by
identified novel loss of function alleles in tetraploid Ppd-A1 in multiple environmental factors. Therefore, the priority require-
emmer wheat that do not confer PI but may induce small ment for extraction of useful functional adaptive trait variation
variations in flowering time. from progenitors is rapid and accurate assaying, extraction and
Compared with work in tetraploid progenitors, little is currently validation of variants to enable quantification of phenotypic
known about the diversity of flowering time response in the effects independent of genetic background and environmental
diploid wheat progenitor Ae. tauschii. Matsouka et al. (2008) effects.
assessed natural flowering time variation in a collection of 200
accessions representing the latitudinal range (30°N–45°N) of the
species. Flowering time phenotypes could be divided into early-, NOVEL PHYSIOLOGICAL TRAITS CAN POTENTIALLY BE MINED
intermediate- and late-flowering groups that enabled detection of FROM PROGENITOR SPECIES
geographical patterns: with early-flowering lines being dominant Cultivars bred for high yield potential under optimal conditions
in southern regions compared to late-flowering lines in northern typically maintain performance in moderately stressful environ-
regions. However, the impacts of environmental differences varied ments (Richards et al. 2002; Foulkes and Reynolds 2015; Voss-Fels
between the western and eastern parts of the species range et al. 2019). The yield potential of a crop can be simplified to a
preventing a clear attribution of genetic effects (Matsouka et al. function of light interception (LI), harvest index (HI) and radiation
2008). use efficiency (RUE, Reynolds et al. 2009). Progression in crop
Range expansion occurs when species adapt beyond native breeding has brought HI and LI close to theoretical maximum
habitats and has been documented for Ae. tauschii associated with (Long et al. 2006) indicating that selection for improved RUE may
shifts in phenology and seed production ability (Matsuoka et al. be the most rewarding opportunity for breeders to increase yield
2015). Of the species within the Aegilops genus, Ae. tauschii is the potential. RUE is effectively the slope of correlation between dry
only diploid species to have expanded its range east and matter content at harvest and total intercepted radiation (Murchie
Matsuoka et al. (2015) suggest that early flowering at least et al. 2009). Optimising RUE is key to utilising available resources
partially explains range expansion into Asia. Further work by when breeding for variable or resource-limited environments.
Koyama et al. (2018) used a F2-based QTL mapping approach to Thus, enhancing crop canopy photosynthesis is an important
determine genetic differences between photoperiod sensitive and breeding target and progenitor species may offer novel physio-
insensitive lines. This allowed for mapping of a QTL locus on 5DL logical variation that can be exploited in breeding.
for heading under short days, proximal to the Vrn-D1 locus, along Crop photosynthesis is a complex process, consisting of
with three QTLs (one on 4D, two on 7D) for flowering under field dynamic networks from the molecular to canopy level (Fig. 1).
conditions. Quantitative variation for vernalisation was also When considering CO2 assimilation expressed on a standardised
observed in Ae. tauschii accessions (Koyama et al. 2018). leaf area basis (A), there are numerous morphological and
Golovnina et al. (2010) identified spring variants of Ae. tauschii biochemical traits underpinning performance. Past experiments
including a recessive Vrn-D1 allele. Vernalisation-insensitive have highlighted that wheat progenitors harbour higher A than
accessions of the species have been previously described in hexaploid wheat cultivars (Evans and Dunstone 1970; Austin et al.
germplasm originating from Pakistan and Afghanistan (Tanaka 1982). Since domestication, due to selection programmes for
and Yamashita 1957; Tsunewaki 1966) but there is little evidence other agronomic traits, there has been limited historic selection
for the use of derived alleles in breeding. Takumi et al. (2011) used pressure from breeders on leaf photosynthetic capacity (Driever
211 accessions collected across the Ae. tauschii habitat range to et al. 2014). If progenitor diversity can be captured to target a
assess flowering in the absence of vernalisation. Sequencing of single aspect of the process of photosynthesis giving a moderate
the Vrn-D1 locus and haplotype analysis revealed distinct variation increase in flag leaf A of modern wheat then, as the canopy
in Ae. tauschii, including a large deletion leading to a loss of carbon fixation is an integrated process multiplied over the entire
vernalisation requirement (Takumi et al. 2011). The authors growing season there could be consequential overall improve-
however conclude that this deletion is discreet from mutations ments in RUE and yield (Parry et al. 2011). To harness diversity
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
294
Fig. 1 A schematic showing key targets for photosynthetic improvement where diversity from wild relatives could be utilised to increase
productivity or stress tolerance in modern wheat. The flag leaf cross-section highlights important traits underpinning CO2 assimilation on a
standardised leaf area basis. When considering photosynthesis on a plant or canopy basis, other targets for improvement include organ size,
ear photosynthesis and CO2 assimilation across the whole canopy.
from wild relatives, components driving high A need to be environmental stress conditions in India and Bangladesh. Aus-
identified to facilitate their use in targeted genetic dissection, type rice has been shown to be a valuable source of novel
direct use in pre-breeding and future application in wheat diversity; varieties developed from this material have been shown
breeding using marker- and phenotypic-based screening to be highly tolerant of drought (Henry et al. 2011) and heat stress
methods. (Li et al. 2015). A range of physiologies underpins such adaptation
The determinants of A (Fig. 1), and thus potential targets for including increased rooting depth and lateral root formation
improvement, include components that govern the rate of resulting in increased water uptake, thus reduced canopy
delivery of CO2 to the sites of carboxylation; the availability of temperature prevented stomatal closure and prolonged photo-
products from photochemical reactions; and downstream synthetic activity in the drought-tolerant rice lines (Henry et al.
enzyme-regulated mechanisms of the Calvin–Benson cycle. Within 2011). In combination, heat and drought stress have a negative
these components, superior characteristics found in progenitors additive effect on many aspects of wheat plant physiology
can be targeted to improve either photosynthetic productivity or (reviewed by Tricker et al. 2018), and identifying a suite of
tolerance under environmental stress in modern cultivars (e.g., tolerance traits pertaining to a fine balance of gas exchange, WUE
Merchuk-Ovnat et al. 2016a, b). and assimilation from wild relatives is a breeding target in order to
The delivery of CO2 to the sites of carboxylation is governed by maintain yield under combined stresses.
several diffusive boundaries, particularly those imposed by the leaf Another diffusive boundary that acts as a limitation to A is the
stomata. When stomata are closed, water loss is minimal, but the diffusion of CO2 across the mesophyll (gm, Fig. 1). This boundary is
closed pores act as the sole limitation to carbon fixation (Farquhar governed by mesophyll anatomical or biochemical features (Evans
et al. 1982). Therefore, there is a fundamental trade-off between et al. 2009; Flexas et al. 2012). There has been limited investigation
the flux of CO2 entering the leaf and flux of H2O exiting (Lawson of how gm varies across wheat ploidy levels. The grasses are
and Blatt 2014). The proportion of CO2 gained in relation to H2O generally considered to have comparatively high gm (Flexas et al.
transpired is termed instantaneous water use efficiency (WUE) 2012), which may have decreased through the domestication
(Farquhar and Richards 1984). Wheat progenitors have been process, as negative correlations have been observed with gm and
shown to maintain higher instantaneous WUE in drought-prone potentially desirable traits such as leaf mass area (Gu et al. 2012).
conditions compared to hexaploid wheat (Li et al. 2017). Mesophyll cell size is thought to have increased across wheat
Furthermore, Merchuk-Ovnat et al. (2016a) found that introgres- ploidy, with ancestral species possessing smaller cells (Dunstone
sions from T. dicocciodes into hexaploid wheat were linked to and Evans 1974; Wilson et al. 2021). Smaller mesophyll cells may
greater grain yield under drought. Plants originating from drier facilitate higher gm due to an increased surface area for gas
climates, such as wild relatives, would require increased hydraulic exchange (Lundgren and Fleming 2020). Further work is required
supply to the leaves to maintain photosynthesis under increased to establish if the comparatively high rates of A found within
evaporative loss (Scoffoni et al. 2016). Austin et al. (1982) found progenitor species are driven by higher gm.
higher stomatal and vein densities in tetraploid wheat flag leaves Improved photochemistry is another trait targeted for improve-
compared to hexaploid varieties, which could reflect a strategy for ment (Fig. 1). In a large wheat wild relative comparison using
maintaining A in drought-prone environments. An alternative 41 species, McAusland et al. (2020) identified accessions that
strategy could aim to reduce stomal density to minimise water outperformed modern varieties in traits linked to photochemistry,
loss and improve drought tolerance (Hughes et al. 2017). As including T. dicoccoides and lines from the Amblyopyrum and
variation in leaf stomatal density and size has been observed Aegilops genera that demonstrated high Photosystem II (PSII)
across wheat ploidy levels (Dunstone et al. 1973; Khazaei et al. operating efficiency or electron transport. They hypothesised that
2009), wild relatives could be a genetic reserve for optimising the high rates of maximum electron transport and carboxylation
balance between CO2 and water loss depending on the targeted resulted in high photosynthetic capacity in some wild relative
breeding environment. accessions. An introgression from wild emmer into bread wheat
In rice, a distinct group of landraces known as aus-type rice has also been linked to improved electron transport rate during
(McNally et al. 2009) evolved and were cultivated under booting (Merchuk-Ovnat et al. 2016b). Under high light intensity,
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
295
not all captured energy is utilised in photochemistry and plants progenitors) to screen for genotypes that show a deviation from
have developed mechanisms for dissipating possibly detrimental the negative correlation between leaf area and A. As a first step,
excess energy through photoprotection (Demmig-Adams and segregating pre-breeding material could be used to extract
Adams 1992). This protection process is termed nonphotochem- extreme individuals based on leaf area and used either for
ical quenching (NPQ). When the leaf is returned to lower light reciprocal recurrent selection or for bulk segregant analysis to
intensities, the time required for the relaxation of NPQ is a limit to move forwards the genetic understanding of the link between A
crop productivity (Kromdijk et al. 2016). Improved RUE and and leaf area.
photosynthetic efficiency have been achieved through manipula- Long et al. (2006) outlined that the efficiency of the canopy to
tion of the NPQ process through genetic engineering (see: intercept light is controlled by canopy characteristics linked to
Kromdijk et al. 2016; Hubbart et al. 2018). However, while there size, architecture, longevity, speed of development and closure.
has been promising diversity observed in NPQ kinetics in diverse Successful breeding efforts across recent decades have limited
relatives of wheat (McAusland et al. 2020), the degree to which opportunities for improvements in canopy LI efficiency (Zhu et al.
natural variation could be exploited from wild ancestors still needs 2010). Furthermore, canopy architecture has been optimised
to be determined. through domestication (Li et al. 2014b), suggesting wild ancestors
The determinants, and limitations, imposed at the sites of may not be a useful source of variation. Canopy conditions are
carboxylation relate to the enzyme-regulated mechanisms of the very heterogeneous, particularly in terms of light distribution
Calvin–Benson cycle (Fig. 1). Johnson et al. (1987) concluded that a (Horton 2000). A crop canopy that responds quickly to these
higher capacity for mesophyll photosynthesis may be linked to changes will be more efficient in maximising resource capture
variation in CO2 assimilation across wheat ploidy. Demand for CO2 (Taylor and Long 2017). Fast photosynthetic and photoprotection
is restricted by the carboxylation and oxygenation activities of the induction has been observed in wild rice accessions (Acevedo‐
enzyme Rubisco (Farquhar et al. 1980), the capacity and efficiency Siaca et al. 2021) and in wild wheat relatives (McAusland et al.
of this enzyme is a major bottleneck in raising wheat yields (Parry 2020), respectively. Incorporating these faster light transition
et al. 2011). Prins et al. (2016) demonstrated the superior Rubisco responses into modern wheat could be an objective for improving
catalytic properties of several wheat genotypes (including resource capture. Targeting earlier photosynthetic improvement
progenitors) compared to the modern wheat variety Cadenza before canopy closure is another potential route for improvement,
when assessed across different temperatures. Scafaro et al. (2012) as pre-anthesis photosynthesis is known to correlate with grain
found a wild relative of rice maintained a higher activation state of yield (Gaju et al. 2016; Carmo-Silva et al. 2017). Gaju et al. (2016)
Rubisco under higher temperatures compared to domesticated found at a pre-anthesis growth stage (during the onset of stem
rice, which was linked to the high heat tolerance of the wild extension) a synthetic-derived hexaploid genotype maintained
relative. Progenitors of wheat, originating from warmer climates, higher A than its recurrent hexaploid parent.
may also possess superior Rubisco kinetics, which could be utilised Taken together, there is good evidence to support the need for
in breeding for marginal environments; this requires further further characterisation of the component traits underpinning
systematic characterisation. Rubisco is also responsible for photosynthesis in wheat progenitors. Although much of the trait
catalysing the oxygenation of ribulose 1,5-bisphosphate. Photo- variation described is likely to be quantitatively controlled, there is
respiration is the energetically expensive process of converting an opportunity to identify specific progenitor accessions for direct
the by-products of the oxygenation reaction and is a significant use as donors in physiological pre-breeding. In addition, the
constraint on wheat productivity (Long et al. 2006; Parry et al. development of protocols and tools for rapid screening of these
2011). physiological traits will enhance future genetic dissection. At
In tobacco, South et al. (2019) showed that genetic engineering present most methods require detailed experimentation and
of pathways linked to photorespiration produced promising specialist equipment so the development of predictive phenotyp-
improvements to biomass production and photosynthetic effi- ing tools also offers promise to enable accurate forward genetic
ciency. Yield penalties linked to photorespiration may lesson studies to discover trait-linked markers, and the selection of
under future predicted climates but will still remain important favourable variants in marker-assisted breeding. This is likely to
(Walker et al. 2016). While the most promising gains in improving yield significant benefits for breeding offering new potential to
photorespiration losses may be through genetic engineering transfer higher WUE for drought tolerance or increased A from
routes, targeting superior Rubisco characteristics from relatives progenitor species.
could hold promise, such as selection for the Rubisco specificity Another strand of potential variation for further investigation
factor that may be higher in plants from drier environments towards application is the photosynthetic potential of reproduc-
(Galmés et al. 2005). Natural sources of variation in Rubisco tive tissues in progenitor species (Fig. 1). Ear photosynthesis is
kinetics (e.g., Prins et al. 2016) may be a more readily available tool heritable, varies across different wheat genotypes and is an
for breeders to utilise in ongoing selection programmes compared important determinant of grain yield (Molero and Reynolds 2020),
to genetic engineering routes. highlighting the importance of ear photosynthesis as a breeding
Targeting photosynthetic improvement should also be con- target. Li et al. (2017) found that ears of T. dicoccoides maintained
sidered on both a leaf and canopy basis (Fig. 1). When considering higher CO2 assimilation during grain-filling when compared to
CO2 capture on a per leaf basis, the total organ surface area and hexaploid wheat, along with higher WUE under drought stress.
thickness are key components. The smaller leaf area typical of Progenitor wheat species, particularly tetraploids, typically have a
progenitor species (Evans and Dunstone 1970) may have more larger awn surface area than hexaploid wheat (Blum 1985). As a
concentrated photosynthetic capacity (Long et al. 2006). McAus- photosynthetic organ, awns have been reported to have high
land et al. (2020) found that the thicker and narrower leaves found instantaneous WUE (Blum 1985; Weyhrich et al. 1995) potentially
in wild relatives underpinned a higher maximum carboxylation explaining why in a drought-prone environment, the presence of
rate, which was also supported by the observed negative awns is reported to be beneficial to grain yield (Evans et al. 1972).
relationship between specific leaf area and photosynthetic Other components of the ear may also harbour useful stress
capacity. Furthermore, leaf surface area and A are typically tolerance characteristics, Araus et al. (1993) found that WUE was
negatively correlated (Evans and Dunstone 1970; Austin et al. 33% higher in the ear bracts compared to the leaf blade using
1982) and a major challenge in utilising photosynthetic diversity carbon isotope analysis, linking the higher efficiency to a lower gs
from wild relatives will be transferring high A found in progenitor and the xeromorphic features of the ear bracts (glumes, paleas
lines into a larger flag leaf typical of modern wheat. This could be and lemnas). Under heat stress, positive correlations have been
addressed by using existing pre-breeding material (derived from observed between grain yield and the contribution of ear
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
296
photosynthesis to grain yield (Molero and Reynolds 2020). systems in this population. However, Christopher et al. (2013)
Progenitors originating from drier and hotter environments may found no co-segregation of root traits with dwarfing genes and
possess strategies, such as high ear CO2 fixation linked to the most studies agree that root and shoot development are under
preservation of photosynthesis under unfavourable conditions the control of different sets of loci (Iannucci et al. 2017). QTL
and these could become increasingly useful for adapting modern clusters for root morphology traits have also been reported to
wheat to more marginal environments. coincide with those for thousand grain weight and yield
Although little data exist on the quantitative differences in ear (Maccaferri et al. 2008; Iannucci et al. 2017) but further work is
photosynthesis in wheat progenitors, and their relative contribu- required to resolve these interactions. El Hassouni et al. (2018)
tions under stress, further work is warranted. As breeders seek to found that in trials with low water availability, durum accessions
incorporate additional diversity into their programmes, the with deep roots achieved a 37–38% yield increase but suffered a
selection of progenitor donors with high ear CO2 fixation could 20–40% yield penalty in irrigated environments.
be prioritised. Further evidence is required to confirm the Previous work has shown yield and biomass increases in
consistency of photosynthetic contributions from the presence synthetic-derived wheat lines can be attributed to a greater
of awns. If consistently higher photosynthetic capacity can be proportion of deep roots (Reynolds et al. 2007). Becker et al. (2016)
demonstrated without reducing photosynthetic activity in other also demonstrated that increased rooting depth and fine root
parts of the plant, then this trait can be readily incorporated as a mass allowed for the maintenance of plant growth under drought
breeding target due to the additional benefit and ease of stress in two synthetic wheat lines, thus maintaining yields.
phenotypic and genotypic selection. In many regions, awned However, a third synthetic line lacked deep roots but tolerated
wheat varieties predominate making it likely this benefit is already drought stress through increased stomatal density and reduced
present and fixed, but it could also be applied where awned stomatal aperture (Becker et al. 2016). Recently Liu et al. (2020)
varieties are not widespread, and/or to prioritise selections within detected eight QTL associated with drought tolerance in a SHW ×
segregating pre-breeding material derived from progenitors. commercial wheat F2 population with most of the positive alleles
attributable to the Ae. tauschii (four QTLs) or tetraploid (durum;
two QTLs) components of the synthetic. Ober et al. (2021)
PROGENITOR SPECIES ARE A SOURCE OF NEW ROOT SYSTEM reviewed the range of wheat trait variation reported in wheat as
ARCHITECTURE IDEOTYPES well as summarised available evidence linking deeper roots to
RSA plays a pivotal role in drought tolerance and nutrient access to soil moisture.
acquisition and enhancing root systems is a target for improving Understanding the RSA diversity available in the wheat gene
climate resilience (recently reviewed by Ober et al. 2021). Deeper pool will allow the selection of targeted root types to suit
roots can extract more water from subsoils, particularly during late environmental conditions such as drought or waterlogging, and
developmental stages and grain fill, thereby improving yield in nutrient availability. This remains a medium- to long-term
water limiting environments (Manschadi et al. 2010). However, the breeding objective as there is still relatively little known about
characterisation of mature RSA in wheat can be time consuming the heritability, environmental and management independence of
making it difficult to use as a selection target in breeding (Richard RSA in elite cultivars (Fradgley et al. 2020). As highlighted by Ober
et al. 2015). Techniques that use early rooting traits (seminal root et al. (2021) many upstream research questions remain including
angle and seminal root number, e.g., the clear pot system the mechanisms by which architectural traits impact water and
developed by Richard et al. 2015) or root crowns extracted from nutrient acquisition. In addition, there remains a gap in under-
the field at maturity (e.g., using the shovelomics method adapted standing the linkage and direction of interactions between root
from maize (Trachsel et al. 2011)) can be used to infer wheat RSA and agronomic/crop production traits, and their environmental
(Fradgley et al. 2020). A ‘pasta strainer’ technique described by El dependencies. Progenitor species typically have a wide eco-
Hassouni et al. (2018) allows characterisation of the mature root geographical adaption range, and it is proposed that this is likely
system when grown within a perforated basket submerged in the to confer functional RSA variation. Whilst surveying large
field. All these tools allow RSA of genotypes to be characterised collections of progenitors for RSA variation is possible, more rapid
into wide or narrow/deep rooting types. progress is likely through the identification of pre-breeding
Wheat progenitor species may be used to augment the diversity material (capturing progenitor variation) with contrasting root
in RSA that exists in the bread wheat gene pool. Tetraploid wheats types and comprehensive analysis of the linkages between trait
have been shown to offer RSA diversity; using recombinant inbred variation and root functions. As for photosynthetic traits, high-
lines of durum × wild emmer, QTLs for drought resistance and throughput screening methods that can be scaled and applied for
related traits were mapped (Peleg et al. 2009). Marker-assisted forward genetic screens and MAS are likely to accelerate progress
selection (MAS) enabled the QTL regions to be introgressed into in exploiting progenitor variation for RSA.
both durum and hexaploid wheat (Merchuk-Ovnat et al. 2016a; b).
This produced one hexaploid wheat isogenic line with introgression
of a QTL from chromosome 7A of the wild emmer donor showing PROSPECTS FOR CLIMATE-RESPONSIVE BREEDING ACROSS
greater productivity (biomass, flag leaf area and grain yield) and CROP SPECIES
photosynthetic capacity than the recurrent parent when grown Major and minor crops worldwide are likely to face both new
under water limiting conditions. RSA was found to differ in this line, limitations and opportunities for maintaining and increasing
with greater development of deep roots and associated root tips productivity due to changing climates. The identification of useful
whilst under drought stress (Merchuk-Ovnat et al. 2016a). This RSA variation as described for wheat progenitor species and the
enhanced the plant’s ability to access water at a greater soil depth successful application of approaches to mobilise it into cultivated
and conferred greater drought tolerance as subsoil water levels are wheat can serve as an exemplar for other crops. In addition to
generally more stable than those in the upper layers of the soil. supporting productivity, this will also incentivise the search for
Iannucci et al. (2017) identified 17 QTLs relating to root and useful variation in their progenitors and wild relatives. Exploration of
shoot morphology in a durum × emmer wheat population, three progenitors or crop wild relatives has already begun in a variety of
of which were previously undescribed (two for the number of root crop species (e.g., legumes (Porch et al. 2013; Coyne et al. 2020)
tips and one for rooting depth). Root morphology QTL co- apples (Volk et al. 2015) and numerous others (reviewed in (Hajjar
segregated with the height reducing Rht-B1 gene on chromosome and Hodgkin 2007; Dempewolf et al. 2017)) to identify genomic
4B, indicating these alleles are involved in the control of both root regions linked to phenotypes of interest for both biotic and abiotic
and shoot traits, with tall plants having longer and larger root stresses. For major cereals such as rice and barley, there are already
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
297
Table 1. Monocot crops and their progenitor species or wild relatives that offer genetic diversity for targeted crop improvement.
Crop Progenitors Breeding priorities linked to References
climate stresses
Maize (Zea mays) Teosinte (Z. mays ssp. parviglumis) Drought, heat, waterlogging Mano and Omori 2013; Challinor et al.
2016
Rice (Oryza sativa) O. rufipogon Drought, heat, flooding, salinity, Zhang et al. 2006; Ishimaru et al. 2010;
C4 photosynthesis Covshoff and Hibberd 2012; Singh et al.
2021
Wheat (Triticum T. turgidum ssp dicoccoides and Drought, heat, C4 Covshoff and Hibberd 2012; Lopes et al.
aestivum) Aegilops tauschii photosynthesis 2015
Barley (Hordeum H. vulgare ssp. spontaneum Drought, heat, waterlogging, C4 Setter and Waters 2003; Talame et al.
vulgare) photosynthesis 2004; Covshoff and Hibberd 2012;
Weigmann et al. 2019
Sorghum (Sorghum S. bicolor subsp. verticilliflorum Cold, drought, heat Ananda et al. 2020
bicolor)
Pearl millet (Pennisetum P. glaucum subsp. monodii Drought and heat Sharma et al. 2020
glaucum)
Oats (Avena sativa) A. ventricosa, A. longiglumis, A. Cold, drought and heat, C4 Covshoff and Hibberd 2012; Ociepa 2019
insularis, A. canariensis and A. photosynthesis
agadiriana
Rye (Secale cereale) S. cereale subsp. vavilovii Drought and heat, C4 Covshoff and Hibberd 2012; Miedaner
photosynthesis and Laidig 2019
Finger millet (Eleusine E. coracana subsp. africana. Drought and salinity Mirza and Marla 2019
coracana)
examples of the successful introgression of traits linked to climate introduce traits of interest, the success rate varies between species
change adaptions such as drought tolerance (Talame et al. 2004; and becomes increasingly difficult with more distantly related
Zhang et al. 2006) and flowering traits (Ishimaru et al. 2010; species. There also remain barriers to using genomics-based
Wiegmann et al. 2019). For minor cereal grain crops there are few advances to accelerate the uptake of novel alleles. Linkage drag is
confirmed examples to date, e.g., sorghum (reviewed in (Ananda traditionally one of the major barriers to incorporating diversity
et al. 2020)), pearl millet (reviewed in (Sharma et al. 2020)), finger from progenitors. Here, unwanted genes are introgressed
millet (blast resistance (Akech et al. 2016)), oats (reviewed in (Ociepa simultaneously with a targeted region from a donor into the
2019)) and rye (plant height and yield (Falke et al. 2009)), indicating desired background. Backcross breeding is typically used to
that allocating resources to the exploration of diversity within increase the recurrent parent (background) genotype and reduce
progenitors and wild relatives would reveal further useful adapta- unwanted genes. This strategy can be complemented by MAS,
tions that could improve the resilience of these crops to changing allowing the selection of a specific trait based on a linked genetic
climates. Examples of monocot crops, their progenitor species and marker. MAS can be employed to facilitate more accurate
breeding priorities linked to changing climates are shown in Table 1. introgression from a progenitor donor and reduce linkage drag
Opportunities also exist to transfer desirable characteristics from from a wild background (Tanksley et al. 1989). This has been used
minor to major cereal grain crops. An avenue that holds much successfully to make introgressions from several wild relatives into
promise, along with numerous technical challenges, is the domesticated wheat (Nevo and Chen 2010; Merchuk-Ovnat et al.
incorporation of the C4 photosynthetic pathway, a characteristic of 2016a; King et al. 2017). Beyond linkage drag, other factors can
a C4 crop (e.g., sorghum or millet), into a C3 crop (e.g., rice or wheat). pose issues to capturing wild diversity. The merging of genomes
The C4 pathway utilises a carbon concentrating mechanism to across wheat species can lead to intergenomic gene suppression
diminish photorespiration, a process that takes place at the sites of (Feldman and Levy 2012). This phenomenon leads to the silencing
carboxylation that limits productivity in C3 crops. The C4 pathway of homoeologous genes and is reported to be common in
evolved due to increased abiotic stress, including heat and drought, hexaploid bread wheat (Bottley et al. 2006). This poses a potential
which are conditions that can enhance photorespiration (Sage problem for utilising newly synthesised wheats in pre-breeding
2004). There is scope for breeding photosynthetic improvements programmes. However, the establishment of homoeologs does
within C4 crop species (von Caemmerer and Furbank 2016). not necessarily result in functional silencing or suppression
However, major cereal crops are still cultivated in climates that through dominance; phenotypes can be influenced by an additive
favour photorespiration, meaning the enhanced water and nitrogen dosage effect or complex interactions linked to the homoeologs
use efficiency characteristics of the C4 pathway is an attractive (Borrill et al. 2015). Another potential roadblock is the genomic
breeding target for C3 crops (Mitchell and Sheehy 2006). Climate instability and radical changes which can occur because of
change could exacerbate this need further, which has contributed to allopolyploidization (Kraitshtein et al. 2010). However, there is
a concerted effort to incorporate the C4 pathway into C3 crops, in evidence to suggest the severity of these changes may be of little
particular rice (e.g., www.c4rice.com). Challenges still need to be consequence to the overall development of the plant (Zhao et al.
overcome before these improvements are available to the breeding 2011). Recent advancements in next-generation sequencing
community and C3 wild progenitors may provide a more accessible provide an opportunity for increasing our understanding of the
source of improvement for major C3 crops. functional genomics that underpin relationships across homo-
eologs (reviewed in Borrill et al. 2015). These tools could
contribute to providing an improved understanding of the
OPPORTUNITIES EXIST TO USE GENOMICS TO ACCELERATE functional genetics of newly formed pre-breeding resources such
THE USE OF PROGENITORS IN CROP BREEDING as synthetic wheats incorporating progenitor diversity.
Whilst traditional breeding approaches have been successfully Advancements in sequencing technologies have facilitated the
used to cross cultivated materials with their wild relatives to discovery of large numbers of DNA markers in crop species. In
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
298
wheat (Winfield et al. 2012), this has led to the development of the draft sequence of Ae. tauschii (Luo et al. 2017). The availability
numerous genotyping platforms (Adamski et al. 2020) that have of reference genomes supports the use of data-driven approaches
aided the application of QTL mapping and have enhanced the to selections, including linking phenotype to gene expression as
accessibility of diversity in progenitors and related species demonstrated by Gálvez et al. (2019) for drought tolerance. This
(Winfield et al. 2016, 2018; Wingen et al. 2017). SNPs are very highlights the potential impact of understanding gene networks
effective markers in high-throughput genotyping due to their underpinning traits, and how genomics may identify novel
abundance across the wheat genome (Rimbert et al. 2018). breeding targets (Gálvez et al. 2019).
Specific platforms have been developed to characterise wheat Resources supporting reverse genetics have also been devel-
progenitors and wild relatives, including the Axiom® HD Wheat oped in progenitor species with Targeting Induced Local Lesions
Genotyping Array (Winfield et al. 2016) and the Axiom® Wheat- in Genomes populations available in the wheat tetraploid (durum
Relative Genotyping Array (Przewieslik-Allen et al. 2019) in wheat Kronos; Krasileva et al. 2017) and diploid species (Ae.
addition to arrays developed for elite varieties (e.g., Axiom® tauschii; Rawat et al. 2018), as well as being available for hexaploid
Wheat Breeder’s Genotyping Array; Allen et al. 2017). The wheat- wheat (cultivar Cadenza; Krasileva et al. 2017). A wheat exome
relative array has been used to aid the introgression of the diploid capture was developed to focus sequencing efforts on exons,
wheat-relative Ambylopyrum muticum into a hexaploid wheat thereby reducing sequencing costs (Winfield et al. 2012). Along
background through MAS (King et al. 2017). Furthermore, the with genome sequences, these provide a useful resource for allele
Wheat Breeders’ array has been used in several studies for mining and gene discovery and could be used in future to support
identifying QTLs in tetraploid wheat (Lucas et al. 2017; Wright et al. gene identification and cloning directly from the progenitor
2020). Low-cost genotyping platforms designed to demonstrate species. Direct cloning of favourable genes from progenitor
potential genetic variability between progenitor species and elite species has been demonstrated using a combination of associa-
varieties are a tool of growing importance in exploring and tion genetics and resistance gene enrichment and sequencing
harnessing diversity and have been deployed in many crops such (AgRenSeq; Arora et al. 2019). This method has been used to both
as barley (Bayer et al. 2017), rice (Chen et al. 2013) and maize (Xu discover and clone functional stem rust resistance genes in a
et al. 2017). panel of diverse Ae. tauschii accessions (Arora et al. 2019).
The availability of sequenced genomes from crop species, for Molecular breeding technologies provide the potential to directly
example, the annotated reference genome assembly of the wheat introduce useful variation discovered in one crop into another,
cultivar Chinese Spring (International Wheat Genome Sequencing either by the introduction of the gene via genetic transformation
Consortium et al. 2018) augmented by the multiple genome or gene editing to introduce variation within homoeologous
assembly of Walkowiak et al. (2020) improve our understanding of genes. The efficiency of the approaches discussed in this review
the size and context of targeted introgressions through knowledge remains to be seen for different genes and crops and can be
of the physical chromosome location of markers used for selection. impacted by the genetic background of particular varieties, but
In addition, the resources can improve our understanding of synteny identifying a set of variants that already exist in nature and that
with ancestral genomes (Grewal et al. 2018). Introgression fragments can be used to introduce variation within genes of interest is an
can be queried to identify the genes and any potentially favourable exciting prospect for the future.
alleles present (Cheng et al. 2019). Due to the reducing expense of
sequencing technologies (Jia et al. 2018), the number of cultivars
sequenced is increasing, including many important elite wheat SUMMARY
varieties (e.g., the 10+ genomes project: www.10wheatgenomes. There is a wealth of variation present in crop progenitor species
com; Montenegro et al. 2017; Walkowiak et al. 2020). Increasing the for traits of relevance to plant breeding including flowering time,
number of modern wheat varieties sequenced, or genotyped physiological response and RSA. Although initial characterisation
through high-density marker arrays, will help characterise the demonstrates that functional variation exists, there remains a
haplotype diversity within the modern wheat gene pool. Haplotypes significant opportunity to systematically characterise this variation
present in low diversity may reflect regions that have been under in order to make it accessible for use in breeding. In particular,
past selection (Fradgley et al. 2019) or where variation has been lost more work is required to fully understand the genetic and
due to the domestication bottleneck (Haudry et al. 2007). Regardless, physiological basis of progenitor trait variation in order to
using this knowledge, targeted comparisons can then be made with accurately inform future breeding strategies. The growing
extended progenitor gene pools to capture novel haplotypes (Uauy availability of sequencing and genomics tools offers great
2017). This comparison is being accelerated in wheat by the potential for targeted and accelerated progress in the systematic
availability of increasing numbers of progenitors sequenced, use of functional progenitor variation. The advances in use of
including Ae. tauschii (Luo et al. 2017), T. urartu (Ling et al. 2013), wheat progenitors and the techniques developed for the capture
T. dicoccoides (Avni et al. 2017) and T. durum (Maccaferri et al. 2019). of novel diversity may be applicable for the improvement of other
A recent study by Cheng et al. (2019) compared re-sequenced cereal crop species.
genome data from a mixture of cultivated and progenitor wheat
accessions, flagging regions of past introgression and identifying
haplotype blocks that are nearly completely fixed in cultivated REFERENCES
varieties. These regions of low diversity highlight the potential for Acevedo‐Siaca LG, Dionora J, Laza R, Paul Quick W, Long SP (2021) Dynamics of
identifying regions to target for improving genetic diversity from photosynthetic induction and relaxation within the canopy of rice and two wild
progenitor species. relatives. Food Energy Secur 10:e286
In addition to the characterisation of haplotype diversity, Adamski NM, Borrill P, Brinton J, Harrington SA, Marchal C, Bentley AR et al. (2020) A
enhanced sequencing resources will also support genetic map- roadmap for gene functional characterisation in crops with large genomes:
lessons from polyploid wheat. eLife 9:e55646. https://doi.org/10.7554/
ping, cloning and functional characterisation from progenitor eLife.55646
species. Kishii (2019) summarised the progress in generating Akech V, Ojulong H, Okori P, Biruma M (2016) Resistance to blast in interspecific
genetic and physical mapping resources for Ae. tauschii docu- finger millet progenies. Fifth RUFORUM Bienn Reg Conf 17–21 Oct 2016, Cape
menting the progression from the early use of restriction fragment Town, South Africa 14, p 725–730
length polymorphism mapping in Ae. tauschii mapping popula- Allen AM, Winfield MO, Burridge AJ, Downie RC, Benbow HR, Barker GLA et al. (2017)
tions (Gill et al. 1991) through to single sequence repeat Characterization of a Wheat Breeders’ Array suitable for high-throughput SNP
genotyping (Nishijima et al. 2018). This supported the production genotyping of global accessions of hexaploid bread wheat (Triticum aestivum).
of a 10 K Ae. tauschii Infinium SNP array by Luo et al. (2013) and Plant Biotechnol J 15:390–401. https://doi.org/10.1111/pbi.12635
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
299
Ananda GKS, Myrans H, Norton SL, Gleadow R, Furtado A, Henry RJ (2020) Wild Dreisigacker S, Kishii M, Lage J, Warburton M (2008) Use of synthetic hexaploid wheat
sorghum as a promising resource for crop improvement. Front Plant Sci to increase diversity for CIMMYT bread wheat improvement. Crop Pasture Sci
11:1–14. https://doi.org/10.3389/fpls.2020.01108 59:413–420. https://doi.org/10.1071/AR07225
Araus JL, Brown HR, Febrero A, Bort J, Serret MD (1993) Ear photosynthesis, carbon Driever SM, Lawson T, Andralojc PJ, Raines CA, Parry MAJ (2014) Natural variation in
isotope discrimination and the contribution of respiratory CO2 to differences in photosynthetic capacity, growth, and yield in 64 field-grown wheat genotypes.
grain mass in durum wheat. Plant, Cell Environ 16:383–392 J Exp Bot 65:4959–4973. https://doi.org/10.1093/jxb/eru253
Arora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y, Matny O et al. (2019) Dubcovsky J, Lijavetzky D, Appendino L, Tranquilli G (1998) Comparative RFLP
Resistance gene cloning from a wild crop relative by sequence capture and mapping of Triticum monococcum genes controlling vernalization requirement.
association genetics. Nat Biotechnol 37:139–143. https://doi.org/10.1038/ Theor Appl Genet 97:968–975
s41587-018-0007-9 Dunstone RL, Evans LT (1974) Role of changes in cell size in the evolution of wheat.
Austin R, Morgan C, Ford M, Bhagwat S (1982) Flag leaf photosynthesis of Triticum Aust J Plant Physiol 1:157–165
aestivum and related diploid and tetraploid species. Ann Bot 49:177–189 Dunstone RL, Gifford RM, Evans LT (1973) Photosynthetic characteristics of modern
Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H et al. (2017) Wild and primitive wheat species in relation to ontogeny and adaption to light. Aust
emmer genome architecture and diversity elucidate wheat evolution and J Biol Sci 26:295–307
domestication. Science 97:93–97. https://doi.org/10.1126/science.aan0032 El Hassouni K, Alahmad S, Belkadi B, Filali-Maltouf A, Hickey LT, Bassi FM (2018) Root
Bayer MM, Rapazote-Flores P, Ganal M, Hedley PE, Macaulay M, Plieske J et al. (2017) system architecture and its association with yield under different water regimes
Development and evaluation of a barley 50k iSelect SNP array. Front Plant Sci in durum wheat. Crop Sci 58:2331–2346
8:1792. https://doi.org/10.3389/fpls.2017.01792 Evans LT, Dunstone RL (1970) Some physiological aspects of evolution in wheat. Aust
Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A Pseudo-Response Reg- J Biol Sci 23:725–742
ulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat Evans LT, Bingham J, Jackson P, Sutherland J (1972) Effect of awns and drought on
(Triticum aestivum L.). Theor Appl Genet 115:721–733 the supply of photosynthate and its distribution within wheat ears. Ann Appl
Becker SR, Byrne PF, Reid SD, Bauerle WL, McKay JK, Haley SD (2016) Root traits Biol 70:67–76. https://doi.org/10.1111/j.1744-7348.1972.tb04689.x
contributing to drought tolerance of synthetic hexaploid wheat in a greenhouse Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 dif-
study. Euphytica 207:213–224. https://doi.org/10.1007/s10681-015-1574-1 fusion pathway inside leaves. J Exp Bot 60:2235–2248. https://doi.org/10.1093/
Bentley AR, Turner AS, Gosman N, Leigh F, Maccaferri M, Dreisigacker S et al. (2011) jxb/erp117
The frequency of photoperiod insensitive Ppd-A1a alleles in tetraploid, hex- Falke KC, Sušić Z, Wilde P, Wortmann H, Möhring J, Piepho HP et al. (2009) Testcross
aploid and synthetic hexaploid wheat germplasm. Plant Breed 130:10–15 performance of rye introgression lines developed by marker-assisted back-
Blum A (1985) Photosynthesis and transpiration in leaves and ears of wheat and crossing using an Iranian accession as donor. Theor Appl Genet 118:1225–1238.
barley varieties. J Exp Bot 36:432–440. https://doi.org/10.1093/jxb/36.3.432 https://doi.org/10.1007/s00122-009-0976-7
Borlaug NE (1968) Wheat breeding and its impact on world food supply. In: Third Farquhar GD, von Caemmerer S, Berry J (1980) A biochemical model of photo-
International Wheat Genetics Symposium, Mexico: CIMMYT, 1–36 synthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90. https://doi.
Borrill P, Adamski N, Uauy C (2015) Genomics as the key to unlocking the polyploid org/10.1007/BF00386231
potential of wheat. N Phytologist 208:1008–1022 Farquhar G, O’Leary M, Berry J (1982) On the relationship between carbon isotope
Bottley A, Xia GM, Koebner RMD (2006) Homoeologous gene silencing in hexaploid discrimination and the intercellular carbon dioxide concentration in leaves.
wheat. Plant J 47:897–906 Aust J Plant Physiol 9:121
Camacho Villa TC, Maxted N, Scholten M, Ford-Lloyd B (2005) Defining and identi- Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with
fying crop landraces. Plant Genet Resour 3:373–384 water-use efficiency of wheat genotypes. Funct Plant Biol 11:539–552
Carmo-Silva E, Andralojc PJ, Scales JC, Driever SM, Mead A, Lawson T et al. (2017) Phe- Feldman M (2001) Origin of cultivated wheat. In: Bonjean AP, Angus WJ (eds) The
notyping of field-grown wheat in the UK highlights contribution of light response of world wheat book: a history of wheat breeding. Intercept Ltd., London. p. 3–56
photosynthesis and flag leaf longevity to grain yield. J Exp Bot 68:3473–3486 Feldman M, Levy AA (2012) Genome evolution due to allopolyploidization in wheat.
Challinor A, Koehler AK, Ramirez-Villegas J, Whitfield S, Das B (2016) Current warming Genetics 192:763–774
will reduce yields unless maize breeding and seed systems adapt immediately. Fleury D, Jefferies S, Kuchl H, Langridge P (2010) Genetic and genomic tools to
Nat Clim Change 6:954–958. https://doi.org/10.1038/nclimate3061 improve drought tolerance in wheat. J Exp Bot 61:3211–22. https://doi.org/
Chen H, Xie W, He H, Yu H, Chen W, Li J et al. (2013) A high-density SNP genotyping 10.1093/jxb/erq152
array for rice biology and molecular breeding molecular. Plant 7:541–553 Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriqui M, Diaz-Espejo A (2012)
Cheng H, Liu J, Wen J, Nie X, Xu L, Chen N et al. (2019) Frequent intra- and inter- Mesophyll diffusion conductance to CO2: an unappreciated central player in
species introgression shapes the landscape of genetic variation in bread wheat. photosynthesis. Plant Sci 193–194:70–84. https://doi.org/10.1016/j.plantsci.
Genome Biol 20:1–16. https://doi.org/10.1186/s13059-019-1744-x 2012.05.009
Chèvre AM, Jahier J, Trottet M (1989) Expression of disease resistance genes in Foulkes MJ, Reynolds MP (2015) Breeding challenge: improving yield potential, 2nd
amphiploid wheats-Triticum tauschii (Coss.) Schmal. Cer Res Comm 17:23–29 edn. Elsevier Inc
Christopher J, Christopher M, Jennings R, Jones S, Fletcher S, Borrell A et al. (2013) Fradgley N, Evans G, Biernaskie JM, Cockram J, Marr EC, Oliver AG et al. (2020) Effects
QTL for root angle and number in a population developed from bread wheats of breeding history and crop management on the root architecture of wheat.
(Triticum aestivum) with contrasting adaptation to water-limited environments. Plant Soil 452:587–600. https://doi.org/10.1007/s11104-020-04585-2
Theor Appl Genet 126:1563–1574. https://doi.org/10.1007/s00122-013-2074-0 Fradgley N, Gardner KA, Cockram J, Elderfield J, Hickey JM, Howell P et al. (2019) A
Cockram J, Jones H, Leigh FJ, O’Sullivan D, Powell W, Laurie D et al. (2007) Control of large-scale pedigree resource of wheat reveals evidence for adaptation and
flowering time in temperate cereals: Genes, domestication, and sustainable selection by breeders. PLoS Biol 17(2):e3000071. https://doi.org/10.1371/
productivity. J Exp Bot 58:1231–1244 journal.pbio.3000071
Colasanti J, Coneva V (2009) Mechanisms of floral induction in grasses: something Gaju O, DeSilva J, Carvalho P, Hawkesford MJ, Griffiths S, Greenland A et al. (2016)
borrowed, something new. Plant Physiol 149:56–62. https://doi.org/10.1104/ Leaf photosynthesis and associations with grain yield, biomass and nitrogen-
pp.108.130500 use efficiency in landraces, synthetic-derived lines and cultivars in wheat. Field
Covshoff S, Hibberd JM (2012) Integrating C4 photosynthesis into C3 crops to Crops Res 193:1–15
increase yield potential. Curr Opin Biotechnol 23:209–214. https://doi.org/ Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ et al. (2005) Rubisco
10.1016/j.copbio.2011.12.011 specificity factor tends to be larger in plant species from drier habitats and in
Cox TS (1997) Deepening the wheat gene pool. J Crop Prod 1:1–25 species with persistent leaves. Plant Cell Environ 28:571–579
Coyne CJ, Kumar S, Wettberg EJB, Marques E, Berger JD, Redden RJ et al. (2020) Gálvez S, Mérida-García R, Camino C, Borrill P, Abrouk M, Raminez-Gonzalez RH et al.
Potential and limits of exploitation of crop wild relatives for pea, lentil, and (2019) Hotspots in the genomic architecture of field drought responses in
chickpea improvement. Legum Sci 2:e36 https://doi.org/10.1002/leg3.36 wheat as breeding targets. Funct Integr Genomics 19:295–309. https://doi.org/
Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants 10.1007/s10142-018-0639-3
to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626 Gaurav K, Arora S, Silva P, Sánchez-Martín J, Horsnell R, Gao L et al. (2021) Population
Dempewolf H, Baute G, Anderson J, Kilian B, Smith C, Guarino L (2017) Past and future genomic analysis of Aegilops tauschii identifies targets for bread wheat
use of wild relatives in crop breeding. Crop Sci 57:1070–1082. https://doi.org/ improvement. Nat Biotechnol 40:422–431 https://doi.org/10.1038/s41587-021-
10.2135/cropsci2016.10.0885 01058-4
Dixon LE, Karsai I, Kiss T, Adamski NM, Liu Z, Ding Y et al. (2019) VERNALIZATION1 Giles RJ, Brown TA (2006) GluDy allele variations in Aegilops tauschii and Triticum
controls developmental responses of winter wheat under high ambient tem- aestivum: implications for the origins of hexaploid wheats. Theor Appl Genet
peratures. Development 146:dev172684. https://doi.org/10.1242/dev.172684 112:1563–1572
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
300
Gill KS, Lubbers EL, Gill BS, Raupp WJ, Cox TS (1991) A genetic linkage map of Triticum mutica) introgression lines and their cytogenetic and molecular characteriza-
tauschii (DD) and its relationship to the D-genome of bread wheat (AABBDD). tion. Front Plant Sci 10:34 https://doi.org/10.3389/fpls.2019.00034
Genome 14:362–374. https://doi.org/10.1139/g91-058 Kishii M (2019) An update of recent use of Aegilops species in wheat breeding. Front
Golovnina KA, Kondratenko EY, Blinov AG, Goncharov NP (2010) Molecular char- Plant Sci 10:585. https://doi.org/10.3389/fpls.2019.00585
acterization of vernalization loci VRN1 in wild and cultivated wheats. BMC Plant Koyama K, Okumura Y, Okamoto E, Nishijima R, Takumi S (2018) Natural variation in
Biol 10:168. https://doi.org/10.1186/1471-2229-10-168 photoperiodic flowering pathway and identification of photoperiod-insensitive
Grazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of accessions in wild wheat, Aegilops tauschii. Euphytica 214:3. https://doi.org/
flowering time variation in Arabidopsis accessions. Plant Physiol 132:1107–14. 10.1007/s10681-017-2089-8
https://doi.org/10.1104/pp.103.021212 Krasileva KV, Vasquez-Gross HA, Howell T, Bailey P, Paraiso F, Clissold L et al. (2017)
Grewal S, Hubbart-Edwards S, Yang C, Scholefield D, Ashling S, Burridge A et al. (2018) Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci USA 114:
Detection of T. urartu introgressions in wheat and development of a panel of E913–E921
interspecific introgression lines. Front Plant Sci 871:1–10. https://doi.org/ Kraitshtein Z, Yaakov B, Khasdan V, Kashkush K (2010) Genetic and epigenetic
10.3389/fpls.2018.01565 dynamics of a retrotransposon after allopolyploidization of wheat. Genetics
Gu J, Yin X, Stomph TJ, Wang H, Struik PC (2012) Physiological basis of genetic 186:801–812
variation in leaf photosynthesis among rice (Oryza sativa L.) introgression lines Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK et al. (2016)
under drought and well-watered conditions. J Exp Bot 63:5137–5153. https:// Improving photosynthesis and crop productivity by accelerating recovery from
doi.org/10.1093/jxb/ers170 photoprotection. Science 354:857–861
Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of Lantican MA, Pingali PL, Rajaram S (2005) Is research on marginal lands catching up?
developments over the last 20 years. Euphytica 156:1–13. https://doi.org/ The case of unfavourable wheat growing environments. Agric Econ 29:353–361
10.1007/s10681-007-9363-0 Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on
Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D, Poncet C et al. (2007) Grinding up photosynthesis and water use efficiency. Plant Physiol 164:1556–1570. https://
wheat: a massive loss of nucleotide diversity since domestication. Mol Biol Evol doi.org/10.1104/pp.114.237107
24:1506–1517 Li J, Wan HS, Yang WY (2014a) Synthetic hexaploid wheat enhances variation and
Henry A, Gowda VRP, Torres RO, McNally KL, Serraj R (2011) Variation in root system adaptive evolution of bread wheat in breeding processes. J Syst Evol
architecture and drought response in rice (Oryza sativa): phenotyping of the 52:735–742
OryzaSNP panel in rainfed lowland fields. Field Crop Res 120:205–214 Li P-F, Cheng Z-G, Ma B-L, Palta JA, Kong H-Y, Mo F et al. (2014b) Dryland wheat
Horton P (2000) Prospects for crop improvement through the genetic manipulation domestication changed the development of aboveground architecture for a
of photosynthesis: morphological and biochemical aspects of light capture. J well-structured canopy. PLoS One 9:e95825
Exp Bot 51:475–485 Li X, Lawas LMF, Malo R, Glaubitz U, Erban A, Mauleon R et al. (2015) Metabolic and
Hubbart S, Smillie IRA, Heatley M, Swarup R, Foo CC, Zhao L et al. (2018) Enhanced transcriptomic signatures of rice floral organs reveal sugar starvation as a factor
thylakoid photoprotection can increase yield and canopy radiation use effi- in reproductive failure under heat and drought stress. Plant Cell Environ
ciency in rice. Commun Biol 1:22 38:2171–2192
Hughes J, Hepworth C, Dutton C, Dunn JA, Hunt L, Stephens J et al. (2017) Reducing Li YP, Li YY, Li DY, Wang SW, Zhang SQ (2017) Photosynthetic response of tetraploid
stomatal density in barley improves drought tolerance without impacting on and hexaploid wheat to water stress. Photosynthetica 55:1–13. https://doi.org/
yield. Plant Physiol 174:776–787 10.1007/s11099-016-0659-y
Hyles J, Bloomfield MT, Hunt JR, Threthowan RM, Trevaskis B (2020) Phenology and Ling H-Q, Zhao S, Liu D, Wang J, Sun H, Zhang C (2013) Draft genome of the wheat
related traits for wheat adaptation. Heredity 125:417–430 https://doi.org/ A-genome progenitor Triticum urartu. Nature 496:87–90. https://doi.org/
10.1038/s41437-020-0320-1 10.1038/nature11997
Iannucci A, Marone D, Russo MA, De Vita P, Miullo V, Ferragonio P et al. (2017) Liu R, Wu F, Yi X, Lin Y, Wang Z, Liu S et al. (2020) Quantitative trait loci analysis for
Mapping QTL for root and shoot morphological traits in a durum wheat × T. root traits in synthetic hexaploid wheat under drought stress conditions. J
dicoccum segregating population at seedling stage. Int J Genomics Integr Agric 19:1947–1960
2017;6876393. https://doi.org/10.1155/2017/6876393 Lobell DB, Field CB (2007) Global scale climate-crop yield relationships and the
International Wheat Genome Sequencing Consortium (IWGSC); IWGSC RefSeq Prin- impacts of recent warming. Environ Res Lett 2:014002
cipal Investigators: Appels A, Eversole K, Feuillet C, Keller B et al. (2018) Shifting Long SP, Zhu X-G, Naidu SL, Ort DR (2006) Can improvement in photosynthesis
the limits in wheat research and breeding using a fully annotated reference increase crop yields? Plant, Cell Environ 29:315–330. https://doi.org/10.1111/
genome Science 361:eaar7191. https://doi.org/10.1126/science.aar7191 j.1365-3040.2005.01493.x
Ishimaru T, Hirabayashi H, Ida M, Takai T, San-Oh YA, Yoshinaga S et al. (2010) A Lopes MS, El-Basyoni I, Baenziger PS, Singh S, Royo C, Ozbek K et al. (2015) Exploiting
genetic resource for early-morning flowering trait of wild rice Oryza officinalis to genetic diversity from landraces in wheat breeding for adaptation to climate
mitigate high temperature-induced spikelet sterility at anthesis. Ann Bot change. J Exp Bo 66:3477–3486. https://doi.org/10.1093/jxb/erv122
106:515–520. https://doi.org/10.1093/aob/mcq124 Lucas SJ, Salantur A, Yazar S, Budak H (2017) High-throughput SNP genotyping of
Jafarzadeh J, Bonnett D, Jannink J-L, Akdemir D, Dreisigacker S, Sorrells ME (2016) modern and wild emmer wheat for yield and root morphology using a com-
Breeding value of primary synthetic wheat genotypes for grain yield. PLoS One bined association and linkage analysis. Funct Integr Genomics 17:667–685.
11:e0162860. https://doi.org/10.1371/journal.pone.0162860 https://doi.org/10.1007/s10142-017-0563-y
Jia M, Guan J, Zhai Z, Geng S, Zhang X, Mao L et al. (2018) Wheat functional genomics Lundgren MR, Fleming AJ (2020) Cellular perspectives for improving mesophyll
in the era of next generation sequencing: an update. Crop J 6:7–14. https://doi. conductance. Plant J 101:845–857
org/10.1016/j.cj.2017.09.003 Luo MC, Gu YQ, You FM, Deal KR, Ma Y, Hu Y et al. (2013) A 4-gigabase physical map
Johnson RC, Kebede H, Mornhinweg DW, Carver BF, Rayburn AL, Nguyen HT (1987) unlocks the structure and evolution of the complex genome of Aegilops tau-
Photosynthetic differences among Triticum accessions at tillering. Crop Sci schii, the wheat D-genome progenitor. Proc Natl Acad Sci USA 110:7940–7945.
27:1046–1050 https://doi.org/10.1073/pnas.1219082110
Jones G, Jones H, Charles MP, Jones MK, College S, Leigh FJ et al. (2012) Phylogeo- Luo MC, Gu YQ, Puiu D, Wang H, Twardziok SO, Deal KR et al. (2017) Genome
graphic analysis of barley DNA as evidence for the spread of Neolithic agri- sequence of the progenitor of the wheat D genome Aegilops tauschii. Nature
culture through Europe. J Archaeol. Science 39:3230–3238 551:498–502. https://doi.org/10.1038/nature24486
Kerber R, Rowland GG (1974) Origin of the free threshing character in hexaploid McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, Ulat VJ et al. (2009) Geno-
wheat. Can J Genet Cytol 16:145–154. https://doi.org/10.1139/g74-014 mewide SNP variation reveals relationships among landraces and modern
Khazaei H, Monneveux P, Hongbo S, Mohammady S (2009) Variation for stomatal varieties of rice. Proc Natl Acad Sci USA 106:12273–12278
characteristics and water use efficiency among diploid, tetraploid and hex- Maccaferri M, Sanguineti MC, Corneti S, Ortega JLA, Ben Salem M, Bort J et al. (2008)
aploid Iranian wheat landraces. Genet Resour Crop Evol 57:307–314. https://doi. Quantitative trait loci for grain yield and adaptation of durum wheat (Triticum
org/10.1007/s10722-009-9471-x durum Desf.) across a wide range of water availability. Genetics 178:489–511
Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare Maccaferri M, Harris NS, Twardziok SO, Pasam RK, Gundlach H, Spannagl B et al.
(Japanese). Agric Hort (Tokyo) 19:13–14. Kihara (2019) Durum wheat genome highlights past domestication signatures and
King J, Grewal S, Yang CY, Hubbart S, Scholefield D, Ashling S et al. (2017) A step future improvement targets. Nat Genet 51:885–895. https://doi.org/10.1038/
change in the transfer of interspecific variation into wheat from Amblyopyrum s41588-019-0381-3
muticum. Plant Biotechnol J 15:217–226. https://doi.org/10.1111/pbi.12606 Mano Y, Omori F (2013) Flooding tolerance in interspecific introgression lines con-
King J, Newell C, Grewal S, Hubbart-Edwards S, Yang C-Y, Scholefield D et al. (2019) taining chromosome segments from teosinte (Zea nicaraguensis) in maize (Zea
Development of stable homozygous wheat/Amblyopyrum muticum (Aegilops mays subsp. mays). Ann Bot 112:1125–1139
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
301
Manschadi AM, Christopher JT, Hammer GL, Devoil P (2010) Experimental and Parry MAJ, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu X-G et al. (2011)
modelling studies of drought‐adaptive root architectural traits in wheat (Triti- Raising yield potential of wheat. II. Increasing photosynthetic capacity and
cum aestivum L.). Plant Biosyst 144:458–462 efficiency. J Exp Bot 62:453–467. https://doi.org/10.1093/jxb/erq304
Martínez-Moreno F, Solís I, Nogueoro D, Blanco A, Özberk İ, Nsarellah N et al. (2020) Peleg Z, Fahima T, Krugman T, Abbo S, Yakir D, Korol AB (2009) Genomic dissection of
Durum wheat in the Mediterranean Rim: historical evolution and genetic drought resistance in durum wheat × wild emmer wheat recombinant inbred
resources. Genet Resour Crop Evol 67:1415–1436 line population. Plant Cell Environ 32:758–779. https://doi.org/10.1111/j.1365-
Matsouka Y, Takumi S, Kawahara T (2008) Flowering time diversification and dispersal in 3040.2009.01956.x
central Eurasian wild wheat Aegilops tauschii Coss.: genealogical and ecological Petersen G, Seberg O, Yde M, Berthelsen K (2006) Phylogenetic relationships of Tri-
framework. PLoS One 3:e3138. https://doi.org/10.1371/journal.pone.0003138 ticum and Aegilops and evidence for the origin of the A, B, and D genomes of
Matsuoka Y, Kawahara T, Takumi S (2015) Intraspecific lineage divergence and its common wheat (Triticum aestivum). Mol Phylogenet Evol 30:70–82
association with reproductive trait change during species range expansion in Porch T, Beaver J, Debouck D, Jackson S, Kelly J, Dempewolf H (2013) Use of wild
central Eurasian wild wheat Aegilops tauschii Coss. (Poaceae). BMC Evol Biol relatives and closely related species to adapt common bean to climate change.
15:213 Agronomy 3:433–461. https://doi.org/10.3390/agronomy3020433
McAusland L, Vialet-Chabrand S, Jauregui I, Burridge A, Hubbart-Edwards S, Fryer MJ Prins A, Orr DJ, Andralojc PJ, Reynolds MP, Carmo-Silva E, Parry MAJ (2016) Rubisco
et al. (2020) Variation in key leaf photosynthetic traits across wheat wild rela- catalytic properties of wild and domesticated relatives provide scope for
tives is accession dependent not species dependent. N Phytol 228:1767–1780. improving wheat photosynthesis. J Exp Bot 67:1827–1838. https://doi.org/
https://doi.org/10.1111/nph.16832 10.1093/jxb/erv574
McFadden E, Sears E (1946) The origin of Triticum spelta and its free-threshing hex- Przewieslik-Allen AM, Burridge AJ, Wilkinson PA, Winfield MO, Shaw DS, McAusland L
aploid relatives. J Hered 37:81–89 et al. (2019) Developing a high-throughput SNP-based marker system to
Merchuk-Ovnat L, Barak V, Fahima T, Ordon F, Lidzbarsky GA, Krugman T et al. (2016a) facilitate the introgression of traits from Aegilops species into bread wheat
Ancestral QTL alleles from wild emmer wheat improve drought resistance and (Triticum aestivum). Front Plant Sci 9:1993. https://doi.org/10.3389/
productivity in modern wheat cultivars. Front Plant Sci 7:452. https://doi.org/ fpls.2018.01993
10.3389/fpls.2016.00452 Rawat N, Schoen A, Singh L, Mahlandt A, Wilson DL, Liu S et al. (2018) TILL-D: An
Merchuk-Ovnat L, Fahima T, Krugman T, Saranga Y (2016b) Ancestral QTL alleles from Aegilops tauschii TILLING resource for wheat improvement. Front Plant Sci
wild emmer wheat improve grain yield, biomass and photosynthesis across 9:1665. https://doi.org/10.3389/fpls.2018.01665
environments in modern wheat. Plant Sci 251:23–34. https://doi.org/10.1016/j. Rey MD, Martín AC, Higgins J, Swarbreck D, Uauy C, Shaw P et al. (2017) Exploiting the
plantsci.2016.05.003 ZIP4 homologue within the wheat Ph1 locus has identified two lines exhibiting
Miedaner T, Laidig F (2019) Hybrid breeding in rye (Secale cereale L.). In: Al-Khayri homoeologous crossover in wheat-wild relative hybrids. Mol Breed 37:95.
JM, Jain SM, Johnson DV (eds) Advances in plant breeding strategies: cer- https://doi.org/10.1007/s11032-017-0700-2
eals. Springer, Cham. pp 343–372. https://doi.org/10.1007/978-3-030-23108- Reynolds M, Dreccer F, Trethowan R (2007) Drought-adaptive traits derived from
8_9 wheat wild relatives and landraces. J Exp Bot 58:177–186
Mirzaghaderi G, Abdolmalaki Z, Ebrahimzadegan R, Bahmani F, Orooji F, Majdi M et al. Reynolds M, Foulkes MJ, Slafer GA, Berry P, Parry MAJ, Snape JW et al. (2009) Raising
(2020) Production of synthetic wheat lines to exploit the genetic diversity of yield potential in wheat. J Exp Bot 60:1899–1918. https://doi.org/10.1093/jxb/
emmer wheat and D genome containing Aegilops species in wheat breeding. erp016
Sci Rep. 10:19698 Reynolds MP, Hays D, Chapman S (2010) Breeding for adaptation to heat and drought
Mirza N, Marla S (2019) Finger millet (Eleusine coracana L. Gartn.) breeding. In: Al-Khayri stress. In: Reynolds MP (ed) Climate change and crop production. CABI, Wall-
JM, Jain SM, Johnson DV (eds) Advances in plant breeding strategies: cereals. ingford, Oxfordshire, p 71–91
Springer, Cham. p 83–132. https://doi.org/10.1007/978-3-030-23108-8_3 Richard CA, Hickey LT, Fletcher S, Jennings R, Chenu K, Christopher JT (2015) High-
Mitchell PL, Sheehy JE (2006) Supercharging rice photosynthesis to increase yield. N throughput phenotyping of seminal root traits in wheat. Plant Methods 11:13.
Phytol 171:688–693. https://doi.org/10.1111/j.1469-8137.2006.01855.x https://doi.org/10.1186/s13007-015-0055-9
Molero G, Reynolds MP (2020) Spike photosynthesis measured at high throughput Richards RA, Rebetzke GJ, Condon AG, van Herwaarden AF (2002) Breeding oppor-
indicates genetic variation independent of flag leaf photosynthesis. Field Crops tunities for increasing the efficiency of water use and crop yield in temperate
Res 255:107866 Cereals. Crop Sci 42:111. https://doi.org/10.2135/cropsci2002.0111
Montenegro JD, Golicz AA, Bayer PE, Hurgobin B, Lee HT, Chan CKK et al. (2017) The Rimbert H, Darrier B, Navarro J, Kitt J, Choulet F, Leveugle M et al. (2018) High
pangenome of hexaploid bread wheat. Plant J 90:1007–1013. https://doi.org/ throughput SNP discovery and genotyping in hexaploid wheat. PLoS One
10.1111/tpj.13515 13:1–19. https://doi.org/10.1371/journal.pone.0186329
Mujeeb-Kazi A, Kaz, AG, Dundas I, Farrakh S (2013) Genetic diversity for wheat Rosenzweig CD, Vicarelli KM, Neofotis P, Wu Q, Casassa G, Menzel A et al. (2008)
improvement as a conduit to food security. Advances in agronomy, 1st edn, vol Attributing physical and biological impacts to anthropogenic climate change.
122. Elsevier Inc Nature 453:353–357. https://doi.org/10.1038/nature06937
Murchie EH, Pinto M, Horton P (2009) Agriculture and the new challenges for pho- Rowland GG, Kerber ER (1974) Telocentric mapping in hexaploid wheat of genes for
tosynthesis research. N Phytol 181:532–552. https://doi.org/10.1111/j.1469- leaf rust resistance and other characters derived from Aegilops squarrosa. Can J
8137.2008.02705.x Genet Cytol 16:137–144 https://doi.org/10.1139/g74-013
Nevo E, Chen G (2010) Drought and salt tolerances in wild relatives for wheat and Sage RF (2004) The evolution of C4 photosynthesis. N Phytol 161:341–370. https://doi.
barley improvement. Plant Cell Environ 33:670–685. https://doi.org/10.1111/ org/10.1111/j.1469-8137.2004.00974.x
j.1365-3040.2009.02107.x Salamini F, Özkan H, Brandolini A, Schäfer-Pregl R, Martin W (2002) Genetics and
Ni Z, Li H, Zhao Y, Peng H, Hu Z, Xin M et al. (2018) Genetic improvement of heat geography of wild cereal domestication in the near east. Nat Rev Genet
tolerance in wheat: recent progress in understanding the underlying molecular 3:429–441
mechanisms. Crop J 6:32–41 Scafaro AP, Yamori W, Carmo-Silva AE, Salvucci ME, von Caemmerer S, Atwell BJ
Nishijima R, Ikeda TM, Takumi S (2018) Genetic mapping reveals a dominant awn- (2012) Rubisco activity is associated with photosynthetic thermotolerance in a
inhibiting gene related to differentiation of the variety anathera in the wild wild rice (Oryza meridionalis). Physiol Plant 146:99–109. https://doi.org/10.1111/
diploid wheat Aegilops tauschii. Genetica 146:75–84. https://doi.org/10.1007/ j.1399-3054.2012.01597.x
s10709-017-9998-2 Schneider A, Molnár I, Molnár-Láng M (2008) Utilisation of Aegilops (goatgrass) spe-
Nishimura K, Moriyama R, Katsura K, Saito H, Takisawa R, Kitajima A et al. (2018) The cies to widen the genetic diversity of cultivated wheat. Euphytica 163:1–19.
early flowering trait of an emmer wheat accession (Triticum turgidum L. ssp. https://doi.org/10.1007/s10681-007-9624-y
dicoccum) is associated with the cis‑element of the Vrn-A3 locus. Theor Appl Scoffoni C, Chatelet DS, Pasquet-kok J, Rawls M, Donoghue MJ, Edwards EJ et al.
Genet 131:2037–2053. https://doi.org/10.1007/s00122-018-3131-5 (2016) Hydraulic basis for the evolution of photosynthetic productivity. Nat
Ober ES, Alahmad S, Cockram J, Forestan C, Hickey LT, Kant J et al. (2021) Wheat root Plants 2:16072. https://doi.org/10.1038/nplants.2016.72
systems as a breeding target for climate resilience. Theor Appl Genet Sears ER (1977) Genetics Society Of Canada Award Of Excellence Lecture: an induced
134:1645–1662. https://doi.org/10.1007/s00122-021-03819-w mutant with homoeologous pairing in common wheat. Can J Genet Cytol 19:4.
Ociepa T (2019) The oat gene pools – review about the use of wild species in https://doi.org/10.1139/g77-063
improving cultivated oat. J Cent Eur Agric 20:251–261. https://doi.org/10.5513/ Setter T, Waters I (2003) Review of prospects for germplasm improvement for
JCEA01/20.1.2044 waterlogging tolerance in wheat, barley and oats. Plant Soil 253:1–34. https://
Ogbonnaya FC, Imtiaz M, Bariana HS, McLean M, Shankar MM, Hollaway GJ (2008) doi.org/10.1023/A:1024573305997
Mining synthetic hexaploids for multiple disease resistance to improve bread Sharma S, Sharma R, Govindaraj M, Mahala RS, Satyavathi CT, Srivastava RK et al.
wheat. Aust J Agric Res 59:421–431 (2020) Harnessing wild relatives of pearl millet (Pennisetum glaucum L. R. Br) for
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
302
germplasm enhancement: challenges and opportunities. Crop Sci 61:177–200. Wilson MJ, Fradera‐Soler M, Summers R, Sturrock CJ, Fleming AJ (2021) Ploidy
https://doi.org/10.1002/csc2.20343 influences wheat mesophyll cell geometry, packing and leaf function. Plant
Singh VJ, Vinod KK, Krishnan SG, Singh AK (2021) Rice adaptation to climate change: Direct 5:e00314
opportunities and priorities in molecular breeding. In: Hossain MA, Hassan L, Winfield MO, Wilkinson PA, Allen AM, Barker GLA, Coghill JA, Burridge A et al. (2012)
Ifterkharuddaula KM, Kumar A, Henry R (eds) Molecular breeding for rice abiotic Targeted re-sequencing of the allohexaploid wheat exome. Plant Biotechnol J
stress tolerance and nutritional quality. John Wiley & Sons, Ltd. pp 1–25 https:// 10:733–742. https://doi.org/10.1111/j.1467-7652.2012.00713.x
doi.org/10.1002/9781119633174.ch1 Winfield MO, Allen AM, Burridge AJ, Barker GLA, Benbow HR, Wilkinson PA et al.
South PF, Cavanagh AP, Liu HW, Ort DR (2019). Synthetic glycolate metabolism (2016) High-density SNP genotyping array for hexaploid wheat and its sec-
pathways stimulate crop growth and productivity in the field. Science 363: ondary and tertiary gene pool. Plant Biotechnol J 14:1195–1206. https://doi.org/
eaat9077. https://doi.org/10.1126/science.aat9077 10.1111/pbi.12485
Swarbreck SM, Wang M, Wang Y, Kindred D, Sylvester-Bradley R, Shi W et al. (2019) A Winfield MO, Allen AM, Wilkinson PA, Burridge AJ, Barker GLA, Coghill JA et al. (2018)
roadmap for lowering crop N requirement. Trends Plant Sci 24:892–904 https:// High-density genotyping of the A.E. Watkins Collection of hexaploid landraces
doi.org/10.1016/j.tplants.2019.06.006. identifies a large molecular diversity compared to elite bread wheat. Plant
Takenaka S, Kawahara T (2012) Evolution and dispersal of emmer wheat (Triticum sp.) Biotechnol J 16:165–175. https://doi.org/10.1111/pbi.12757
from novel haplotypes of Ppd-1 (photoperiod response) genes and their sur- Wingen LU, Orford S, Goram R, Leverington-Waite M, Bilham L, Patsiou TS et al.
rounding DNA sequences. Theor Appl Genet 125:999–1014. https://doi.org/ (2014) Establishing the A. E. Watkins landrace cultivar collection as a resource
10.1007/s00122-012-1890-y for systematic gene discovery in bread wheat. Theor Appl Genet
Takumi S, Koyama K, Fujiwara K, Kobayashi F (2011) Identification of a large deletion 127:1831–1842
in the first intron of the Vrn-D1 locus, associated with loss of vernalization Wingen LU, West C, Leverington M, Collier S, Orford S, Goram R et al. (2017) Wheat
requirement in wild wheat progenitor Aegilops tauschii Coss. Genes Genet Syst landrace genome diversity. Genetics 205:1657–1676. https://doi.org/10.1534/
86:183–195 genetics.116.194688
Talame V, Sanguineti MC, Chiapparino E, Bahri H, Salem M, Forster BP et al. (2004) Worland AJ, Snape JW (2001) Genetic basis of worldwide wheat varietal improve-
Identification of Hordeum spontaneum QTL alleles improving field performance ment. In: Bonjean AP, Angus WP (eds) World wheat book – a history of wheat
of barley grown under rainfed conditions. Ann Appl Biol 144:309–319. https:// breeding. Lavoisier Publishing, Paris, France, p 59–100
doi.org/10.1111/j.1744-7348.2004.tb00346.x Wright TIC, Burnett AC, Griffiths H, Kadner M, Powell JS, Oliveira HR et al. (2020)
Tanaka M, Yamashita K (1957) Growth habit of Aegilops squarrosa strains collected in Identification of quantitative trait loci relating to flowering time, flag leaf and
Pakistan, Afghanistan and Iran. Wheat Inform Serv 6:16–18 awn characteristics in a novel Triticum dicoccum mapping population. Plants
Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic 9:829. https://doi.org/10.3390/plants9070829
potential from the wild. Science 5329:1063–1066 Würschum T, Rapp M, Miedaner T, Longin CFH, Leiser WL (2019) Copy number var-
Tanksley SD, Young ND, Paterson AH, Bonierbale MW (1989) RFLP mapping in plant iation of Ppd-B1 is the major determinant of heading time in durum wheat. BMC
breeding: new tools for an old science. Bio/Technol 7:257–264. https://doi.org/ Genet 20:1–8. https://doi.org/10.1186/s12863-019-0768-2
10.1038/nbt0389-257 Xu C, Ren Y, Jian Y, Guo Z, Zhang Y, Xie C et al. (2017) Development of a maize 55 K
Taylor SH, Long SP (2017) Slow induction of photosynthesis on shade to sun tran- SNP array with improved genome coverage for molecular breeding. Mol Breed
sitions in wheat may cost at least 21% of productivity. Philos Trans R Soc B: Biol 37:20. https://doi.org/10.1007/s11032-017-0622-z
Sci 372:20160543 Yoshida T, Nishida H, Zhu J, Nitcher R, Distelfield A, Akashi Y et al. (2010) Vrn-D4 is a
Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2011) Shovelomics: high throughput vernalisation gene located on the centromeric region of chromosome 5D in
phenotyping of maize (Zea mays L.) root architecture in the field. Plant Soil hexaploid wheat. Theor Appl Genet 120:543–552
341:75–87. https://doi.org/10.1007/s11104-010-0623-8 Yu H, Luedeling E, Xu J (2010) Winter and spring warming result in delayed spring
Tricker PJ, ElHabti A, Schmidt J, Fleury D (2018) The physiological and genetic basis of phenology on the Tibetan Plateau. Proc Natl Acad Sci USA 107:22151–22156
combined drought and heat tolerance in wheat. J Exp Bot 69:3195–3210. Zhao N, Zhu B, Li M, Wang L, Xu L, Zhang H et al. (2011) Extensive and heritable
https://doi.org/10.1093/jxb/ery081 epigenetic remodeling and genetic stability accompany allohexaploidization of
Tsunewaki K (1966) Comparative gene analysis of common wheat and its wheat. Genetics 188:499–510
ancestral species. II. Waxiness, growth habit and awnedness. Jpn J Bot Zhang X, Zhou S, Fu Y, Su Z, Wang X, Sun C (2006) Identification of a drought
19:175–229 tolerant introgression line derived from Dongxiang common wild rice (O.
Uauy C (2017) Wheat genomics comes of age. Curr Opin Plant Biol 36:142–148. rufipogon Griff.). Plant Mol Biol 62:247–259. https://doi.org/10.1007/s11103-
https://doi.org/10.1016/j.pbi.2017.01.007 006-9018-x
Ullah S, Bramley H, Daetwyler H, He S, Mahmood T, Thistlethwaite R et al. (2018) Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater
Genetic contribution of emmer wheat (Triticum dicoccon Schrank) to heat tol- yield. Annu Rev Plant Biol 61:235–261
erance of bread wheat. Front Plant Sci 9:1529
van Slageren MW (1994) Wild wheats: a monograph of Aegilops L. and Amblyo-
pyrum (Jaub. and Spach) Eig (Poaceae). Wageningen Agricultural University,
1994. ACKNOWLEDGEMENTS
Volk GM, Chao CT, Norelli J, Brown SK, Fazio G, Peace C et al. (2015) The vulnerability
We acknowledge support from the Biotechnology and Biological Sciences Research
of US apple (Malus) genetic resources. Genet Resour Crop Evol 62:765–794.
Council (BBSRC) Cross-Institute Strategic Programme ‘Designing Future Wheat’ BB/
https://doi.org/10.1007/s10722-014-0194-2
P016855/1. We thank Lorna McAusland (University of Nottingham) for the image of a
von Caemmerer S, Furbank RT (2016) Strategies for improving C4 photosynthesis.
cleared flag leaf (Fig. 1), Bethany Love (NIAB) for the image of the wheat ear (Fig. 1)
Curr Opin Plant Biol 31:125–134. https://doi.org/10.1016/j.pbi.2016.04.003
and Howard Griffiths (University of Cambridge) for insightful discussions on
Voss-Fels KP, Stahl A, Wittkop B, Lichthardt C, Nagler S, Rose T (2019) Breeding
physiological variation. This paper is dedicated to the memory of our friend Shigeo
improves wheat productivity under contrasting agrochemical input levels. Nat
Takumi from Kobe University, Japan who passed away on 4 June 2020. We are
Plants 5:706–714. https://doi.org/10.1038/s41477-019-0445-5
grateful for his kindness and for all that he contributed to the understanding of
Walker BJ, VanLoocke A, Bernacchi CJ, Ort DR (2016) The costs of photorespiration to
variation in Aegilops tauschii.
food production now and in the future. Annu Rev Plant Biol 67:107–129
Walkowiak S, Gao L, Monat C, Haberer G, Kassa MT, Brinton J (2020) Multiple wheat
genomes reveal global variation in modern breeding. Nature 588:277–283.
https://doi.org/10.1038/s41586-020-2961-x
Weyhrich RA, Carver BF, Martin BC (1995) Photosynthesis and water-use efficiency AUTHOR CONTRIBUTIONS
of awned and awnletted near-isogenic lines of hard red winter wheat. Crop FJL, TICW, RAH and ARB developed and designed the review content and format. SD
Sci 35:172–176. https://doi.org/10.2135/cropsci1995.0011183X003500010 was responsible for broadening the review scope to include further cereal crop
032x species and progenitors. All authors contributed to writing and reviewing the
Weigmann M, Maurer A, Pham A, March TJ, Al-Abdallat A, Thomas WTB, Bull HJ et al. manuscript.
(2019) Barley yield formation under abiotic stress depends on the interplay
between flowering time genes and environmental cues. Sci Rep 9:1–16. https://
doi.org/10.1038/s41598-019-42673-1
Wilhelm EP, Turners AS, Laurie DA (2009) Photoperiod insensitive Ppd-A1a mutations COMPETING INTERESTS
in tetraploid wheat (Triticum durum Desf.). Theor Appl Genet 118:285–294 The authors declare no competing interests.
Heredity (2022) 128:291 – 303
F.J. Leigh et al.
303
ADDITIONAL INFORMATION Open Access This article is licensed under a Creative Commons
Correspondence and requests for materials should be addressed to Alison R. Bentley. Attribution 4.0 International License, which permits use, sharing,
adaptation, distribution and reproduction in anymedium or format, as long as you give
Reprints and permission information is available at http://www.nature.com/reprints appropriate credit to the original author(s) and the source, provide a link to the Creative
Commons license, and indicate if changes were made. The images or other third party
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims material in this article are included in the article’s Creative Commons license, unless
in published maps and institutional affiliations. indicated otherwise in a credit line to the material. If material is not included in the
article’s Creative Commons license and your intended use is not permitted by statutory
regulation or exceeds the permitted use, you will need to obtain permission directly
from the copyright holder. To view a copy of this license, visit http://creativecommons.
org/licenses/by/4.0/.
© The Author(s) 2022
Heredity (2022) 128:291 – 303