Global Food Security 33 (2022) 100636 Contents lists available at ScienceDirect Global Food Security journal homepage: www.elsevier.com/locate/gfs Responsible plant nutrition: A new paradigm to support food system transformation Achim Dobermann a,*, Tom Bruulsema b, Ismail Cakmak c, Bruno Gerard d, Kaushik Majumdar e, Michael McLaughlin f, Pytrik Reidsma g, Bernard Vanlauwe h, Lini Wollenberg i, Fusuo Zhang j, Xin Zhang k a International Fertilizer Association (IFA), Paris, France b Plant Nutrition Canada, Ottawa, Ontario, Canada c Sabanci University, Istanbul, Turkey d Mohamed VI Polytechnic University (UM6P), Benguérir, Morocco e African Plant Nutrition Institute (APNI), Benguérir, Morocco f School of Agriculture Food and Wine, University of Adelaide, Adelaide, Australia g Plant Production Systems, Wageningen University & Research, the Netherlands h International Institute of Tropical Agriculture (IITA), Nairobi, Kenya i CGIAR Climate Change, Agriculture & Food Security Program, Burlington, VT, USA j Center for Resources, Environment and Food Security, China Agricultural University, Beijing, China k University of Maryland Center for Environmental Science, Frostburg, MD, USA A R T I C L E I N F O A B S T R A C T Keywords: The coming 10–20 years will be most critical for making the transition to a global food system in which mineral Plant nutrition nutrients in agriculture must be managed in a more holistic manner. Fertilizers play a particular role in that Nutrients because they are among the key drivers for securing global food security and improving human nutrition through Nutrient use efficiency increased crop yields and nutritional quality. A new paradigm for responsible plant nutrition follows a food Fertilizer Sustainable intensification systems and circular economy approach to achieve multiple socioeconomic, environmental and health objec- Circular economy tives. Achieving that requires utilizing all available organic and inorganic nutrient sources with high efficiency, tailored to the specific features of food systems and agroecosystems in different world regions. Critical actions include: (i) sustainability-driven nutrient roadmaps, (ii) digital crop nutrition solutions, (iii) nutritious crops, (iv) nutrient recovery and recycling, (v) climate-smart fertilizers, and (vi) accelerated innovation. The outcome of this transformation will be a new societal plant nutrition optimum rather than a purely economic optimum. New partnerships and sustainability-focused business models will create added value for all actors in the nutrient chain and benefit farmers as well as consumers. Research needs to become more problem-driven and merge excellent science with entrepreneurial innovation approaches in order to develop robust solutions faster and at larger scale. Evidence-based policies should focus on creating and supporting the necessary nutrient stewardship roadmaps, including realistic national targets, progressive regulation and incentives that support technology and business innovation. 1. The complex role of crop nutrients in feeding the world annual rate of about 2.2% during the past 60 years (Fuglie, 2018). Along sustainably with that, nutrient land productivity has increased by 2.7–2.9% per year for calories and proteins, and between 2.1 and 4.6% for fats, although Historically, economic development has been faster in world regions with huge variation across the world (Tuninetti et al., 2020). Agricul- where fertilizer use and crop yields rose in parallel (McArthur and tural production growth has relied on both cropland expansion and McCord, 2017). World agricultural output has grown at an average intensification, with both also driving a massive rise in global fertilizer Abbreviations: GHG, greenhouse gas emissions; NuUE, nutrient use efficiency; NUE, nitrogen use efficiency; SDG, Sustainable Development Goal. * Corresponding author. International Fertilizer Association (IFA), 49 avenue d’Iena, 75116 Paris, France. E-mail address: adobermann@fertilizer.org (A. Dobermann). https://doi.org/10.1016/j.gfs.2022.100636 Received 22 December 2021; Received in revised form 28 March 2022; Accepted 30 March 2022 Available online 10 April 2022 2211-9124/© 2022 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 consumption. During the Green Revolution, except for much of the Af- Although estimates vary widely, the global N surplus on cropland – rican continent, the prevailing mode of agricultural production growth calculated as N inputs from fertilizer, manure, biological N fixation and has been through increasing yields and efficiency of inputs (Fuglie, other sources minus N removed with harvested products – has increased 2018), but including periods of regional land expansion in response to from less than 20 million t N yr− 1 in 1961 to roughly 90 million t N yr− 1 food security concerns or global market opportunities. A major concern in 2010 (Zhang et al., 2021b). Of even greater concern is the global is that for all of the world’s most important crops – rice, wheat, maize divide, ranging from large nutrient surpluses in some regions to nutrient and soybean – the relative contribution of cropland expansion to total deficits in others (Fig. 1). production increase was larger during 2002–2014 than during the When interpreting Fig. 1 it should be noted that environmental 1980–2002 period (Cassman and Grassini, 2020). Just in the past two pollution only starts to increase when the N surplus is well above zero decades, global cropland area has increased by another 63 million ha, (McLellan et al., 2018; Quemada et al., 2020). Likewise, a small N sur- whereas forest land declined by 94 million ha (FAO, 2021). plus or a neutral N balance may already indicate the presence of soil N However, significant intensification and expansion of agricultural mining over time, which is also not desirable. In recent decades, regional production both had wide-ranging social, economic and environmental differences have become further aggravated by transnational nutrient impacts. On one hand, higher crop yields and more productive animals transfers associated with global trade of feed and food (Grote et al., have saved billions of people from starvation and millions of hectares of 2005; Parviainen and Helenius, 2020). Many high-income countries natural ecosystems from being converted to agriculture since the 1960s thus outsource a significant amount of the pressure on natural resources (Pingali, 2012; Stevenson et al., 2013). On the other hand, intensive to lower-income countries (Sun et al., 2020), but they also have to face animal and crop production to support the emerging food consumption the consequences of nutrient excess caused by imports of nutrients. patterns have caused externalities that are difficult to manage. Of great On a global scale, future growth in primary crop production needs to concern are losses of reactive forms of nitrogen (N) and phosphorus (P) be decoupled from growth in fertilizer consumption, while also ac- into the environment, impacting water quality, biodiversity, air quality counting for the huge differences among regions and countries in terms and greenhouse gas (GHG) emissions. It has been suggested that of historical levels of fertilizer use and future needs. Hence, national anthropogenic perturbation levels of global N and P flows may already nutrient roadmaps and solutions for improving nutrient use efficiency exceed limits that are deemed to be a safe operating space for humanity (NuUE) will require defining specific NuUE targets for the key agricul- (Steffen et al., 2015), although the validity of such “Planetary Bound- tural sub-sectors, and carefully crafted regulatory and supporting pol- aries” remains under debate (Biermann and Kim, 2020). Furthermore, icies that also take into account the needs of farmers and the agro-food while hunger and malnutrition have significantly declined in recent industry as a whole. Encouraging progress has been made in increasing decades, they have stubbornly persisted in sub-Saharan Africa (SSA) and NuUE in regions such as North America, Western and Central Europe in other regions (Pingali et al., 2017), including micronutrient-related the past 30 years, and more recently also in China (Zhang et al., 2015). deficiencies that particularly affect women and children. What further improvements are feasible and realistic in different parts of Food security through increased crop yields will remain hugely the world? What would be the best possible nutrient use efficiencies that important in light of an expected population of about 9.5 billion by 2050 ensure high crop yields and avoid excessive surpluses as well as (Vollset et al., 2020), but future yield increases should go hand-in-hand long-term depletion of soil nutrient stocks over time? How can this be with improvements in environmental and socio-economic outcomes. implemented across the world, including regions in which subsistence The coming 10–20 years will be critical for making the transition to a farming remains dominant? global food system in which we produce and consume food in a more sustainable manner (Willett et al., 2019; Herrero et al., 2020), miti- (2) What are the key measures to double or triple crop yields in Africa gating much of the estimated $12 trillion hidden health, environmental with increasing and balanced nutrient inputs? and socio-economic costs of it (FOLU, 2019). Over 20 different mineral elements are known to be critical for plant, animal and/or human health Crop yields in most African countries have risen very slowly, causing (Zoroddu et al., 2019; Brown et al., 2021) and many of them enter the the land area under cultivation to more than double in size, whereas food system through crops and grasslands, i.e. from soil, fertilizers, agricultural growth in Asia has been largely driven by yield increases on organic manures, biological N fixation and few other sources. Hence, existing land (Fig. 2). plant nutrients are at the core of the food system transformation because Africa has massive nutrient deficits that must be overcome to in- they drive both primary food production and many of the externalities crease crop yields and achieve higher levels of food security within the caused by it. next few decades (van Ittersum et al., 2016; Berge et al., 2019). Annual Here we present a new paradigm for managing plant nutrients average nutrient balances in sub-Saharan Africa were estimated to be throughout their life cycle, but we also point out that the priorities and about − 26 kg N ha− 1, -3 kg P ha− 1, and -19 kg K ha− 1 in 2000 (Stoor- specific solutions for that will vary widely. We present this new para- vogel et al., 1993). Although fertilizer use has increased somewhat since digm mainly from the perspective of the fertilizer industry and the new then, crop yields have increased somewhat too. Hence, in most coun- roles it should play in the food system, recognizing, however, that many tries, net nutrient input-output balances have not improved at all. In other stakeholders have to make big changes as well. reality, there are widespread and unsustainable levels of soil nutrient depletion in most of sub-Saharan Africa, which has been known for a 2. Tough challenges for future plant nutrition long time. . In 2006, at a historic Africa Fertilizer Summit in Abuja, Nigeria, Future plant nutrition solutions will have to address multiple global heads of state and government declared that “Given the strategic and regional challenges related to nutrients in the food system. In that importance of fertilizer in achieving the African Green Revolution to end context, below we discuss ten higher-level, interconnected questions hunger, the African Union Member States resolve to increase the level of that need to be tackled with urgency. use of fertilizer from the current average of 8 kg per hectare to an average of at least 50 kg per hectare by 2015”. However, excluding (1) How can future growth in primary crop production be decoupled South Africa, average fertilizer use in sub-Saharan Africa in 2019 was from growth in fertilizer consumption? How can we overcome only about 15 kg N + P O − 1 2 5+K2O ha (Source: IFASTAT). Only two the current global nutrient imbalance? countries have achieved the 50 kg ha− 1 target (Kenya and Botswana), whereas six have at least moved to the 30–50 kg ha− 1 range (Ethiopia, For many decades, rising crop production was closely coupled with Zimbabwe, Zambia, Malawi, Benin and Mali), or have much higher increasing input of N and other nutrients, mostly from fertilizer. fertilizer rates in specific crops already, such as maize in Ethiopia 2 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 Fig. 1. Global cropland nitrogen surplus or deficit in 2015. Source: Xin Zhang and Guolin Yao, University of Maryland Center for Environmental Science; updated from previous estimates. analysis for China suggests that the simultaneous implementation of just four measures - improved farm management practices with nitrogen use reductions; machine deep placement of fertilizer; enhanced-efficiency fertilizer use; and improved manure management – would increase crop yields and NUE, reduce N losses to water and massively improve air quality (Guo et al., 2020). Total benefits of US$30 billion per year would exceed the estimated US$18 billion per year in costs. (4) Can nutrient losses and waste along the whole agri-food chain be halved? Although accurate data are not available, estimates suggest that at global scale only around 16–20% of nitrogen compounds entering the food system may reach useful products, with up to 80% lost to the environment in different forms (Sutton et al., 2012; Zhang et al., 2020). However, there are huge variations in full-chain NUE among countries, Fig. 2. Relative changes in grain yield and land area used for growing cereals and such estimates also do not account for N that contributes to net (rice, wheat, maize, barley, sorghum, millet) in Asia and Africa, and in selected increases in soil organic matter, which may also be a desirable outcome countries of sub-Saharan Africa. Data shown are 5-year averages for 1961–2015 with regard to soil health and GHG mitigation. In Europe, due to and a 3-year average for the period 2016–2018. The average of 1961–1965 was set as 100. Source: FAOSTAT (https://www.fao.org/faostat/). structural differences of the agricultural sector, full-chain NUE ranges from 10% in Ireland to 40% in Italy (Erisman et al., 2018). Global supply chains are needed to ensure adequate and stable food supply, but po- (Assefa et al., 2021). Fertilizer alone will not be sufficient to lift crop tential also exists for more local food production and reduced food yields, but it is the key ingredient to trigger a uniquely African Green movement (Kinnunen et al., 2020). Whether that would also reduce Revolution in areas that are favorable for intensification (Vanlauwe and nutrient losses and GHG emissions is not yet fully clear. Dobermann, 2020). This must be based on good information, incentives Reducing food waste and shifting to healthier diets would positively for efficient use of nutrients to avoid environmental harm, and specific impact NuUE, nutrient losses and fertilizer requirements in national measures to tackle the still persistent forms of malnutrition. food systems, but the best outcomes can be achieved in combination with other measures that enhance crop and animal productivity (Ma (3) What data-driven technologies, business solutions and policies et al., 2019). Besides, transitions to more plant-based diets may also will accelerate the adoption of more precise nutrient manage- create additional wastewater P burdens and treatment requirements ment solutions by farmers? (Forber et al., 2020). New technologies will likely increase the recovery of nutrients from different organic wastes in the food system in forms In many countries, farmers apply too much fertilizers because they that allow safe recycling back to crop production, thus enabling a more are affordable and they do not want to risk losses of yield. In other sit- circular nutrient economy. What levels of reductions in full-chain uations, farmers may not apply sufficient nutrients or apply them in the nutrient losses and increases in nutrient recovery and recycling can wrong ways because of lack of access, affordability, or information and realistically be achieved and at what cost? knowledge. Many good examples exist worldwide for how to overcome this through more precise management of nutrients (Chen et al., 2014; (5) How can nutrient cycles in crop and livestock farming be closed? Chivenge et al., 2021), but only few have found wider adoption, even in high-income countries with sophisticated policies and technologies About 25 billion poultry birds, 2.2 billion sheep and goats, 1.7 billion (Silva et al., 2021; Cassman and Dobermann, 2022). Understanding and cattle and buffaloes, and 1 billion pigs are now raised and consumed by overcoming that will be of particular importance for increasing nitrogen humans. In many countries, globally operating production and con- use efficiency (NUE) in crop production from currently about 50% to at sumption drivers and supply chains (Sun et al., 2020) have caused a least 70% within the next two decades, a level that is entire feasible if separation and concentration of crop and livestock farming, resulting in many of the available, known measures could be implemented widely spatially disconnected, leaky nutrient cycles. The massive growth of the (Hutchings et al., 2020). The potential benefits could be large. A recent livestock sector has led to low NuUE in the whole food chain, increased 3 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 waste and large GHG emissions (Erisman et al., 2018; Uwizeye et al., climate change-linked stress conditions. Balanced plant nutrition has 2020). Farmed animals consume more than one-third of the world’s particular roles in increasing the tolerance to drought (Waraich et al., cereal grain, as well as about a quarter of all pulses and starchy roots and 2011), heat (Mengutay et al., 2013; Sarwar et al., 2019) or high radia- tubers grown. Global livestock supply chains currently emit 65 Tg N yr− 1 tion (Marschner and Cakmak, 1989), and can thus be an important tool to air and water in the form of NO (29 Tg N yr− 1), NH (26 Tg N yr− 13 3 ), for managing climatic risks. Several nutrients are also directly involved NO (8 Tg N yr− 1x ) and N2O (2 Tg N yr− 1), which is equivalent to in reducing pathogenic infection and increasing disease resistance of one-third of the human-induced N emissions (Uwizeye et al., 2020). crop plants (Wang et al., 2013; Elmer and Datnoff, 2014; Cabot et al., Sustainable livestock production involves many steps (Eisler et al., 2019), mainly by improving cell wall stability and increasing the pool of 2014), including more pasture-based systems and re-integration of crop defense metabolites against pathogen attack (Marschner, 2012). and livestock farming. If used for what they are good at - converting Changes in seasonality, precipitation and extreme weather events will by-products from the food system and forage resources into valuable affect the timing and efficiency of nutrient uptake, requiring integration food and manure - farm animals can play a huge role in future, more of nutrient advisories with early warning and climate information circular farming and food systems (van Zanten et al., 2019). Moreover, systems. optimized micronutrient strategies are required for pasture-based live- stock systems because inadequate micronutrients in soils and pasture (8) What are realistic options and targets for reducing fertilizer- can affect micronutrient absorption and hence animal health and pro- related greenhouse gas emissions? duction, while animal excreta can also be the major input of micro- nutrients to pasture (Kao et al., 2020). Besides healthier diets with In 2015, annual food-system GHG emissions amounted to 18 Gt CO2 reduced meat consumption, recoupling livestock and cropping systems equivalent, representing 34% of total global GHG emissions (Crippa offers a major path to sustainable agriculture (Herrero et al., 2010), but et al., 2021). About 71% of that came from agricultural production and mixed crop–livestock systems often require higher capital to establish land use. Therefore, all pathways that limit global warming to well and are also more difficult to manage (Thornton and Herrero, 2015). below 2 ◦C require land-based mitigation and land-use change (IPCC, What future farm structures, technologies and supply chains will enable 2019). Improvements in the efficiency of agricultural production pro- a better crop-livestock integration? cesses and reductions in land conversions have led to fairly stable levels of total GHG emissions from agriculture production and land use over (6) How can we sustain and improve soil health? the last 30 years, resulting in a 35% decrease on a per capita basis (Crippa et al., 2021). At issue is, what more can be done across the entire Soils are a growing medium for crops, but they also support other nutrient chain to reduce agricultural GHG emissions, including fertilizer essential ecosystem services, such as: water purification, carbon production (Scope 1 and Scope 2 emissions), farm management of nu- sequestration, nutrient cycling and the provision of habitats for biodi- trients (Scope 3 emissions) and nutrient recycling. At present, energy use versity (Bünemann et al., 2018). Translating these multiple functions in ammonia synthesis alone accounts for more than 1% of global GHG into practical indicators and approaches for soil and nutrient manage- emissions (measured in carbon dioxide equivalents). ment remains challenging (Bünemann et al., 2018; Rinot et al., 2019). Besides decarbonizing the industrial production of fertilizers, farm Incentivizing multi-objective management is also difficult when current gate emissions of nitrous oxide (N2O) from mineral and organic fertil- management focuses on a single primary function, such as crop pro- izers are of particular interest because they amount to about 0.6 GtCO2e duction. There is no ideal soil for everything, but purpose-driven eval- and 1.0 GtCO2e, which together comprises nearly 10% of total food and uation of specific soil functions offers a more pragmatic route to soil land use GHG emissions (based on FAO data released in 2021). They can health management (Vogel et al., 2019). be reduced through a range of interventions, including novel fertilizer Carbon and nutrient inputs are important triggers for sustaining and products and improved agronomic practices (Maaz et al., 2021), and improving soil health in crop production, which also increases the addressing them may have greater leverage than soil carbon gains resilience of crop production systems to climate warming (Deng et al., achievable from agricultural practice changes (Lawrence et al., 2021). 2020). Whereas in the past the emphasis in plant nutrition has been on Farmer awareness is however low and often limited by critical barriers soil fertility, i.e. the nutrient supplying capacity of soils, a new paradigm (Gomes and Reidsma, 2021). Sequestration of atmospheric CO2 in soils has to contribute to broader aspects of soil health. For example, can also contribute to reducing global warming and improving soil sequestration of atmospheric CO2 in soils can potentially contribute to health. However, the mitigation potential of practices such as conser- reducing global warming and improving soil health, but it requires vation agriculture or crop residue incorporation has often been over- continuous inputs of organic material and nutrients (particularly N and stated (Poulton et al., 2018; Corbeels et al., 2020). The process would P) to form stable soil organic matter, and having these nutrients avail- require increased biomass production for continuous organic matter able in the right places (van Groenigen et al., 2017; Spohn, 2020; Martin inputs, balanced nutrient inputs of nitrogen, phosphorus and sulfur et al., 2021). How can a holistic plant nutrition approach manage macro- (Kirkby et al., 2016; Huang et al., 2020; Spohn, 2020), reducing soil and micro-nutrients for high crop productivity and NuUE, but also uti- disturbance and preventing erosion to form stable soil organic matter. lize biological N fixation, optimize carbon storage and turnover, in- Social, economic, and verification impediments would also need to be crease soil biodiversity, and avoid soil acidification or other forms of overcome (Amundson and Biardeau, 2018). Besides wanting to degradation? sequester more carbon from the atmosphere, an immediate need is to actually prevent further soil carbon losses because global warming may (7) How will mineral nutrition of crops change in changing climates? further accelerate the decomposition of soil organic matter (Nottingham et al., 2020). Mineral nutrients in soils and crops have important and still difficult to predict positive as well as negative interactions with global climate (9) How can cropping systems deliver high quality, more nutritious change (Lynch and Clair, 2004; Soares et al., 2019), although negative food? impacts of climate change appear to outweigh positive ones (St.Clair and Lynch, 2010). Rising atmospheric CO2 may increase crop yields, but it More than 2 billion people in the world are affected by various forms may also cause declining nutritional quality, particularly in crops that of micronutrient malnutrition (e.g. iron, zinc, iodine, selenium), which rely on C3-photosynthesis, such as wheat, barley, rice, soybean and increases child mortality, childhood stunting, anemia and susceptibility others (Brouder and Volenec, 2017; Soares et al., 2019; Ebi et al., 2021). to many infectious diseases, but also affects many cognitive functions. In The mineral status of plants will become even more important under Africa, correlations can be found between soil nutrients and child 4 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 mortality, stunting, wasting and underweight (Berkhout et al., 2019). In understanding the mechanisms of nutrient cycling and their functions in 2011 3.5 billion people were at risk of calcium (Ca) deficiency due to microbial and plant metabolism (Marschner, 2012). Human re- inadequate dietary supply, mostly in Africa and Asia (Kumssa et al., quirements and mass balance principles also make it clear that fertilizers 2015). Current agricultural practices have also contributed to a decline will continue to be major ingredients of more sustainable food systems. in dietary potassium (K) intake and rise in hypokalemia prevalence in However, future plant nutrition must meet multiple objectives that the US population (Sun and Weaver, 2020). directly and indirectly contribute to many of the SDGs that now guide Cereals alone are grown on half of the world’s cropland and they also humanity (Ladha et al., 2020). Integrated, tailored plant nutrition consume half of the world’s fertilizer. They are hugely important for strategies and practices need to minimize tradeoffs between productiv- human nutrition as major sources of dietary energy, essential proteins, ity and the environment, and they need to be viable in the farming and mineral elements, and diverse bioactive food components (Poole et al., business systems of different nations and localities. Integration in this 2020). However, mineral nutrient concentrations of cereal crops appear context has several dimensions: a multi-nutrient food system approach, to have declined in recent decades due to higher yields, narrower crop greater recycling and utilization of all available nutrient sources, genetics, and/or soil nutrient depletion (Fan et al., 2008). Thus far, at alignment with agronomic and stewardship practices, and compliance global scale the benefits of increased yield to supply more food for with high sustainability standards. expanding populations appear to outweigh such nutrient dilution effects Therefore, as a key element of sustainable intensification of crop (Marles, 2017). On the other hand, increasing cereal grain food pro- production, the new paradigm for responsible plant nutrition encom- cessing results in Mg loss and reduced dietary Mg intake worldwide passes a broad array of scientific and engineering know-how, technol- (Rosanoff and Kumssa, 2020). A handful of micronutrient-poor crops ogies, agronomic practices, business models and policies that directly or dominate the global food and feed chains and have often also decreased indirectly affect the production, utilization and recycling of mineral crop diversity or displaced traditional crops with higher nutrient den- nutrients in agri-food systems. Following a food systems and circular sity, such as pulses (Welch et al., 2013). What plant nutrition solutions economy approach, responsible plant nutrition aims to (Fig. 3): can be effectively deployed at large scales to improve human nutrition through more nutritious crops and cropping systems? Who should pay • Improve income, productivity, nutrient efficiency and resilience of for that? farmers and businesses supporting them • Increase nutrient recovery and recycling from waste and other (10) How can we better monitor nutrients and implement nutrient under-utilized resources stewardship? • Lift and sustain soil health, including soil carbon • Enhance human health through nutrition-sensitive agriculture Numerous efforts have been made in recent years to develop and • Minimize greenhouse gas emissions, nutrient pollution and biodi- evaluate indicators for nutrient performance in fields and farms (Que- versity loss mada et al., 2020), at national (Karimi et al., 2020) and at global scale (Zhang et al., 2015). Assessing nutrient footprints (Einarsson and Besides applying nutrients in the right manner, it also entails other Cederberg, 2019) or GHG emissions (Walling and Vaneeckhaute, 2020) measures that contribute to optimizing nutrient flows. Crop genetic and life cycles (Hasler et al., 2015) of different types of fertilizers have improvement, better crop rotations, legumes, soil tillage, liming, residue also become more common, including in industry. Governments have management, water management, pests and diseases management, increasing requirements for monitoring progress against Sustainable livestock, nutrient recycling from waste streams, data and effective in- Development Goals (SDGs), including nutrient-related targets and in- formation transfer are all important measures for reducing nutrient dicators in SDG 2 (Gil et al., 2019) and others. At global level, an In- losses and increasing NuUE. Responsible plant nutrition will contribute ternational Code of Conduct for the Sustainable Use and Management of much to a more nature-positive approach of food production and con- Fertilizers has recently been published by FAO (22). In industry, com- sumption that has recently been proposed. We note, however, that the panies have increasing requirements for Environmental, Social, and latter requires a much clearer definition and that it should not aim to Governance (ESG) monitoring and reporting to demonstrate higher blindly copy nature because nature has not been optimized for human levels of transparency, traceability, quality control, accountability and food production. On the other hand, many proven, good agronomic sustainability throughout all business areas. practices are not that different from commonly proposed agroecological At issue is how all these diverse efforts can be made more coherent principles (FAO, 2018; Wezel et al., 2020), and should therefore be and operational, and how the underlying data can be improved to adapted more widely. reduce the huge uncertainties associated with even basic information on Below we elaborate on six key actions required to implement nutrient use and NuUE (Zhang et al., 2021b). Of particular importance responsible plant nutrition worldwide. We also refer to several specific are efforts to benchmark NuUE for individual fields because those are examples, which are described in greater detail in the Supplementary often more useful than looking at average balances for whole farms or Information document. aggregated over larger spatial scales. Field-level indicators are most useful for farmers to diagnose their fields in relation to the level of yield 3.1. Action 1: Sustainability-driven nutrient roadmaps for a given level of nutrient input and management practice (and vice versa), serving as a concrete starting point to identify pathways for We define nutrient roadmaps as a combination of sustainability- improvement (Tenorio et al., 2020). driven policies, technologies and business models that aim to optimize Digital technologies offer great potential for better monitoring, nutrient use and NuUE in agriculture within each country in the next analysis, benchmarking, reporting and certification of sustainability 10–20 years. They by and large don’t exist yet. They must be linked to efforts across the entire nutrient chain, including tracking the impact of the SDGs and tailored to the specific food systems and natural endow- better practices, technologies and policies. This will become critical for ments in every country, with ambitious but realistic targets for NuUE as business transformation, evidence-based policy making, and stake- the key driver for productivity and reduced nutrient losses. For nitrogen, holder communication. for example, spatially explicit boundaries can be defined to meet air and water quality targets, while also having to meet minimum production 3. Responsible plant nutrition: key elements of a new paradigm requirements (Vries et al., 2021). Nutrient monitoring, nutrient stew- ardship principles (International Plant Nutrition Institute, 2016) and Mineral nutrients play a central role in agricultural production as new sustainability standards (e.g. sustainable sourcing and certification well as natural ecosystems. Impressive progress has been made in schemes) will increasingly guide policy making, business innovation and 5 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 Fig. 3. The five interconnected aims (left) of the new paradigm for responsible plant nutrition, and six key actions to take (right). farming practices. low level and drives crop yields and farming profits. Hence, starting Specific targets and priorities for designing such nutrient roadmaps from very high NuUE levels that actually represent a situation of soil and managing nutrients will vary, depending on each country’s agri- mining, NuUE declines and nutrient surplus starts to grow (Fig. 4). Many cultural sectors, natural capital, nutrient use history and sustainable countries in sub-Saharan Africa are still at the upper left end of this development priorities. Once fertilizers become readily available and trajectory. Their first priority must be to increase fertilizer use in order other technologies enable a better crop yield response, farms and to jump-start crop yield growth (Vanlauwe and Dobermann, 2020), but countries typically move along a common trajectory over many decades, do it as part of an integrated soil fertility management approach that but at varying speed (Fig. 4). The current position of several countries or utilizes all available resources and focuses on local adaptation of agro- world regions is shown for illustrative purposes. nomic interventions (see SI Example 1). At the early stages of economic development (Phase A in Fig. 4), Historically, this then leads to a longer intensification period (Phase fertilizer use, often done through blanket applications, rises from a very B in Fig. 4) during which fertilizer use and crop yields rise further, but NuUE declines even more and nutrient surpluses may become excessive. Often this is also caused by sustained fertilizer subsidies, which provide little incentive for balanced fertilizer use and optimizing NuUE. India is a good example for that, where numerous fertilizer price regulating and subsidy schemes have played a major role in driving fertilizer con- sumption since the 1970s (see SI Example 2.) As a result, N and P fer- tilizer use on cropland in India more than doubled, but the use efficiency of these nutrients declined to about 30–40% and has remained virtually unchanged at that low level. In that situation the top priority is a shift towards smarter policies that provide clear incentives to increase NuUE. Towards the end of Phase B, due to rising environmental and public health concerns, the political pressure increases and countries begin to take mitigation measures, including stricter regulation to limit nutrient use. China has entered this phase in recent years through its new green development priorities (see SI Example 3). The new policies now limit fertilizer use and focus on better technologies and agronomic practices. Consequently, NuUE has started to increase again in China in recent years (Fig. 4). That is when farms and countries start moving into phase C, which is characterized by a mix of mandatory regulation, voluntary schemes, new technologies and precision nutrient management prac- tices becoming more widely adopted by farmers. Nutrient stewardship schemes play an increasing role in all that, which, for example, have been successfully promoted by the fertilizer industry and other stake- holders in North America (see SI Example 4). The emphasis in phase C is on enabling continued growth of crop yields and profitability through rising NuUE, while decreasing the nutrient surplus. In practice, this may result in stagnating or even declining fertilizer consumption, as has been the case for most of Fig. 4. Generalized development pathway for nutrient use efficiency (NuUE) in crop production. The green line represents the general evolution in fertilizer use Western Europe and North America in recent decades. But there are over many decades. The blue curve shows the typical progression of NuUE limits for the NuUE and nutrient surpluses that can be achieved, i.e. (defined as the nutrient output/nutrient input ratio) in a country, region or farms and countries will slowly but steadily approach biophysical and farm over time, whereas the red curve illustrates the corresponding nutrient socioeconomic limits (Fig. 4). Countries, businesses and farmers can do surplus and risk of environmental pollution. (For interpretation of the refer- much to move faster towards those limits. The latter also represent ences to colour in this figure legend, the reader is referred to the Web version of ambitious but realistic targets to aim for in a particular mix of farming this article.) 6 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 systems. The NUE indicator developed by the European Nitrogen Expert ha in size, and croplands with severe yield gaps, climate-stressed loca- Panel is an excellent analytical tool for monitoring the performance of a tions and food-insecure populations often have poor service coverage farm (or a country) relative to an optimal zone in which high N output (Mehrabi et al., 2020). This gap needs to be overcome for more (crop yield) is achieved with high NUE and low N surplus (see SI knowledge-based, digital information, advisory and market integration Example 5). It provides a sound basis for setting targets, benchmarking solutions to reach impact at large scale. A lot can also be gained by farms or regions, and monitoring progress over time. Besides improving working at scales above fields and farms, i.e. at landscape and national NuUE at the field and farm level, it is important to recognize that levels in terms of targeting better fertilizer specific formulations and nutrient pollution for a region (e.g., indicated by a large nutrient surplus crop specific application recommendations, particularly in smallholder shown in Fig. 1) is also affected by the nutrient application rate and the farming (Xu et al., 2019). extent of crop production in the region, as well as the legacy effect of nutrient applications in previous years and decades (Quan et al., 2021). 3.3. Action 3: Nutrient recovery and recycling For example, even though the USA has made significant progress in improving NUE, the N surplus level for the Corn Belt is still high. Food systems and circular economy strategies require actions at Therefore, further reduction in regional nutrient pollution may require different stages and scales to optimize NuUE for the full nutrient chain efforts beyond field-level NUE improvement and may take time to (from soil to plate and back to soil). Hence, better crop-livestock inte- become tangible. gration, less food (nutrient) waste and increased nutrient recovery and In summary, targets, roadmaps and specific solutions for nutrients recycling for higher nutrient use efficiency will play increasing role in will differ among regions and countries. In many (Zone C in Fig. 4), the responsible plant nutrition paradigm (Fig. 5). This is an area of decoupling of agricultural productivity growth from growth in fertilizer exciting developments, including numerous researchers and startup use is already ongoing and NuUE has been increasing substantially (e.g. companies working on specific technologies and business solutions. North America, Western Europe, Japan), but there is still a gap to close. Political incentives, novel technologies and shifts in behavior will drive In others (Zone B), decoupling must accelerate to close large NuUE gaps even greater efforts on nutrient recovery and recycling from multiple and reduce nutrient pollution faster. In yet others (Zone A), coupling is waste streams, as a key contribution to circular bio-based economies needed to increase crop yields and improve soil health through (see SI Example 7 for a more detailed discussion). increasing nutrient inputs, but doing so in a sustainable manner. Such circular systems need to be safe and healthy for animals, Differentiated nutrient roadmaps will thus also lead to regional shifts in humans and the environment, and also allow the creation of sustainable fertilizer use, reducing nutrient surpluses in countries in some countries business models. System designs that fit into practice will have to meet while ensuring that more nutrients are moved to where they are most numerous principles and criteria (Cordell et al., 2011; Muscat et al., lacking (Fig. 1), particularly to many parts of Africa (Zhang, 2017). A 2021), also to facilitate decision-making by different stakeholders critical issue to resolve is how to develop context-specific targets and involved (Vaneeckhaute, 2021). While a circular bio-economy requires roadmaps for responsible nutrient use in a country or agricultural sector. connected sectors, examples of single sector circularity are major first Participatory backcasting approaches may be of particular interest for steps. Such examples include the reuse of side-streams within the agri- such purposes (Kanter et al., 2016). cultural sector and up-cycling of materials, which are relevant in the context of responsible plant nutrition. 3.2. Action 2: Digital crop nutrition solutions Besides tighter integration of crop and livestock production, closing nutrient cycles will also require recovering more nutrients from human On their own, smart phones or other digital tools cannot achieve excreta and waste, particularly also in developing countries. Good po- good crop nutrition in the field because the latter will always depend on tential exists for this through new technologies, but there are also sig- farmers making the right decisions. However, data- and knowledge- nificant sociocultural, infrastructure and other challenges to overcome driven digital solutions and technologies will increasingly allow (van der Hoek et al., 2018; Lohman et al., 2020; van der Kooij et al., tailoring nutrient applications to local needs in a more precise manner, 2020). Another concern is how to minimize contamination risks that and reaching many more farmers than a few agronomists could do on may be associated with such waste streams, including heavy metals such their own. New soil and crop diagnostic tools and sensors, high- as cadmium (Cd). Manure or sewage sludge tend to add more Cd over resolution soil, crop and climate data, mechanistic real-time predic- smaller areas of land compared to mineral or recycled granular fertil- tion models, and artificial intelligence-based decision support are all izers that add smaller amounts over much larger land areas. Significant expected to play an increasing role in responsible plant nutrition, pro- advances have been made in understanding the behavior of Cd in agri- vided that they are robust in performance and of real benefit to farmers. cultural systems and a range of management options are now available Of particular promise are approaches that harness data to accelerate for farmers to minimize Cd uptake into crops and forages. (McLaughlin the process of optimizing crop and soil management practices that et al., 2021). It has also been proposed that the use of recycled fertilizers govern both yields and nutrient use efficiency at production scale should be regulated based on their pollutant-to-nutrient ratio (Weis- (Cassman and Grassini, 2020; Mulders et al., 2021). Artificial intelli- sengruber et al., 2018). Composts, for example, may present a greater gence approaches will play an increasing role in developing self-learning risk due to low nutrient contents, i.e. higher application rates to achieve fertilizer advisory solutions, particularly once it becomes possible to the same nutrient input. move seamlessly from data to prescriptive analytics and automated Overall, this will lead to a more diversified, more decentralized decision making with less human interference (Smith, 2020). production of recycled fertilizers that are expected to meet the standards Besides high-tech solutions for commercial farming, ‘low-tech’ site- of ‘normal’ mineral fertilizers, including having equivalent agronomic specific nutrient management (SSNM) approaches have shown consis- performance (Huygens and Saveyn, 2018; Huygens et al., 2020). Sig- tent, large increases in crop yields and profits and NUE in many crops nificant opportunities also exist for more microbial and other bio-based grown by smallholder farmers in Asia and Africa (see SI Example 6). solutions to enhance nutrient supply, efficiency or recycling, as part of Across a wide range of countries and environments, relative to the the growing bioeconomy. Improved full-chain nutrient flow monitoring, farmer practice, SSNM in rice, wheat and maize increased grain yield by benchmarking and life-cycle analysis need to support the development 12% and profitability by 15% with 10% less fertilizer nitrogen applied of such solutions, along with certification and supporting as well as (Chivenge et al., 2021). Upscaling this to millions of farmers requires regulating policies. At present, government regulations are often too digitally supported advisory systems and viable business solutions. outdated and inconsistent among countries in order to properly enable Worldwide, only 24–37% of farms of <1 ha in size are served by third these new developments. This presents a huge barrier for accelerating generation (3G) or 4G services, compared to 74–80% of farms of >200 investment and upscaling. 7 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 Fig. 5. Major nutrient flows in circular crop- livestock-human systems. Red arrows indicate fertil- izer inputs into the system. Fertile land is primarily used to produce food for humans and some supple- mentary feed for livestock, also from crop residues (orange arrows). Grassland is primarily used for livestock, including grazing. By-products and waste are recycled back to agriculture or used for making new bio-based products (brown arrows). Leakages out of the circular system are minimized. Source: Re- drawn and modified from (van Zanten et al., 2019). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) 3.4. Action 4: Nutritious crops (Meenakshi et al., 2010). At issue is where will this be most effective, and how it can be mainstreamed into agriculture, particularly if farmers Fertilizer programs implemented in the past mainly focused on do not get paid for such additional food quality value. Finland, for improving soil fertility and crop yields as well as farm incomes, with example, is the only country in the world in which all crop fertilizers main emphasis given to N, P and K fertilizers. Little or no priority has must contain 10–15 mg selenium kg− 1 (Alfthan et al., 2015). This been given to nutritional outcomes for human health. Responsible plant mandatory practice was introduced in 1985 because Finnish soils were nutrition solutions must also consider the whole nutritional contribution low in available Se and so was the Se concentration in the blood plasma of food crops, towards addressing the triple burden of undernutrition, of Finns. This fertilizer enrichment practice has led to a 15-fold increase micronutrient malnutrition, overweight/obesity and non- in selenium concentration of spring cereals, resulting in effective and communicable diseases (Poole et al., 2020). safe increases in selenium intake and health of the whole population In principle, the choice of what to eat and how much lies with con- (Fig. 6). Similar results have been obtained through fertilizer-based sumers, which would then also create market demands to be met by fortification of maize in Malawi (Chilimba et al., 2012), and in many growing different crops, including crops with better nutritional value. other crop-nutrient combinations (see SI Example 8). Depending on the local context, nutrition-sensitive crop production may An important issue is to also update regulatory approaches for fer- include more diverse crop rotations, enhancing protein and micro- tilizers in order to justify and encourage more investments in nutri- nutrient contents through N, P and K fertilizer management (Singh et al., tionally enhanced fertilizers solutions. Current definitions of essential or 2018; Zhang et al., 2021a), as well as biofortification of staple crops with beneficial elements for plant growth are partially outdated and even micronutrients through breeding and/or fertilizers (Cakmak and Kut- compromise fertilizer regulation and practice. A new definition has man, 2018; Garg et al., 2018). The latter involves the targeted use of recently been proposed, which is better aligned with nutrients deemed fertilizer products that deliver micronutrients of importance to crops, essential or beneficial for crops, animal and humans, thus following a animals and humans, which is of particular relevance in regions where more holistic ’one nutrition‘ concept (Brown et al., 2021). much of the food is grown and consumed locally. Enriching these crops At the same time it is vital that impurities in fertilizers do not with certain minerals has a direct impact on human health without any adversely affect soil or food quality, with cadmium being the element change in actual consumer behavior. Besides essential plant nutrients requiring most careful management in mineral fertilizers (Chaney, such as iron or zinc, this should increasingly include nutrients that are of 2012). For fertilizers manufactured from recycle or waste streams, there particular importance to animals and humans, such as iodine (Fuge and are a range of contaminants that must be considered and managed to Johnson, 2015) or selenium (Alfthan et al., 2015). End-to-end connec- ensure the production of clean food and to avoid soil pollution. tivity and traceability will be important elements of such a strategy. Improving micronutrient concentrations in food crops would also be Biofortification of staple crops with micronutrients offers cost- useful in reducing intestinal absorption and retention of heavy metals effective opportunities for combating micronutrient malnutrition such as cadmium in the body (Reeves and Chaney, 2008). 8 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 3.6. Action 6: Accelerated innovation Future plant nutrition research and innovation needs to foster co- creation and sharing of knowledge for more rapid development and deployment of new technologies and better practices at scale. There are major knowledge gaps that require re-orienting research investments at global and regional scales towards issues that are most critical for developing the right nutrient roadmaps and solutions. For example, proper benchmarking of the main cropping systems at global level is an important innovation area to identify priority areas and suitable solu- tions for increasing yields and nutrient use efficiency in parallel. Un- fortunately, examples of this type of field-based assessments with the required level of granularity and agronomic context are still scarce (Yuan et al., 2021). Besides more investment by both public and private sector, accel- erating innovation also requires more openness, sharing of data and other resources, and coordinated action of public and private sector players in agricultural innovation (Berthet et al., 2018). A massive cul- ture change is needed in science and science funding, towards a Fig. 6. Changes in wheat grain and blood selenium in healthy Finns since Se- problem-focused and leaner science approach, transdisciplinary collab- enrichment of NPK fertilizers was introduced in 1985. Source: re-drawn from orations, use of digital tools, entrepreneurship, and early and frequent (Alfthan et al., 2015). engagement with key stakeholders and end users, including farmers in particular (Karp et al., 2015; Herrero et al., 2020). 3.5. Action 5: Climate-smart fertilizers 4. Who needs to do what? Fertilizers will increasingly be produced in an environmentally friendly manner and they will embody greater amounts of knowledge to Responsible plant nutrition is a complex and global challenge which control the release of nutrients to the plant (see SI Example 9). Across can only be tackled through concrete action by all those directly the plant nutrition sector, low-emission fertilizer production and involved in the nutrient cycle, and those influencing it (Fig. 7). transportation technologies, novel fertilizer formulations or inhibitors, Policy makers at all levels need to create clear, science-based and as well as more precise nutrient application and agronomic field man- harmonized regulatory frameworks for nutrients, but also dynamic agement (van Loon et al., 2019; Maaz et al., 2021) offer opportunities to policies that incentivize innovation in technologies, practices and directly and indirectly reduce fertilizer-related emissions of CO and business models. They must set out a clear vision for national or regional 2 N O, provided that the surrounding market conditions and policies roadmaps with sound targets for nutrients, nutrition and environmental 2 enable that. Significant reductions in pre-farm GHG emissions can be indicators. This is particularly important as many farmers currently achieved by utilizing renewable energy in fertilizer production. Decar- perceive the continuous change of laws and regulations as one of their bonizing ammonia production has become a particular necessity and main challenges (Paas et al., 2021). Policy makers can drive changes in opportunity in the fertilizer industry (IEA, 2021), with various new food consumption, as well as provide progressive incentives for the technologies being piloted to produce ‘green ammonia’ from adoption of better practices by farmers. Policies need to properly bal- carbon-neutral energy sources, but also use ammonia for energy storage ance food production and environmental goals. Technical assistance and and transport. Such a new ammonia economy has the potential to feed extension services must be supported adequately to promote sustainable and power the world in a whole new and perhaps even more decen- practices. Policy makers also need to ensure that farmers all over the tralized manner (Rouwenhorst et al., 2019). world have affordable access to the internet and digital services. Innovation in fertilizer technology and formulation will lead to The global fertilizer industry has recently recognized the need for a environmentally-friendly fertilizers that maximize nutrient capture by sustainability- and innovation-driven plant nutrition approach as its the crop and minimize losses of nutrients (see SI Example 9). Important core business strategy (International Fertilizer Association, 2018). Fer- innovation areas include bio-based coatings (Chen et al., 2018), ‘smart tilizer companies will have to increasingly become providers of inte- fertilizers’ where nutrients are released from granules on contact with grated plant nutrition solutions that are based on new business models plant roots (Zhang et al., 2013), and a whole range of new materials (e.g. that do what is right for people and the planet. Sustainability and nanomaterials, graphene, metal-organic frameworks, etc.) offering innovation, including transparent monitoring and reporting, will drive pathways for tailoring nutrient release to be more in synchrony with the transformation strategy for the entire industry, for every product and plant demand. Progress is also being made in other innovation areas that solution sold. Revenue growth primarily needs to be driven by growth in could lead to specific improvements in NuUE, for example through new performance value offered to farmers and society, not volume of fertil- microbial formulations that are based on a deeper understanding of the izers sold. soil-plant microbiome (Fierer, 2017), or the use of biostimulants (Rou- Farmers, farm advisers and service providers carry the primary phael and Colla, 2020). As with all new technologies, the challenge is to responsibility for improving nutrient use efficiency, reducing nutrient introduce these innovations into the market so that they can be manu- losses, recycling nutrients and promoting soil health at the farm scale, factured easily, are cost and quality competitive at farm level, perform which has huge implications at larger scales. They need to be able to reliably and will be safe. Risks and benefits need to be evaluated thor- fully adapt and adopt new knowledge, technology, and services, and oughly and independently in field studies, particularly with regard to they need to be rewarded for good practices. Many farmers are entre- environmental or health risks that may be associated with technologies preneurs and willing to change, and they are also aware of their role as such as nano-fertilizers (Dimkpa and Bindraban, 2018; Hofmann et al., stewards of land, water, climate and biodiversity. But doing things 2020). Robust, evidence-based regulatory approaches have to be differently requires lowering risks and other adoption barriers for them. developed to enable safe and wider use of many of these new products. Food traders, processors and retailers have enormous power to influence nutrient cycles, both through influencing what consumers eat or drink and how it is being produced. Vertically integrated, data-driven 9 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 Fig. 7. The agri-food chain from a nutrient management perspective. Blue boxes show actors who directly contribute to nutrient use and losses at different stages. Red arrows indicate greenhouse gas emissions, nutrient losses into the environment and waste that can happen in all parts of the chain. All opportunities to reduce emissions and losses must be exploited, while also increasing nutrient recovery and return to farming and industry (green arrows). The grey box shows actors who influence the primary actors, drive innovation or set the societal framework for action. Source: Modified from (Kanter et al., 2020). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) and more transparent supply chains that meet sustainable production 5. Conclusions: a vision of success standards and reduce production losses will become more widespread, including more direct sourcing from farmers. These developments offer The coming 10–20 years will be of major importance for trans- numerous opportunities for implementing more holistic approaches to forming the world’s nutrient cycles and management systems, across the nutrient management. Monetizing such sustainable production practices entire nutrient and fertilizer value chain. The primary change will be a is both a key challenge and an opportunity. new societal plant nutrition optimum rather than a purely economic Consumers will drive significant changes in plant nutrition through optimum, which, most importantly must also benefit farmers and all changes towards healthier diets as well as an increasing emphasis on other primary actors in the nutrient chain. The implication is that society food that is produced in a more sustainable manner. Specific trends will as a whole will need to share more of the cost of achieving the desired differ among regions and income groups. On a global scale, changes in societal (environmental) outcomes, but the mechanisms for that are far food behavior may be relatively slow and will also be partly compen- from clear. In any case, the new nutrient economy will have to become sated by growing food consumption due to rising populations and in- an integral component of a low carbon emission, nature-positive and come growth in low and middle income countries. However, an circular food system that supports a rising global population. Compared immediate responsibility of consumers is to reduce excessive meat to where we are in 2020, concrete outcomes that can be achieved within consumption, waste less food and ensure recycling of waste that does one generation, by 2040, include: occur. Utility services providers and waste processors are an important 1. Widely accepted standards for quantifying and monitoring nutrients and relatively new category of actors in the nutrient cycle, but their role along the food supply chain inspire solutions for improving overall will increase substantially in the coming years. Particularly in densely nutrient use efficiency, increasing recycling and reducing nutrient populated areas their needs and actions will increasingly co-define how waste across the whole agri-food system. Ambitious targets, policies farming and nutrient management will be done. This requires deepening and investments stimulate collective actions by governments, busi- the collaboration with other groups of actors and jointly developing a nesses, farmers and other stakeholders towards sustainable, inte- common understanding as well as common standards to meet. grated, and tailored plant nutrition solutions. Investors: Investment in plant nutrition research and innovation 2. On a global scale, crop yield growth meets food, feed and bio- will need to increase massively to meet the complex plant nutrition industry demand and outpaces growth in mineral fertilizer con- challenges we face. Public, private and philanthropic investors should sumption, while cropland expansion and deforestation have been increasingly invest in technologies, businesses and organizations that halted. Global crop NUE – the nitrogen output in products harvested support key elements of the new paradigm, including creating a growing from cropland as a proportion of nitrogen input – has increased to ecosystem of startup companies and other enterprises. Use of blended 70%. public and private capital can de-risk and leverage more private 3. Through responsible consumption, increased recycling, and better investment. management practices nutrient waste along the food system has been Scientists: Science and engineering will underpin all efforts to halved. Nitrogen and P surpluses in hotspots have been reduced to achieve the multiple objectives of the new plant nutrition paradigm, but safe levels which minimize eutrophication and other environmental the entire science culture must change too, towards new ways of harm. working that stimulate new discoveries and achieve faster translation 4. Soil nutrient depletion and carbon loss have been halted. Forward- into practice. Greater focus on explicit pathways to agronomic appli- looking policies and investments have triggered changes in farming cations, reality checks and rigor in claims of utility are needed, as well as systems and management practices that increase soil health, more sharing of know-how and critical resources, more open innovation including soil organic matter. Regional soil nutrient deficits have and entrepreneurship. been reduced substantially, particularly in sub-Saharan Africa, Civil society organizations play significant roles for the new where fertilizer use has tripled and crop yield has at least doubled, paradigm through informing the public, grassroots mobilization, including improved nutritional outputs. Millions of hectares of monitoring, alerting and influencing, and inclusive dissemination of degraded agricultural land have been restored, including through the new technologies and practices. This is a big responsibility, which use of mineral and organic fertilizers and nutrient-containing waste should follow an evidence-based approach. Co-developing concrete so- or by-products. lutions in partnership with government, industry, science and farmers 5. Extreme forms of chronic hunger and nutrient-related malnutrition should replace the often found emphasis on single issues or controversial have been eradicated through integrated strategies that include the debates. targeted use of micronutrient-enriched fertilizers and nutrient- 10 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 biofortified crops. A new generation of more nutritious cereals and Amundson, R., Biardeau, L., 2018. Opinion: soil carbon sequestration is an elusive other staple crops is increasingly grown by farmers, driven by con- climate mitigation tool. Proc. Natl. Acad. Sci. U. S. A 115, 11652–11656. Assefa, B.T., Reidsma, P., Chamberlin, J., van Ittersum, M.K., 2021. Farm- and sumer and market demand. Policy and decision makers support community-level factors underlying the profitability of fertiliser usage for Ethiopian mineral fertilization strategies for meeting specific human nutri- smallholder farmers. Agrekon 60, 460–479. tional needs where markets do not provide the needed incentives. Berge, H.F.M. ten, Hijbeek, R., van Loon, M.P., Rurinda, J., Tesfaye, K., Zingore, S., Craufurd, P., van Heerwaarden, J., Brentrup, F., Schröder, J.J., Boogaard, H.L., 6. The fertilizer industry follows rigorous and transparent sustainability Groot, H.L.E.de, van Ittersum, M.K., 2019. Maize crop nutrient input requirements standards for the entire life cycle of its products and business oper- for food security in sub-Saharan Africa. Global Food Secur. 23, 9–21. ations. Greenhouse gas emissions from fertilizer production and use Berkhout, E.D., Malan, M., Kram, T., 2019. Better soils for healthier lives? An have been reduced by at least 30% through increased energy effi- econometric assessment of the link between soil nutrients and malnutrition in Sub- Saharan Africa. PLoS One 14, e0210642. ciency, carbon capture and storage and other novel technologies and Berthet, E.T., Hickey, G.M., Klerkx, L., 2018. Opening design and innovation processes in products. At least 10% of the world’s fertilizer-N is produced from agriculture: insights from design and management sciences and future directions. green ammonia with very low or zero carbon emission. Agric. Syst. 165, 111–115. Biermann, F., Kim, R.E., 2020. The boundaries of the Planetary Boundary framework: a 7. Investments in plant nutrition research and innovation by public and critical appraisal of approaches to define a “safe operating space” for humanity. private sector have tripled compared to present levels. Many com- Annu. Rev. Environ. Resour. 45, 497–521. panies spend 5% or more of their gross revenue on research and Brouder, S.M., Volenec, J.J., 2017. Future climate change and plant macronutrient use efficiency. In: Hossain, M.A., Kamiya, T., Burritt, D.J. (Eds.), Plant Macronutrient innovation. Collaborative, open innovation approaches allow for Use Efficiency. Molecular and Genomic Perspectives in Crop Plants. Academic Press, scientific discoveries to become quickly translated into practical London United Kingdom, pp. 357–379. solutions and knowledge. Innovative, value-oriented business Brown, P.H., Zhao, F.-J., Dobermann, A., 2021. What is a Plant Nutrient? Changing Definitions to Advance Science and innovation in Plant Nutrition. Plant Soil. https:// models drive growth throughout the industry. doi.org/10.1007/s11104-021-05171-w. 8. Consumers appreciate the benefits of plant nutrients, including Bünemann, E.K., Bongiorno, G., Bai, Z., Creamer, R.E., Deyn, G.de, Goede, R.de, mineral fertilizers as a primary nutrient source. A nutrient footprint Fleskens, L., Geissen, V., Kuyper, T.W., Mäder, P., Pulleman, M., Sukkel, W., van Groenigen, J.W., Brussaard, L., 2018. Soil quality – a critical review. Soil Biol. standard with high visual recognition informs consumer choices. Biochem. 120, 105–125. Information on improvement of soil health and nutrient balances is Cabot, C., Martos, S., Llugany, M., Gallego, B., Tolr├á, R., Poschenrieder, C., 2019. A role widely available, and their linkage to the mitigation of air, water and for zinc in plant defense against pathogens and herbivores. Front. Plant Sci. 10, climate issues will be broadly acknowledged. 1171. Cakmak, I., Kutman, U.B., 2018. Agronomic biofortification of cereals with zinc: a 9. Farmers all over the world have access to affordable, diverse and review. Eur. J. Soil Sci. 69, 172–180. appropriate plant nutrition solutions, and they are being rewarded Cassman, K.G., Dobermann, A., 2022. Nitrogen and the future of agriculture: 20 years on. for implementing better nutrient management and stewardship Ambio 51, 17–24. Cassman, K.G., Grassini, P., 2020. A global perspective on sustainable intensification practices that increase their prosperity and enable them to exit research. Nat. Sustain. 3, 262–268. poverty traps. Customized crop nutrition products and solutions Chaney, R.L., 2012. Food safety issues for mineral and organic fertilizers. Adv. Agronomy account for at least 30% of the global crop nutrition market value. 117, 51–116. Chen, X., Cui, Z., Fan, M., Vitousek, P., Zhao, M., Ma, W., Wang, Z., Zhang, W., Yan, X., Yang, J., Deng, X., Gao, Q., zhang, Q., Guo, S., Ren, J., Li, S., Ye, Y., Wang, Z., Such outcomes can be best met through strategies that integrate Huang, J., Tang, Q., Sun, Y., Peng, X., Zhang, J., He, M., Zhu, Y., Xue, J., Wang, G., more efficient food production practices with healthier diets, wasting Wu, L., An, N., Wu, L., Ma, L., Zhang, W., Zhang, F., 2014. Producing more grain with lower environmental costs. Nature 514, 486–489. less, recycling more and appropriate level of trade. Achieving them now, Chen, J., Lü, S., Zhang, Z., Zhao, X., Li, X., Ning, P., Liu, M., 2018. Environmentally within one human generation, will require significant investments and a friendly fertilizers: a review of materials used and their effects on the environment. far more concerted effort by everyone involved, from the fertilizer in- Sci. Total Environ. 613–614, 829–839. Chilimba, A.D., Young, S.D., Black, C.R., Meacham, M.C., Lammel, J., Broadley, M.R., dustry to farmers and consumers of food and other agricultural products. 2012. Agronomic biofortification of maize with selenium (Se) in Malawi. Field Crop. Res. 125, 118–128. Chivenge, P., Saito, K., Bunquin, M.A., Sharma, S., Dobermann, A., 2021. Co-benefits of Declaration of competing interest nutrient management tailored to smallholder agriculture. Global Food Secur. 30, 100570. St Clair, S.B, Lynch, J.P., 2010. The opening of Pandora’s Box: climate change impacts on The authors declare that they have no known competing financial soil fertility and crop nutrition in developing countries. Plant Soil 335, 101–115. interests or personal relationships that could have appeared to influence Corbeels, M., Cardinael, R., Powlson, D., Chikowo, R., Gerard, B., 2020. Carbon the work reported in this paper. sequestration potential through conservation agriculture in Africa has been largely overestimated. Soil Tillage Res. 196, 104300. Cordell, D., Rosemarin, A., Schröder, J.J., Smit, A.L., 2011. Towards global phosphorus Acknowledgements security: a systems framework for phosphorus recovery and reuse options. Chemosphere 84, 747–758. Crippa, M., Solazzo, E., Guizzardi, D., Monforti-Ferrario, F., Tubiello, F.N., Leip, A., All members of the Scientific Panel on Responsible Plant Nutrition 2021. Food systems are responsible for a third of global anthropogenic GHG (SPRPN) have contributed equally to this paper. Opinions expressed in emissions. Nature Food 2, 198–209. this article are those of the individual members of the panel, not that of Deng, X., Huang, Y., Qin, Z., 2020. Soil indigenous nutrients increase the resilience of maize yield to climatic warming in China. Environ. Res. Lett. 15, 94047. the organizations they work for. An earlier, short version of this paper Dimkpa, C.O., Bindraban, P.S., 2018. Nanofertilizers: new products for the industry? was previously published as an Issue Brief by the SPRPN and is available J. Agric. Food Chem. 66, 6462–6473. at www.sprpn.org. Ebi, K.L., Anderson, C.L., Hess, J.J., Kim, S.-H., Loladze, I., Neumann, R.B., Singh, D., Ziska, L., Wood, R., 2021. Nutritional quality of crops in a high CO2 world: an agenda for research and technology development. Environ. Res. Lett. 16, 64045. Appendix A. Supplementary data Einarsson, R., Cederberg, C., 2019. Is the nitrogen footprint fit for purpose? An assessment of models and proposed uses. J. Environ. Manag. 240, 198–208. Eisler, M.C., Lee, M.R.F., Tarlton, J.F., Martin, G.B., Beddington, J., Dungait, J.A.J., Supplementary data to this article can be found online at https://doi. Greathead, H., Liu, J., Mathew, S., Miller, H., Misselbrook, T., Murray, P., Vinod, V. org/10.1016/j.gfs.2022.100636. K., van Saun, R., Winter, M., 2014. Agriculture: steps to sustainable livestock. Nature 507, 32–34. Elmer, W.H., Datnoff, L.E., 2014. Mineral nutrition and suppression of plant disease. In: References van Alfen, N.K. (Ed.), Encyclopedia of Agriculture and Food Systems. Elsevier/ Academic Press, Amsterdam, pp. 231–244. Alfthan, G., Eurola, M., Ekholm, P., Venäläinen, E.-R., Root, T., Korkalainen, K., Erisman, J., Leach, A., Bleeker, A., Atwell, B., Cattaneo, L., Galloway, J., 2018. An Hartikainen, H., Salminen, P., Hietaniemi, V., Aspila, P., Aro, A., 2015. Effects of integrated approach to a nitrogen use efficiency (NUE) indicator for the food nationwide addition of selenium to fertilizers on foods, and animal and human production–consumption chain. Sustainability 10, 925. health in Finland: from deficiency to optimal selenium status of the population. J. Trace Elem. Med. Biol. 31, 142–147. 11 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 Fan, M.-S., Zhao, F.-J., Fairweather-Tait, S.J., Poulton, P.R., Dunham, S.J., McGrath, S.P., Kao, P.T., Darch, T., McGrath, S.P., Kendall, N.R., Buss, H.L., Warren, H., Lee, M., 2020. 2008. Evidence of decreasing mineral density in wheat grain over the last 160 years. Factors influencing elemental micronutrient supply from pasture systems for grazing J. Trace Elem. Med. Biol. 22, 315–324. ruminants. Adv. Agron. 164, 161–229. FAO, 2018. The 10 Elements of Agroecology. Guiding the Transition to Sustainable Food Karimi, R., Pogue, S.J., Kröbel, R., Beauchemin, K.A., Schwinghamer, T., Henry and Agricultural Systems. http://www.fao.org/3/i9037en/i9037en.pdf. Janzen, H., 2020. An updated nitrogen budget for Canadian agroecosystems. Agric. FAO, 2021. The State of the World’s Land and Water Resources for Food and Agriculture Ecosyst. Environ. 304, 107046. – Systems at Breaking Point. Synthesis Report. FAO, Rome. Karp, A., Beale, M.H., Beaudoin, F., Eastmond, P.J., Neal, A.L., Shield, I.F., Townsend, B. Fierer, N., 2017. Embracing the unknown: disentangling the complexities of the soil J., Dobermann, A., 2015. Growing innovations for the bioeconomy. Nat. Plants 1, microbiome. Nat. Rev. Microbiol. 15, 579. 15193. FOLU, 2019. Growing better: ten critical transitions to transform food and land use. The Kinnunen, P., Guillaume, J.H.A., Taka, M., D’Odorico, P., Siebert, S., Puma, M.J., Food and Land Use Coalition. https://www.foodandlandusecoalition.org/globa Jalava, M., Kummu, M., 2020. Local food crop production can fulfil demand for less l-report/. than one-third of the population. Nature Food 1, 229–237. Forber, K.J., Rothwell, S.A., Metson, G.S., Jarvie, H.P., Withers, P.J.A., 2020. Plant-based Kirkby, C.A., Richardson, A.E., Wade, L.J., Conyers, M., Kirkegaard, J.A., 2016. Inorganic diets add to the wastewater phosphorus burden. Environ. Res. Lett. 15, 94018. nutrients increase humification efficiency and C-sequestration in an annually Fuge, R., Johnson, C.C., 2015. Iodine and human health, the role of environmental cropped soil. PLoS One 11, e0153698. geochemistry and diet, a review. Appl. Geochem. 63, 282–302. Kumssa, D.B., Joy, E.J.M., Ander, E.L., Watts, M.J., Young, S.D., Walker, S., Broadley, M. Fuglie, K.O., 2018. Is agricultural productivity slowing? Global Food Secur. 17, 73–83. R., 2015. Dietary calcium and zinc deficiency risks are decreasing but remain Garg, M., Sharma, N., Sharma, S., Kapoor, P., Kumar, A., Chunduri, V., Arora, P., 2018. prevalent. Sci. Rep. 5, 10974. Biofortified crops generated by breeding, agronomy, and transgenic approaches are Ladha, J.K., Jat, M.L., Stirling, C.M., Chakraborty, D., Pradhan, P., Krupnik, T.J., improving lives of millions of people around the world. Front. Nutr. 5, 12. Sapkota, T.B., Pathak, H., Rana, D.S., Tesfaye, K., Gerard, B., 2020. Achieving the Gil, J.D.B., Reidsma, P., Giller, K., Todman, L., Whitmore, A., van Ittersum, M., 2019. sustainable development goals in agriculture: the crucial role of nitrogen in cereal- Sustainable development goal 2: improved targets and indicators for agriculture and based systems. Adv. Agron. 163, 39–116. food security. Ambio 48, 685–698. Lawrence, N.C., Tenesaca, C.G., VanLoocke, A., Hall, S.J., 2021. Nitrous oxide emissions Gomes, A., Reidsma, P., 2021. Time to transition: barriers and opportunities to farmer from agricultural soils challenge climate sustainability in the US Corn Belt. Proc. adoption of soil GHG mitigation practices in Dutch agriculture. Front. Sustain. Food Natl. Acad. Sci. U. S. A 118. Syst. 5, 335. Lohman, H.A.C., Trimmer, J.T., Katende, D., Mubasira, M., Nagirinya, M., Nsereko, F., Grote, U., Craswell, E., Vlek, P., 2005. Nutrient flows in international trade: ecology and Banadda, N., Cusick, R.D., Guest, J.S., 2020. Advancing sustainable sanitation and policy issues. Environ. Sci. Pol. 8, 439–451. agriculture through investments in human-derived nutrient systems. Environ. Sci. Guo, Y., Chen, Y., Searchinger, T.D., Zhou, M., Pan, D., Yang, J., Wu, L., Cui, Z., Technol. 54, 9217–9227. Zhang, W., Zhang, F., Ma, L., Sun, Y., Zondlo, M.A., Zhang, L., Mauzerall, D.L., 2020. Lynch, J.P., St Clair, S.B, 2004. Mineral stress: the missing link in understanding how Air quality, nitrogen use efficiency and food security in China are improved by cost- global climate change will affect plants in real world soils. Field Crop. Res. 90, effective agricultural nitrogen management. Nature Food 1, 648–658. 101–115. Hasler, K., Bröring, S., Omta, S., Olfs, H.-W., 2015. Life cycle assessment (LCA) of Ma, L., Bai, Z., Ma, W., Guo, M., Jiang, R., Liu, J., Oenema, O., Velthof, G.L., different fertilizer product types. Eur. J. Agron. 69, 41–51. Whitmore, A.P., Crawford, J., Dobermann, A., Schwoob, M., Zhang, F., 2019. Herrero, M., Thornton, P.K., Notenbaert, A.M., Wood, S., Msangi, S., Freeman, H.A., Exploring future food provision scenarios for China. Environ. Sci. Technol. 53, Bossio, D., Dixon, J., Peters, M., van de Steeg, J., Lynam, J., Parthasarathy Rao, P., 1385–1393. Macmillan, S., Gerard, B., McDermott, J., Seré, C., Rosegrant, M., 2010. Smart Maaz, T.M., Sapkota, T.B., Eagle, A.J., Kantar, M.B., Bruulsema, T.W., Majumdar, K., investments in sustainable food production: revisiting mixed crop-livestock systems. 2021. Meta-analysis of yield and nitrous oxide outcomes for nitrogen management in Science (New York, N.Y.) 327, 822–825. agriculture. Global Change Biol. 27, 2343–2360. Herrero, M., Thornton, P.K., Mason-D’Croz, D., Palmer, J., Benton, T.G., Bodirsky, B.L., Marles, R.J., 2017. Mineral nutrient composition of vegetables, fruits and grains: the Bogard, J.R., Hall, A., Lee, B., Nyborg, K., Pradhan, P., Bonnett, G.D., Bryan, B.A., context of reports of apparent historical declines. J. Food Compos. Anal. 56, 93–103. Campbell, B.M., Christensen, S., Clark, M., Cook, M.T., Boer, I.J.M. de, Downs, C., Marschner, P. (Ed.), 2012. Marschner’s Mineral Nutrition of Higher Plants, third ed. Dizyee, K., Folberth, C., Godde, C.M., Gerber, J.S., Grundy, M., Havlik, P., Jarvis, A., Academic Press, Amsterdam, London. King, R., Loboguerrero, A.M., Lopes, M.A., McIntyre, C.L., Naylor, R., Navarro, J., Marschner, H., Cakmak, I., 1989. High light intensity enhances chlorosis and necrosis in Obersteiner, M., Parodi, A., Peoples, M.B., Pikaar, I., Popp, A., Rockström, J., leaves of zinc, potassium, and magnesium deficient bean (Phaseolus vulgaris) plants. Robertson, M.J., Smith, P., Stehfest, E., Swain, S.M., Valin, H., van Wijk, M., van J. Plant Physiol. 134, 308–315. Zanten, H.H.E., Vermeulen, S., Vervoort, J., West, P.C., 2020. Innovation can Martin, M.P., Dimassi, B., Román Dobarco, M., Guenet, B., Arrouays, D., Angers, D.A., accelerate the transition towards a sustainable food system. Nature Food 1, 266–272. Blache, F., Huard, F., Soussana, J.-F., Pellerin, S., 2021. Feasibility of the 4 per 1000 Hofmann, T., Lowry, G.V., Ghoshal, S., Tufenkji, N., Brambilla, D., Dutcher, J.R., aspirational target for soil carbon: a case study for France. Global Change Biol. 27, Gilbertson, L.M., Giraldo, J.P., Kinsella, J.M., Landry, M.P., Lovell, W., Naccache, R., 2458–2477. Paret, M., Pedersen, J.A., Unrine, J.M., White, J.C., Wilkinson, K.J., 2020. McArthur, J.W., McCord, G.C., 2017. Fertilizing growth: agricultural inputs and their Technology readiness and overcoming barriers to sustainably implement effects in economic development. J. Dev. Econ. 127, 133–152. nanotechnology-enabled plant agriculture. Nature Food 1, 416–425. McLaughlin, M.J., Smolders, E., Zhao, F.J., Grant, C., Montalvo, D., 2021. Managing Huang, X., Terrer, C., Dijkstra, F.A., Hungate, B.A., Zhang, W., van Groenigen, K.J., 2020. cadmium in agricultural systems. Adv. Agron. 166, 1–129. New soil carbon sequestration with nitrogen enrichment: a meta-analysis. Plant Soil McLellan, E.L., Cassman, K.G., Eagle, A.J., Woodbury, P.B., Sela, S., Tonitto, C., 454, 299–310. Marjerison, R.D., van Es, H.M., 2018. The nitrogen balancing act: tracking the Hutchings, N.J., Sørensen, P., Cordovil, C.M., Leip, A., Amon, B., 2020. Measures to environmental performance of food production. Bioscience 68, 194–203. increase the nitrogen use efficiency of European agricultural production. Global Meenakshi, J.V., Johnson, N.L., Manyong, V.M., DeGroote, H., Javelosa, J., Yanggen, D. Food Secur. 26, 100381. R., Naher, F., Gonzalez, C., García, J., Meng, E., 2010. How cost-effective is Huygens, D., Saveyn, H.G.M., 2018. Agronomic efficiency of selected phosphorus biofortification in combating micronutrient malnutrition? An ex ante assessment. fertilisers derived from secondary raw materials for European agriculture. A meta- World Development 38, 64–75. analysis. Agron. Sustain. Dev. 38. Mehrabi, Z., McDowell, M.J., Ricciardi, V., Levers, C., Martinez, J.D., Mehrabi, N., Huygens, D., Orveillon, D., Lugato, E., Tavazzi, S., Comero, S., Jones, A., Gawlik, B., Wittman, H., Ramankutty, N., Jarvis, A., 2020. The global divide in data-driven Saveyn, H., 2020. Technical Proposals for the Safe Use of Processed Manure above farming. Nat. Sustain. https://doi.org/10.1038/s41893-020-00631-0. the Threshold Established for Nitrate Vulnerable Zones by the Nitrates Directive (91/ Mengutay, M., Ceylan, Y., Kutman, U.B., Cakmak, I., 2013. Adequate magnesium 676/EEC). Publications Office of the European Union, Luxembourg. nutrition mitigates adverse effects of heat stress on maize and wheat. Plant Soil 368, IEA, 2021. Ammonia Technology Roadmap. Towards More Sustainable Nitrogen 57–72. Fertiliser Production. International Energy Agency (IEA), Paris, France. Mulders, P.J., van den Heuvel, E.R., van den Borne, J., van de Molengraft, R., International Fertilizer Association, 2018. IFA 2030 Scenarios. Digging Deeper, Thinking Heemels, W., Reidsma, P., 2021. Data science at farm level: explaining and Harder, Planning Further. https://www.fertilizer.org/Public/About_IFA/IFA2030. predicting within-farm variability in potato growth and yield. Eur. J. Agron. 123, aspx. 126220. International Plant Nutrition Institute, 2016. 4R Plant Nutrition Manual: A Manual for Muscat, A., Olde, E.M. de, Ripoll-Bosch, R., van Zanten, H.H.E., Metze, T.A.P., improving the Management of Plant Nutrition. metric version. IPNI, Norcross, GA, Termeer, C.J.A.M., van Ittersum, M.K., Boer, I.J.M. de, 2021. Principles, drivers and USA. opportunities of a circular bioeconomy. Nature Food 2, 561–566. IPCC, 2019. Climate Change and Land. IPCC Special Report on Climate Change, Nottingham, A.T., Meir, P., Velasquez, E., Turner, B.L., 2020. Soil carbon loss by Desertification, Land Degradation, Sustainable Land Management, Food Security, experimental warming in a tropical forest. Nature 584, 234–237. and Greenhouse Gas Fluxes in Terrestrial Ecosystems. https://www.ipcc.ch/srccl/. Paas, W., Accatino, F., Bijttebier, J., Black, J.E., Gavrilescu, C., Krupin, V., Manevska- Kanter, D.R., Schwoob, M.H., Baethgen, W.E., Bessembinder, J., Carriquiry, M., Tasevska, G., Ollendorf, F., Peneva, M., San Martin, C., Zinnanti, C., Appel, F., Dobermann, A., Ferraro, B., Lanfranco, B., Mondelli, M., Penengo, C., Saldias, R., Courtney, P., Severini, S., Soriano, B., Vigani, M., Zawalińska, K., van Ittersum, M.K., Silva, M.E., Lima, J.M.S.de, 2016. Translating the Sustainable Development Goals Meuwissen, M.P., Reidsma, P., 2021. Participatory assessment of critical thresholds into action: a participatory backcasting approach for developing national for resilient and sustainable European farming systems. J. Rural Stud. 88, 214–226. agricultural transformation pathways. Global Food Secur. 10, 71–79. Parviainen, T., Helenius, J., 2020. Trade imports increasingly contribute to plant nutrient Kanter, D.R., Bartolini, F., Kugelberg, S., Leip, A., Oenema, O., Uwizeye, A., 2020. inputs: case of the Finnish food system 1996–2014. Sustainability 12, 702. Nitrogen pollution policy beyond the farm. Nature Food 1, 27–32. Pingali, P.L., 2012. Green revolution: impacts, limits, and the path ahead. Proc. Natl. Acad. Sci. U. S. A 109, 12302–12308. 12 A. Dobermann et al. G l o b a l F o o d S e c u r i t y 33 (2022) 100636 Pingali, P., Mittra, B., Rahman, A., 2017. The bumpy road from food to nutrition security van Ittersum, M.K., van Bussel, L.G.J., Wolf, J., Grassini, P., van Wart, J., Guilpart, N., – slow evolution of India’s food policy. Global Food Secur. 15, 77–84. Claessens, L., Groot, H. de, Wiebe, K., Mason-D’Croz, D., Yang, H., Boogaard, H., van Poole, N., Donovan, J., Erenstein, O., 2020. Agri-nutrition Research: Revisiting the Oort, P.A.J., van Loon, M.P., Saito, K., Adimo, O., Adjei-Nsiah, S., Agali, A., Bala, A., Contribution of Maize and Wheat to Human Nutrition and Health. Food Policy, Chikowo, R., Kaizzi, K., Kouressy, M., Makoi, J.H.J.R., Ouattara, K., Tesfaye, K., 101976. Cassman, K.G., 2016. Can sub-Saharan Africa feed itself? Proc. Natl. Acad. Sci. Unit. Poulton, P., Johnston, J., Macdonald, A., White, R., Powlson, D., 2018. Major limitations States Am. 113, 14964–14969. to achieving "4 per 1000" increases in soil organic carbon stock in temperate regions: van Loon, M.P., Hijbeek, R., Berge, H.F.M. ten, Sy, V. de, Broeke, G.A. ten, Solomon, D., evidence from long-term experiments at Rothamsted Research, United Kingdom. van Ittersum, M.K., 2019. Impacts of intensifying or expanding cereal cropping in Global Change Biol. 24, 2563–2584. sub-Saharan Africa on greenhouse gas emissions and food security. Global Change Quan, Z., Zhang, X., Fang, Y., Davidson, E.A., 2021. Different quantification approaches Biol. 25, 3720–3730. for nitrogen use efficiency lead to divergent estimates with varying advantages. van Zanten, H.H., van Ittersum, M.K., Boer, I.J. de, 2019. The role of farm animals in a Nature Food 2, 241–245. circular food system. Global Food Secur. 21, 18–22. Quemada, M., Lassaletta, L., Jensen, L.S., Godinot, O., Brentrup, F., Buckley, C., Vaneeckhaute, C., 2021. Integrating resource recovery process and watershed modelling Foray, S., Hvid, S.K., Oenema, J., Richards, K.G., Oenema, O., 2020. Exploring to facilitate decision-making regarding bio-fertilizer production and application. npj nitrogen indicators of farm performance among farm types across several European Clean Water 4, 15. case studies. Agric. Syst. 177, 102689. Vanlauwe, B., Dobermann, A., 2020. Sustainable intensification of agriculture in sub- Reeves, P.G., Chaney, R.L., 2008. Bioavailability as an issue in risk assessment and Saharan Africa: first things first. Front. Agr. Sci. Eng. 7, 376–382. management of food cadmium: a review. Sci. Total Environ. 398, 13–19. Vogel, H.-J., Eberhardt, E., Franko, U., Lang, B., Ließ, M., Weller, U., Wiesmeier, M., Rinot, O., Levy, G.J., Steinberger, Y., Svoray, T., Eshel, G., 2019. Soil health assessment: Wollschläger, U., 2019. Quantitative evaluation of soil functions: potential and state. a critical review of current methodologies and a proposed new approach. Sci. Total Front. Environ. Sci. 7. Environ. 648, 1484–1491. Vollset, S.E., Goren, E., Yuan, C.-W., Cao, J., Smith, A.E., Hsiao, T., Bisignano, C., Rosanoff, A., Kumssa, D.B., 2020. Impact of rising body weight and cereal grain food Azhar, G.S., Castro, E., Chalek, J., Dolgert, A.J., Frank, T., Fukutaki, K., Hay, S.I., processing on human magnesium nutrition. Plant Soil 457, 5–23. Lozano, R., Mokdad, A.H., Nandakumar, V., Pierce, M., Pletcher, M., Robalik, T., Rouphael, Y., Colla, G., 2020. Editorial: biostimulants in agriculture. Front. Plant Sci. 11, Steuben, K.M., Wunrow, H.Y., Zlavog, B.S., Murray, C.J.L., 2020. Fertility, mortality, 40. migration, and population scenarios for 195 countries and territories from 2017 to Rouwenhorst, K.H., van der Ham, A.G., Mul, G., Kersten, S.R., 2019. Islanded ammonia 2100: a forecasting analysis for the Global Burden of Disease Study. Lancet. https:// power systems: technology review & conceptual process design. Renew. Sustain. doi.org/10.1016/S0140-6736(20)30677-2. Energy Rev. 114, 109339. Vries, W. de, Schulte-Uebbing, L., Kros, H., Voogd, J.C., Louwagie, G., 2021. Spatially Sarwar, M., Saleem, M.F., Ullah, N., Ali, S., Rizwan, M., Shahid, M.R., Alyemeni, M.N., explicit boundaries for agricultural nitrogen inputs in the European Union to meet Alamri, S.A., Ahmad, P., 2019. Role of mineral nutrition in alleviation of heat stress air and water quality targets. Sci. Total Environ. 786, 147283. in cotton plants grown in glasshouse and field conditions. Sci. Rep. 9, 13022. Walling, E., Vaneeckhaute, C., 2020. Greenhouse gas emissions from inorganic and Silva, J.V., van Ittersum, M.K., Berge, H.F. ten, Spätjens, L., Tenreiro, T.R., Anten, N.P., organic fertilizer production and use: a review of emission factors and their Reidsma, P., 2021. Agronomic analysis of nitrogen performance indicators in variability. J. Environ. Manag. 276, 111211. intensive arable cropping systems: an appraisal of big data from commercial farms. Wang, M., Zheng, Q., Shen, Q., Guo, S., 2013. The critical role of potassium in plant Field Crop. Res. 269, 108176. stress response. Int. J. Mol. Sci. 14, 7370–7390. Singh, B.R., Timsina, Y.N., Lind, O.C., Cagno, S., Janssens, K., 2018. Zinc and iron Waraich, E.A., Ahmad, R., Ashraf, M.Y., 2011. Role of mineral nutrition in alleviation of concentration as affected by nitrogen fertilization and their localization in wheat drought stress in plants. Aust. J. Crop. Sci. 5, 764. grain. Front. Plant Sci. 9, 307. Weissengruber, L., Möller, K., Puschenreiter, M., Friedel, J.K., 2018. Long-term soil Smith, M.J., 2020. Getting value from artificial intelligence in agriculture. Anim. Prod. accumulation of potentially toxic elements and selected organic pollutants through Sci. 60, 46. application of recycled phosphorus fertilizers for organic farming conditions. Soares, J.C., Santos, C.S., Carvalho, S.M.P., Pintado, M.M., Vasconcelos, M.W., 2019. Nutrient Cycl. Agroecosyst. 110, 427–449. Preserving the nutritional quality of crop plants under a changing climate: Welch, R.M., Graham, R.D., Cakmak, I., 2013. Linking agricultural production practices importance and strategies. Plant Soil 443, 1–26. to improving human nutrition and health, 13-15 November. In: Expert Paper Written Spohn, M., 2020. Increasing the organic carbon stocks in mineral soils sequesters large for ICN2 Second International Conference on Nutrition Preparatory Technical amounts of phosphorus. Global Change Biol. 26, 4169–4177. Meeting. Rome, Italy. http://www.fao.org/3/a-as574e.pdf. Steffen, W., Richardson, K., Rockström, J., Cornell, S.E., Fetzer, I., Bennett, E.M., Wezel, A., Herren, B.G., Kerr, R.B., Barrios, E., Gonçalves, A.L.R., Sinclair, F., 2020. Biggs, R., Carpenter, S.R., Vries, W. de, Wit, C.A. de, Folke, C., Gerten, D., Heinke, J., Agroecological principles and elements and their implications for transitioning to Mace, G.M., Persson, L.M., Ramanathan, V., Reyers, B., Sörlin, S., 2015. Planetary sustainable food systems. A review. Agron. Sustain. Dev. 40, 40. boundaries: guiding human development on a changing planet. Science 347, Willett, W., Rockström, J., Loken, B., Springmann, M., Lang, T., Vermeulen, S., 1259855. Garnett, T., Tilman, D., DeClerck, F., Wood, A., Jonell, M., Clark, M., Gordon, L.J., Stevenson, J.R., Villoria, N., Byerlee, D., Kelley, T., Maredia, M., 2013. Green Revolution Fanzo, J., Hawkes, C., Zurayk, R., Rivera, J.A., Vries, W. de, Majele Sibanda, L., research saved an estimated 18 to 27 million hectares from being brought into Afshin, A., Chaudhary, A., Herrero, M., Agustina, R., Branca, F., Lartey, A., Fan, S., agricultural production. Proc. Natl. Acad. Sci. Unit. States Am. 110, 8363–8368. Crona, B., Fox, E., Bignet, V., Troell, M., Lindahl, T., Singh, S., Cornell, S.E., Srinath Stoorvogel, J.J., Smaling, E.M.A., Janssen, B.H., 1993. Calculating soil nutrient balances Reddy, K., Narain, S., Nishtar, S., Murray, C.J.L., 2019. Food in the Anthropocene: in Africa at different scales. 1.Supra-national scale. Fert. Res. 35, 227–235. the EAT–Lancet Commission on healthy diets from sustainable food systems. Lancet Sun, H., Weaver, C.M., 2020. Rise in potassium deficiency in the US population linked to 393, 447–492. agriculture practices and dietary potassium deficits. J. Agric. Food Chem. 68, Xu, X., He, P., Pampolino, M.F., Qiu, S., Zhao, S., Zhou, W., 2019. Spatial variation of 11121–11127. yield response and fertilizer requirements on regional scale for irrigated rice in Sun, Z., Scherer, L., Tukker, A., Behrens, P., 2020. Linking global crop and livestock China. Sci. Rep. 9, 3589. consumption to local production hotspots. Global Food Secur. 25, 100323. Yuan, S., Linquist, B.A., Wilson, L.T., Cassman, K.G., Stuart, A.M., Pede, V., Miro, B., Sutton, M.A., Bleeker, A., Howard, C.M., Bekunda, M., Grizetti, B., Vries, W. de, van Saito, K., Agustiani, N., Aristya, V.E., Krisnadi, L.Y., Zanon, A.J., Heinemann, A.B., Grinsven, H.J.M., Abrol, Y.P., Adhya, T.K., Billen, G., 2012. Our Nutrient World: the Carracelas, G., Subash, N., Brahmanand, P.S., Li, T., Peng, S., Grassini, P., 2021. Challenge to Produce More Food and Energy with Less Pollution. https://www.unen Sustainable intensification for a larger global rice bowl. Nat. Commun. 12, 7163. vironment.org/resources/report/our-nutrient-world-challenge-produce-more-food- Zhang, X., 2017. A plan for efficient use of nitrogen fertilizers. Nature 543, 322–323. and-energy-less-pollution. Zhang, X., Chabot, D., Sultan, Y., Monreal, C., DeRosa, M.C., 2013. Target-molecule- Tenorio, F.A., McLellan, E.L., Eagle, A.J., Cassman, K.G., Andersen, D., Krausnick, M., triggered rupture of aptamer-encapsulated polyelectrolyte microcapsules. ACS Appl. Oaklund, R., Thorburn, J., Grassini, P., 2020. Benchmarking impact of nitrogen Mater. Interfaces 5, 5500–5507. inputs on grain yield and environmental performance of producer fields in the Zhang, X., Davidson, E.A., Mauzerall, D.L., Searchinger, T.D., Dumas, P., Shen, Y., 2015. western US Corn Belt. Agric. Ecosyst. Environ. 294, 106865. Managing nitrogen for sustainable development. Nature 528, 51–59. Thornton, P.K., Herrero, M., 2015. Adapting to climate change in the mixed crop and Zhang, X., Davidson, E.A., Zou, T., Lassaletta, L., Quan, Z., Li, T., Zhang, W., 2020. livestock farming systems in sub-Saharan Africa. Nat. Clim. Change 5, 830–836. Quantifying nutrient budgets for sustainable nutrient management. Global Tuninetti, M., Ridolfi, L., Laio, F., 2020. Ever-increasing agricultural land and water Biogeochem 34. Cycles. productivity: a global multi-crop analysis. Environ. Res. Lett. 15, 0940a2. Zhang, W., Zhang, W., Wang, X., Liu, D., Zou, C., Chen, X., 2021a. Quantitative Uwizeye, A., Boer, I.J.M. de, Opio, C.I., Schulte, R.P.O., Falcucci, A., Tempio, G., evaluation of the grain zinc in cereal crops caused by phosphorus fertilization. A Teillard, F., Casu, F., Rulli, M., Galloway, J.N., Leip, A., Erisman, J.W., Robinson, T. meta-analysis. Agron. Sustain. Dev. 41. P., Steinfeld, H., Gerber, P.J., 2020. Nitrogen emissions along global livestock supply Zhang, X., Zou, T., Lassaletta, L., Mueller, N.D., Tubiello, F.N., Lisk, M.D., Lu, C., chains. Nature Food 1, 437–446. Conant, R.T., Dorich, C.D., Gerber, J., Tian, H., Bruulsema, T., Maaz, T.M., van der Hoek, J., Duijff, R., Reinstra, O., 2018. Nitrogen recovery from wastewater: Nishina, K., Bodirsky, B.L., Popp, A., Bouwman, L., Beusen, A., Chang, J., Havlík, P., possibilities, competition with other resources, and adaptation pathways. Leclère, D., Canadell, J.G., Jackson, R.B., Heffer, P., Wanner, N., Zhang, W., Sustainability 10, 4605. Davidson, E.A., 2021b. Quantification of global and national nitrogen budgets for van der Kooij, S., van Vliet, B.J., Stomph, T.J., Sutton, N.B., Anten, N.P., Hoffland, E., crop production. Nature Food 2, 529–540. 2020. Phosphorus recovered from human excreta: a socio-ecological-technical Zoroddu, M.A., Aaseth, J., Crisponi, G., Medici, S., Peana, M., Nurchi, V.M., 2019. The approach to phosphorus recycling. Resour. Conserv. Recycl. 157, 104744. essential metals for humans: a brief overview. J. Inorg. Biochem. 195, 120–129. van Groenigen, J.W., van Kessel, C., Hungate, B.A., Oenema, O., Powlson, D.S., van Groenigen, K.J., 2017. Sequestering soil organic carbon: a nitrogen dilemma. Environ. Sci. Technol. 51, 4738–4739. 13