Progress in understanding drought tolerance: from alleles to cropping systems

Progress in understanding drought tolerance: from alleles to cropping systems Abortion, crop yield, dehydration, drought tolerance, osmotic adjustment, root architecture, seed development, turgor management Improving crop yields under rainfed environments is key to meeting the food security demands of an ever-increasing population, but climate change-associated expansion of drought-affected arable land means that resilient crops and agronomic practices are critical. High-throughput plant phenomics and modern genetic approaches must be directed towards precise understanding of factors controlling crop yield. This special issue covers root dynamics, turgor management under desiccation, molecular responses to dehydration, impact of drought on plant development and seed abortion, and adjustment of traits to the most frequent patterns of drought. It also addresses interdisciplinary views for enhancing genetic gains and achieving a more sustainable climate-resilient agronomy. Drought is a devastating factor for global agronomic production. Although it is uncertain whether episodes of drought will be more severe with climate change (Sheffield et al., 2012), their prevalence and year-to-year variability are major features in future modelling scenarios (Sun et al., 2012; Harrison et al., 2014; see also Box 1). Understanding the mechanisms underpinning plant behaviour under drought is a challenge due to differences in (i) the traits that control plant water status under rapidly changing soil water availability and evaporative demand, (ii) the response of plants to changes in water status, its genetic variability and differences between species (e.g. between cereals and legumes), and (iii) interactions with other factors such as the duration and position of the crop cycle in the season, the frequency of episodes with high temperature and the soil chemical composition (e.g. soil salinity or presence of Al). Box 1. New climate-resilient crops and agronomic practices High temperatures and water deficits associated with climate change are projected to become increasingly erratic, resulting in an expansion of drought-affected arable land worldwide. In such environments, increasing or maintaining crop yields will become gradually more difficult due to the decreasing availability of irrigation water. Therefore, the adoption of climate-resilient crops and agronomic practices is critically important. It is essential to design cropping systems and genotypes that can jointly overcome limitations of crops yields under well-identified drought scenarios. For instance, sorghum is usually grown at high density (as shown). Canopies with half the plant density, obtained by skipping one row out of two (reproducing the crop-free path in the image every second row), reduce canopy cover and offer the advantage of delaying soil water depletion at the end of the cropping season, thereby reducing the risk of failure in very dry years, although it reduces yield in milder years (Whish et al., 2005). This technique may require genotypes with different shoot and root architecture and phenology compared with those used in pure stands. Over past decades, crop physiologists have increasingly focused on molecular aspects of stress tolerance while intensive research and breeding have allowed the selection of climate-resilient cultivars with improved yields. Drought research has progressed rapidly, as can be seen in successive InterDrought conferences (Belhassen, 1997; Araus et al., 2007; Blum, 2013; Tuberosa et al., 2014; see also Tardieu et al., 2017) (see also Box 2, a tribute to Abraham Blum). While initially focused on identifying tolerant lines and understanding the role of proxy traits, research has now reached a position where it can also uncover and allow the manipulation of genes/QTLs and mechanisms involved in cellular and whole-plant responses related to acclimation to drought scenarios. Several loci and genes have been characterized to develop the concept and models of complex drought tolerance traits (Tricker et al., 2018). This paves the way to mapping and cloning of genetic loci governing drought tolerance through turgor management and hormonal regulation, plant architecture and seed development biology, corroborated by transcriptional and post-transcriptional response networks. Drought tolerance involves cell-to-cell to whole-plant level hydraulic or metabolic readjustment, and hormone signalling able to control growth under water deficit. Now, researchers are able to debate the interactions between roots, shoots, the rhizosphere and reproductive traits and how they collectively affect crop yield under the diversity of climatic scenarios involving limited water availability (Tardieu et al., 2018). Box 2. A tribute to Abraham Blum (1934-2018) Abraham Blum passed away on 10 March 2018. During his career, he published two influential books and over 160 scientific papers in peer-reviewed journals, the vast majority of which focused on the functional basis of drought tolerance in cereals as related to proxy traits involved in the adaptive response to water deficit. In a number of thought-provoking and at the time controversial manuscripts (e.g. Blum, 2005, 2009, 2016), he challenged some of the commonly held beliefs concerning drought resistance in crops. Abraham pioneered and championed the study of traits and proxies (e.g. cell membrane stability, canopy temperature, waxiness, osmotic adjustment, ABA accumulation, stem reserve mobilization) able to enhance our understanding of crop plasticity under environmental constraints while providing information for predicting yield under such conditions. Amongst adaptive proxies, he was a strong advocate for osmotic adjustment (Blum, 2017) and canopy temperature (Blum et al., 1982). He was also a strong advocate of a multidiciplinary approach for investigating and enhancing drought resistance in crops. In this, his foremost and greatly appreciated contributions to those engaged in drought-related research were management of the www.plantstress.com website and organization of the InterDrought congress series, which he chaired twice, in 2005 (Rome) and 2009 (Shanghai). The InterDrought V conference (Hyderabad, 2017) community sent their good wishes to Abraham during his illness, completely covering a poster with messages of support. We and the entire InterDrought community will miss Abraham greatly for his tremendous enthusiasm, optimism and endless dedication; his vast knowledge and contributions, and as a dear friend, teacher and colleague. Farewell Abraham. Today there is also a recognition of the diversity of drought scenarios in each region of the world in current and future climates, even in a single field over different years, and the importance of fitting plant phenology and traits to the most likely scenarios in a given region (Olesen et al., 2011; Mickelbart et al., 2015; Chenu et al., 2018). This raises the necessity of adopting probabilistic approaches to drought tolerance based on both crop modelling and genomic prediction in identifying where and when any combination of alleles or traits are beneficial in specific drought scenarios (Ewert et al., 2015; Tardieu et al., 2018). Furthermore, the importance attached to modelling approaches has increased, together with an improved ability of the scientific community to more-accurately measure and forecast environmental conditions, and to simulate the behaviour of genotypes in a range of environmental conditions (Chenu et al., 2018), including those associated with climate change. Physiological and molecular basis of drought tolerance in plants Standard terminology is now accepted for plant water status, following Hsiao (1973), who defined ‘hydrated’, ‘mild stress’, ‘moderate stress’, ‘severe stress’ and ‘desiccation’ based on the timing and severity of water deficit. In this issue, Zhang and Bartels (2018) distinguish dehydration and desiccation tolerances, an essential distinction for phenotyping and interpreting survival and recovery (Blum and Tuberosa, 2018). These processes are achieved through multiple interactions involving stomatal conductance, carotenoid degradation and anthocyanin accumulation along with ABA and cytokinin accumulation, the intervention of osmoprotectants (e.g. sucrose, glycine, proline) and ROS-scavenging enzymes. Turner (2018) presents 40 years of research on the beneficial role of osmotic adjustment on turgor maintenance in drought-prone environments. The genetic variations and breeding of turgor maintenance for crops resilience to water-limited environments is discussed, including examples of drought-tolerant wheat genotypes that control osmoregulation in both leaves and pollen through the expression of the OR gene. A crop canopy is formed of individual plants which, although they share a common genome, have markedly different features. Borrás and Vitantonio-Mazzini (2018) analyse the role of plant-to-plant variability for plant development and ear growth, in particular via measured genetic progress over past decades. This progress is in part determined by (i) the ability of plants to produce high individual yield at high densities while maintaining sufficient uniformity between plants and (ii) the rate of silk extrusion for a given ear or plant biomass. Failure of fertilization and arrested ovary growth can cause ovary/grain abortion, often considered to be a consequence of the availability of sucrose to ovaries (Boyer and McLaughlin, 2007; Ruan et al., 2010). Here, Turc and Tardieu (2018) propose another view, that abortion under progressive water deficit is essentially due to developmental processes as affected by water deficit. This is the case in maize, pea and sunflower, with a cessation of growth of the youngest reproductive organs that occurs earlier under water deficit than in well-watered conditions, due to the effect of drought on the respective timing of the development of ovary cohorts and the signalling between oldest and youngest reproductive organs. Drought and heat episodes are often synchronous so a combined tolerance is essential, although the genetic architectures of tolerances to drought and high temperatures differ appreciably (Tricker et al., 2018). After reviewing traits with comparative advantages, these authors conclude that the maintenance of plant water status is essential for tolerance to both stresses, via fine tuning of gas exchange and plant hydraulic conductance, including the adaptive response of root systems, together with more classically described traits such as cell protection at high temperatures. This involves improving several plant plasticity traits at a time, a difficult task that can be envisaged by combining phenomics, quantitative genetics, QTL cloning and genome editing (Salvi and Tuberosa, 2015). Root system traits Plant roots release a broad variety of chemical compounds to attract useful microorganisms in the rhizosphere which in turn influence plant health and growth (Huang et al., 2014). Ahmed et al. (2018) present the root architectural and anatomical traits, together with rhizosphere traits, that affect plant water uptake. The hydraulic continuity of the rhizosphere is studied using a physical approach, and its consequences on the growth, transpiration and yield of the crop canopy are discussed. The traits and QTLs associated with root-system architecture can have markedly different effects depending on environmental scenarios (Varshney et al., 2014). A view on root system architecture in response to water deficit in legumes is presented by Ye et al. (2018). It brings together genetic and genomics approaches for analysing quantitative trait loci (QTLs) associated with root system architecture and the beneficial root traits that can accelerate the genetic improvement of yield under water deficit. There are already several studies where introgression of root traits has been successful in enhancing crop productivity (Varshney et al., 2016). Lynch (2018) also addresses this question and proposes that the high investment in root systems that was favoured by natural selection for crop ancestors that suffered multiple stresses and intense competition may no longer be useful in agricultural high-input agrosystems. More parsimonious root systems centred on water capture are desirable, via reduced root branching and a root anatomy that decreases the root carbon cost. Functional–structural models capable of stimulating the dynamics of root–soil interactions allow the value of these traits in different agrosystems to be evaluated. In particular, parsimonious root systems are probably less useful in low-input fields characterized by multiple stress-related cues in addition to water deficit. Interdisciplinary approaches Although the concept of converging or integrating distinct disciplines is not new in plant research, it remains challenging (see Mir et al., 2012). Convergence not only concerns the small area of intersection between different disciplines, but also new approaches that represent the merging and integration of different technologies, disciplines and modelling. Chenu et al. (2018) integrate modelling and phenomic approaches for addressing complex traits in cereals and cover advances in cereal genomics using integrated approach including the identification of a number of significant QTLs for transpiration efficiency (biomass produced for unit of water used) in sorghum. Despite of progress in genetics, genomics and phenotyping, trait selection in breeding is limited by our ability to understand interactions within the plant and with the environment and to identify traits of most relevance for the target population of environments. Studying and extending integrated approaches via modelling can capitalize on insights gained by the drought community and elsewhere. Genomics is generating new tools, such as functional molecular markers and informatics, as well as new knowledge about statistics and inheritance phenomena that could increase the efficiency and accuracy of crop improvement (Varshney et al., 2005). Here, one review on integrating genomics, phenomics, systems modeling and agronomy for enhancing genetic gains in legumes emphasizes the role of selection intensity, generation interval and improved operational efficiencies in breeding (Varshney et al., 2018). It also addresses increase in profitability of farming and availability of affordable notorious food with enhanced genetic gains in terms of not only productivity but also nutritional and market traits. Conclusion The range of topics covered in this special issue should help in the integration of disciplines needed to support crop improvement and the design of novel cropping systems allowing better yields of drought-stressed plants. We hope it will provide new inspiration and creative opportunities to address the challenges posed by climate change, and anticipate convergence to continue in coming years. Acknowledgements Guest editors would like to thank all authors who contributed their research and ideas to this special issue, and as organizers of the InterDrought V conference (Hyderabad, 2017) extend this also to speakers at that meeting. We are also grateful to our organizations and to a number of donors, especially the United States Agency for International Agricultural Development, Indian Council of Agricultural Research and ICRISAT for their special support and co-organizing the conference. R. K. V. is thankful to his colleagues, especially Ms Annapurna Chitkineni for her help in organizing the conference and Dr K. Himabindu and Dr Rakesh Kumar for their help and assistance in editing the special issue. We dedicate this special issue to the memory of Abraham Blum who passed away on 10 March 2018. References Ahmed MA , Passioura J , Carminati A . 2018 . Hydraulic processes in roots and the rhizosphere pertinent to increasing yield of water-limited grain crops: a critical review . Journal of Experimental Botany 69 , 3255 – 3265 . Google Scholar CrossRef Search ADS Araus JL , Blum A , Nguyen HT , Parry MAJ , Tuberosa R . 2007 . Integrated approaches to sustain and improve plant production under drought stress: preface . Journal of Experimental Botany 58 , 2 . Belhassen E , ed. 1997 . Drought tolerance in higher plants: genetical, physiological and molecular biological analysis . Kluwer Academic Publishers : Dordrecht, The Netherlands . Google Scholar CrossRef Search ADS Blum A . 2005 . Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive ? Australian Journal of Agricultural Research 56 , 1159 – 1168 . Google Scholar CrossRef Search ADS Blum A . 2009 . Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress . Field Crops Research 112 , 119 – 123 . Google Scholar CrossRef Search ADS Blum A . 2013 . The Interdrought conference in perspective . Journal of Experimental Botany 64 , 5773 – 5774 . Google Scholar CrossRef Search ADS PubMed Blum A . 2016 . Stress, strain, signaling, and adaptation–not just a matter of definition . Journal of Experimental Botany 67 , 562 – 565 . Google Scholar CrossRef Search ADS PubMed Blum A . 2017 . Osmotic adjustment is a prime drought stress adaptive engine in support of plant production . Plant, Cell & Environment 40 , 4 – 10 . Google Scholar CrossRef Search ADS PubMed Blum A , Mayer J , Gozlan G . 1982 . Infrared thermal sensing of plant canopies as a screening technique for dehydration avoidance in wheat . Field Crops Research 5 , 137 – 146 . Google Scholar CrossRef Search ADS Blum A , Tuberosa R . 2018 . Dehydration survival of crop plants and its measurement . Journal of Experimental Botany 69 , 975 – 981 . Google Scholar CrossRef Search ADS PubMed Borrás L , Vitantonio-Mazzini LN . 2018 . Maize reproductive development and kernel set under limited plant growth environments . Journal of Experimental Botany 69 , 3235 – 3243 . Boyer JS , McLaughlin JE . 2007 . Functional reversion to identify controlling genes in multigenic responses: analysis of floral abortion . Journal of Experimental Botany 58 , 267 – 277 . Google Scholar CrossRef Search ADS PubMed Chenu K , Oosterom VJE , Mclean G et al. 2018 . Integrating modelling and phenotyping approaches to identify and screen complex traits – transpiration efficiency in cereals . Journal of Experimental Botany 69 , 3181 – 3194 . Ewert F , Rotter RP , Bindi M et al. 2015 . Crop modelling for integrated assessment of risk to food production from climate change . Environmental Modelling & Software 72 , 287 – 303 . Google Scholar CrossRef Search ADS Harrison MT , Tardieu F , Dong Z , Messina CD , Hammer GL . 2014 . Characterizing drought stress and trait influence on maize yield under current and future conditions . Global Change Biology 20 , 867 – 878 . Google Scholar CrossRef Search ADS PubMed Hsiao TC . 1973 . Plant responses to water stress . Annual Review of Plant Physiology 24 , 519 – 570 . Google Scholar CrossRef Search ADS Huang X , Chaparro JM , Reardon KF , Zhang R , Shen Q , Vivanco JM . 2014 . Rhizosphere interactions: root exudates, microbes, and microbial communities . Botany 92 , 267 – 275 . Google Scholar CrossRef Search ADS Lynch J . 2018 . Rightsizing root phenotypes for drought resistance . Journal of Experimental Botany 69 , 3279 – 3292 . Mickelbart MV , Hasegawa PM , Bailey-Serres J . 2015 . Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability . Nature Reviews. Genetics 16 , 237 – 251 . Google Scholar CrossRef Search ADS PubMed Mir RR , Zaman-Allah M , Sreenivasulu N , Trethowan R , Varshney RK . 2012 . Integrated genomics, physiology and breeding approaches for improving drought tolerance in crops . Theoretical and Applied Genetics . 125 , 625 – 645 . Google Scholar CrossRef Search ADS PubMed Olesen JE , Trnka M , Kersebaum KC , Skjelvag AO , Seguin B , Peltonen-Sainio P , Rossi F , Kozyra J , Micale F . 2011 . Impacts and adaptation of European crop production systems to climate change . European Journal of Agronomy 34 , 96 – 112 . Google Scholar CrossRef Search ADS Ruan YL , Jin Y , Yang YJ , Li GJ , Boyer JS . 2010 . Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat . Molecular Plant 3 , 942 – 955 . Google Scholar CrossRef Search ADS PubMed Salvi S , Tuberosa R . 2015 . The crop QTLome comes of age . Current Opinion in Biotechnology 32 , 179 – 185 . Google Scholar CrossRef Search ADS PubMed Sheffield J , Wood EF , Roderick ML . 2012 . Little change in global drought over the past 60 years . Nature 491 , 435 – 438 . Google Scholar CrossRef Search ADS PubMed Sun FB , Roderick ML , Farquhar GD . 2012 . Changes in the variability of global land precipitation . Geophysical Research Letters 39 , L19402 . Google Scholar CrossRef Search ADS Tardieu F , Simonneau T , Muller B . 2018 . The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach . Annual Review of Plant Biology 69 , 733 – 759 . Google Scholar CrossRef Search ADS PubMed Tardieu F , Varshney RK , Tuberosa R . 2017 . Improving crop performance under drought - cross-fertilization of disciplines . Journal of Experimental Botany 68 , 1393 – 1398 . Google Scholar PubMed Tricker PJ , ElHabti A , Schmidt J , Fleury D . 2018 . The physiological and genetic basis of combined drought and heat tolerance in wheat . Journal of Experimental Botany 69 , 3195 – 3210 . Tuberosa R , Turner NC , Cakir M . 2014 . Two decades of InterDrought conferences: are we bridging the genotype-to-phenotype gap ? Journal of Experimental Botany 65 , 6137 – 6139 . Google Scholar CrossRef Search ADS PubMed Turc O , Tardieu F . 2018 . Drought affects abortion of reproductive organs by exacerbating developmentally driven processes via expansive growth and hydraulics . Journal of Experimental Botany 69 , 3245 – 3254 . Turner NC . 2018 . Turgor maintenance by osmotic adjustment – 40 years of progress . Journal of Experimental Botany 69 , 3223 – 3233 . Varshney RK , Gaur PM , Chamarthi SK , Krishnamurthy L , Tripathi S , Kashiwagi J , Samineni S , Singh VK , Thudi M , Jaganathan D . 2016 . Fast-track introgression of “QTL-hotspot” for root traits and other drought tolerance traits in JG 11, an elite and leading variety of chickpea (Cicer arietinum L.) . The Plant Genome 6 , 1 – 9 . Google Scholar CrossRef Search ADS Varshney RK , Graner A , Sorrells ME . 2005 . Genomics-assisted breeding for crop improvement . Trends in Plant Science 10 , 621 – 630 . Google Scholar CrossRef Search ADS PubMed Varshney RK , Thudi M , Nayak SN et al. 2014 . Genetic dissection of drought tolerance in chickpea (Cicer arietinum L.) . Theoretical and Applied Genetics . 127 , 445 – 462 . Google Scholar CrossRef Search ADS PubMed Varshney RK , Thudi M , Pande MK et al. 2018 . Accelerating genetic gains in legumes for the development of prosperous smallholder agriculture: integrating genomics, phenotyping, systems modelling and agronomy . Journal of Experimental Botany 69 , 3293 – 3312 . Whish J , Butler G , Castor M , Cawthray S , Broad I , Carberry P , Hammer G , McLean G , Routley R , Yeates S . 2005 . Modelling the effects of row configuration on sorghum yield reliability in north-eastern Australia . Australian Journal of Agricultural Research 56 , 11 – 23 . Google Scholar CrossRef Search ADS Ye H , Roorkiwal M , Valliyodan B , Zhou L , Chen P , Varshney RK , Nguyen H . 2018 . Genetic diversity of root system architecture in response to drought stress in grain legumes . Journal of Experimental Botany 69 , 3267 – 3277 . Zhang Q , Bartels D . 2018 . Molecular responses to dehydration and desiccation in desiccation-tolerant angiosperm plants . Journal of Experimental Botany 69 , 3211 – 3222 . © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Experimental Botany Oxford University Press

Progress in understanding drought tolerance: from alleles to cropping systems

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Experimental Biology.
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0022-0957
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Abstract

Abortion, crop yield, dehydration, drought tolerance, osmotic adjustment, root architecture, seed development, turgor management Improving crop yields under rainfed environments is key to meeting the food security demands of an ever-increasing population, but climate change-associated expansion of drought-affected arable land means that resilient crops and agronomic practices are critical. High-throughput plant phenomics and modern genetic approaches must be directed towards precise understanding of factors controlling crop yield. This special issue covers root dynamics, turgor management under desiccation, molecular responses to dehydration, impact of drought on plant development and seed abortion, and adjustment of traits to the most frequent patterns of drought. It also addresses interdisciplinary views for enhancing genetic gains and achieving a more sustainable climate-resilient agronomy. Drought is a devastating factor for global agronomic production. Although it is uncertain whether episodes of drought will be more severe with climate change (Sheffield et al., 2012), their prevalence and year-to-year variability are major features in future modelling scenarios (Sun et al., 2012; Harrison et al., 2014; see also Box 1). Understanding the mechanisms underpinning plant behaviour under drought is a challenge due to differences in (i) the traits that control plant water status under rapidly changing soil water availability and evaporative demand, (ii) the response of plants to changes in water status, its genetic variability and differences between species (e.g. between cereals and legumes), and (iii) interactions with other factors such as the duration and position of the crop cycle in the season, the frequency of episodes with high temperature and the soil chemical composition (e.g. soil salinity or presence of Al). Box 1. New climate-resilient crops and agronomic practices High temperatures and water deficits associated with climate change are projected to become increasingly erratic, resulting in an expansion of drought-affected arable land worldwide. In such environments, increasing or maintaining crop yields will become gradually more difficult due to the decreasing availability of irrigation water. Therefore, the adoption of climate-resilient crops and agronomic practices is critically important. It is essential to design cropping systems and genotypes that can jointly overcome limitations of crops yields under well-identified drought scenarios. For instance, sorghum is usually grown at high density (as shown). Canopies with half the plant density, obtained by skipping one row out of two (reproducing the crop-free path in the image every second row), reduce canopy cover and offer the advantage of delaying soil water depletion at the end of the cropping season, thereby reducing the risk of failure in very dry years, although it reduces yield in milder years (Whish et al., 2005). This technique may require genotypes with different shoot and root architecture and phenology compared with those used in pure stands. Over past decades, crop physiologists have increasingly focused on molecular aspects of stress tolerance while intensive research and breeding have allowed the selection of climate-resilient cultivars with improved yields. Drought research has progressed rapidly, as can be seen in successive InterDrought conferences (Belhassen, 1997; Araus et al., 2007; Blum, 2013; Tuberosa et al., 2014; see also Tardieu et al., 2017) (see also Box 2, a tribute to Abraham Blum). While initially focused on identifying tolerant lines and understanding the role of proxy traits, research has now reached a position where it can also uncover and allow the manipulation of genes/QTLs and mechanisms involved in cellular and whole-plant responses related to acclimation to drought scenarios. Several loci and genes have been characterized to develop the concept and models of complex drought tolerance traits (Tricker et al., 2018). This paves the way to mapping and cloning of genetic loci governing drought tolerance through turgor management and hormonal regulation, plant architecture and seed development biology, corroborated by transcriptional and post-transcriptional response networks. Drought tolerance involves cell-to-cell to whole-plant level hydraulic or metabolic readjustment, and hormone signalling able to control growth under water deficit. Now, researchers are able to debate the interactions between roots, shoots, the rhizosphere and reproductive traits and how they collectively affect crop yield under the diversity of climatic scenarios involving limited water availability (Tardieu et al., 2018). Box 2. A tribute to Abraham Blum (1934-2018) Abraham Blum passed away on 10 March 2018. During his career, he published two influential books and over 160 scientific papers in peer-reviewed journals, the vast majority of which focused on the functional basis of drought tolerance in cereals as related to proxy traits involved in the adaptive response to water deficit. In a number of thought-provoking and at the time controversial manuscripts (e.g. Blum, 2005, 2009, 2016), he challenged some of the commonly held beliefs concerning drought resistance in crops. Abraham pioneered and championed the study of traits and proxies (e.g. cell membrane stability, canopy temperature, waxiness, osmotic adjustment, ABA accumulation, stem reserve mobilization) able to enhance our understanding of crop plasticity under environmental constraints while providing information for predicting yield under such conditions. Amongst adaptive proxies, he was a strong advocate for osmotic adjustment (Blum, 2017) and canopy temperature (Blum et al., 1982). He was also a strong advocate of a multidiciplinary approach for investigating and enhancing drought resistance in crops. In this, his foremost and greatly appreciated contributions to those engaged in drought-related research were management of the www.plantstress.com website and organization of the InterDrought congress series, which he chaired twice, in 2005 (Rome) and 2009 (Shanghai). The InterDrought V conference (Hyderabad, 2017) community sent their good wishes to Abraham during his illness, completely covering a poster with messages of support. We and the entire InterDrought community will miss Abraham greatly for his tremendous enthusiasm, optimism and endless dedication; his vast knowledge and contributions, and as a dear friend, teacher and colleague. Farewell Abraham. Today there is also a recognition of the diversity of drought scenarios in each region of the world in current and future climates, even in a single field over different years, and the importance of fitting plant phenology and traits to the most likely scenarios in a given region (Olesen et al., 2011; Mickelbart et al., 2015; Chenu et al., 2018). This raises the necessity of adopting probabilistic approaches to drought tolerance based on both crop modelling and genomic prediction in identifying where and when any combination of alleles or traits are beneficial in specific drought scenarios (Ewert et al., 2015; Tardieu et al., 2018). Furthermore, the importance attached to modelling approaches has increased, together with an improved ability of the scientific community to more-accurately measure and forecast environmental conditions, and to simulate the behaviour of genotypes in a range of environmental conditions (Chenu et al., 2018), including those associated with climate change. Physiological and molecular basis of drought tolerance in plants Standard terminology is now accepted for plant water status, following Hsiao (1973), who defined ‘hydrated’, ‘mild stress’, ‘moderate stress’, ‘severe stress’ and ‘desiccation’ based on the timing and severity of water deficit. In this issue, Zhang and Bartels (2018) distinguish dehydration and desiccation tolerances, an essential distinction for phenotyping and interpreting survival and recovery (Blum and Tuberosa, 2018). These processes are achieved through multiple interactions involving stomatal conductance, carotenoid degradation and anthocyanin accumulation along with ABA and cytokinin accumulation, the intervention of osmoprotectants (e.g. sucrose, glycine, proline) and ROS-scavenging enzymes. Turner (2018) presents 40 years of research on the beneficial role of osmotic adjustment on turgor maintenance in drought-prone environments. The genetic variations and breeding of turgor maintenance for crops resilience to water-limited environments is discussed, including examples of drought-tolerant wheat genotypes that control osmoregulation in both leaves and pollen through the expression of the OR gene. A crop canopy is formed of individual plants which, although they share a common genome, have markedly different features. Borrás and Vitantonio-Mazzini (2018) analyse the role of plant-to-plant variability for plant development and ear growth, in particular via measured genetic progress over past decades. This progress is in part determined by (i) the ability of plants to produce high individual yield at high densities while maintaining sufficient uniformity between plants and (ii) the rate of silk extrusion for a given ear or plant biomass. Failure of fertilization and arrested ovary growth can cause ovary/grain abortion, often considered to be a consequence of the availability of sucrose to ovaries (Boyer and McLaughlin, 2007; Ruan et al., 2010). Here, Turc and Tardieu (2018) propose another view, that abortion under progressive water deficit is essentially due to developmental processes as affected by water deficit. This is the case in maize, pea and sunflower, with a cessation of growth of the youngest reproductive organs that occurs earlier under water deficit than in well-watered conditions, due to the effect of drought on the respective timing of the development of ovary cohorts and the signalling between oldest and youngest reproductive organs. Drought and heat episodes are often synchronous so a combined tolerance is essential, although the genetic architectures of tolerances to drought and high temperatures differ appreciably (Tricker et al., 2018). After reviewing traits with comparative advantages, these authors conclude that the maintenance of plant water status is essential for tolerance to both stresses, via fine tuning of gas exchange and plant hydraulic conductance, including the adaptive response of root systems, together with more classically described traits such as cell protection at high temperatures. This involves improving several plant plasticity traits at a time, a difficult task that can be envisaged by combining phenomics, quantitative genetics, QTL cloning and genome editing (Salvi and Tuberosa, 2015). Root system traits Plant roots release a broad variety of chemical compounds to attract useful microorganisms in the rhizosphere which in turn influence plant health and growth (Huang et al., 2014). Ahmed et al. (2018) present the root architectural and anatomical traits, together with rhizosphere traits, that affect plant water uptake. The hydraulic continuity of the rhizosphere is studied using a physical approach, and its consequences on the growth, transpiration and yield of the crop canopy are discussed. The traits and QTLs associated with root-system architecture can have markedly different effects depending on environmental scenarios (Varshney et al., 2014). A view on root system architecture in response to water deficit in legumes is presented by Ye et al. (2018). It brings together genetic and genomics approaches for analysing quantitative trait loci (QTLs) associated with root system architecture and the beneficial root traits that can accelerate the genetic improvement of yield under water deficit. There are already several studies where introgression of root traits has been successful in enhancing crop productivity (Varshney et al., 2016). Lynch (2018) also addresses this question and proposes that the high investment in root systems that was favoured by natural selection for crop ancestors that suffered multiple stresses and intense competition may no longer be useful in agricultural high-input agrosystems. More parsimonious root systems centred on water capture are desirable, via reduced root branching and a root anatomy that decreases the root carbon cost. Functional–structural models capable of stimulating the dynamics of root–soil interactions allow the value of these traits in different agrosystems to be evaluated. In particular, parsimonious root systems are probably less useful in low-input fields characterized by multiple stress-related cues in addition to water deficit. Interdisciplinary approaches Although the concept of converging or integrating distinct disciplines is not new in plant research, it remains challenging (see Mir et al., 2012). Convergence not only concerns the small area of intersection between different disciplines, but also new approaches that represent the merging and integration of different technologies, disciplines and modelling. Chenu et al. (2018) integrate modelling and phenomic approaches for addressing complex traits in cereals and cover advances in cereal genomics using integrated approach including the identification of a number of significant QTLs for transpiration efficiency (biomass produced for unit of water used) in sorghum. Despite of progress in genetics, genomics and phenotyping, trait selection in breeding is limited by our ability to understand interactions within the plant and with the environment and to identify traits of most relevance for the target population of environments. Studying and extending integrated approaches via modelling can capitalize on insights gained by the drought community and elsewhere. Genomics is generating new tools, such as functional molecular markers and informatics, as well as new knowledge about statistics and inheritance phenomena that could increase the efficiency and accuracy of crop improvement (Varshney et al., 2005). Here, one review on integrating genomics, phenomics, systems modeling and agronomy for enhancing genetic gains in legumes emphasizes the role of selection intensity, generation interval and improved operational efficiencies in breeding (Varshney et al., 2018). It also addresses increase in profitability of farming and availability of affordable notorious food with enhanced genetic gains in terms of not only productivity but also nutritional and market traits. Conclusion The range of topics covered in this special issue should help in the integration of disciplines needed to support crop improvement and the design of novel cropping systems allowing better yields of drought-stressed plants. We hope it will provide new inspiration and creative opportunities to address the challenges posed by climate change, and anticipate convergence to continue in coming years. Acknowledgements Guest editors would like to thank all authors who contributed their research and ideas to this special issue, and as organizers of the InterDrought V conference (Hyderabad, 2017) extend this also to speakers at that meeting. 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Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

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Journal of Experimental BotanyOxford University Press

Published: Jun 6, 2018

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