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Progress in understanding drought tolerance: from alleles to cropping systems

Progress in understanding drought tolerance: from alleles to cropping systems Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 Journal of Experimental Botany, Vol. 69, No. 13 pp. 3175–3179, 2018 doi:10.1093/jxb/ery187 eXtra Botany Special Issue Editorial Varshney et al. Progress in understanding drought tolerance: from alleles to cropping systems Improving crop yields under rainfed environments is related to acclimation to drought scenarios. Several loci and key to meeting the food security demands of an ever- genes have been characterized to develop the concept and Received 14 May 2018; Editorial decision ; Accepted 14 May 2018 increasing population, but climate change-associated models of complex drought tolerance traits (Tricker et  al., expansion of drought-affected arable land means that 2018). This paves the way to mapping and cloning of gen- resilient crops and agronomic practices are critical. etic loci governing drought tolerance through turgor manage- High-throughput plant phenomics and modern genetic ment and hormonal regulation, plant architecture and seed approaches must be directed towards precise under- development biology, corroborated by transcriptional and standing of factors controlling crop yield. This spe- post-transcriptional response networks. Drought tolerance cial issue covers root dynamics, turgor management involves cell-to-cell to whole-plant level hydraulic or meta- under desiccation, molecular responses to dehydra- bolic readjustment, and hormone signalling able to control tion, impact of drought on plant development and seed growth under water deficit. Now, researchers are able to abortion, and adjustment of traits to the most frequent debate the interactions between roots, shoots, the rhizosphere patterns of drought. It also addresses interdisciplin- and reproductive traits and how they collectively affect crop ary views for enhancing genetic gains and achieving a yield under the diversity of climatic scenarios involving more sustainable climate-resilient agronomy. limited water availability (Tardieu et al., 2018). Today there is also a recognition of the diversity of drought scenarios in each region of the world in current and future cli- Drought is a devastating factor for global agronomic produc- mates, even in a single field over different years, and the import- tion. Although it is uncertain whether episodes of drought ance of fitting plant phenology and traits to the most likely will be more severe with climate change (Sheffield et al., 2012), scenarios in a given region (Olesen et al., 2011; Mickelbart et al., their prevalence and year-to-year variability are major fea- 2015; Chenu et al., 2018). This raises the necessity of adopting tures in future modelling scenarios (Sun et al., 2012; Harrison probabilistic approaches to drought tolerance based on both et al., 2014; see also Box 1). Understanding the mechanisms crop modelling and genomic prediction in identifying where underpinning plant behaviour under drought is a challenge and when any combination of alleles or traits are beneficial in due to differences in (i) the traits that control plant water sta- specific drought scenarios (Ewert et  al., 2015; Tardieu et  al., tus under rapidly changing soil water availability and evap- 2018). Furthermore, the importance attached to modelling orative demand, (ii) the response of plants to changes in approaches has increased, together with an improved ability of water status, its genetic variability and differences between the scientific community to more-accurately measure and fore- species (e.g. between cereals and legumes), and (iii) interac- cast environmental conditions, and to simulate the behaviour of tions with other factors such as the duration and position of genotypes in a range of environmental conditions (Chenu et al., the crop cycle in the season, the frequency of episodes with 2018), including those associated with climate change. high temperature and the soil chemical composition (e.g. soil salinity or presence of Al). Over past decades, crop physiologists have increasingly focused on molecular aspects of stress tolerance while intensive Physiological and molecular basis of research and breeding have allowed the selection of climate- drought tolerance in plants resilient cultivars with improved yields. Drought research has progressed rapidly, as can be seen in successive InterDrought Standard terminology is now accepted for plant water status, conferences (Belhassen, 1997; Araus et al., 2007; Blum, 2013; following Hsiao (1973), who defined ‘hydrated’, ‘mild stress’, Tuberosa et al., 2014; see also Tardieu et al., 2017) (see also ‘moderate stress’, ‘severe stress’ and ‘desiccation’ based on Box 2, a tribute to Abraham Blum). While initially focused the timing and severity of water deficit. In this issue, Zhang on identifying tolerant lines and understanding the role of and Bartels (2018) distinguish dehydration and desiccation proxy traits, research has now reached a position where it can tolerances, an essential distinction for phenotyping and inter- also uncover and allow the manipulation of genes/QTLs and preting survival and recovery (Blum and Tuberosa, 2018). mechanisms involved in cellular and whole-plant responses These processes are achieved through multiple interactions © 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. Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 3176 | Special Issue Editorial 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 geno- types 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. involving stomatal conductance, carotenoid degradation Failure of fertilization and arrested ovary growth can cause and anthocyanin accumulation along with ABA and cytoki- ovary/grain abortion, often considered to be a consequence of nin accumulation, the intervention of osmoprotectants (e.g. the availability of sucrose to ovaries (Boyer and McLaughlin, sucrose, glycine, proline) and ROS-scavenging enzymes. 2007; Ruan et al., 2010). Here, Turc and Tardieu (2018) pro- Turner (2018) presents 40 years of research on the beneficial pose another view, that abortion under progressive water defi- role of osmotic adjustment on turgor maintenance in drought- cit is essentially due to developmental processes as affected by prone environments. The genetic variations and breeding of water deficit. This is the case in maize, pea and sunflower, with turgor maintenance for crops resilience to water-limited envi- a cessation of growth of the youngest reproductive organs that ronments is discussed, including examples of drought-tolerant occurs earlier under water deficit than in well-watered condi- wheat genotypes that control osmoregulation in both leaves tions, due to the effect of drought on the respective timing of and pollen through the expression of the OR gene. the development of ovary cohorts and the signalling between A crop canopy is formed of individual plants which, oldest and youngest reproductive organs. although they share a common genome, have markedly differ- Drought and heat episodes are often synchronous so a com- ent features. Borrás and Vitantonio-Mazzini (2018) analyse the bined tolerance is essential, although the genetic architectures role of plant-to-plant variability for plant development and ear of tolerances to drought and high temperatures differ appreci- growth, in particular via measured genetic progress over past ably (Tricker et al., 2018). After reviewing traits with compara- decades. This progress is in part determined by (i) the ability of tive advantages, these authors conclude that the maintenance plants to produce high individual yield at high densities while of plant water status is essential for tolerance to both stresses, maintaining sufficient uniformity between plants and (ii) the via fine tuning of gas exchange and plant hydraulic conduct- rate of silk extrusion for a given ear or plant biomass. ance, including the adaptive response of root systems, together Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 Special Issue Editorial | 3177 Box 2. A tribute to Abraham Blum (1934-2018) Abraham Blum passed away on 10 March 2018. During his career, he published two influ- ential 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 com- monly 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 re- serve 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. with more classically described traits such as cell protection at et  al. (2018) present the root architectural and anatomical high temperatures. This involves improving several plant plas- traits, together with rhizosphere traits, that affect plant water ticity traits at a time, a difficult task that can be envisaged by uptake. The hydraulic continuity of the rhizosphere is studied combining phenomics, quantitative genetics, QTL cloning and using a physical approach, and its consequences on the growth, genome editing (Salvi and Tuberosa, 2015). transpiration and yield of the crop canopy are discussed. The traits and QTLs associated with root-system archi- tecture can have markedly different effects depending on Root system traits environmental scenarios (Varshney et  al., 2014). A  view on Plant roots release a broad variety of chemical compounds to root system architecture in response to water deficit in leg- attract useful microorganisms in the rhizosphere which in turn umes is presented by Ye et al. (2018). It brings together gen- influence plant health and growth (Huang et al., 2014). Ahmed etic and genomics approaches for analysing quantitative trait Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 3178 | Special Issue Editorial loci (QTLs) associated with root system architecture and the allowing better yields of drought-stressed plants. We hope beneficial root traits that can accelerate the genetic improve- it will provide new inspiration and creative opportunities to ment of yield under water deficit. There are already several address the challenges posed by climate change, and antici- studies where introgression of root traits has been successful pate convergence to continue in coming years. 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 Acknowledgements by natural selection for crop ancestors that suffered multiple Guest editors would like to thank all authors who contributed their research stresses and intense competition may no longer be useful in and ideas to this special issue, and as organizers of the InterDrought V conference (Hyderabad, 2017) extend this also to speakers at that meeting. agricultural high-input agrosystems. More parsimonious root We are also grateful to our organizations and to a number of donors, espe- systems centred on water capture are desirable, via reduced cially the United States Agency for International Agricultural Development, root branching and a root anatomy that decreases the root Indian Council of Agricultural Research and ICRISAT for their special sup- port and co-organizing the conference. R. K. V. is thankful to his colleagues, carbon cost. Functional–structural models capable of stimu- especially Ms Annapurna Chitkineni for her help in organizing the confer- lating the dynamics of root–soil interactions allow the value ence and Dr K. Himabindu and Dr Rakesh Kumar for their help and assist- of these traits in different agrosystems to be evaluated. In par- ance in editing the special issue. We dedicate this special issue to the memory of Abraham Blum who ticular, parsimonious root systems are probably less useful in passed away on 10 March 2018. low-input fields characterized by multiple stress-related cues in addition to water deficit. Keywords: Abortion, crop yield, dehydration, drought tolerance, osmotic adjustment, root architecture, seed development, turgor management. Interdisciplinary approaches 1, 2 Rajeev K. Varshney, * Roberto Tuberosa, and Although the concept of converging or integrating distinct Francois Tardieu disciplines is not new in plant research, it remains challeng- ing (see Mir et al., 2012). Convergence not only concerns the 1 Center of Excellence in Genomics & Systems Biology (CEGSB), small area of intersection between different disciplines, but International Crops Research Institute for the Semi-Arid Tropics also new approaches that represent the merging and integra- (ICRISAT), Hyderabad, India tion of different technologies, disciplines and modelling. Department of Agricultural and Food Sciences, University of Chenu et  al. (2018) integrate modelling and phenomic Bologna, Italy approaches for addressing complex traits in cereals and Université de Montpellier, INRA, LEPSE, Montpellier, France* Correspondence: r.k.varshney@cgiar.org or roberto.tuberosa@ cover advances in cereal genomics using integrated approach unibo.it or francois.tardieu@inra.fr 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, gen- omics and phenotyping, trait selection in breeding is limited by our ability to understand interactions within the plant and References with the environment and to identify traits of most relevance Ahmed MA, Passioura J, Carminati A. 2018. Hydraulic processes in for the target population of environments. Studying and roots and the rhizosphere pertinent to increasing yield of water-limited grain crops: a critical review. Journal of Experimental Botany 69, 3255–3265. extending integrated approaches via modelling can capitalize Araus JL, Blum A, Nguyen HT, Parry MAJ, Tuberosa R. 2007. on insights gained by the drought community and elsewhere. Integrated approaches to sustain and improve plant production under Genomics is generating new tools, such as functional drought stress: preface. Journal of Experimental Botany 58, 2. molecular markers and informatics, as well as new knowledge Belhassen E, ed. 1997. Drought tolerance in higher plants: genetical, about statistics and inheritance phenomena that could increase physiological and molecular biological analysis. Kluwer Academic Publishers: Dordrecht, The Netherlands. the efficiency and accuracy of crop improvement (Varshney Blum A. 2005. Drought resistance, water-use efficiency, and yield et al., 2005). Here, one review on integrating genomics, phe- potential—are they compatible, dissonant, or mutually exclusive? nomics, systems modeling and agronomy for enhancing gen- Australian Journal of Agricultural Research 56, 1159–1168. etic gains in legumes emphasizes the role of selection intensity, Blum A. 2009. Effective use of water (EUW) and not water-use efficiency generation interval and improved operational efficiencies in (WUE) is the target of crop yield improvement under drought stress. Field Crops Research 112, 119–123. breeding (Varshney et al., 2018). It also addresses increase in Blum A. 2013. The Interdrought conference in perspective. Journal of profitability of farming and availability of affordable notori- Experimental Botany 64, 5773–5774. ous food with enhanced genetic gains in terms of not only Blum A. 2016. Stress, strain, signaling, and adaptation–not just a matter productivity but also nutritional and market traits. of definition. Journal of Experimental Botany 67, 562–565. Blum A. 2017. Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant, Cell & Environment 40, 4–10. Conclusion Blum A, Mayer J, Gozlan G. 1982. Infrared thermal sensing of plant canopies as a screening technique for dehydration avoidance in wheat. The range of topics covered in this special issue should help Field Crops Research 5, 137–146. in the integration of disciplines needed to support crop Blum A, Tuberosa R. 2018. Dehydration survival of crop plants and its measurement. Journal of Experimental Botany 69, 975–981. improvement and the design of novel cropping systems Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 Special Issue Editorial | 3179 Borrás L, Vitantonio-Mazzini LN. 2018. Maize reproductive Sun FB, Roderick ML, Farquhar GD. 2012. Changes in the variability of development and kernel set under limited plant growth environments. global land precipitation. Geophysical Research Letters 39, L19402. Journal of Experimental Botany 69, 3235–3243. Tardieu F, Simonneau T, Muller B. 2018. The physiological basis of Boyer JS, McLaughlin JE. 2007. Functional reversion to identify drought tolerance in crop plants: a scenario-dependent probabilistic controlling genes in multigenic responses: analysis of floral abortion. approach. Annual Review of Plant Biology 69, 733–759. Journal of Experimental Botany 58, 267–277. Tardieu F, Varshney RK, Tuberosa R. 2017. Improving crop Chenu K, Oosterom VJE, Mclean G, et al. 2018. Integrating modelling performance under drought - cross-fertilization of disciplines. Journal of and phenotyping approaches to identify and screen complex traits – Experimental Botany 68, 1393–1398. transpiration efficiency in cereals. Journal of Experimental Botany 69, Tricker PJ, ElHabti A, Schmidt J, Fleury D. 2018. The physiological 3181–3194. and genetic basis of combined drought and heat tolerance in wheat. Ewert F, Rotter RP, Bindi M, et al. 2015. Crop modelling for integrated Journal of Experimental Botany 69, 3195–3210. assessment of risk to food production from climate change. Environmental Tuberosa R, Turner NC, Cakir M. 2014. Two decades of InterDrought Modelling & Software 72, 287–303. conferences: are we bridging the genotype-to-phenotype gap? Journal of Harrison MT, Tardieu F, Dong Z, Messina CD, Hammer GL. 2014. Experimental Botany 65, 6137–6139. Characterizing drought stress and trait influence on maize yield Turc O, Tardieu F. 2018. Drought affects abortion of reproductive organs under current and future conditions. Global Change Biology 20, by exacerbating developmentally driven processes via expansive growth 867–878. and hydraulics. Journal of Experimental Botany 69, 3245–3254. Hsiao TC. 1973. Plant responses to water stress. Annual Review of Plant Turner NC. 2018. Turgor maintenance by osmotic adjustment – 40 years Physiology 24, 519–570. of progress. Journal of Experimental Botany 69, 3223–3233. Huang X, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM. Varshney RK, Gaur PM, Chamarthi SK, Krishnamurthy L, Tripathi S, 2014. Rhizosphere interactions: root exudates, microbes, and microbial Kashiwagi J, Samineni S, Singh VK, Thudi M, Jaganathan D. 2016. communities. Botany 92, 267–275. Fast-track introgression of “QTL-hotspot” for root traits and other drought Lynch J. 2018. Rightsizing root phenotypes for drought resistance. tolerance traits in JG 11, an elite and leading variety of chickpea (Cicer Journal of Experimental Botany 69, 3279–3292. arietinum L.). The Plant Genome 6, 1–9. Mickelbart MV, Hasegawa PM, Bailey-Serres J. 2015. Genetic Varshney RK, Graner A, Sorrells ME. 2005. Genomics-assisted mechanisms of abiotic stress tolerance that translate to crop yield stability. breeding for crop improvement. Trends in Plant Science 10, 621–630. Nature Reviews. Genetics 16, 237–251. Varshney RK, Thudi M, Nayak SN, et al. 2014. Genetic dissection of Mir RR, Zaman-Allah M, Sreenivasulu N, Trethowan R, Varshney drought tolerance in chickpea (Cicer arietinum L.). Theoretical and Applied RK. 2012. Integrated genomics, physiology and breeding approaches for Genetics. 127, 445–462. improving drought tolerance in crops. Theoretical and Applied Genetics. Varshney RK, Thudi M, Pande MK, et al. 2018. Accelerating genetic 125, 625–645. gains in legumes for the development of prosperous smallholder Olesen JE, Trnka M, Kersebaum KC, Skjelvag AO, Seguin B, agriculture: integrating genomics, phenotyping, systems modelling and Peltonen-Sainio P, Rossi F, Kozyra J, Micale F. 2011. Impacts and agronomy. Journal of Experimental Botany 69, 3293–3312. adaptation of European crop production systems to climate change. Whish J, Butler G, Castor M, Cawthray S, Broad I, Carberry P, European Journal of Agronomy 34, 96–112. Hammer G, McLean G, Routley R, Yeates S. 2005. Modelling the Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS. 2010. Sugar input, effects of row configuration on sorghum yield reliability in north-eastern metabolism, and signaling mediated by invertase: roles in development, Australia. Australian Journal of Agricultural Research 56, 11–23. yield potential, and response to drought and heat. Molecular Plant 3, Ye H, Roorkiwal M, Valliyodan B, Zhou L, Chen P, Varshney RK, Nguyen 942–955. H. 2018. Genetic diversity of root system architecture in response to drought Salvi S, Tuberosa R. 2015. The crop QTLome comes of age. Current stress in grain legumes. Journal of Experimental Botany 69, 3267–3277. Opinion in Biotechnology 32, 179–185. Zhang Q, Bartels D. 2018. Molecular responses to dehydration Sheffield J, Wood EF, Roderick ML. 2012. Little change in global and desiccation in desiccation-tolerant angiosperm plants. Journal of drought over the past 60 years. Nature 491, 435–438. Experimental Botany 69, 3211–3222. 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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Abstract

Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 Journal of Experimental Botany, Vol. 69, No. 13 pp. 3175–3179, 2018 doi:10.1093/jxb/ery187 eXtra Botany Special Issue Editorial Varshney et al. Progress in understanding drought tolerance: from alleles to cropping systems Improving crop yields under rainfed environments is related to acclimation to drought scenarios. Several loci and key to meeting the food security demands of an ever- genes have been characterized to develop the concept and Received 14 May 2018; Editorial decision ; Accepted 14 May 2018 increasing population, but climate change-associated models of complex drought tolerance traits (Tricker et  al., expansion of drought-affected arable land means that 2018). This paves the way to mapping and cloning of gen- resilient crops and agronomic practices are critical. etic loci governing drought tolerance through turgor manage- High-throughput plant phenomics and modern genetic ment and hormonal regulation, plant architecture and seed approaches must be directed towards precise under- development biology, corroborated by transcriptional and standing of factors controlling crop yield. This spe- post-transcriptional response networks. Drought tolerance cial issue covers root dynamics, turgor management involves cell-to-cell to whole-plant level hydraulic or meta- under desiccation, molecular responses to dehydra- bolic readjustment, and hormone signalling able to control tion, impact of drought on plant development and seed growth under water deficit. Now, researchers are able to abortion, and adjustment of traits to the most frequent debate the interactions between roots, shoots, the rhizosphere patterns of drought. It also addresses interdisciplin- and reproductive traits and how they collectively affect crop ary views for enhancing genetic gains and achieving a yield under the diversity of climatic scenarios involving more sustainable climate-resilient agronomy. limited water availability (Tardieu et al., 2018). Today there is also a recognition of the diversity of drought scenarios in each region of the world in current and future cli- Drought is a devastating factor for global agronomic produc- mates, even in a single field over different years, and the import- tion. Although it is uncertain whether episodes of drought ance of fitting plant phenology and traits to the most likely will be more severe with climate change (Sheffield et al., 2012), scenarios in a given region (Olesen et al., 2011; Mickelbart et al., their prevalence and year-to-year variability are major fea- 2015; Chenu et al., 2018). This raises the necessity of adopting tures in future modelling scenarios (Sun et al., 2012; Harrison probabilistic approaches to drought tolerance based on both et al., 2014; see also Box 1). Understanding the mechanisms crop modelling and genomic prediction in identifying where underpinning plant behaviour under drought is a challenge and when any combination of alleles or traits are beneficial in due to differences in (i) the traits that control plant water sta- specific drought scenarios (Ewert et  al., 2015; Tardieu et  al., tus under rapidly changing soil water availability and evap- 2018). Furthermore, the importance attached to modelling orative demand, (ii) the response of plants to changes in approaches has increased, together with an improved ability of water status, its genetic variability and differences between the scientific community to more-accurately measure and fore- species (e.g. between cereals and legumes), and (iii) interac- cast environmental conditions, and to simulate the behaviour of tions with other factors such as the duration and position of genotypes in a range of environmental conditions (Chenu et al., the crop cycle in the season, the frequency of episodes with 2018), including those associated with climate change. high temperature and the soil chemical composition (e.g. soil salinity or presence of Al). Over past decades, crop physiologists have increasingly focused on molecular aspects of stress tolerance while intensive Physiological and molecular basis of research and breeding have allowed the selection of climate- drought tolerance in plants resilient cultivars with improved yields. Drought research has progressed rapidly, as can be seen in successive InterDrought Standard terminology is now accepted for plant water status, conferences (Belhassen, 1997; Araus et al., 2007; Blum, 2013; following Hsiao (1973), who defined ‘hydrated’, ‘mild stress’, Tuberosa et al., 2014; see also Tardieu et al., 2017) (see also ‘moderate stress’, ‘severe stress’ and ‘desiccation’ based on Box 2, a tribute to Abraham Blum). While initially focused the timing and severity of water deficit. In this issue, Zhang on identifying tolerant lines and understanding the role of and Bartels (2018) distinguish dehydration and desiccation proxy traits, research has now reached a position where it can tolerances, an essential distinction for phenotyping and inter- also uncover and allow the manipulation of genes/QTLs and preting survival and recovery (Blum and Tuberosa, 2018). mechanisms involved in cellular and whole-plant responses These processes are achieved through multiple interactions © 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. Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 3176 | Special Issue Editorial 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 geno- types 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. involving stomatal conductance, carotenoid degradation Failure of fertilization and arrested ovary growth can cause and anthocyanin accumulation along with ABA and cytoki- ovary/grain abortion, often considered to be a consequence of nin accumulation, the intervention of osmoprotectants (e.g. the availability of sucrose to ovaries (Boyer and McLaughlin, sucrose, glycine, proline) and ROS-scavenging enzymes. 2007; Ruan et al., 2010). Here, Turc and Tardieu (2018) pro- Turner (2018) presents 40 years of research on the beneficial pose another view, that abortion under progressive water defi- role of osmotic adjustment on turgor maintenance in drought- cit is essentially due to developmental processes as affected by prone environments. The genetic variations and breeding of water deficit. This is the case in maize, pea and sunflower, with turgor maintenance for crops resilience to water-limited envi- a cessation of growth of the youngest reproductive organs that ronments is discussed, including examples of drought-tolerant occurs earlier under water deficit than in well-watered condi- wheat genotypes that control osmoregulation in both leaves tions, due to the effect of drought on the respective timing of and pollen through the expression of the OR gene. the development of ovary cohorts and the signalling between A crop canopy is formed of individual plants which, oldest and youngest reproductive organs. although they share a common genome, have markedly differ- Drought and heat episodes are often synchronous so a com- ent features. Borrás and Vitantonio-Mazzini (2018) analyse the bined tolerance is essential, although the genetic architectures role of plant-to-plant variability for plant development and ear of tolerances to drought and high temperatures differ appreci- growth, in particular via measured genetic progress over past ably (Tricker et al., 2018). After reviewing traits with compara- decades. This progress is in part determined by (i) the ability of tive advantages, these authors conclude that the maintenance plants to produce high individual yield at high densities while of plant water status is essential for tolerance to both stresses, maintaining sufficient uniformity between plants and (ii) the via fine tuning of gas exchange and plant hydraulic conduct- rate of silk extrusion for a given ear or plant biomass. ance, including the adaptive response of root systems, together Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 Special Issue Editorial | 3177 Box 2. A tribute to Abraham Blum (1934-2018) Abraham Blum passed away on 10 March 2018. During his career, he published two influ- ential 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 com- monly 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 re- serve 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. with more classically described traits such as cell protection at et  al. (2018) present the root architectural and anatomical high temperatures. This involves improving several plant plas- traits, together with rhizosphere traits, that affect plant water ticity traits at a time, a difficult task that can be envisaged by uptake. The hydraulic continuity of the rhizosphere is studied combining phenomics, quantitative genetics, QTL cloning and using a physical approach, and its consequences on the growth, genome editing (Salvi and Tuberosa, 2015). transpiration and yield of the crop canopy are discussed. The traits and QTLs associated with root-system archi- tecture can have markedly different effects depending on Root system traits environmental scenarios (Varshney et  al., 2014). A  view on Plant roots release a broad variety of chemical compounds to root system architecture in response to water deficit in leg- attract useful microorganisms in the rhizosphere which in turn umes is presented by Ye et al. (2018). It brings together gen- influence plant health and growth (Huang et al., 2014). Ahmed etic and genomics approaches for analysing quantitative trait Downloaded from https://academic.oup.com/jxb/article/69/13/3175/5033811 by DeepDyve user on 14 July 2022 3178 | Special Issue Editorial loci (QTLs) associated with root system architecture and the allowing better yields of drought-stressed plants. We hope beneficial root traits that can accelerate the genetic improve- it will provide new inspiration and creative opportunities to ment of yield under water deficit. There are already several address the challenges posed by climate change, and antici- studies where introgression of root traits has been successful pate convergence to continue in coming years. 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 Acknowledgements by natural selection for crop ancestors that suffered multiple Guest editors would like to thank all authors who contributed their research stresses and intense competition may no longer be useful in and ideas to this special issue, and as organizers of the InterDrought V conference (Hyderabad, 2017) extend this also to speakers at that meeting. agricultural high-input agrosystems. More parsimonious root We are also grateful to our organizations and to a number of donors, espe- systems centred on water capture are desirable, via reduced cially the United States Agency for International Agricultural Development, root branching and a root anatomy that decreases the root Indian Council of Agricultural Research and ICRISAT for their special sup- port and co-organizing the conference. R. K. V. is thankful to his colleagues, carbon cost. Functional–structural models capable of stimu- especially Ms Annapurna Chitkineni for her help in organizing the confer- lating the dynamics of root–soil interactions allow the value ence and Dr K. Himabindu and Dr Rakesh Kumar for their help and assist- of these traits in different agrosystems to be evaluated. In par- ance in editing the special issue. We dedicate this special issue to the memory of Abraham Blum who ticular, parsimonious root systems are probably less useful in passed away on 10 March 2018. low-input fields characterized by multiple stress-related cues in addition to water deficit. Keywords: Abortion, crop yield, dehydration, drought tolerance, osmotic adjustment, root architecture, seed development, turgor management. Interdisciplinary approaches 1, 2 Rajeev K. Varshney, * Roberto Tuberosa, and Although the concept of converging or integrating distinct Francois Tardieu disciplines is not new in plant research, it remains challeng- ing (see Mir et al., 2012). Convergence not only concerns the 1 Center of Excellence in Genomics & Systems Biology (CEGSB), small area of intersection between different disciplines, but International Crops Research Institute for the Semi-Arid Tropics also new approaches that represent the merging and integra- (ICRISAT), Hyderabad, India tion of different technologies, disciplines and modelling. Department of Agricultural and Food Sciences, University of Chenu et  al. (2018) integrate modelling and phenomic Bologna, Italy approaches for addressing complex traits in cereals and Université de Montpellier, INRA, LEPSE, Montpellier, France* Correspondence: r.k.varshney@cgiar.org or roberto.tuberosa@ cover advances in cereal genomics using integrated approach unibo.it or francois.tardieu@inra.fr including the identification of a number of significant QTLs for transpiration efficiency (biomass produced for unit of water used) in sorghum. 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Journal of Experimental Botany – Oxford University Press

Published: Jun 6, 2018

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