Climate change challenges, plant science solutions.

Climate change is a defining challenge of the 21st century, and this decade is a critical time for action to mitigate the worst effects on human populations and ecosystems. Plant science can play an important role in developing crops with enhanced resilience to harsh conditions (e.g. heat, drought, salt stress, flooding, disease outbreaks) and engineering efficient carbon-capturing and carbon-sequestering plants. Here, we present examples of research being conducted in these areas and discuss challenges and open questions as a call to action for the plant science community.

Tools for using the International Rice Genebank to breed for climate-resilient varieties.

Traditional rice varieties have been critical for developing improved stress-tolerant rice varieties. Tools to analyze the genome sequences of traditional varieties are accelerating the identification and deployment of genes conferring climate change resilience.

The strength and pattern of natural selection on gene expression in rice.

Levels of gene expression underpin organismal phenotypes1,2, but the nature of selection that acts on gene expression and its role in adaptive evolution remain unknown1,2. Here we assayed gene expression in rice (Oryza sativa)3, and used phenotypic selection analysis to estimate the type and strength of selection on the levels of more than 15,000 transcripts4,5. Variation in most transcripts appears (nearly) neutral or under very weak stabilizing selection in wet paddy conditions (with median standardized selection differentials near zero), but selection is stronger under drought conditions. Overall, more transcripts are conditionally neutral (2.83%) than are antagonistically pleiotropic6 (0.04%), and transcripts that display lower levels of expression and stochastic noise7-9 and higher levels of plasticity9 are under stronger selection. Selection strength was further weakly negatively associated with levels of cis-regulation and network connectivity9. Our multivariate analysis suggests that selection acts on the expression of photosynthesis genes4,5, but that the efficacy of selection is genetically constrained under drought conditions10. Drought selected for earlier flowering11,12 and a higher expression of OsMADS18 (Os07g0605200), which encodes a MADS-box transcription factor and is a known regulator of early flowering13-marking this gene as a drought-escape gene11,12. The ability to estimate selection strengths provides insights into how selection can shape molecular traits at the core of gene action.

Evolutionary systems biology reveals patterns of rice adaptation to drought-prone agro-ecosystems.

Rice (Oryza sativa) was domesticated around 10,000 years ago and has developed into a staple for half of humanity. The crop evolved and is currently grown in stably wet and intermittently dry agro-ecosystems, but patterns of adaptation to differences in water availability remain poorly understood. While previous field studies have evaluated plant developmental adaptations to water deficit, adaptive variation in functional and hydraulic components, particularly in relation to gene expression, has received less attention. Here, we take an evolutionary systems biology approach to characterize adaptive drought resistance traits across roots and shoots. We find that rice harbors heritable variation in molecular, physiological, and morphological traits that is linked to higher fitness under drought. We identify modules of co-expressed genes that are associated with adaptive drought avoidance and tolerance mechanisms. These expression modules showed evidence of polygenic adaptation in rice subgroups harboring accessions that evolved in drought-prone agro-ecosystems. Fitness-linked expression patterns allowed us to identify the drought-adaptive nature of optimizing photosynthesis and interactions with arbuscular mycorrhizal fungi. Taken together, our study provides an unprecedented, integrative view of rice adaptation to water-limited field conditions.

Oryza glumaepatula: A wild relative to improve drought tolerance in cultivated rice.

Developing drought-resistant rice (Oryza sativa, L.) is essential for improving field productivity, especially in rain-fed areas affected by climate change. Wild relatives of rice are potential sources for drought-resistant traits. Therefore, we compared root growth and drought response among 22 wild Oryza species, from which Oryza glumaepatula was selected as a promising source for further exploration. A geographically diverse panel of 69 O. glumaepatula accessions was then screened for drought stress-related traits, and 6 of these accessions showed lower shoot dry weight (SDW) reduction, greater percentage of deep roots, and lower stomatal density (STO) under drought than the drought tolerant O. sativa variety, Sahbhagi dhan. Based on whole-genome resequencing of all 69 O. glumaepatula accessions and variant calling to a high-quality O. glumaepatula reference genome, we detected multiple genomic loci colocating for SDW, root dry weight at 30 to 45 cm depth, and STO in consecutive drought trials. Geo-referencing indicated that the potential drought donors originated in flood-prone locations, corroborating previous hypotheses about the coexistence of flood and drought tolerance within individual Oryza genomes. These findings present potential donor accessions, traits, and genomic loci from an AA genome wild relative of rice that, together with the recently developed reference genome, may be useful for further introgression of drought tolerance into the O. sativa backgrounds.

Integrated root phenotypes for improved rice performance under low nitrogen availability.

Greater nitrogen efficiency would substantially reduce the economic, energy and environmental costs of rice production. We hypothesized that synergistic balancing of the costs and benefits for soil exploration among root architectural phenes is beneficial under suboptimal nitrogen availability. An enhanced implementation of the functional-structural model OpenSimRoot for rice integrated with the ORYZA_v3 crop model was used to evaluate the utility of combinations of root architectural phenes, namely nodal root angle, the proportion of smaller diameter nodal roots, nodal root number; and L-type and S-type lateral branching densities, for plant growth under low nitrogen. Multiple integrated root phenotypes were identified with greater shoot biomass under low nitrogen than the reference cultivar IR64. The superiority of these phenotypes was due to synergism among root phenes rather than the expected additive effects of phene states. Representative optimal phenotypes were predicted to have up to 80% greater grain yield with low N supply in the rainfed dry direct-seeded agroecosystem over future weather conditions, compared to IR64. These phenotypes merit consideration as root ideotypes for breeding rice cultivars with improved yield under rainfed dry direct-seeded conditions with limited nitrogen availability. The importance of phene synergism for the performance of integrated phenotypes has implications for crop breeding.

Aus rice root architecture variation contributing to grain yield under drought suggests a key role of nodal root diameter class.

The aus rice variety group originated in stress-prone regions and is a promising source for the development of new stress-tolerant rice cultivars. In this study, an aus panel (~220 genotypes) was evaluated in field trials under well-watered and drought conditions and in the greenhouse (basket, herbicide and lysimeter studies) to investigate relationships between grain yield and root architecture, and to identify component root traits behind the composite trait of deep root growth. In the field trials, high and stable grain yield was positively related to high and stable deep root growth (r = 0.16), which may indicate response to within-season soil moisture fluctuations (i.e., plasticity). When dissecting component traits related to deep root growth (including angle, elongation and branching), the number of nodal roots classified as 'large-diameter' was positively related to deep root growth (r = 0.24), and showed the highest number of colocated genome-wide association study (GWAS) peaks with grain yield under drought. The role of large-diameter nodal roots in deep root growth may be related to their branching potential. Two candidate loci that colocated for yield and root traits were identified that showed distinct haplotype distributions between contrasting yield/stability groups and could be good candidates to contribute to rice improvement.

What happens at night? Physiological mechanisms related to maintaining grain yield under high night temperature in rice.

High night temperature (HNT) causes substantial yield loss in rice (Oryza sativa L.). In this study, the physiological processes related to flag leaf dark respiration (Rn) and grain filling under HNT were explored in a multi-parent advanced generation intercross population developed for heat tolerance (MAGICheat ) along with selected high temperature tolerant breeding lines developed with heat-tolerant parents. Within a subset of lines, flag leaf Rn under HNT treatment was related to lower spikelet number per panicle and thus reduced yield. HNT enhanced the nighttime reduction of non-structural carbohydrates (NSC) in stem tissue, but not in leaves, and stem nighttime NSC reduction was negatively correlated with yield. Between heading and harvest, the major difference in NSC concentration was found for starch, but not for soluble sugar. HNT weakened the relationship between NSC remobilization and harvest index at both the phenotypic and genetic level. By using genome-wide association studies, an invertase inhibitor, MADS box transcription factors and a UDP-glycosyltransferase that were identified as candidate genes orchestrating stem NSC remobilization in the control treatment were lost under HNT. With the identification of physiological and genetic components related to rice HNT response, this study offers promising prebreeding materials and trait targets to sustain yield stability under climate change.

Establishment method affects rice root plasticity in response to drought and its relationship with grain yield stability.

By responding to the variable soil environments in which they are grown, the roots of rice crops are likely to contribute to yield stability across a range of soil moistures, nutrient levels, and establishment methods. In this study, we explored different approaches to quantification of root plasticity and characterization of its relationship with yield stability. Using four different statistical approaches (plasticity index, slope, AMMI, and factor analytic) on a set of 17 genotypes including several recently-developed breeding lines targeted to dry direct-seeding, we identified only very few direct relationships between root plasticity and yield stability. However, genotypes identified as having combined yield stability and root plasticity showed higher grain yields across trials. Furthermore, root plasticity was expressed to a greater degree in puddled transplanted trials rather than under dry direct-seeding. Significant interactions between nitrogen and water resulted in contrasting relationships between nitrogen-use efficiency and biomass stability between puddled-transplanted and direct-seeded conditions. These results reflect the complex interaction between nitrogen, drought, and even different types of drought (as a result of the establishment method) on rice root growth, and suggest that although rice root plasticity may confer stable yield across a range of environments, it might be necessary to more narrowly define the targeted environments to which it will be most beneficial.

Rice breeding for yield under drought has selected for longer flag leaves and lower stomatal density.

Direct selection for yield under drought has resulted in the release of a number of drought-tolerant rice varieties across Asia. In this study, we characterized the physiological traits that have been affected by this strategy in breeding trials across sites in Bangladesh, India, and Nepal. Drought- breeding lines and drought-tolerant varieties showed consistently longer flag leaves and lower stomatal density than our drought-susceptible check variety, IR64. The influence of environmental parameters other than drought treatments on leaf traits was evidenced by close grouping of treatments within a site. Flag-leaf length and width appeared to be regulated by different environmental parameters. In separate trials in the Philippines, the same breeding lines studied in South Asia showed that canopy temperature under drought and harvest index across treatments were most correlated with grain yield. Both atmospheric and soil stress strengthened the relationships between leaf traits and yield. The stable expression of leaf traits among genotypes and the identification of the environmental conditions in which they contribute to yield, as well as the observation that some breeding lines showed longer time to flowering and higher canopy temperature than IR64, suggest that selection for additional physiological traits may result in further improvements of this breeding pool.

Genetic gain for rice yield in rainfed environments in India.

The complexity of genotype × environment interactions under drought reduces heritability, which determines the effectiveness of selection for drought tolerance and development of drought tolerant varieties. Genetic progress measured through changes in yield performance over time is important in determining the efficiency of breeding programmes in which test cultivars are replaced each year on the assumption that the new cultivars will surpass the older cultivars. The goal of our study was to determine the annual rate of genetic gain for rice grain yield in a drought-prone rainfed system in a series of multi-environment trials conducted from 2005 to 2014 under the Drought Breeding Network of Indian sites in collaboration with the International Rice Research Institute (IRRI). Our results show a positive trend in grain yield with an annual genetic yield increase of about 0.68 % under irrigated control, 0.87 % under moderate reproductive stage drought stress and 1.9 % under severe reproductive stage drought stress due to breeding efforts. The study also demonstrates the effectiveness of direct selection for grain yield under both irrigated control as well as managed drought stress screening to improve yield in typical rainfed systems. IRRI's drought breeding programme has exhibited a significant positive trend in genetic gain for grain yield over the years under both drought stress as well as favorable irrigated control conditions. Several drought tolerant varieties released from the programme have outperformed the currently grown varieties under varied conditions in the rainfed environments on farmers' fields.

Rice yield formation under high day and night temperatures-A prerequisite to ensure future food security.

Increasing temperatures resulting from climate change dramatically impact rice crop production in Asia. Depending on the specific stage of rice development, heat stress reduces tiller/panicle number, decreases grain number per plant and lower grain weight, thus negatively impacting yield formation. Hence improving rice crop tolerance to heat stress in terms of sustaining yield stability under high day temperature (HDT), high night temperature (HNT), or combined high day and night temperature (HDNT) will bolster future food security. In this review article, we highlight the phenological alterations caused by heat and the underlying molecular-physiological and genetic mechanisms operating under different types of heat conditions (HDT, HNT, and HDNT) to understand heat tolerance. Based on our synthesis of HDT, HNT, and HDNT effects on rice yield components, we outline future breeding strategies to contribute to sustained food security under climate change.

A balancing act: how plants integrate nitrogen and water signals.

Nitrogen (N) and water (W) are crucial inputs for plant survival as well as costly resources for agriculture. Given their importance, the molecular mechanisms that plants rely on to signal changes in either N or W status have been under intense scrutiny. However, how plants sense and respond to the combination of N and W signals at the molecular level has received scant attention. The purpose of this review is to shed light on what is currently known about how plant responses to N are impacted by W status. We review classic studies which detail how N and W combinations have both synergistic and antagonistic effects on key plant traits, such as root architecture and stomatal aperture. Recent molecular studies of N and W interactions show that mutations in genes involved in N metabolism affect drought responses, and vice versa. Specifically, perturbing key N signaling genes may lead to changes in drought-responsive gene expression programs, which is supported by a meta-analysis we conduct on available transcriptomic data. Additionally, we cite studies that show how combinatorial transcriptional responses to N and W status might drive crop phenotypes. Through these insights, we suggest research strategies that could help to develop crops adapted to marginal soils depleted in both N and W, an important task in the face of climate change.

Leaf morphology, rather than plant water status, underlies genetic variation of rice leaf rolling under drought.

Soil drying causes leaf rolling in rice, but the relationship between leaf rolling and drought tolerance has historically confounded selection of drought-tolerant genotypes. In this study on tropical japonica and aus diversity panels (170-220 genotypes), the degree of leaf rolling under drought was more affected by leaf morphology than by stomatal conductance, leaf water status, or maintenance of shoot biomass and grain yield. A range of canopy temperature and leaf rolling (measured as change in normalized difference vegetation index [ΔNDVI]) combinations were observed among aus genotypes, indicating that some genotypes continued transpiration while rolled. Association mapping indicated colocation of genomic regions for leaf rolling score and ΔNDVI under drought with previously reported leaf rolling genes and gene networks related to leaf anatomy. The relatively subtle variation across these large diversity panels may explain the lack of agreement of this study with earlier reports that used small numbers of genotypes that were highly divergent in hydraulic traits driving leaf rolling differences. This study highlights the large range of physiological responses to drought among rice genotypes and emphasizes that drought response processes should be understood in detail before incorporating them into a varietal selection programme.

Yield stability of selected rice breeding lines and donors across conditions of mild to moderately severe drought stress.

Although mild to moderately severe drought stress may have less of an effect on rice grain yield than severe drought stress during reproductive stage, its prevalence across rice farmers' fields at the global level may be more economically significant. In this study, field experiments were conducted on selected genotypes with known tolerance to severe reproductive-stage drought in order to identify those that would produce high and stable grain yield across seasons and soil moisture conditions varying from well-watered to mild and moderately severe drought stress. Mild stress generally occurred during wet seasons and moderate stress happened during dry seasons. The drought stress was mild enough such that the time to flowering was similar under drought stress and well-watered conditions in either season. However, significant grain yield reductions were incurred even at mild drought levels. Using an AMMI1 biplot analysis, IR83142-B-7-B-B, Binuhangin, IR77298-14-1-2-13, IR70215-70-CPA-3-4-1-3 and IR77298-14-1-2 were identified as the genotypes with the highest and most stable grain yields in both well-watered and mild to moderately severe drought stress environments. In a characterization of traits conferring drought tolerance among the highest yielding genotypes under mild to moderate drought stress, genotypes Binuhangin and IR70215-70-CPA-3-4-1-3 stood out for multiple physiological traits under drought. However, no direct correlations among genotypes between stomatal conductance, normalized difference vegetation index (NDVI) or root dry weight with grain or total dry matter yield were observed under any soil moisture level. These results reflect the complex interaction of drought response traits contributing to grain yield. The genotypic variation and physiological responses observed in this study point to the potential of developing varieties targeted to mild and moderate drought stress using yield as the selection criterion.

Rice Root Architectural Plasticity Traits and Genetic Regions for Adaptability to Variable Cultivation and Stress Conditions.

Future rice (Oryza sativa) crops will likely experience a range of growth conditions, and root architectural plasticity will be an important characteristic to confer adaptability across variable environments. In this study, the relationship between root architectural plasticity and adaptability (i.e. yield stability) was evaluated in two traditional × improved rice populations (Aus 276 × MTU1010 and Kali Aus × MTU1010). Forty contrasting genotypes were grown in direct-seeded upland and transplanted lowland conditions with drought and drought + rewatered stress treatments in lysimeter and field studies and a low-phosphorus stress treatment in a Rhizoscope study. Relationships among root architectural plasticity for root dry weight, root length density, and percentage lateral roots with yield stability were identified. Selected genotypes that showed high yield stability also showed a high degree of root plasticity in response to both drought and low phosphorus. The two populations varied in the soil depth effect on root architectural plasticity traits, none of which resulted in reduced grain yield. Root architectural plasticity traits were related to 13 (Aus 276 population) and 21 (Kali Aus population) genetic loci, which were contributed by both the traditional donor parents and MTU1010. Three genomic loci were identified as hot spots with multiple root architectural plasticity traits in both populations, and one locus for both root architectural plasticity and grain yield was detected. These results suggest an important role of root architectural plasticity across future rice crop conditions and provide a starting point for marker-assisted selection for plasticity.

Root aquaporins contribute to whole plant water fluxes under drought stress in rice (Oryza sativa L.).

Aquaporin activity and root anatomy may affect root hydraulic properties under drought stress. To better understand the function of aquaporins in rice root water fluxes under drought, we studied the root hydraulic conductivity (Lpr) and root sap exudation rate (Sr) in the presence or absence of an aquaporin inhibitor (azide) under well-watered conditions and following drought stress in six diverse rice varieties. Varieties varied in Lpr and Sr under both conditions. The contribution of aquaporins to Lpr was generally high (up to 79% under well-watered conditions and 85% under drought stress) and differentially regulated under drought. Aquaporin contribution to Sr increased in most varieties after drought, suggesting a crucial role for aquaporins in osmotic water fluxes during drought and recovery. Furthermore, root plasma membrane aquaporin (PIP) expression and root anatomical properties were correlated with hydraulic traits. Three chromosome regions highly correlated with hydraulic traits of the OryzaSNP panel were identified, but did not co-locate with known aquaporins. These results therefore highlight the importance of aquaporins in the rice root radial water pathway, but emphasize the complex range of additional mechanisms related to root water fluxes and drought response.

Environmental and physiological effects on grouping of drought-tolerant and susceptible rice varieties related to rice (Oryza sativa) root hydraulics under drought.

Background and Aims Root hydraulic limitations (i.e. intra-plant restrictions to water movement) may be related to crop performance under drought, and groupings in the hydraulic function of drought-tolerant and drought-susceptible rice (Oryza sativa) varieties have been previously reported. This study aimed to better understand the environmental and physiological relationships with rice root hydraulics under drought. Methods Xylem sap bleeding rates in the field (gsap g-1shoot) were measured on seasonal and diurnal time frames, during which time environmental conditions were monitored and physiological measurements were conducted. Complementary experiments on the effects of vapour pressure deficit (VPD) on root hydraulic conductivity and on transpiration rates of de-rooted tillers were conducted in growth chambers. Key Results The diurnal effects on bleeding rate were more closely related to irradiance than VPD, and VPD effects on root hydraulic conductivity measured on 21-day-old plants were due to effects on plant growth including root surface area, maximum root depth and root:shoot ratio. Leaf osmotic potential was related to the grouping of drought-tolerant and drought-susceptible varieties in rice root hydraulics, and these groupings were independent of differences in phenology. Low single-tiller bleeding rates were observed under high evapo-transpirational demand, higher bleeding rates were observed at more negative leaf osmotic potentials in drought-susceptible varieties, and drought-tolerant and susceptible varieties differed in the VPD-induced increase in transpiration rates of de-rooted tillers. Low root suberin amounts in some of the drought-susceptible varieties may have resulted in higher ion transport, as evidenced by higher sap K+ concentration and higher bleeding rates in those varieties. Conclusions These results provide evidence of the environmental effects on shoots that can influence root hydraulics. The consistent groupings of drought-tolerant and susceptible varieties suggest that traits affecting plant osmotic status may regulate root hydraulic response to drought in rice.

Traits and QTLs for development of dry direct-seeded rainfed rice varieties.

The development of rice varieties for dry direct-seeded conditions can be accelerated by selecting suitable traits. In the present investigation, traits hypothesized to be important for direct-seeded conditions in rainfed systems, including seedling emergence, early vegetative vigour, nutrient uptake, nodal root number, and root hair length and density, were characterized to study the genetic control of these traits and their relationship with grain yield under seedling- and reproductive-stage drought stress. Two BC2F4 mapping populations derived from crosses of Aus276, a drought-tolerant aus variety, with MTU1010 and IR64, high-yielding indica mega-varieties, were developed and studied to identify quantitative trait loci (QTLs) that showed large and consistent effects. A total of 26 QTLs associated with 23 traits and 20 QTLs associated with 13 traits were mapped in the Aus276/3*IR64 and Aus276/3*MTU1010 populations, respectively. qGY6.1, qGY10.1, qGY1.1, and qEVV9.1 were found to be effective in both populations under a wide range of conditions. QTLs for several seedling-stage traits co-located with QTLs for grain yield, including early vegetative vigour and root hair length. On chromosome 5, several QTLs for nutrient uptake co-located with QTLs for root hair density and nematode gall rating. Six lines were selected from both populations based on grain yield and the presence of QTLs, and these lines typically showed improved seedling-stage traits (nodal root number, dry shoot weight, and root hair length and density). The co-located QTLs identified here can be used in research aimed at increasing the yield and adaptability of rainfed rice to direct-seeded conditions.