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Differential transpiration is a newly discovered acclimation strategy of annual plants that mitigates the negative impacts of combined water deficit (WD) and heat stress (HS) on plant reproduction. Under conditions of WD + HS, transpiration of vegetative tissues is suppressed in plants such as soybean and tomato, while transpiration of reproductive tissues is not (termed ‘Differential Transpiration’; DT). This newly identified acclimation process enables the cooling of reproductive organs under conditions of WD + HS, limiting HS‐induced damage to plant reproduction. However, the thresholds at which DT remains active and effectively cools reproductive tissues, as well as the developmental stages at which it is activated in soybean, remain unknown. Here, we report that DT occurs at most nodes (leaf developmental stages) of soybean plants subjected to WD + HS, and that it can function under extreme conditions of WD + HS (i.e.,18% of field water capacity and 42°C combined). Our findings reveal that DT is an effective acclimation strategy that protects reproductive processes from extreme conditions of WD + HS at almost all developmental stages. In addition, our findings suggest that, under field conditions, DT could also be active in plants subjected to low or mild levels of WD during a heat wave. 

An increase in the frequency and intensity of heat waves, floods, droughts and other environmental stresses, resulting from climate change, is threatening agricultural food production worldwide. Heat waves are especially problematic to grain yields, as the reproductive processes of almost all our main grain crops are highly sensitive to heat. At times, heat waves can occur together with drought, high ozone levels, pathogen infection and/or waterlogging stress that suppress the overall process of plant cooling by transpiration. We recently reported that under conditions of heat and water-deficit stress combination, the stomata on sepals and pods of soybean (Glycine max) remain open, while the stomata on leaves close. This process, termed ‘differential transpiration’, enabled the cooling of reproductive organs, while leaf temperature increased owing to suppressed transpiration. In this review article, we focus on the impacts on crops of heat waves occurring in isolation and of heat waves combined with drought or waterlogging stress, address the main processes impacted in plants by these stresses and discuss ways to mitigate the negative effects of isolated heat waves and of heat waves that occur together with other stresses (i.e. stress combination), on crops, with a focus on the process of differential transpiration. This article is part of the theme issue ‘Crops under stress: can we mitigate the impacts of climate change on agriculture and launch the ‘Resilience Revolution’?’. 

Abstract The complexity of environmental factors affecting crops in the field is gradually increasing due to climate change-associated weather events, such as droughts or floods combined with heat waves, coupled with the accumulation of different environmental and agricultural pollutants. The impact of multiple stress conditions on plants was recently termed “multifactorial stress combination” (MFSC) and defined as the occurrence of 3 or more stressors that impact plants simultaneously or sequentially. We recently reported that with the increased number and complexity of different MFSC stressors, the growth and survival of Arabidopsis (Arabidopsis thaliana) seedlings declines, even if the level of each individual stress is low enough to have no significant effect on plants. However, whether MFSC would impact commercial crop cultivars is largely unknown. Here, we reveal that a MFSC of 5 different low-level abiotic stresses (salinity, heat, the herbicide paraquat, phosphorus deficiency, and the heavy metal cadmium), applied in an increasing level of complexity, has a significant negative impact on the growth and biomass of a commercial rice (Oryza sativa) cultivar and a maize (Zea mays) hybrid. Proteomics, element content, and mixOmics analyses of MFSC in rice identified proteins that correlate with the impact of MFSC on rice seedlings, and analysis of 42 different rice genotypes subjected to MFSC revealed substantial genetic variability in responses to this unique state of stress combination. Taken together, our findings reveal that the impacts of MFSC on 2 different crop species are severe and that MFSC may substantially affect agricultural productivity. 

Abstract Climate change is causing an increase in the frequency and intensity of droughts, heat waves, and their combinations, diminishing agricultural productivity and destabilizing societies worldwide. We recently reported that during a combination of water deficit (WD) and heat stress (HS), stomata on leaves of soybean (Glycine max) plants are closed, while stomata on flowers are open. This unique stomatal response was accompanied by differential transpiration (higher in flowers, while lower in leaves) that cooled flowers during a combination of WD + HS. Here, we reveal that developing pods of soybean plants subjected to a combination of WD + HS use a similar acclimation strategy of differential transpiration to reduce internal pod temperature by approximately 4 °C. We further show that enhanced expression of transcripts involved in abscisic acid degradation accompanies this response and that preventing pod transpiration by sealing stomata causes a significant increase in internal pod temperature. Using an RNA-Seq analysis of pods developing on plants subjected to WD + HS, we also show that the response of pods to WD, HS, or WD + HS is distinct from that of leaves or flowers. Interestingly, we report that although the number of flowers, pods, and seeds per plant decreases under conditions of WD + HS, the seed mass of plants subjected to WD + HS increases compared to plants subjected to HS, and the number of seeds with suppressed/aborted development is lower in WD + HS compared to HS. Taken together, our findings reveal that differential transpiration occurs in pods of soybean plants subjected to WD + HS and that this process limits heat-induced damage to seed production. 

Leaf fungal microbiomes can be fundamental drivers of host plant success, as they contain pathogens that devastate crop plants and taxa that enhance nutrient uptake, discourage herbivory, and antagonize pathogens. We measured leaf fungal diversity with amplicon sequencing across an entire growing season in a diversity panel of switchgrass ( Panicum virgatum ). We also sampled a replicated subset of genotypes across 3 additional sites to compare the importance of time, space, ecology, and genetics. We found a strong successional pattern in the microbiome shaped both by host genetics and environmental factors. Further, we used genome-wide association (GWA) mapping and RNA sequencing to show that 3 cysteine-rich receptor-like kinases (crRLKs) were linked to a genetic locus associated with microbiome structure. We confirmed GWAS results in an independent set of genotypes for both the internal transcribed spacer (ITS) and large subunit (LSU) ribosomal DNA markers. Fungal pathogens were central to microbial covariance networks, and genotypes susceptible to pathogens differed in their expression of the 3 crRLKs, suggesting that host immune genes are a principal means of controlling the entire leaf microbiome. 

Abstract Ionomics measures elemental concentrations in biological organisms and provides a snapshot of physiology under different conditions. In this study, we evaluate genetic variation of the ionome in outbred, perennial switchgrass in three environments across the species’ native range, and explore patterns of genotype-by-environment interactions. We grew 725 clonally replicated genotypes of a large full sib family from a four-way linkage mapping population, created from deeply diverged upland and lowland switchgrass ecotypes, at three common gardens. Concentrations of 18 mineral elements were determined in whole post-anthesis tillers using ion coupled plasma mass spectrometry (ICP-MS). These measurements were used to identify quantitative trait loci (QTL) with and without QTL-by-environment interactions (QTLxE) using a multi-environment QTL mapping approach. We found that element concentrations varied significantly both within and between switchgrass ecotypes, and GxE was present at both the trait and QTL level. Concentrations of 14 of the 18 elements were under some genetic control, and 77 QTL were detected for these elements. Seventy-four percent of QTL colocalized multiple elements, half of QTL exhibited significant QTLxE, and roughly equal numbers of QTL had significant differences in magnitude and sign of their effects across environments. The switchgrass ionome is under moderate genetic control and by loci with highly variable effects across environments.