Summary Heat waves occurring during droughts can have a devastating impact on yield, especially if they happen during the flowering and seed set stages of the crop cycle. Global warming and climate change are driving an alarming increase in the frequency and intensity of combined drought and heat stress episodes, critically threatening global food security.Because high temperature is detrimental to reproductive processes, essential for plant yield, we measured the inner temperature, transpiration, sepal stomatal aperture, hormone concentrations and transcriptomic response of closed soybean flowers developing on plants subjected to a combination of drought and heat stress.Here, we report that, during a combination of drought and heat stress, soybean plants prioritize transpiration through flowers over transpiration through leaves by opening their flower stomata, while keeping their leaf stomata closed. This acclimation strategy, termed ‘differential transpiration’, lowers flower inner temperature by about 2–3°C, protecting reproductive processes at the expense of vegetative tissues.Manipulating stomatal regulation, stomatal size and/or stomatal density of flowers could serve as a viable strategy to enhance the yield of different crops and mitigate some of the current and future impacts of global warming and climate change on agriculture. 
                        more » 
                        « less   
                    
                            
                            Differential transpiration between pods and leaves during stress combination in soybean
                        
                    
    
            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. 
        more » 
        « less   
        
    
                            - Award ID(s):
- 2110017
- PAR ID:
- 10405851
- Date Published:
- Journal Name:
- Plant Physiology
- ISSN:
- 0032-0889
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
- 
            
- 
            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.more » « less
- 
            SUMMARY Global warming and climate change are driving an alarming increase in the frequency and intensity of extreme climate events, such as droughts, heat waves, and their combination, inflicting heavy losses to agricultural production. Recent studies revealed that the transcriptomic responses of different crops to water deficit (WD) or heat stress (HS) are very different from that to a combination of WD + HS. In addition, it was found that the effects of WD, HS, and WD + HS are significantly more devastating when these stresses occur during the reproductive growth phase of crops, compared to vegetative growth. As the molecular responses of different reproductive and vegetative tissues of plants to WD, HS, or WD + HS could be different from each other and these differences could impact many current and future attempts to enhance the resilience of crops to climate change through breeding and/or engineering, we conducted a transcriptomic analysis of different soybean (Glycine max) tissues to WD, HS, and WD + HS. Here we present a reference transcriptomic dataset that includes the response of soybean leaf, pod, anther, stigma, ovary, and sepal to WD, HS, and WD + HS conditions. Mining this dataset for the expression pattern of different stress response transcripts revealed that each tissue had a unique transcriptomic response to each of the different stress conditions. This finding is important as it suggests that enhancing the overall resilience of crops to climate change could require a coordinated approach that simultaneously alters the expression of different groups of transcripts in different tissues in a stress‐specific manner.more » « less
- 
            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’?’.more » « less
- 
            SUMMARY Global warming, climate change, and industrial pollution are altering our environment subjecting plants, microbiomes, and ecosystems to an increasing number and complexity of abiotic stress conditions, concurrently or sequentially. These conditions, termed, “multifactorial stress combination” (MFSC), can cause a significant decline in plant growth and survival. However, the impacts of MFSC on reproductive tissues and yield of major crop plants are largely unknown. We subjected soybean (Glycine max) plants to a MFSC of up to five different stresses (water deficit, salinity, low phosphate, acidity, and cadmium), in an increasing level of complexity, and conducted integrative transcriptomic‐phenotypic analysis of their reproductive and vegetative tissues. We reveal that MFSC has a negative cumulative effect on soybean yield, that each set of MFSC condition elicits a unique transcriptomic response (that is different between flowers and leaves), and that selected genes expressed in leaves or flowers of soybean are linked to the effects of MFSC on different vegetative, physiological, and/or reproductive parameters. Our study identified networks and pathways associated with reactive oxygen species, ascorbic acid and aldarate, and iron/copper signaling/metabolism as promising targets for future biotechnological efforts to augment the resilience of reproductive tissues of major crop plants to MFSC. In addition, we provide unique phenotypic and transcriptomic datasets for dissecting the mechanistic effects of MFSC on the vegetative, physiological, and reproductive processes of a crop plant.more » « less
 An official website of the United States government
An official website of the United States government 
				
			 
					 
					
 
                                    