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Climate change and enhanced pollution levels are subjecting plants and crops to an increased number of different stressors, simultaneously or sequentially, generating conditions of multifactorial stress combination (MFSC). Although MFSC was shown to severely diminish plant growth, yield, and survival, how plants acclimate to increased levels of stress complexity is largely unknown. Here, we reveal that theArabidopsis thalianatranscriptional regulator basic helix-loop-helix 35 (bHLH35) is required for plant acclimation to a specific set of MFSC conditions that includes a combination of salinity, excess light, and heat, occurring simultaneously (but not to each of these stresses applied individually or in any other combination). Under the three-stress combination, bHLH35 interacts with no apical meristem/transcription activator factor/cup-shaped cotyledon 69 (NAC069), binds the promoter oflateral organ boundaries domain 31 (LBD31), and regulates the expression of transcripts involved in flavonoid metabolism and ethylene signaling. Our findings uncover a high degree of specificity in plant responses to stress combination, suggesting that different conditions of MFSC could require the function of specific genetic programs for acclimation. 

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. 

NEET proteins are conserved 2Fe-2S proteins that regulate the levels of iron and reactive oxygen species in plant and mammalian cells. Previous studies of seedlings with constitutive expression of AtNEET, or its dominant-negative variant H89C (impaired in 2Fe-2S cluster transfer), revealed that disrupting AtNEET function causes oxidative stress, chloroplast iron overload, activation of iron-deficiency responses, and cell death. Because disrupting AtNEET function is deleterious to plants, we developed an inducible expression system to study AtNEET function in mature plants using a time-course proteomics approach. Here, we report that the suppression of AtNEET cluster transfer function results in drastic changes in the expression of different members of the ferredoxin (Fd), Fd-thioredoxin (TRX) reductase (FTR), and TRX network of Arabidopsis, as well as in cytosolic cluster assembly proteins. In addition, the expression of Yellow Stripe-Like 6 (YSL6), involved in iron export from chloroplasts was elevated. Taken together, our findings reveal new roles for AtNEET in supporting the Fd-TFR-TRX network of plants, iron mobilization from the chloroplast, and cytosolic 2Fe-2S cluster assembly. In addition, we show that the AtNEET function is linked to the expression of glutathione peroxidases (GPXs), which play a key role in the regulation of ferroptosis and redox balance in different organisms. 

Abstract Plants can send long-distance cell-to-cell signals from a single tissue subjected to stress to the entire plant. This ability is termed “systemic signaling” and is essential for plant acclimation to stress and/or defense against pathogens. Several signaling mechanisms are associated with systemic signaling, including the reactive oxygen species (ROS) wave, calcium wave, hydraulic wave, and electric signals. The ROS wave coordinates multiple physiological, molecular, and metabolic responses among different parts of the plant and is essential for systemic acquired acclimation (SAA) to stress. In addition, it is linked with several plant hormones, including jasmonic acid (JA), salicylic acid (SA), and abscisic acid (ABA). However, how these plant hormones modulate the ROS wave and whether they are required for SAA is not clear. Here we report that SA and JA play antagonistic roles in modulating the ROS wave in Arabidopsis (Arabidopsis thaliana). While SA augments the ROS wave, JA suppresses it during responses to local wounding or high light (HL) stress treatments. We further show that ethylene and ABA are essential for regulation of the ROS wave during systemic responses to local wounding treatment. Interestingly, we found that the redox-response protein NONEXPRESSOR OF PATHOGENESIS RELATED PROTEIN 1 is required for systemic ROS accumulation in response to wounding or HL stress, as well as for SAA to HL stress. Taken together, our findings suggest that interplay between JA and SA might regulate systemic signaling and SAA during responses of plants to abiotic stress or wounding.