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Abstract Multifactorial stress combination (MFSC) is emerging as a major constraint to crop productivity under different climate change scenarios. While the physiological impacts of MFSC have been previously characterized in different plant species, the molecular and metabolic effects of MFSC remain poorly defined. Here, we used an integrative multi-omics approach to dissect the response of tomato (Solanum lycopersicum) plants to an MFSC of up to 6 low-intensity abiotic stressors. Our analysis uncovered a complexity-dependent molecular program in tomato. Transcriptomic analysis identified a core set of 194 transcripts commonly altered across all stress conditions, along with 155 transcription factors (TFs) specifically regulated under high-complexity conditions (4-, 5-, and 6-stress combinations). Focusing on heat-associated MFSC responses, we identified 103 transcripts uniquely responsive to these conditions, including 2 TFs (Zinc finger TF 32 and a B3 family protein) that may act as master regulators of all heat-associated MFSCs. Metabolomic profiling revealed a pronounced reprogramming of primary metabolism under MFSC, marked by decreased levels of tricarboxylic acid intermediates and accumulation of sugars, γ-aminobutyric acid, and branched-chain amino acids, suggesting a trade-off that favors osmoprotection and redox homeostasis over energy-intensive processes. Comparative analyses across tomato, Arabidopsis, Chlamydomonas, rice, and soybean highlighted a conserved molecular signature associated with MFSC. Integrated omics correlation analysis uncovered functional links among phytohormone signaling, photosynthetic efficiency, and key MFSC-related transcripts and metabolic hubs. Together, we reveal a coordinated and complexity-dependent molecular program in tomato, offering insights into plant adaptation to MFSC and identifying candidate regulatory and metabolic markers for engineering climate-resilient crops. 

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 Global change factors associated with climate change and increased pollution are subjecting plants, microbes, and different ecosystems to conditions of multifactorial stress combination (MFSC). While recent studies have centered on the effects of MFSC on different plants and ecosystems, much less is known about how these conditions impact unicellular organisms. Here, we report on the physiological and proteomic responses of wild-type and respiratory burst oxidase homolog 1 (rbo1) mutant cells of Chlamydomonas reinhardtii to an MFSC of 5 different abiotic stresses. While several similarities were found between plant and C. reinhardtii responses to MFSC, our work revealed that MFSC induces aggregation in the unicellular organism C. reinhardtii. We further show that MFSC-induced aggregation is enhanced in the rbo1 mutant and can be triggered by H2O2. As aggregation typically leads to reduced growth, respiration, and photosynthesis, enhanced aggregation of unicellular organisms in different ecosystems subjected to MFSC could explain part of the negative impacts of MFSC on the services they provide. Our findings shed light on the response of unicellular organisms to MFSC and suggest that one of the main drivers leading to multicellularity during evolution was early conditions of MFSC under an oxygenated environment. 

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. 

Abstract To successfully survive, develop, grow and reproduce, multicellular organisms must coordinate their molecular, physiological, developmental and metabolic responses among their different cells and tissues. This process is mediated by cell‐to‐cell, vascular and/or volatile communication, and involves electric, chemical and/or hydraulic signals. Within this context, stomata serve a dual role by coordinating their responses to the environment with their neighbouring cells at the epidermis, but also with other stomata present on other parts of the plant. As stomata represent one of the most important conduits between the plant and its above‐ground environment, as well as directly affect photosynthesis, respiration and the hydraulic status of the plant by controlling its gas and vapour exchange with the atmosphere, coordinating the overall response of stomata within and between different leaves and tissues plays a cardinal role in plant growth, development and reproduction. Here, we discuss different examples of local and systemic stomatal coordination, the different signalling pathways that mediate them, and the importance of systemic stomatal coordination to our food supply, ecosystems and weather patterns, under our changing climate. We further discuss the potential biotechnological implications of regulating systemic stomatal responses for enhancing agricultural productivity in a warmer and CO₂‐rich environment. 

SUMMARY The complexity of environmental conditions encountered by plants in the field, or in nature, is gradually increasing due to anthropogenic activities that promote global warming, climate change, and increased levels of pollutants. While in the past it seemed sufficient to study how plants acclimate to one or even two different stresses affecting them simultaneously, the complex conditions developing on our planet necessitate a new approach of studying stress in plants: Acclimation to multiple stress conditions occurring concurrently or consecutively (termed, multifactorial stress combination [MFSC]). In an initial study of the plant response to MFSC, conducted withArabidopsis thalianaseedlings subjected to an MFSC of six different abiotic stresses, it was found that with the increase in the number and complexity of different stresses simultaneously impacting a plant, plant growth and survival declined, even if the effects of each stress involved in such MFSC on the plant was minimal or insignificant. In three recent studies, conducted with different crop plants, MFSC was found to have similar effects on a commercial rice cultivar, a maize hybrid, tomato, and soybean, causing significant reductions in growth, biomass, physiological parameters, and/or yield traits. As the environmental conditions on our planet are gradually worsening, as well as becoming more complex, addressing MFSC and its effects on agriculture and ecosystems worldwide becomes a high priority. In this review, we address the effects of MFSC on plants, crops, agriculture, and different ecosystems worldwide, and highlight potential avenues to enhance the resilience of crops to MFSC.