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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. 

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.