Plants require water for growth and development, but excessive water negatively affects their productivity and viability. Flash floods occasionally result in complete submergence of plants in agricultural and natural ecosystems. When immersed in water, plants encounter multiple stresses including low oxygen, low light, nutrient deficiency, and high risk of infection. As floodwaters subside, submerged plants are abruptly exposed to higher oxygen concentration and greater light intensity, which can induce post-submergence injury caused by oxidative stress, high light, and dehydration. Recent studies have emphasized the significance of multiple stress tolerance in the survival of submergence and prompt recovery following desubmergence. A mechanistic understanding of acclimation responses to submergence at molecular and physiological levels can contribute to the deciphering of the regulatory networks governing tolerance to other environmental stresses that occur simultaneously or sequentially in the natural progress of a flood event.

Complete inundation at the early seedling stage is a common environmental constraint for soybean production throughout the world. As floodwaters subside, submerged seedlings are subsequently exposed to reoxygenation stress in the natural progression of a flood event. Here, we characterized the fundamental acclimation responses to submergence and reoxygenation in soybean at the seedling establishment stage. Approximately 90% of seedlings succumbed during 3 d of inundation under constant darkness, whereas 10 d of submergence were lethal to over 90% of seedlings under 12 h light/12 h dark cycles, indicating the significance of underwater photosynthesis in seedling survival. Submergence rapidly decreased the abundance of carbohydrate reserves and ATP in aerial tissue of seedlings although chlorophyll breakdown was not observed. The carbohydrate and ATP contents were recovered upon de-submergence, but sudden exposure to oxygen also induced lipid peroxidation, confirming that reoxygenation induced oxidative stress. Whole transcriptome analysis recognized genome-scale reconfiguration of gene expression that regulates various signalling and metabolic pathways under submergence and reoxygenation. Comparative analysis of differentially regulated genes in shoots and roots of soybean and other plants defines conserved, organspecific and species-specific adjustments which enhance adaptability to submergence and reoxygenation through different metabolic pathways.

Flooding and drought are serious constraints that reduce crop productivity worldwide. Previous studies identified genes conferring tolerance to both water extremes in various plants. However, overlapping responses to flooding and drought at the genome-scale remain obscure. Here, we defined overlapping and stress-specific transcriptomic and hormonal responses to submergence, drought and recovery from these stresses in soybean (Glycine max). We performed comparative RNA-sequencing and hormone profiling, identifying genes, hormones and biological processes that are differentially regulated in an overlapping or stress-specific manner. Overlapping responses included positive regulation of trehalose and sucrose metabolism and negative regulation of cellulose, tubulin, photosystem II and I, and chlorophyll biosynthesis, facilitating the economization of energy reserves under both submergence and drought. Additional energyconsuming pathways were restricted in a stress-specific manner. Downregulation of distinct pathways for energy saving under each stress suggests energy-consuming processes that are relatively unnecessary for each stress adaptation are turned down. Our newly developed transcriptomic-response analysis revealed that abscisic acid and ethylene responses were activated in common under both stresses, whereas stimulated auxin response was submergence-specific. The energy-saving strategy is the key overlapping mechanism that underpins adaptation to both submergence and drought in soybean. Abscisic acid and ethylene are candidate hormones that coordinate transcriptomic energy-saving processes under both stresses. Auxin may be a signaling component that distinguishes submergence-specific regulation of the stress response.

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