Integrative phenotypic-transcriptomic analysis of soybean plants subjected to multifactorial stress combination

ABSTRACT Global warming, climate change, and industrial pollution are altering our environment subjecting crops to an increasing number and complexity of abiotic stress conditions, concurrently or sequentially. Recent studies revealed that a combination of 3 or more stresses simultaneously impacting a plant (termed ‘multifactorial stress combination’; MFSC) can cause a drastic decline in plant growth and survival, even if the level of each stress involved in the MFSC has a negligible effect on plants. However, the impacts of MFSC on crops are largely unknown. We subjected soybean 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 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 are linked to the effects of MFSC on different vegetative, physiological, and/or reproductive parameters. We further reveal that the transcriptomic response of soybean and Arabidopsis to MFSC shares common features associated with reactive oxygen and iron/copper signaling/metabolism. Our study provides unique phenotypic and transcriptomic datasets for dissecting the mechanistic effects of MFSC on the vegetative, physiological, and reproductive processes of a crop plant.