Comparative multi-omic analyses reveal gene regulatory networks controlling physiological and metabolic responses to drought in upland cotton

Abstract

AbstractDrought stress substantially impacts crop physiology resulting in alteration of growth and productivity. Although many drought-responsive genes have been identified, and to a lesser extent functionally characterized, how these genes link drought stress to critical stress-responsive crop traits is still unclear. In this study, the transcriptomes of 22 genetically diverse upland cotton accessions grown under well-watered and water-limited conditions in the Arizona low desert were sequenced. Six cotton fiber-related traits, four reflectance-based vegetation indices, and the levels of 451 metabolites were collected to estimate the physiological response of the accessions to stress. After data processing, a SNP-based phylogeny clearly clustered 21 accessions to three subgroups (Foreign, U.S., and Mixed), but the analysis of transcriptome profiles and physiological responses to drought highlighted differences incongruent with the accession’s phylogenetic relatedness. Co-expression network analysis revealed that genes highly correlated to fiber yield, reflectance-based vegetation indices, and carbohydrate levels were also correlated with drought-responsive transcription factors (TFs). Based on integrated information from TF-binding sites enrichment tests and published functional studies, DREB2A was identified as a potential hub regulator that cooperatively works with HSFA6B to target a network of genes associated with improved fiber yield. Additional TFs, including bZIP53 and four ERFs, were identified as stress response regulators linking carbon metabolism, in particular sucrose and trehalose-6-phosphate, with nutrient cycling under drought stress. Thus, despite the close phylogenetic relationships between these accessions, some stand out as having developed distinct regulatory networks connecting drought stress and production-related responses. Understanding and modulating these pathways represent high value targets for improving cotton production under reduced water conditions.