Overexpression of cowpea NAC transcription factors promoted growth and stress tolerance by boosting photosynthetic activity in Arabidopsis

Abstract

ATAF-like NAC transcription factors are bonafide regulators of stress-signaling. However, their overexpression often exerts growth-retardation by activating ABA-hypersensitivity, chloroplast-degradation, or carbon-starvation. To improve tolerance to multiple stress complying with growth sustainability, we examined two ATAF orthologs, VuNAC1 and VuNAC2, isolated from a drought-hardy cowpea genotype, for a harmonized regulation of stress and growth signaling. The genes were induced by dehydration, NaCl, polyethylene glycol, heat, cold, ABA, and light. Analysis of the promoter-elements and regulatory network corroborated the integration of circadian, hormonal, stress, developmental, and nutrition signals, being VuNAC1/2 the central transcriptional-switch interfacing growth and stress responses. The constitutive gene overexpression in Arabidopsis resulted in an improved embryonic, rosette, and inflorescence growth, under optimum as well as limiting nutrition, in association with increased photosynthetic activity and stomatal-density. The transgenic seedlings manifested tolerance to dehydration, salinity, aluminum, cadmium, and H2O2 toxicity, in addition to ABA-mediated seed dormancy and hypersensitivity. The soil-grown plants survived severe drought and hypersalinity by maintaining the water-status and membrane integrity through the accumulation of stress protectants, such as proline, glutathione, and ascorbate. Unlike their orthologs from other species, VuNAC1/2 conferred tolerance to multiple abiotic stresses in line with improved growth attributes via regulation of photosynthetic controls and nutritional balance, suggesting growth being a crucial component of stress-tolerance and recovery. Such unique stress-responsive transcription factors, which also confer photosynthetic gain, could be sustainable biotechnological tools for developing stress-tolerant crops and translating the improved growth into yield without unintended trade-offs.