Abstract
Abiotic and biotic stress significantly limit crop yields. However, most stress-tolerance genes identified to date provide resistance to either biotic or abiotic stress and inhibit normal plant growth, limiting their application in breeding. We identified the soybean (Glycine max) NAC transcription factor gene GmST2, which is induced by salt and Botrytis cinerea stresses. Through comprehensive analyses of transgenic GmST2-overexpressing lines, CRISPR-Cas9 mutants, and heterologous expression systems in Arabidopsis thaliana and Nicotiana tabacum, we demonstrate that GmST2 confers dual resistance to salinity stress and B. cinerea while simultaneously enhancing plant growth under non-stressed conditions. RNA-seq revealed the enrichment of genes in the jasmonic acid (JA) pathway in GmST2-overexpressing soybean. GmST2 directly binds to the promoters of GmAOC3 and GmAOC4, encoding key enzymes involved in JA biosynthesis, to promote their transcription, thereby enhancing JA accumulation and salt tolerance. Furthermore, we identified GmPRL1b, a WD40-repeat protein, as a nuclear interactor that promotes GmST2 protein accumulation and functions upstream of GmST2 in regulating JA pathway genes. The elucidated GmPRL1b-GmST2-GmAOC3/4 regulatory module coordinates JA-mediated cross-protection against concurrent abiotic and biotic stresses. Evolutionary analysis indicates that GmST2 has undergone selection during soybean domestication, with the identified elite haplotype exhibiting enhanced salt tolerance. Our findings provide a molecular framework for developing stress-resilient soybean cultivars, effectively addressing the trade-off between stress resistance and plant productivity.