Ectopic Expression of <i>ScALDH21</i> From a Desert Moss Enhances Cotton Resistance to Verticillium Wilt via the Modulation of Jasmonates and Phenylpropanoid Pathways

Biotic stresses, particularly Verticillium wilt (VW), lead to a global decline in cotton yields. Here, we demonstrate that ectopic expression of ScALDH21, a gene from the desiccation-tolerant moss Syntrichia caninervis Mitt. and absent in angiosperms, enhances cotton's resistance to VW. Multi-year, multiple location field evaluations showed that transgenic cotton lines consistently exhibited two major advantages: markedly improved resistance to VW, and significantly reduced yield loss, with an approximate 23.8% yield increase relative to non-transgenic counterparts under pathogen infection conditions. This disease resistance is associated with enhanced capacity of the transgenic lines to scavenge reactive oxygen species (ROS), induced by pathogen infection. This finding aligns with the ScALDH21-conferred detoxification function. Transcriptome analyses revealed a significant alteration in expression pattern of those genes that regulate phenylpropanoid and jasmonic acid (JA) pathways. Correspondingly, the accumulation of lignin and defence-related metabolites (e.g., rutin, cyanidin and jasmonates) significantly increased, suggesting that ScALDH21-mediated activation of the phenylpropanoid and JA pathways contributes to enhanced resistance. Analyses of ScALDH21 binding activity using CUT&Tag and EMSA assays showed that it can bind to specific gene promoters within the cotton genome, highlighting that ScALDH21 not only catalyses the detoxification of aldehydes but also gains transcriptional regulatory roles. In summary, we demonstrate that expression of the heterologous ScALDH21 in cotton leads to enhancement of resistance to VW and elucidated the mechanism. Our findings further demonstrate a promising strategy to improve biotic resistance in crops by utilizing unique functional genes from evolutionarily distant species in extreme environments.