Natural Variations in the Activity of Hydroxycinnamoyl Transferases Promote Accumulation of Metabolites Conferring Rice Resistance

Plant-derived secondary metabolites act as regulators of in planta defence. Plant phenylpropanoid metabolic compounds, including final metabolites such as lignin and flavonoids, and a few intermediate metabolites play critical roles in defence. Here, we functionally characterised two rice hydroxycinnamoyl transferases OsSHT1 and OsSHT2, which are responsible for catalysing branches of the phenylpropanoid metabolic pathway and regulating resistance to bacterial pathogens. Both OsSHT1 and OsSHT2 can use p-Coumaroyl-CoA and feruloyl-CoA as acyl donors and prefer spermidine as an acyl acceptor, as verified by in vitro biochemical assays and in vivo metabolic analysis. Knocking out OsSHT1 and OsSHT2 blocked the branching of the phenylpropanoid metabolic pathway, resulting in an accumulation of intermediate metabolites p-Coumaric acid and ferulic acid and final metabolites lignin and flavonoids. These intermediate metabolites exhibit antimicrobial activity towards phytopathogenic bacteria and final metabolites enhance rice immunity. Haplotype analysis and population genetics revealed rice accessions with lower expression levels of OsSHT1 and OsSHT2 accumulate higher concentrations of phenolic compounds and exhibit enhanced resistance. Furthermore, OsMYB30 binds directly to the promoters of OsSHT1 and OsSHT2, thereby suppressing their expression and negatively regulating rice resistance to bacterial pathogens. The OsMYB30^D239 variant is considered to be an elite haplotype due to its greater stability and stronger inhibitory effect on the expression of OsSHT1 and OsSHT2. Taken together, these findings demonstrate that there is a link between phenylpropanoid metabolism and immune responses via the OsMYB30-OsSHTs module, advancing our understanding of phenylpropanoid metabolites-mediated resistance and providing elite haplotypes for rice breeding.