NbVQ1 physically turns off the NbWRKY45-NbCAT2 module to promote reactive oxygen species burst and disease resistance in plants under high-potassium regime.

Potassium (K) nutrition is a critical determinant of plant disease resistance, but the molecular mechanisms linking K status to defense activation remain unclear. Presently, we systematically investigated the detailed mechanisms by NbVQ1-NbWRKY45-NbCAT2 module in regulating plant immunity under different K statuses. Typically, elevating K content to high (sufficient level) status enhanced pathogen-induced immune responses, particularly reactive oxygen species burst, thereby conferring broad-spectrum resistance in Nicotiana benthamiana. Central to this process was the NbVQ1-NbWRKY45-NbCAT2 module, which functioned as a switch for pathogen-triggered reactive oxygen species burst. In low-K plants, NbWRKY45 was upregulated through a self-amplifying loop, thereby inducing NbCAT2 expression to scavenge reactive oxygen species and ultimately compromising plant disease resistance. In contrast, adding K promoted NbVQ1 expression, which proved essential for the K-enhanced plant resistance. NbVQ1 interacted with the WRKYGQK domain of NbWRKY45 through its VQ motif, thereby disrupting the binding affinity of NbWRKY45 to NbCAT2 promoter and causing NbCAT2 downregulation. This transcriptional suppression of NbCAT2 resulted in stronger reactive oxygen species bursts and improved the resistance of N. benthamiana to Botrytis cinerea and Phytophthora parasitica under high-K status. Notably, K+ could promote the interaction between NbVQ1 and NbWRKY45, directly explicating nutrient-associated immune potentiation mechanism. Moreover, this K-dependent resistance mechanism mediated by VQ1-WRKY45-CAT2 module was conserved in Arabidopsis thaliana, while suppression of NbWRKY45 also increased plant drought tolerance. Overall, this study established the VQ-WRKY-CAT module as a molecular switch for K-promoted reactive oxygen species immunity and provided mechanistic evidence for coupling K nutrition with transcriptional regulation of plant immunity.