Phenylalanine metabolism-dependent lignification confers rhizobacterium-induced plant resistance

Abstract Phenylalanine metabolism serves as an important route for production of diverse secondary metabolites including phenylpropanoids. The phenylpropanoid pathway is involved in plant immunity, but whether it can regulate rhizobacteria-induced resistance is poorly understood. In this study, we confirmed a growth-promoting rhizobacterium strain JR48 could induce resistance, strengthen salicylic acid (SA) signaling, and increase lignin content during Phytophthora capsici infection. We conducted transcriptome sequencing to analyze the effect of JR48 on expression of pepper (Capsicum annuum L.) genes, generated transgene and loss-of-function genetic materials to specify the function of peroxidase genes, and implemented metabolomics analysis to uncover the resistance-inducing metabolites of JR48. JR48 activated expression of several pepper peroxidase genes in the phenylpropanoid pathway during pathogen infection. These peroxidases positively regulated lignification-mediated pathogen resistance, and the phenylpropanoid pathway acted downstream of SA signaling to confer JR48-induced resistance. Further, JR48 was capable of producing phenylpyruvate to enhance phenylalanine accumulation, thereby reinforcing phenylalanine metabolism-dependent lignification and resistance. Our results revealed that JR48 produces phenylpyruvate to refuel phenylalanine metabolism and reinforces SA signaling to further activate expression of peroxidase genes. This study uncovers immune components previously hidden in metabolic pathways and a recent mechanism underlying rhizobacteria-induced plant resistance.