Host Metabolic Alterations Mediate Phyllosphere Microbes Defense upon Xanthomonas oryzae pv oryzae Infection

Abstract

Rice bacterial leaf blight, caused by Xanthomonas oryzae pv oryzae (Xoo), is a significant threat to global food security. Although the microbiome plays an important role in protecting plant health, how the phyllosphere microbiome is recruited and the underlying disease resistance mechanism remain unclear. This study investigates how rice phyllosphere microbiomes respond to pathogen invasion through a comprehensive multiomics approach, exploring the mechanisms of microbial defense and host resistance. We discovered that Xoo infection significantly reshapes the physicosphere microbial community. The bacterial network became more complex, with increased connectivity and interactions following infection. Metabolite profiling revealed that l-ornithine was a key compound to recruiting three keystone microbes, Brevundimonas (YB12), Pantoea (YN26), and Stenotrophomonas (YN10). These microbes reduced the disease index by up to 67.6%, and these microbes demonstrated distinct defense mechanisms. Brevundimonas directly antagonized Xoo by disrupting cell membrane structures, while Pantoea and Stenotrophomonas enhanced plant immune responses by significantly increasing salicylic acid and jasmonic acid levels and activating defense-related enzymes. Our findings provide novel insights into plant–microbe interactions, demonstrating how host metabolic changes recruit and activate beneficial phyllosphere microbes to combat pathogenic invasion. This research offers promising strategies for sustainable agricultural practices and disease management.