An Extracellular miRNA Reshapes Cell Wall Integrity to Prime Systemic Immunity in Tomato

Plant small RNAs (sRNAs) are well established as intracellular regulators of gene expression and, more recently, as mediators of trans-kingdom RNA interference against invading pathogens. However, whether extracellular sRNAs can modulate plant immunity through host-intrinsic mechanisms remains largely unexplored. Here, using the tomato-Phytophthora capsici pathosystem, we systematically profiled apoplastic sRNAs during infection and uncovered a selective enrichment of specific sRNAs in the apoplast. Among them, miR408b was strongly induced upon pathogen invasion and preferentially accumulated extracellularly. Rather than entering pathogen cells, apoplastic miR408b functioned as a mobile immune signal, undergoing systemic movement to distal tissues. We identified SlGAUT12, encoding a galacturonosyltransferase required for homogalacturonan biosynthesis, as a direct target of miR408b and a negative regulator of tomato immunity. miR408b-mediated silencing of SlGAUT12 compromised cell wall integrity (CWI) and promoted the accumulation of immunogenic oligogalacturonides (OGs), thereby robustly activating damage-associated molecular pattern (DAMP)-triggered immunity (DTI). Together, our findings reveal an unrecognized role of apoplastic miRNAs in coordinating systemic plant immunity through cell wall remodeling and DAMP signaling, and provide new molecular targets for the development of RNA-based disease control strategies.