The TRAPPIII complex regulates development and virulence of Fusarium graminearum by coordinating autophagy and intracellular transport.

TRAnsport Protein Particle (TRAPP) is a conserved multi-subunit tethering complex known to be involved in intracellular movement of proteins. However, its components and molecular functions in filamentous fungi remain poorly characterized. Here, we identify four TRAPPIII-specific subunits (FgTrs85, TRAPPC11, TRAPPC12, and TRAPPC13) in the phytopathogenic fungus Fusarium graminearum. Genetic and functional analyses reveal that FgTrs85 serves as the core subunit, collaborating with auxiliary subunits TRAPPC11, TRAPPC12, and TRAPPC13 to orchestrate fungal perithecium formation, growth, and virulence. TRAPPIII localizes to the phagophore assembly site and promotes autophagosome biogenesis by recruiting FgAtg9 through interactions involving FgTrs85 and TRAPPC13. Notably, TRAPPIII mutants exhibit more severe growth defects than autophagy-deficient strains, suggesting that the roles of TRAPPIII extend beyond autophagy. TRAPPIII regulates ER-to-Golgi and endosome-to-Golgi transport by ensuring the proper localization of secretory regulators (FgSec22, FgRud3, FgSnc1). Moreover, the overexpression of FgRab1-GTP largely suppresses all phenotypic defects associated with perithecium formation, growth, and virulence in TRAPPIII mutants, suggesting the function of TRAPPIII as a guanine nucleotide exchange factor that activates FgRab1. Altogether, our results demonstrate that TRAPPIII coordinates autophagy and intracellular transport to regulate fungal development, growth and virulence in F. graminearum.