Temporally Programmed Virulence Cascade Drives Progressive Maize Root Rot by Fusarium graminearum

Abstract

Fusarium graminearum threatens grain safety through trichothecene mycotoxins, yet how it temporally orchestrates virulence during early root colonization—which compromises seedling vigor and facilitates stem invasion—remains unclear. We performed high-resolution transcriptomics of F. graminearum infecting maize roots every 6 h over 48 hpi, revealing three infection phases: Penetration Initiation (0–6 hpi), Colonization Establishment (12 hpi), and Systemic Disruption (18–48 hpi). Among 6,839 fungal genes, we delineated a three-phase virulence program: rapid activation of protein synthesis enables early secretion of effectors and hydrolases that facilitate host attachment and penetration; sustained deployment of diverse hydrolases and immunosuppressive effectors enables colonization through combined nutrient acquisition and defense suppression; and late-phase vascular degradation coupled with deoxynivalenol (DON) biosynthesis may contribute to systemic host disruption by compromising tissue integrity and disarming immunity. This program coincides with a shift from ROS scavenging to endogenous signaling that may promote toxin production and invasive growth. Notably, we identified FgCPA1, a conserved Phase II carboxypeptidase A essential for root colonization, whose protease domain triggers light-independent cell death in N. benthamiana independent of its signal peptide. This temporal framework uncovers phase-specific coordination of tissue invasion and mycotoxin production, providing actionable targets for anti-virulence strategies to safeguard grain quality.