Breaking dependence on melanisation imparts diversity to a dogmatic invasion strategy of phytopathogenic fungi

Abstract

Abstract Colletotrichum and Pyricularia are destructive fungal phytopathogens that typically invade plants by forming a heavily melanised, unicellular infection structure known as an appressorium, enabling melanised appressorium-mediated entry (MAE). Appressorial melanisation is essential for invasion by these phytopathogens. Here, we report Colletotrichum fungi that can invade plants via nonmelanised appressorium-mediated entry (NMAE). Multifaceted analyses revealed interspecific variation in the degree of melanisation dependence across appressorial functions. NMAE-type appressoria accomplished these functions regardless of melanisation, thus being capable of early invasion. Comprehensive screening identified a monophyletic NMAE-type Colletotrichum group with rapid expansion. Critically, we identified an eccentric NMAE-type strain with erratic appressorial melanisation. We also rediscovered appressorium-independent hyphal tip-based entry (HTE)-type strains. Collectively, these findings establish a key paradigm for the plant infection strategy of Colletotrichum fungi. In contrast to the widely accepted view based on the MAE of Colletotrichum , this study suggests that appressorial melanisation is not universally required, underscoring the need to consider the emergence of NMAE- and HTE-type pathogens.