Plant-associated fungi co-opt ancient antimicrobials for host manipulation

Abstract

Evolutionary histories of effector proteins secreted by fungal pathogens to mediate plant colonization remain largely elusive. While most functionally characterized effectors modulate plant immunity, recent discoveries have revealed previously unknown functions in targeting host-associated microbiota. We now developed an antimicrobial activity predictor for effector candidates (AMAPEC) and identified a wealth of antimicrobial effectors, including many highly conserved ones—suggesting ancient evolutionary origins. Unexpectedly, several plant immunomodulatory effectors display antimicrobial activity. We propose that these evolved from ancestral antimicrobials while perhaps retaining their original functions. In addition to roles in suppressing host immunity, they may manipulate plant microbiota to promote colonization. We show that the Verticillium dahliae effector Vd424Y affects host microbiota during infection and, more recently, evolved to target plant cell nuclei to manipulate host immunity. Thus, we argue that microbial antagonism is a fundamental fungal effector function and suggest that fungi repurposed ancient antimicrobials to serve diverse roles during host-pathogen coevolution.