A fungal secondary metabolism gene cluster enables mutualist-pathogen transition in root endophyteColletotrichum tofieldiae

Abstract

Plant associated fungi show diverse lifestyles from pathogenic to mutualistic to the host; however, the principles and mechanisms through which they shift the lifestyles require elucidation. The root fungus Colletotrichum tofieldiae (Ct) promotes Arabidopsis thaliana growth under phosphate limiting conditions. We reveal a Ct strain, designated Ct3, that severely inhibits plant growth. Ct3 pathogenesis occurs through activation of host abscisic acid (ABA) pathways via a fungal secondary metabolism gene cluster related to sesquiterpene ABA and botrydial (BOT) biosynthesis. ABA_BOT cluster activation during root infection suppresses host nutrient uptake-related genes and changes the mineral contents, suggesting its role in manipulating host nutrition states. Conversely, disruption or environmental suppression of the cluster renders Ct3 beneficial for plant growth, in a manner dependent on host phosphate starvation response regulators. Our findings indicate that a fungal metabolism cluster provides a means by which infectious fungi modulate lifestyles along the parasitic_mutualistic continuum in fluctuating environments.

A fungal transcription factorBOT6facilitates the transition of a beneficial root fungus into an adapted anthracnose pathogen

“…Moreover, it has been reported that ABA-BOT gene expression in Ct3 becomes restricted at the later colonization phase (Fig. 1E) 17 . In relation to this, despite that constitutive expression of CtBOT6 leads to a drastic increase in Ct4 biomass in A. thaliana roots as well as leaves, the conidia and setae formation that is typical to Colletotrichum pathogen are not observed in both tissues even at 22 dpi.…”

“…From the perspective of microbes, virulence factors driving microbes from mutualistic toward pathogenic lifestyles have been characterized; the presence or absence of specific virulence factors in their genome defines pathogenicity 14, 15, 16 . Further, the activation of virulence determinants in particular fungal strains within the same fungal species or under specific environmental conditions induces a transition in lifestyle from mutualistic to pathogenic 17 . These findings suggest that microbes capable of conquering nonhost resistance can continuously define the appropriate infection strategies.…”

“…Although pathogenic fungi also produce ABA, its role during plant-microbe interactions has been unexplored in detail 29, 38 . While Ct activates the ABA pathway in plants in a putative ABA-BOT cluster-dependent manner, which leads to plant growth inhibition 17 , it is unclear how the ABA signaling pathway is integrated into either beneficial or pathogenic lifestyles of Ct.…”

“…The Colletotrichum tofieldiae Ct3 (MAFF712333) and Ct4 (MAFF712334) strains and the Colletotrichum incanum (MAFF238704) strain were used as the wild-type strains in this study 17 .…”

“…Fungi are maintained on Mathurs media with 3% agar granulated (Difco) at 25°C in normal light conditions. Fungal transformation was performed as previously described 17 . Briefly, the knock-in vector (see below) was introduced into Agrobacterium C58C1 strains by electroporation.…”