Conserved secreted effectors determine endophytic growth and multi-host plant compatibility in a vascular wilt fungus

Abstract

Fungal interactions with plant roots, either beneficial or detrimental, have a major impact on agriculture and ecosystems. The soil inhabiting ascomycete Fusarium oxysporum (Fo) constitutes a species complex of worldwide distribution causing vascular wilt in more than a hundred different crops. Individual isolates of the fungus exhibit host-specific pathogenicity, determined by proteinaceous effectors termed secreted in xylem (SIX). However, such isolates can also colonize roots of non-host plants asymptomatically as endophytes, or even protect them against pathogenic isolates. The molecular determinants of multi-host plant colonization are currently unknown. Here, we identified a set of fungal effectors termed ERCs (Early Root Compatibility effectors), which are secreted during early biotrophic growth of Fo on both host and non-host plants. In contrast to the strain-specific SIX effectors, which are encoded on accessory genomic regions, ERCs are encoded on core regions and are found across the entire Fo species complex as well as in other phytopathogens, suggesting a conserved role in fungus-plant associations. Targeted deletion of ERC genes in a pathogenic Fo isolate resulted in reduced virulence on the host plant and rapid activation of plant immune responses, while in a non-pathogenic isolate it led to impaired root colonization and loss of biocontrol ability. Strikingly, some ERCs also contribute to Fo infection on the non-vascular land plant Marchantia polymorpha. Our results reveal an evolutionarily conserved mechanism for multi-host colonization by root infecting fungi.

Marchantia polymorpha model reveals conserved infection mechanisms in the vascular wilt fungal pathogen Fusarium oxysporum

“…1e,f). The pattern of intercellular hyphal penetration and growth of Fo observed in Mp resembled that reported previously for Fol4287 on tomato roots (Pérez‐Nadales & Di Pietro, 2011; Redkar et al ., 2021). Furthermore, SEM analysis showed Fol4287 and Fo47 hyphae traversing airpores of Mp and growing within the air chambers (Fig.…”

“…The ascomycete fungus Fusarium oxysporum (Fo) represents a species complex with worldwide distribution that provokes devastating losses in more than 150 different crops (Dean et al ., 2012). Fo exhibits a hemibiotroph lifestyle with an initial biotrophic phase characterised by intercellular growth in the root cortex, followed by invasion of the vasculature and transition to the necrotrophic phase resulting in maceration and death of the colonised host (Redkar et al ., 2021). In the soil, Fo is able to locate roots by sensing secreted plant peroxidases via its sex pheromone receptors and the cell wall integrity mitogen activated protein kinase (MAPK) pathway (Turrà et al ., 2015).…”

Degradation of α-Subunits, Doa1 and Doa4, are Critical for Growth, Development, Programmed Cell Death Events, Stress Responses, and Pathogenicity in the Watermelon Fusarium Wilt Fungus Fusarium oxysporum f. sp. niveum

“…5−7 Four SIX effectors, namely, FolSIX1, FolSIX3, FolSIX5, and FolSIX6, are crucial for F. oxysporum f. sp. lycopersici virulence, 5,8 whereas FolSIX1, FolSIX3, and FolSIX4 can be recognized by host resistance proteins to confer effector-triggered immunity. 8−10 Genetic approaches, including random mutagenesis and targeted gene disruption, have led to the identification of dozens of pathogenicity genes in F. oxysporum.…”

Spatially distinct phytohormone responses of individualArabidopsis thalianaroot cells to infection and colonization byFusarium oxysporum

“…sp., and whether a f. sp. is pathogenic, non-compatible, or beneficial to a certain plant (Ma et al ., 2010; Redkar et al ., 2022). F. oxysporum hyphae grow in the soil and are chemotactically guided toward the root of their host plant (Wang et al ., 2022 a ).…”