A conserved enzyme of smut fungi facilitates cell-to-cell movement in the plant bundle sheath

Abstract

The smut fungi are one of the largest groups of fungal plant pathogens, causing disease in all cereal crops. They directly penetrate their hosts and establish a biotrophic interaction. During colonization of the plant, smut fungi secrete a wide range of effector proteins, which suppress plant immunity and modulate cellular functions as well as development of the host, thereby determining the pathogens life-style and virulence potential. The conserved effector Erc1 (enzyme required for cell-to-cell movement) contributes to virulence of the corn smut Ustilago maydis in maize leaves, but not on the tassel. Erc1 binds to host cell wall components and has a 1,3-B-glucanase activity, which is required to attenuate B-glucan-induced defense responses in host leaves. Confocal microscopy revealed that Erc1 has a cell type-specific virulence function, being necessary for fungal cell-to-cell movement in the plant bundle sheath. This cell type-specific virulence function of Erc1 is fully conserved in the barley pathogen Ustilago hordei, which has a functionally conserved Erc1 orthologue. Thus, Erc1 is an enzymatically active core virulence factor with a cell type-specific virulence function in different hosts, which is important for cell-to-cell movement during host colonization of pathogenic smut fungi.

Co‐evolution within the plant holobiont drives host performance

“…While effectors with antimicrobial activity were initially described in the context of plant infection by the pathogenic soil‐borne and broad host‐range pathogen Verticillium dahliae , other fungal pathogens may produce such effectors too. More recently, it was reported that the soil‐borne white root rot pathogen Rosellinia necatrix expresses antimicrobial effector proteins during host colonization, while smut fungi express a conserved extracellular ribonuclease with broad‐spectrum cytotoxic activity to compete with host‐associated bacteria on the leaves of host plants (preprint: Chavarro‐Carrero et al , 2023; preprint: Ökmen et al , 2023). Pathogenic oomycetes seem to rely on a similar strategy, since Albugo candida secretes antimicrobials into the apoplast of A. thaliana leaves to repress the growth of keystone bacteria (Gómez‐Pérez et al , 2023).…”