A highly polymorphic effector protein promotes fungal virulence through suppression of plant‐associated Actinobacteria

Abstract

Summary Plant pathogens secrete effector proteins to support host colonization through a wide range of molecular mechanisms, while plant immune systems evolved receptors to recognize effectors or their activities to mount immune responses to halt pathogens. Importantly, plants do not act as single organisms, but rather as holobionts that actively shape their microbiota as a determinant of health. The soil‐borne fungal pathogen Verticillium dahliae was recently demonstrated to exploit the VdAve1 effector to manipulate the host microbiota to promote vascular wilt disease in the absence of the corresponding immune receptor Ve1. We identify a multiallelic V. dahliae gene displaying c. 65% sequence similarity to VdAve1, named VdAve1‐like (VdAve1L), which shows extreme sequence variation, including alleles that encode dysfunctional proteins, indicative of selection pressure to overcome host recognition. We show that the orphan cell surface receptor Ve2, encoded at the Ve locus, does not recognize VdAve1L. Additionally, we demonstrate that the full‐length variant VdAve1L2 possesses antimicrobial activity, like VdAve1, yet with a divergent activity spectrum, that is exploited by V. dahliae to mediate tomato colonization through the direct suppression of antagonistic Actinobacteria in the host microbiota. Our findings open up strategies for more targeted biocontrol against microbial plant pathogens.

Co‐evolution within the plant holobiont drives host performance

“…Similar to plant-microbe co-evolution, evolutionary arms races likely rule microbial evolution within holobionts. As previously mentioned, the wilt pathogen V. dahliae evolved antimicrobial effector proteins targeting antagonists in the plant microbiota to successfully colonize the plant and cause disease (Snelders et al, 2020(Snelders et al, , 2021(Snelders et al, , 2022(Snelders et al, , 2023. Under the selection pressure of the antimicrobials secreted by V. dahliae, protective strains insensitive to these effectors will be selected.…”

“…Intriguingly, it was recently uncovered that fungi exploit effectors with antibacterial and antifungal activities that modulate the composition of plant‐associated communities (Snelders et al , 2020, 2021, 2023). This extends the range of previously considered effector activities, typically thought‐out to mainly act in manipulation of host physiology to support host colonization, frequently through modulation of host immune signaling.…”

The soil-borne white root rot pathogenRosellinia necatrixexpresses antimicrobial proteins during host colonization

“…The copyright holder for this preprint (which this version posted April 10, 2023. ; https://doi.org/10.1101/2023.04.10.536216 doi: bioRxiv preprint plant as well as outside the host in the soil to support host colonization (Snelders et al, 2020;2023). One of them is the effector protein VdAve1 that was shown to display selective antimicrobial activity and facilitate colonization of tomato and cotton plants through host microbiota manipulation by suppressing antagonistic bacteria, such as members of the Spingomonadaceae (Snelders et al, 2020).…”

“…However, recent studies have uncovered additional functions of pathogen effector proteins in host colonization (Wilson and McDowell, 2022). For example, the soil-borne pathogen Verticillium dahliae secretes effector proteins to modulate microbiota compositions inside the host plant as well as outside the host in the soil to support host colonization (Snelders et al, 2020; 2021; 2022; 2023). One of them is the effector protein VdAve1 that was shown to display selective antimicrobial activity and facilitate colonization of tomato and cotton plants through host microbiota manipulation by suppressing antagonistic bacteria, such as members of the Spingomonadaceae (Snelders et al, 2020).…”

Battle of the bugs: how an oomycete pathogen shapes the microbiota of its host

“…Taken together with the intimate association between plants and their microbiota, and the importance of the microbiota for plant health, this broader definition of effectors has led to the hypothesis that pathogens have evolved to target hostassociated microbiota, in addition to the endogenous immune system of the host, using effectors to facilitate disease establishment (Snelders et al, 2018). Indeed, several fungal pathogens were recently shown to secrete effectors with antimicrobial activities that directly manipulate the microbiota of their hosts (Snelders et al, 2020(Snelders et al, , 2021(Snelders et al, , 2023Chavarro-Carrero et al, 2023;€ Okmen et al, 2023). Whether this also applied to oomycete plant pathogens was unknown until now.…”