AMAPEC v1.0
AMAPEC is a machine learning framework developed in the Thomma lab to predict antimicrobial activity in fungal secreted effector proteins.
Effector-Mediated Manipulation of Plant-Associated Microbiota
Plants coexist with diverse microbial communities that influence their growth, health and resistance to disease. Consequently, successful pathogens must compete not only with their hosts, but also with the beneficial microorganisms that inhabit plant-associated environments. Our research aims to understand how fungal pathogens overcome these microbial barriers and how interactions between pathogens and microbiota shape disease development.
In their evolutionary tug of war, microbial pathogens as well as plant hosts may have evolved to contest antagonists and recruit cooperators in order to influence the outcome of the interaction to their advantage; for hosts to remain healthy, and for the pathogen to succeed in disease establishment (figure taken from Roevenich et al. 2014).
Traditionally, fungal effector proteins have been studied as molecules that manipulate host physiology and suppress immune responses. However, research in our group has revealed that effectors can also act directly on microorganisms. We discovered that the vascular wilt pathogen Verticillium dahliae secretes effector proteins with selective antimicrobial activity that suppress bacterial competitors in the plant microbiota and in soil. These findings established that fungal pathogens can actively manipulate microbiome composition to promote host colonization.
Fungal pathogens secrete effector proteins to overcome microbial barriers during plant host colonization. Left: in healthy plants, immune responses (shield) and resident microbiota antagonize pathogen growth, restricting colonization of host tissues. Right: fungi evolved to secrete effector proteins (red circles), some of which display selective antimicrobial activity to manipulate microbiota by targeting antagonistic niche competitors, while others suppress plant immune responses that affect microbiota compositions in turn (figure taken from Mesny et al. 2024).
Plants are not passive participants in this interaction. Upon pathogen attack, they can recruit beneficial microorganisms that help suppress disease, a phenomenon often referred to as the plant "cry for help". We recently demonstrated that fungal pathogens can counteract this defense strategy through the secretion of antimicrobial effectors that specifically target disease-suppressive bacteria recruited by the host. Thus, pathogen success is determined not only by interactions with the plant, but also by an ongoing battle for control over the plant-associated microbiota.
Our work further revealed that microbiome-targeting effectors are evolutionarily ancient. Many fungal effectors appear to have originated from antimicrobial proteins that mediated microbial competition long before fungi evolved intimate associations with plants. During evolution, these proteins were co-opted into effector repertoires, where they acquired new functions in host colonization while retaining their capacity to shape microbial communities.
Annotated phylogenetic tree and heatmap describing a diverse dataset of 150 fungal genomes and the presence/absence of the 150 most conserved secreted protein families in these fungi, respectively. Many of these conserved secreted proteins are predicted antimicrobials (red annotation at the bottom; figure taken from Mesny et al. 2024).
Current research focuses on identifying microbiome-targeting effectors across the fungal kingdom, understanding how they influence bacterial and fungal communities in natural environments, and determining how microbiome manipulation contributes to disease development and adaptation. By integrating molecular plant pathology, microbial ecology, microbiome research and evolutionary biology, we aim to uncover the principles that govern interactions among plants, pathogens and the complex communities of microorganisms that surround them.
Most relevant literature
Mesny et al. (2026). Plant-associated fungi co-opt ancient antimicrobials for host manipulation. Sci Adv. 12: eaec1406.
Punt et al. (2026). Differential contributions of an antimicrobial effector from Verticillium dahliae to virulence and tomato microbiota assembly across natural soils. Microbiome 14: 111.
Kraege A et al. (2026). Undermining the cry for help: the phytopathogenic fungus Verticillium dahliae secretes an antimicrobial effector protein to undermine host recruitment of antagonistic Pseudomonas bacteria. New Phytol. 249: 406-417.
Mesny F et al (2024). Meddling with the microbiota: Fungal tricks to infect plant hosts. Curr Opin Plant Biol. 82: 102622.
Chavarro-Carrero et al. (2024). The soil-borne white root rot pathogen Rosellinia necatrix expresses antimicrobial proteins during host colonization. PLoS Pathog. 20 :e1011866.
Mesny F et al. (2023). Co-evolution within the plant holobiont drives host performance. EMBO Rep. 24 :e57455.
Snelders et al. (2023). A highly polymorphic effector protein promotes fungal virulence through suppression of plant-associated Actinobacteria. New Phytol. 237: 944-958.
Snelders NC et al. (2022). Microbiota manipulation through the secretion of effector proteins is fundamental to the wealth of lifestyles in the fungal kingdom. FEMS Microbiol Rev. 46: fuac022.
Snelders et al. (2021). An ancient antimicrobial protein co-opted by a fungal plant pathogen for in planta mycobiome manipulation. Proc Natl Acad Sci U S A 118: e2110968118.
Snelders et al. (2020). Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins. Nature Plants 6: 1365-1374.
Snelders et al. (2018). Plant pathogen effector proteins as manipulators of host microbiomes? Molecular Plant Pathology 19: 257-259.
Rovenich H, Boshoven JC, Thomma BPHJ (2014). Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Current Opinion in Plant Biology 20: 96-103.