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Thomma, B.

Publications and source records attributed to Thomma, B..

At least 19 recordsLinked to original sources

Decoupled evolution of antimicrobial repertoires in lichen-forming fungi

Lichens are stable multipartite symbioses in which a fungal mycobiont associates with one or more photosynthetic partners while hosting complex microbiomes. Secreted antimicrobial proteins (AMPs) have recently emerged as important mediators of fungal interactions with surrounding microbial communities, yet their evolutionary distribution and diversity in lichen-forming fungi remain largely unexplored. Here, we predicted AMP repertoires across 80 phylogenetically diverse lichen-forming fungi representing three photobiont association types. Contrary to our expectation, average repertoire size did not differ between chlorolichens, cyanolichens and tripartite lichens (363 AMPs per species overall), even though repertoire size varied almost five-fold among species and 23 AMP families showed photobiont-associated enrichment or depletion. This quantitative conservation masks extensive compositional turnover, with families occurring in at least 90% of species coexisting alongside numerous lineage-specific groups. Pooled population sequencing of 11 Umbilicaria phaea populations along two elevational gradients further revealed recurrent AMP presence-absence variation within a single species. In contrast to AMPs, biosynthetic gene clusters (BGCs) and carbohydrate-active enzymes (CAZymes), which include known antimicrobials, were markedly reduced in cyanolichens relative to chlorolichens. Lichen-forming fungi thus combine a conserved baseline antimicrobial protein capacity, whose composition nonetheless turns over between lineages and populations, with chemical and enzymatic systems that differentiate along photobiont association and may support ecological and lifestyle-associated adaptation.

microbiology↗

Structural homology reveals cerato-platanins as conserved antimicrobials repeatedly co-opted for fungal host colonization

Fungal cerato-platanins (CPs) are small ([~]12 kDa) secreted proteins broadly conserved across filamentous fungi and implicated in a striking diversity of biological processes, ranging from fungal development to interactions with plant hosts. However, a core molecular activity unifying these diverse functions has remained elusive. Fungal pathogens secrete effector proteins, including CPs, to manipulate host physiology and promote colonization. Increasing evidence demonstrates that particular fungal effectors possess antimicrobial activity that enables pathogens to reshape host-associated microbiota during infection, and that antimicrobial activity is strongly enriched among evolutionarily conserved secreted proteins. These findings suggests that intermicrobial competition represents an ancient and fundamental fungal trait, and that several effectors that manipulate plant hosts evolved from ancient antimicrobials. Here, we identify antimicrobial activity as the conserved core function of the CP family, from which diverse roles in environmental adaptation and host interaction evolved. Structural analysis of the Verticillium dahliae secretome identified a structural cluster containing the CP protein CP1 and the previously characterized antimicrobial effector Ave1, providing the first structural link between CPs and antimicrobial activity. Accordingly, functional assays demonstrate that V. dahliae CPs exhibit selective antimicrobial activity in vitro. Expanding this analysis to a wide diversity of phylogenetic lineages and ecological lifestyles revealed that antimicrobial features are broadly conserved across the CP family. Together, our findings identify antimicrobial activity as an ancient and conserved molecular function that unifies the CP family and support a model in which host-manipulating effector functions evolved from ancestral proteins that mediate inter-microbial competition.

microbiology↗

A chromosome-scale super-pangenome of the lichen genus Peltigera reveals genome architecture and expanded interaction repertoires shared across pathogenic and mutualistic fungi

Fungi engage in associations with other organisms across a continuum from pathogenic to mutualistic lifestyles. Hence, they require a compendium of molecular capacities, including partner recognition, extracellular signaling, nutrient exchange, immune modulation, and control of microbial competitors. In filamentous pathogens such traits are frequently associated with compartmentalized genomes, including rapidly evolving secreted proteins known as effectors and expanded receptor families, but it remains unclear whether similar genomic principles shape mutualistic fungal symbioses. Here, we generated a chromosome-scale super-pangenome for the lichen-forming genus Peltigera, comprising 41 mycobiont assemblies representing eleven species, together with genomes of associated Nostoc and, in tripartite species, Coccomyxa photobionts. The mycobiont genomes revealed extensive variation in genome size, transposable element content, biosynthetic gene clusters, and lineage-specific gene content, with pronounced expansions in tripartite species. Across Peltigera, secreted protein encoding genes were preferentially located in TE-rich regions. We further identified Starship-like transposon elements, expanded antimicrobial protein repertoires, and a large, previously underestimated repertoire of fungal GPCRs dominated by Pth11-like receptors. Layer-specific transcriptomics of a P. rufescens thallus showed differential expression of several interaction-associated gene families, e.g. lectins, antimicrobial proteins and Pth11-like GPCRs. These data indicate that pathogenic and mutualistic fungi might exhibit shared genomic principles, including genome compartmentalization, mobile-element-associated diversification, and the expansion of molecular repertoires involved in recognition, extracellular control and signaling.

genomics↗

A fungal pathogen effector that shapes host plant microbiota kills bacteria through lipoteichoic acid binding and membrane disruption

Antimicrobial proteins are ancient and widespread molecules that contribute to survival across all domains of life. We previously showed that fungal plant pathogens secrete antimicrobial proteins to suppress antagonistic members of the host microbiota and thereby promote host colonization. The soil-borne plant pathogen Verticillium dahliae employs the bactericidal protein VdAve1 for this purpose. Here, we elucidate the mode of action of VdAve1 and define its mechanism as a distinct type of antimicrobial activity. Nuclear magnetic resonance (NMR) analysis revealed that VdAve1 adopts a jelly-roll barrel-like fold. Functionally, VdAve1 disrupts bacterial plasma membranes, and synthetic peptides derived from its positively charged regions retain antimicrobial activity, indicating that these regions contribute to its function. We further show that the bacterial model system Bacillus subtilis responds to VdAve1 by modifying teichoic acids, and that loss of these modifications increases bacterial sensitivity. Consistent with this, VdAve1 binds lipoteichoic acid (LTA), a major component of the Gram-positive cell wall. Together, our findings support a model in which VdAve1 binds LTA to localize at the bacterial surface, where it perturbs the plasma membrane, leading to membrane collapse and cell death. SIGNIFICANCE STATEMENTPlant-pathogenic microbes secrete effector proteins to promote host colonization. While these proteins are typically studied for their roles in host manipulation, some affect host-associated microbial communities by exhibiting antimicrobial activity. However, their modes of action remain largely unexplored. The fungal plant pathogen Verticillium dahliae secretes the antimicrobial effector VdAve1 to inhibit bacterial antagonists in the host microbiota. Here, we characterize the mode of action of VdAve1. We show that VdAve1 binds lipoteichoic acid, a major component of the cell wall of Gram-positive bacteria. This promotes VdAve1 accumulation close to the plasma membrane, and through electrostatic interactions it disrupts the plasma membrane. We further determine VdAve1 structure by NMR, revealing VdAve1 adopts a {beta}-barrel-like fold. Together, our findings show the mechanism by which a fungal effector inhibits bacterial growth and thereby how it may influence host-associated bacterial communities.

microbiology↗

Bacteria rewire fungal antimicrobial gene expression in microbial arms races

Microbial communities are shaped by antagonistic interactions, yet how competitors evade antimicrobial strategies in a community context remains unclear. Fungi deploy antimicrobial proteins (AMPs) to suppress bacterial niche competitors, but how bacteria counteract these defences is unknown. Here we show that soil microbiota suppress fungal AMP expression, revealing a previously unrecognized mode of intermicrobial interference. In the soil-borne pathogen Verticillium dahliae, AMP genes are highly conserved yet broadly repressed in the presence of natural microbial communities. This repression extends across diverse fungi, suggesting a widespread phenomenon. Correlation analyses of AMP expression and community compositions linked the bacterial genera Leptothrix and Devosia to repression of the V. dahliae AMPs VdL1 and VdD1, respectively. Both AMPs antagonize these bacterial taxa, and microbiota-mediated repression of VdL1 reduces its contribution to fungal soil colonization. Together, our findings reveal that bacteria can evade fungal antagonism by suppressing AMP deployment, highlighting community-level control of microbial competition.

microbiology↗

A structurally unique effector shared between Verticillium dahliae and Fusarium oxysporum is involved in cotton defoliation and virulence on other hosts

Defoliating (D) strains of the vascular wilt fungus Verticillium dahliae cause severe yield losses in cotton and olive worldwide, yet the genetic basis underlying this pathotype has remained unknown. Here, we combined comparative genomics, functional genetics, structural analysis, and phylogenomics to uncover the molecular determinant of defoliation. We identified a small, D pathotype-specific genomic region encoding two duplicated secreted effector genes. Simultaneous deletion of both gene copies abolished pathogenicity and defoliation in cotton, olive, Nicotiana benthamiana, and Arabidopsis thaliana, whereas single deletions reduced virulence and genetic complementation restored disease symptoms. Conversely, expression of the D effector in non-defoliating strains was sufficient to induce defoliation. Moreover, or exogenous application of the purified protein, induced wilting and defoliation as well. Structural analyses revealed that D homologs share a conserved but previously uncharacterized protein fold and are distributed across Verticillium and Fusarium species, exhibiting functional diversification and host-specific activity. Phylogenomic and genomic context analyses indicate repeated horizontal transfer events mediated by giant transposable elements known as Starships. Together, our findings identify the D effector as a central pathogenicity factor that drives defoliation and virulence, and demonstrate how Starship-mediated horizontal gene transfer shapes the emergence and dissemination of an agriculturally devastating fungal trait.

plant biology↗

Differential contributions of an antimicrobial effector from Verticillium dahliae to virulence and tomato microbiota assembly across natural soils

Throughout their life cycle plants associate with diverse and complex microbial communities, known as their microbiota. These microbiota contribute to plant performance and health, in part by providing a microbial barrier against invading plant pathogens. To colonize plant hosts, pathogens not only have to overcome host immune responses, but also breach the microbial barrier, for which they secrete so-called effector proteins. Accordingly, the soil-borne fungal plant pathogen Verticillium dahliae secretes the antimicrobial effector Ave1 to suppress antagonistic microbes and facilitate host colonization. Notably, many pathogens, including V. dahliae, have life stages outside their host plants, for instance in soil, where they encounter diverse microbial communities. Yet, how antimicrobial effectors support establishment across these environments remains poorly understood. To address this, we established a collection of natural soil samples with diverse physicochemical properties and microbiota compositions. Using this collection, we show for three plant species, barley, tomato and cotton, that root-associated bacterial and fungal communities are primarily shaped by the type of soil, whereas the phyllosphere microbiota is mainly determined by plant species. On tomato, we furthermore show that Ave1 differentially contributes to virulence on diverse soils, as Ave1 altered the tomato microbiota on all soils tested, but the taxa affected by these shifts varied depending on the specific soils. Our findings suggest that while Ave1-mediated microbiota manipulation occurs across soils, its impact on fungal virulence is influenced by the specific composition of the soil-derived microbiota assembled by the host.

plant biology↗

Undermining the cry for help: The phytopathogenic fungus Verticillium dahliae secretes an antimicrobial effector protein to undermine host recruitment of antagonistic Pseudomonas bacteria

During pathogen attack, plants recruit beneficial microbes in a "cry for help" to mitigate disease development. Simultaneously, pathogens secrete effectors to promote host colonization through various mechanisms, including targeted host microbiota manipulation. Here, we characterize the Av2 effector of the vascular wilt fungus Verticillium dahliae as a suppressor of the cry for help. Inspired by in silico antimicrobial activity prediction, we investigated the antimicrobial activity of Av2 in vitro. Furthermore, its role in V. dahliae virulence was assessed through microbiota sequencing of inoculated plants, microbial co-cultivation assays, and inoculations in a gnotobiotic plant cultivation system. We show that Av2 inhibits bacterial growth, and acts as a virulence factor during host colonization. Microbiota sequencing revealed involvement of Av2 in suppression of Pseudomonas spp. recruitment upon plant inoculation with V. dahliae, suggesting that Av2 suppresses the cry for help. We show that several Pseudomonas spp. are antagonistic to V. dahliae and sensitive to Av2 treatment. We conclude that V. dahliae secretes Av2 to supress the cry for help by inhibiting the recruitment of antagonistic Pseudomonas spp. to pave the way for successful plant invasion.

plant biology↗

A gnotobiotic system reveals multifunctional effector roles in plant-fungal pathogen dynamics

Plants host diverse microbiota that influence physiological processes and can enhance resilience against invading pathogens that, in turn, evolved effector proteins to manipulate host microbiota in their favor. However, the complexity of microbial communities and their interactions complicates mechanistic research on processes governing microbiota assembly and function. Gnotobiotic systems are valuable tools to study plant microbiota by reducing complexity and enabling controlled microbiota reconstitution experiments. Despite their utility, no gnotobiotic systems have been established to investigate the role of antimicrobial effector proteins in the interactions between plants, their microbiota, and fungal pathogens. Here, we present a refined gnotobiotic system designed to study these interactions, establishing protocols for infections with the fungal pathogen Verticillium dahliae across multiple host plants under sterile conditions. We demonstrate that a synthetic microbial community (SynCom) derived from a culture collection generated for this study can be applied in this system where it interferes with fungal infections. Additionally, using our gnotobiotic system we reveal that specific antimicrobial effectors of V. dahliae, like Ave1L2, contribute to fungal virulence in a microbiota-dependent manner, whereas other antimicrobial effectors, such as Ave1, seem to possess functions beyond microbiota manipulation.

plant biology↗

Starship giant transposons dominate plastic genomic regions in a fungal plant pathogen and drive virulence evolution

Starships form a recently discovered superfamily of giant transposons in Pezizomycotina fungi, implicated in mediating horizontal transfer of diverse cargo genes between fungal genomes. Their elusive nature has long obscured their significance, and their impact on genome evolution remains poorly understood. Here, we reveal a surprising abundance and diversity of Starships in the phytopathogenic fungus Verticillium dahliae. Remarkably, Starships dominate the plastic genomic compartments involved in host colonization, are enriched in virulence-associated genes, and exhibit genetic and epigenetic characteristics associated with adaptive genome evolution. We further uncover extensive horizontal transfer of Starships between Verticillium species and, strikingly, from distantly related Fusarium fungi. Finally, we demonstrate how Starship activity facilitated the de novo formation of a novel virulence gene. Our findings illuminate the profound influence of Starship dynamics on fungal genome evolution and the development of virulence.

microbiology↗

The soil-borne white root rot pathogen Rosellinia necatrix expresses antimicrobial proteins during host colonization

Rosellinia necatrix is a prevalent soil-borne plant-pathogenic fungus that is the causal agent of white root rot disease in a broad range of host plants. The limited availability of genomic resources for R. necatrix has complicated a thorough understanding of its infection biology. Here, we sequenced nine R. necatrix strains with Oxford Nanopore sequencing technology, and with DNA proximity ligation we generated a gapless assembly of one of the genomes into ten chromosomes. Whereas many filamentous pathogens display a so-called two-speed genome with more dynamic and more conserved compartments, the R. necatrix genome does not display such genome compartmentalization. It has recently been proposed that fungal plant pathogens may employ effectors with antimicrobial activity to manipulate the host microbiota to promote infection. In the predicted secretome of R. necatrix, 26 putative antimicrobial effector proteins were identified, nine of which are expressed during plant colonization. Two of the candidates were tested, both of which were found to possess selective antimicrobial activity. Intriguingly, some of the inhibited bacteria are antagonists of R. necatrix growth in vitro and can alleviate R. necatrix infection on cotton plants. Collectively, our data show that R. necatrix encodes antimicrobials that are expressed during host colonization and that may contribute to modulation of host-associated microbiota to stimulate disease development.

plant biology↗

Three-dimensional chromatin organization promotes genome evolution in a fungal plant pathogen

The spatial organization of eukaryotic genomes is linked to their biological functions, although it is not clear how this impacts the overall evolution of a genome. Here, we uncover the three-dimensional (3D) genome organization of the phytopathogen Verticillium dahliae, known to possess distinct genomic regions, designated adaptive genomic regions (AGRs), enriched in transposable elements and genes that mediate host infection. Short-range DNA interactions form clear topologically associating domains (TADs) with gene-rich boundaries that show reduced levels of gene expression and reduced genomic variation. Intriguingly, TADs are less clearly structured in AGRs than in the core genome. At a global scale, the genome contains bipartite long-range interactions, particularly enriched for AGRs and more generally containing segmental duplications. Notably, the patterns observed for V. dahliae are also present in other Verticillium species. Thus, our analysis links 3D genome organization to evolutionary features conserved throughout the Verticillium genus.

microbiology↗

A single Verticillium dahliae effector determines pathogenicity on tomato by targeting auxin response factors

SUMMARYVerticillium dahliae is a xylem-invading fungal pathogen that causes devastating vascular wilt diseases on hundreds of plant hosts, including tomato (Solanum lycopersicum). Although individual V. dahliae strains are typically characterized by their broad host range, differential pathogenicity occurs on nearly all hosts. Currently, the molecular basis underlying such pathogenicity differences remains unknown. We used comparative genomics to identify a single effector gene that specifically occurs in tomato-pathogenic V. dahliae strains and is expressed during tomato colonization. Functional analyses showed that this Tom1 effector governs pathogenicity on tomato, as Tom1 deletion prohibited tomato colonization, while introduction of Tom1 into non-pathogenic V. dahliae or into saprophytic sister species V. tricorpus and V. nubilum resulted in disease. Through proteomics-based approaches, auxin response factors (ARFs) were identified as in planta targets of Tom1. Intriguingly, repression of SlARF2a expression by virus-induced gene silencing fully impaired V. dahliae colonization of tomato, solidifying its role as susceptibility target.Collectively, our findings indicate that a single effector, Tom1, mediates pathogenicity of V. dahliae on tomato by targeting auxin response factors.

plant biology↗

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

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, and may thus be targeted by pathogen effectors as such. 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 absence of the corresponding immune receptor Ve1. We now identified a multiallelic V. dahliae gene displaying ~65% sequence similarity to VdAve1, named VdAve1-like (VdAve1L). Interestingly, VdAve1L 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 Ve1 locus, does not recognize VdAve1L. Furthermore, we show that the full-length variant VdAve1L2 possesses antimicrobial activity, like VdAve1, yet with a divergent activity spectrum. Altogether, VdAve1L2 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.

plant biology↗

An ancient antimicrobial protein co-opted by a fungal plant pathogen for in planta mycobiome manipulation

Microbes typically secrete a plethora of molecules to promote niche colonization. Soil-dwelling microbes are well-known producers of antimicrobials that are exploited to outcompete microbial co-inhabitants. Also plant pathogenic microbes secrete a diversity of molecules into their environment for niche establishment. Upon plant colonization, microbial pathogens secrete so-called effector proteins that promote disease development. While such effectors are typically considered to exclusively act through direct host manipulation, we recently reported that the soil-borne fungal xylem-colonizing vascular wilt pathogen Verticillium dahliae exploits effector proteins with antibacterial properties to promote host colonization through the manipulation of beneficial host microbiota. Since fungal evolution preceded land plant evolution, we now speculate that a subset of the pathogen effectors involved in host microbiota manipulation evolved from ancient antimicrobial proteins of terrestrial fungal ancestors that served in microbial competition prior to the evolution of plant pathogenicity. Here, we show that V. dahliae has co-opted an ancient antimicrobial protein as effector, named VdAMP3, for mycobiome manipulation in planta. We show that VdAMP3 is specifically expressed to ward off fungal niche competitors during resting structure formation in senescing mesophyll tissues. Our findings indicate that effector-mediated microbiome manipulation by plant pathogenic microbes extends beyond bacteria and also concerns eukaryotic members of the plant microbiome. Finally, we demonstrate that fungal pathogens can exploit plant microbiome-manipulating effectors in a life-stage specific manner, and that a subset of these effectors has evolved from ancient antimicrobial proteins of fungal ancestors that likely originally functioned in manipulation of terrestrial biota. SIGNIFICANCE STATEMENTMicrobes secrete a diversity of molecules into their environment to mediate niche colonization. During host ingress, plant pathogenic microbes secrete effector proteins that facilitate disease development, many of which deregulate host immune responses. We recently demonstrated that plant pathogens additionally exploit effectors with antibacterial activities to manipulate beneficial plant microbiota to promote host colonization. Here, we show that the fungal pathogen Verticillium dahliae has co-opted an ancient antimicrobial protein, that likely served in microbial competition in terrestrial environments before land plants existed, as effector for the manipulation of fungal competitors during host colonization. Thus, we demonstrate that pathogen effector repertoires comprise antifungal proteins, and speculate such effectors could be exploited for the development of novel antimycotics.

microbiology↗

DNA methylation in Verticillium dahliae requires only one of three putative DNA methyltransferases, yet is dispensable for growth, development and virulence

DNA methylation is an important epigenetic control mechanism that in many fungi is restricted to genomic regions containing transposons. Two DNA methyltransferases, Dim2 and Dnmt5, are known to perform methylation at cytosines in fungi. While most ascomycete fungi encode both Dim2 and Dnmt5, only few functional studies have been performed in species containing both. In this study, we report functional analysis of both Dim2 and Dnmt5 in the plant pathogenic fungus Verticillium dahliae. Our results show that Dim2, but not Dnmt5 or the putative sexual-cycle related DNA methyltransferase Rid, is responsible for nearly all DNA methylation. Single or double DNA methyltransferase mutants did not show altered development, virulence, or transcription of genes or transposons. In contrast, Hp1 and Dim5 mutants that are impacted in chromatin-associated processes upstream of DNA methylation are severely affected in development and virulence and display extensive transcriptional reprogramming in specific hypervariable genomic regions (so-called lineage-specific (LS) regions) that contain genes associated with host colonization. As these LS regions are largely devoid of DNA methylation and of Hp1- and Dim5-associated heterochromatin, the differential transcription is likely caused by pleiotropic effects rather than by differential DNA methylation. Overall, our study suggests that Dim2 is the main DNA methyltransferase in V. dahliae and, in conjunction with work on other fungi, is likely the main active DNMT in ascomycetes, irrespective of Dnmt5 presence. We speculate that Dnmt5 acts under specific, presently enigmatic, conditions or, alternatively, acts in DNA-associated processes other than DNA methylation.

microbiology↗

Three LysM effectors of Zymoseptoria tritici collectively disarm chitin-triggered plant immunity

SUMMARYChitin is a major structural component of fungal cell walls and acts as a microbe-associated molecular pattern (MAMP) that, upon recognition by a plant host, triggers the activation of immune responses. In order to avoid the activation of these responses, the Septoria tritici blotch (STB) pathogen of wheat, Zymoseptoria tritici, secretes LysM effector proteins. Previously, the LysM effectors Mg1LysM and Mg3LysM were shown to protect fungal hyphae against host chitinases. Furthermore, Mg3LysM, but not Mg1LysM, was shown to suppress chitin-induced reactive oxygen species (ROS) production. Whereas initially a third LysM effector gene was disregarded as a presumed pseudogene, we now provide functional data to show that also this gene encodes a LysM effector, named Mgx1LysM, that is functional during wheat colonization. While Mg3LysM confers a major contribution to Z. tritici virulence, Mgx1LysM and Mg1LysM contribute to Z. tritici virulence with smaller effects. All three LysM effectors display partial functional redundancy. We furthermore demonstrate that Mgx1LysM binds chitin, suppresses the chitin-induced ROS burst and is able to protect fungal hyphae against chitinase hydrolysis. Finally, we demonstrate that Mgx1LysM is able to undergo chitin-induced polymerisation. Collectively, our data show that Zymoseptoria tritici utilizes three LysM effectors to disarm chitin-triggered wheat immunity.Competing Interest StatementThe authors have declared no competing interest.View Full Text

plant biology↗

Comparative genomics of Verticillium dahliae isolates reveals the in planta-secreted effector protein recognized in V2 tomato plants

Plant pathogens secrete effector molecules during host invasion to promote host colonization. However, some of these effectors become recognized by host receptors, encoded by resistance genes, to mount defense response and establish immunity. Recently, a novel resistance was identified in tomato, mediated by the single dominant V2 locus, to control strains of the soil-borne vascular wilt fungus Verticillium dahliae that belong to race 2. We performed comparative genomics between race 2 strains and resistance-breaking race 3 strains to identify the avirulence effector that activates V2 resistance, termed Av2. We identified 277 kb of race 2-specific sequence comprising only two genes that encode predicted secreted proteins, both of which are expressed by V. dahliae during tomato colonization. Subsequent functional analysis based on genetic complementation into race 3 isolates confirmed that one of the two candidates encodes the avirulence effector Av2 that is recognized in V2 tomato plants. The identification of Av2 will not only be helpful to select tomato cultivars that are resistant to race 2 strains of V. dahliae, as the corresponding V2 resistance gene has not yet been mapped, but also to monitor adaptations in the V. dahliae population to deployment of V2-containing tomato cultivars in agriculture.

plant biology↗