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 coinhabitants. 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.

微生物通常会分泌大量分子来促进生态位定殖。土壤微生物是众所周知的抗菌剂生产者，人们利用这些微生物在竞争中击败共生微生物。此外，植物病原微生物将多种分子分泌到其环境中以建立生态位。在植物定植后，微生物病原体会分泌所谓的效应蛋白，促进疾病的发展。虽然此类效应器通常被认为仅通过直接宿主操纵发挥作用，但我们最近报道，土传、真菌、木质部定植的维管束枯萎病病原体大丽黄萎病菌利用具有抗菌特性的效应蛋白，通过操纵有益的宿主微生物群来促进宿主定植。 。由于真菌进化先于陆地植物进化，我们现在推测，参与宿主微生物群操纵的病原体效应子的一个子集是从陆地真菌祖先的古老抗菌蛋白进化而来的，这些蛋白在植物致病性进化之前参与微生物竞争。在这里，我们发现大丽花弧菌选择了一种古老的抗菌蛋白作为效应子，名为 VdAMP3，用于植物中真菌组的操作。我们发现，在衰老叶肉组织的静息结构形成过程中，VdAMP3 被特异性表达以抵御真菌生态位竞争者。我们的研究结果表明，植物病原微生物效应介导的微生物组操纵不仅限于细菌，还涉及植物微生物组的真核成员。最后，我们证明真菌病原体可以以生命阶段特定的方式利用植物微生物组操纵效应器，并且这些效应器的一个子集是从真菌祖先的古老抗菌蛋白进化而来的，这些蛋白最初可能在操纵陆地生物群中发挥作用。