Microbiome Manipulation by Verticillium Dahliae

Essentially, every multicellular organism functions as “metaorganism” because it typically harbors highly complex microbial communities that are symbiotically associated and that affect physiological activities. Consequently, it is recognized that the microbiota, the assemblage of microorganisms an organism associates with, is an important health determinant. This is no less true for plants. The most extensive microbial colonization of plants occurs at roots in the so-called rhizosphere, to which microbes that live in bulk soil are attracted in their search for carbon and other food sources. However, also above-ground plant parts form a widespread microbial habitat, known as the phyllosphere, as well as the plant’s interior, known as the endosphere. Accumulating evidence suggests that plants actively shape their microbiota. For example, through secretion of root exudates plants define rhizosphere microbiome compositions. In this manner, plants appear to be able to specifically attract beneficial microbes to suppress pathogen invasion in a “cry for help”.

During evolution, microbial pathogens evolved to target the most essential elements of the immune system of their hosts in order to subvert host immunity and support host colonization. To this end, these pathogens secrete so-called effectors that are characterized by their wide breadth of cellular destinations and biochemical targets inside plant hosts. However, if we accept that a host’s microbiota is a key determinant of its health, it is likely that pathogens evolved to target that microbiota to cause dysbiosis and thus weaken its host. Furthermore, considering the crucial role of effectors in disease development, it is likely that microbial pathogens employ their effector catalogues to establish dysbiosis.

Verticillium dahliae is a soil-borne fungus that causes vascular wilt disease on hundreds of plant species, including a wide diversity of crops such as tomato, potato, olive and cotton. The fungus survives in the soil through extremely persistent resting structures called microsclerotia, that are able to germinate in response to plant root exudates. Subsequently, the fungus grows through the rhizosphere to infect plant roots, after which the fungus enters the water-conducting xylem vessels for systemic colonization, eventually resulting in the typical vascular wilt disease. We recently demonstrated that the previously identified secreted virulence effector VdAve1 displays antimicrobial activity and selectively targets co-inhabitants of the tomato and cotton microbiota. More specifically, we showed that Ave1 negatively affects Sphingomonads that antagonize V. dahliae growth.  Additionally, we showed that V. dahliae exploits the secreted effector VdAMP2 for microbiome manipulation in the soil. Thus, we have demonstrated that the fungal plant pathogen V. dahliae uses effector proteins to modulate microbiome compositions in the soil, in the rhizosphere and in the endosphere. We infer that the V. dahliae effector catalogue, but also those of other pathogens, represent an untapped resource for novel antibiotics.

Most relevant literature

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 (2016). Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Current Opinion in Plant Biology 20: 96-103.