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- Title
Verticillium dahliae Vta3 promotes ELV1 virulence factor gene expression in xylem sap, but tames Mtf1-mediated late stages of fungus-plant interactions and microsclerotia formation.
- Authors
Maurus, Isabel; Harting, Rebekka; Herrfurth, Cornelia; Starke, Jessica; Nagel, Alexandra; Mohnike, Lennart; Chen, Ying-Yu; Schmitt, Kerstin; Bastakis, Emmanouil; Süß, Marian T.; Leonard, Miriam; Heimel, Kai; Valerius, Oliver; Feussner, Ivo; Kronstad, James W.; Braus, Gerhard H.
- Abstract
Verticillium transcription activator of adhesion 3 (Vta3) is required for plant root colonization and pathogenicity of the soil-borne vascular fungus Verticillium dahliae. RNA sequencing identified Vta3-dependent genetic networks required for growth in tomato xylem sap. Vta3 affects the expression of more than 1,000 transcripts, including candidates with predicted functions in virulence and morphogenesis such as Egh16-like virulence factor 1 (Elv1) and Master transcription factor 1 (Mtf1). The genes encoding Elv1 and Mtf1 were deleted and their functions in V. dahliae growth and virulence on tomato (Solanum lycopersicum) plants were investigated using genetics, plant infection experiments, gene expression studies and phytohormone analyses. Vta3 contributes to virulence by promoting ELV1 expression, which is dispensable for vegetative growth and conidiation. Vta3 decreases disease symptoms mediated by Mtf1 in advanced stages of tomato plant colonization, while Mtf1 induces the expression of fungal effector genes and tomato pathogenesis-related protein genes. The levels of pipecolic and salicylic acids functioning in tomato defense signaling against (hemi-) biotrophic pathogens depend on the presence of MTF1, which promotes the formation of resting structures at the end of the infection cycle. In summary, the presence of VTA3 alters gene expression of virulence factors and tames the Mtf1 genetic subnetwork for late stages of plant disease progression and subsequent survival of the fungus in the soil. Author summary: Verticillium dahliae causes significant economic losses to a wide range of valuable crops worldwide. The fungus can overwinter in the soil for years until it infects the roots of suitable host plants and colonizes the xylem sap, resulting in plant disease. V. dahliae needs the transcriptional regulator Vta3 for colonization of the tomato xylem sap, where it promotes gene expression of the virulence factor Elv1 but reduces expression of the transcription factor Mtf1 for fungal virulence and development. We discovered that Vta3 induced ELV1 expression is exclusively important for virulence but not necessary for V. dahliae growth or spore production. Vta3 delays Mtf1 action, which triggers plant immune responses and is required for late stages of infection. In summary, the presence of VTA3 alters gene expression of virulence factors and suppresses the Mtf1 subnetwork for late stages of plant disease progression. At the end of the infection cycle, Mtf1 initiates the formation of resting structures that allow the fungus to survive in the soil and later to re-infect host plants. A better understanding of the genetic networks underlying V. dahliae development and virulence is essential for developing new strategies to control growth and distribution of the fungus in fields.
- Subjects
VERTICILLIUM dahliae; PLANT-fungus relationships; GENE expression; XYLEM; PLANT colonization; FUNGAL genes; TOMATOES
- Publication
PLoS Pathogens, 2023, Vol 18, Issue 1, p1
- ISSN
1553-7366
- Publication type
Article
- DOI
10.1371/journal.ppat.1011100