The Verticillium dahliae Sho1-MAPK pathway regulates melanin biosynthesis and is required for cotton infection

Authors: LI, JUN-JIAO - Chinese Academy Of Agricultural Sciences; ZHOU, LEI - Chinese Academy Of Agricultural Sciences; YIN, CHUN-MEI - Chinese Academy Of Agricultural Sciences; ZHANG, DAN-DAN - Chinese Academy Of Agricultural Sciences; Klosterman, Steven; WANG, BAO-LI - Chinese Academy Of Agricultural Sciences; SONG, JIAN - Chinese Academy Of Agricultural Sciences; WANG, DAN - Chinese Academy Of Agricultural Sciences; HU, XIAOPING - Northwest A&f University; SUBBARAO, KRISHNA - University Of California; CHEN, JIE-YIN - Chinese Academy Of Agricultural Sciences; DAI, XIAO-FENG - Chinese Academy Of Agricultural Sciences

Submitted to: Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/28/2019
Publication Date: 11/24/2019
Citation: Li, J.-J., Zhou, L., Yin, C.-M., Zhang, D.-D., Klosterman, S.J., Wang, B.-L., Song, J., Wang, D., Hu, X.-P., Subbarao, K.V., Chen, J.-Y., Dai, X.-F. 2019. The Verticillium dahliae Sho1-MAPK pathway regulates melanin biosynthesis and is required for cotton infection. Environmental Microbiology. 21(12):4852-4874. https://doi.org/10.1111/1462-2920.14846.
DOI: https://doi.org/10.1111/1462-2920.14846

Interpretive Summary: The fungus Verticillium dahliae is a soilborne plant pathogen that penetrates plant roots, invades the water conducting xylem tissue of the plant to cause wilt. This work characterizes signaling mechanisms in the pathogen required for penetration on surfaces of cellophane membranes, which mimic harder surfaces of plant cell walls. This research shows that the same mechanism is required for full pathogenicity on plants. The work provides concrete evidence for the roles of four proteins of Vst50, Vst11, Vst7, and Sho1 in cellophane membrane penetration and pathogenesis. The work also illustrates a correlation between melanin production in the fungus and membrane penetration, and further that melanin may be directly involved in the penetration of two strains of V. dahliae since two melanin biosynthetic pathway inhibitors prevented cellophane membrane penetration. This study dissects role of several genes in V. dahliae whose products play roles in regulating signaling for plant penetration and for survival, and knowledge on how these products function may be useful to devise alternative approaches to kill or inhibit the fungus for disease control.

Technical Abstract: Verticillium dahliae is a soil-borne fungus that causes vascular wilt on numerous plants worldwide. The fungus survives in the soil for up to 14'years by producing melanized microsclerotia. The protective function of melanin in abiotic stresses is well documented. Here, we found that the V. dahliae tetraspan transmembrane protein VdSho1, a homolog of the Saccharomyces cerevisiae Sho1, acts as an osmosensor, and is required for plant penetration and melanin biosynthesis. The deletion mutant 'Sho1 was incubated on a cellophane membrane substrate that mimics the plant epidermis, revealing that the penetration of 'Sho1 strain was reduced compared to the wild-type strain. Furthermore, VdSho1 regulates melanin biosynthesis by a signalling mechanism requiring a kinase-kinase signalling module of Vst50-Vst11-Vst7. Strains, 'Vst50, 'Vst7 and 'Vst11 also displayed defective penetration and melanin production like the 'Sho1 strain. Defects in penetration and melanin production in 'Sho1 were restored by overexpression of Vst50, suggesting that Vst50 lies downstream of VdSho1 in the regulatory pathway governing penetration and melanin biosynthesis. Data analyses revealed that the transmembrane portion of VdSho1 was essential for both membrane penetration and melanin production. This study demonstrates that Vst50-Vst11-Vst7 module regulates VdSho1-mediated plant penetration and melanin production in V. dahliae, contributing to virulence.