A polyketide synthase from Verticillium dahliae modulates melanin biosynthesis and hyphal growth to promote virulence

Authors: LI, HUAN - Nanjing Forestry University; WANG, DAN - Chinese Academy Of Agricultural Sciences; ZHANG, DAN-DAN - Chinese Academy Of Agricultural Sciences; GENG, QI - Nanjing Forestry University; LI, JUN-JIAO - Liaoning Academy Of Agricultural Sciences; SHENG, RUO-CHENG - Nanjing Forestry University; XUE, HUI-SHAN - Chinese Academy Of Agricultural Sciences; ZHU, HE - Liaoning Academy Of Agricultural Sciences; KONG, ZHI-QIANG - Chinese Academy Of Agricultural Sciences; DAI, XIAO-FENG - Chinese Academy Of Agricultural Sciences; Klosterman, Steven; SUBBARAO, KRISHNA - University Of California; CHEN, FENG-MAO - Nanjing Forestry University; CHEN, JIE-YIN - Chinese Academy Of Agricultural Sciences

Submitted to: BMC Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/13/2022
Publication Date: 5/30/2022
Citation: Li, H., Wang, D., Zhang, D.D., Geng, Q., Li, J.J., Sheng, R.C., Xue, H.S., Zhu, H., Kong, Z.Q., Dai, X.F., Klosterman, S.J., Subbarao, K.V., Chen, F.M., Chen, J.Y. 2022. A polyketide synthase from Verticillium dahliae modulates melanin biosynthesis and hyphal growth to promote virulence. BMC Biology. 20. Article 125. https://doi.org/10.1186/s12915-022-01330-2.
DOI: https://doi.org/10.1186/s12915-022-01330-2

Interpretive Summary: Verticillium dahliae is a plant pathogenic fungus that penetrates plant roots, invades the water conducting xylem tissue of plants to cause disease symptoms of chlorosis and wilt. The fungus reproduces asexually by producing large numbers of short-lived conidia and survives long term in soils by producing survival structures known as microsclerotia, which are heavily melanized. In this study, we identified a gene in V. dahliae encoding a protein that that acts as a powerful negative regulator of microsclerotia and melanin production, and mutation of this gene also rendered the fungus defective in pathogenicity. Identification of the genes that control aspects of survival, asexual reproduction, and virulence in V. dahliae may lead to alternative control measures that inhibit its reproduction and formation of survival structures.

Technical Abstract: During the disease cycle, plant pathogenic fungi exhibit a morphological transition between hyphal growth (the phase of active infection) and the production of long-term survival structures that remain dormant during “overwintering.” Verticillium dahliae is a major plant pathogen that produces heavily melanized microsclerotia (MS) that survive in the soil for 14 or more years. These MS are multicellular structures produced during the necrotrophic phase of the disease cycle. Polyketide synthases (PKSs) are responsible for catalyzing production of many secondary metabolites including melanin. While MS contribute to long-term survival, hyphal growth is key for infection and virulence, but the signaling mechanisms by which the pathogen maintains hyphal growth are unclear. We analyzed the VdPKSs that contain at least one conserved domain potentially involved in secondary metabolism (SM), and screened the effect of VdPKS deletions in the virulent strain AT13. Among the five VdPKSs whose deletion affected virulence on cotton, we found that VdPKS9 acted epistatically to the VdPKS1-associated melanin pathway to promote hyphal growth. The decreased hyphal growth in VdPKS9 mutants was accompanied by the up-regulation of melanin biosynthesis and MS formation. Overexpression of VdPKS9 transformed melanized hyphaltype (MH-type) into the albinistic hyaline hyphal-type (AH-type), and VdPKS9 was upregulated in the AH-type population, which also exhibited higher virulence than the MH-type. We show that VdPKS9 is a powerful negative regulator of both melanin biosynthesis and MS formation in V. dahliae. These findings provide insight into the mechanism of how plant pathogens promote their virulence by the maintenance of vegetative hyphal growth during infection and colonization of plant hosts, and may provide novel targets for the control of melanin-producing filamentous fungi.