The fungal myosin I is essential for Fusarium toxisome formation

Guangfei Tang, Yun Chen, Jin Rong Xu, H. Corby Kistler, Zhonghua Ma

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93 Scopus citations

Abstract

Myosin-I molecular motors are proposed to function as linkers between membranes and the actin cytoskeleton in several cellular processes, but their role in the biosynthesis of fungal secondary metabolites remain elusive. Here, we found that the myosin I of Fusarium graminearum (FgMyo1), the causal agent of Fusarium head blight, plays critical roles in mycotoxin biosynthesis. Inhibition of myosin I by the small molecule phenamacril leads to marked reduction in deoxynivalenol (DON) biosynthesis. FgMyo1 also governs translation of the DON biosynthetic enzyme Tri1 by interacting with the ribosome-associated protein FgAsc1. Disruption of the ATPase activity of FgMyo1 either by the mutation E420K, down-regulation of FgMyo1 expression or deletion of FgAsc1 results in reduced Tri1 translation. The DON biosynthetic enzymes Tri1 and Tri4 are mainly localized to subcellular structures known as toxisomes in response to mycotoxin induction and the FgMyo1-interacting protein, actin, participates in toxisome formation. The actin polymerization disruptor latrunculin A inhibits toxisome assembly. Consistent with this observation, deletion of the actin-associated proteins FgPrk1 and FgEnd3 also results in reduced toxisome formation. Unexpectedly, the FgMyo1-actin cytoskeleton is not involved in biosynthesis of another secondary metabolite tested. Taken together, this study uncovers a novel function of myosin I in regulating mycotoxin biosynthesis in filamentous fungi.

Original languageEnglish (US)
Article numbere1006827
JournalPLoS pathogens
Volume14
Issue number1
DOIs
StatePublished - Jan 2018

Bibliographical note

Funding Information:
This research was supported by the National Natural Science Fund for Distinguished Young Scholar (31525020) to ZM, National Science Foundation (31672064) to YC, Natural Science Foundation of Zhejiang Province for Distinguished Young Scholar (LR17C140001) to YC, China Agriculture Research System (CARS-3-1-15) to ZM, the Fundamental Research Funds for the Central Universities (2017FZA6014) to ZM, and Dabeinong Funds for Discipline Development and Talent Training in Zhejiang University to ZM. Further support was by award 2014-67013-21561 from the Agriculture and Food Research Initiative of the National Institute of Food and Agriculture, United States Department of Agriculture to HCK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Publisher Copyright:
© 2018 Tang et al.

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