A phosphorylated transcription factor regulates sterol biosynthesis in Fusarium graminearum

Authors: LIU, ZUNYONG - Zhejiang University; JIAN, YUNQING - Zhejiang University; CHEN, YUN - Zhejiang University; Kistler, Harold; HE, PING - Texas A&M University; MA, ZHONGHUA - Zhejiang University; YIN, YANNI - Zhejiang University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/15/2019
Publication Date: 4/1/2019
Citation: Liu, Z., Jian, Y., Chen, Y., Kistler, H.C., He, P., Ma, Z., Yin, Y. 2019. A phosphorylated transcription factor regulates sterol biosynthesis in Fusarium graminearum. Nature Communications. https://doi.org/10.1038/s41467-019-09145-6.
DOI: https://doi.org/10.1038/s41467-019-09145-6

Interpretive Summary: Many fungicides that are used for control of plant diseases are chemicals that inhibit sterol synthesis in plant pathogenic fungi. Sterols are important compounds for the functioning of fungal cells and fungicides often target enzymes for specific steps in the fungal sterol biosynthetic pathway. Fungi can compensate for fungicide treatment simply by making more enzymes that make sterols. How fungi regulate these enzymes therefore is critical to understanding how fungi may become resistant to fungicide treatments. This work describes how fungi regulate the sterol synthesis pathway. Surprisingly, the sterol regulatory machinery for many fungal pathogens of plants is different than that for animals or for simple fungi such as yeast. This knowledge may be useful for designing fungicides that retain their ability to kill fungi even after multiple fungicide treatments.

Technical Abstract: In most eukaryotes, sterol biosynthesis is controlled by transcription factor sterol regulatory element binding protein (SREBP) or Upc2. Here, we however found that the SREBP and Upc2 orthologs are not involved in sterol biosynthesis in Fusarium graminearum. We identified a novel sterol regulator (hereafter named FgSR) in this fungus, and found FgSR forms a homodimer to bind its target gene promoters. Unexpectedly, FgSR is phosphorylated by the MAPKK kinase FgSsk2, and phosphorylated FgSR activates the transcription of sterol biosynthesis genes via recruiting the SWI/SNF complex to remodel chromatin at the target genes. Furthermore, we identified a 16-bp cis-element of FgSR that contains two conserved CGAA repeated sequences. Interestingly, FgSR orthologs exist only in Sordariomycetes and Leotiomycetes fungi. Additionally, FgSR also controls virulence mainly via modulating deoxynivalenol (DON) biosynthesis and responses to phytoalexin and DNA damage. Overall, this study uncovers a novel master regulator, FgSR that governs sterol biosynthesis and virulence in an important pathogenic fungus.