Plant defense compound triggers mycotoxin synthesis by regulating H2B ub1 and H3K4 me2/3 deposition

Authors: MA, TIANLING - Zhejiang University; ZHANG, LIXIN - Zhejiang University; WANG, MINHUI - Zhejiang University; LI, LIQING - Zhejiang University; JIAN, YUNQING - Zhejiang University; WU, LIANG - Zhejiang University; Kistler, Harold; MA, ZHONGHUA - Zhejiang University; YIN, YANNI - Zhejiang University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/31/2021
Publication Date: 9/4/2021
Citation: Ma, T., Zhang, L., Wang, M., Li, L., Jian, Y., Wu, L., Kistler, H.C., Ma, Z., Yin, Y. 2021. Plant defense compound triggers mycotoxin synthesis by regulating H2B ub1 and H3K4 me2/3 deposition. New Phytologist. 232(5):2106-2123. https://doi.org/10.1111/nph.17718.
DOI: https://doi.org/10.1111/nph.17718

Interpretive Summary: Certain fungi can be harmful not only because they cause destructive diseases on crop plants but also because they may contaminate food with harmful toxins. The fungus Fusarium graminearum causes head blight disease on wheat and barley and contaminates grain with a substance called vomitoxin. Novel approaches to control vomitoxin levels in grain are sought. This manuscript describes a team effort to look for how fungal genes for producing the vomitoxin are triggered by the plant. Plants normally respond to fungal infections by producing nitrogen-rich defense chemicals known as polyamines. The head blight pathogen responds to polyamines by producing a nitrogen-sensing protein which specifically binds to regions on the fungal chromosome containing the genes for vomitoxin production. Once there, the nitrogen-sensing protein modifies the resident fungal chromosomal proteins and by doing so, enables the genes for the toxin to be expressed. By understanding how toxin production is triggered by the plant, efforts now can turn to manipulation the signal pathway to keep vomitoxin levels low by keeping genes for toxin production turned off. Such an approach could reduce levels of vomitoxin in grain infected with the fungus.

Technical Abstract: Fusarium graminearum produces the mycotoxin deoxynivalenol (DON) which promotes its expansion during infection of its plant host, wheat. Conditional expression of DON production during infection is poorly characterized. In this study, we show that wheat produces the defense compound putrescine, which induces hyper-transcription of the DON biosynthetic genes (FgTRIs) and subsequently leads to DON accumulation during infection. Further, we find that transcription factor FgAreA regulates putrescine-mediated transcription of FgTRIs by facilitating the enrichment of histone H2B mono-ubiquitination (H2B ub1) and histone 3 lysine 4 di- and tri-methylations (H3K4 me2/3) on FgTRIs. Importantly, we identify a DNA-binding domain (bZIP) specifically within the Fusarium H2B ub1 E3 ligase Bre1, and show that the binding of this bZIP domain to FgTRIs depends upon FgAreA-mediated chromatin rearrangement. Interestingly, H2B ub1 regulates H3K4 me2/3 via the methyltransferase complex COMPASS component FgBre2, which is different from Saccharomyces cerevisiae. Taken together, our findings reveal the molecular mechanisms by which host-generated putrescine induces DON production during F. graminearum infection. Our results also provide a novel insight into the role of putrescine during phytopathogen-host interactions and broadens our knowledge of H2B ub1 biogenesis and crosstalk between H2B ub1 and H3K4 me2/3 in eukaryotes.