Final piece to the Fusarium pigmentation puzzle – Unraveling of the phenalenone biosynthetic pathway responsible for perithecial pigmentation in the Fusarium solani species complex

Authors: NIELSEN, MIKKEL - Aalborg University; SORENSEN, TRINE - Aalborg University; PEDERSEN, TOBIAS - Aalborg University; WESTPHAL, KLAUS - Aalborg University; DE QUINCOCES, LORENA D. - Aalborg University; SONDERGAARD, TEIS - Aalborg University; WIMMER, REINHARD - Aalborg University; Brown, Daren; SORENSEN, JENS - Aalborg University

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/4/2024
Publication Date: 7/14/2024
Citation: Nielsen, M.R., Sorensen, T., Pedersen, T.B., Westphal, K.R., Fernandez De Quincoces, L.D., Sondergaard, T.E., Wimmer, R., Brown, D.W., Sorensen, J.L. 2024. Final piece to the Fusarium pigmentation puzzle – Unraveling of the phenalenone biosynthetic pathway responsible for perithecial pigmentation in the Fusarium solani species complex. Fungal Genetics and Biology. https://doi.org/10.1016/j.fgb.2024.103912.
DOI: https://doi.org/10.1016/j.fgb.2024.103912

Interpretive Summary: Fusarium fungi cause disease on many different plants and can contaminate infected crops with toxins that are hazardous to livestock, pets and people. The U.S. and economies across the world suffer hundred-million-dollar losses each year due to toxin contaminated foods and feeds. A distinctive feature of some Fusarium is the color of their fruiting bodies. While most Fusarium produce dark fruiting bodies, others have a red color. Here we identified a cluster of genes in Fusarium vanettenii involved in the synthesis of the fruiting body pigment and characterized a new chemical, corymbiferan lactone F, that contributes to the red color. These results provide a new approach to distinguish between different Fusarium that cause different plant diseases and will be used by plant pathologists and other scientists to develop novel strategies to limit or control toxin contamination of grain to keep our food supply safe.

Technical Abstract: The Fusarium solani species complex (FSSC) is comprised of important pathogens of plants and humans. A distinctive feature of FSSC species is perithecial pigmentation. While the dark perithecial pigments of other Fusarium species are derived from fusarubins synthesized by polyketide synthase 12 (PKS12), the perithecial pigment of FSSC are derived from an unknown metabolite synthesized by PKS35. Here, we confirm in FSSC species Fusarium vanettenii that PKS35 (fsnI) is required for perithecial pigment synthesis by deletion analysis and that fsnI is closely related to phnA from Penicillium herquei, as well as duxI from Talaromyces stipentatus, which produce prephenalenone as an early intermediate in herqueinone and duclauxin synthesis respectively. The production of prephenalenone by expression of fsnI in Saccharomyces cerevisiae indicates that it is also an early intermediate in perithecial pigment synthesis. We next identified a conserved cluster of 10 genes flanking fsnI in F. vanettenii that when expressed in F. graminearum led to the production of a novel corymbiferan lactone F as a likely end product of the phenalenone biosynthetic pathway in FSSC.