Gene cluster conservation provides insight into cercosporin biosynthesis and extends production to the genus Colletotrichum

Ronnie de Jonge*, Malaika K. Ebert, Callie R. Huitt-Roehl, Paramita Pal, Jeffrey C. Suttle, Rebecca E. Spanner, Jonathan D. Neubauer, Wayne M. Jurick, Karina A. Stott, Gary A. Secor, Bart P.H.J. Thomma, Yves Van De Peer, Craig A. Townsend, Melvin D. Bolton

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

15 Citations (Scopus)

Abstract

Species in the genus Cercospora cause economically devastating diseases in sugar beet, maize, rice, soy bean, and other major food crops. Here, we sequenced the genome of the sugar beet pathogen Cercospora beticola and found it encodes 63 putative secondary metabolite gene clusters, including the cercosporin toxin biosynthesis (CTB) cluster. We show that the CTB gene cluster has experienced multiple duplications and horizontal transfers across a spectrum of plant pathogenic fungi, including the wide-host range Colletotrichum genus as well as the rice pathogen Magnaporthe oryzae. Although cercosporin biosynthesis has been thought to rely on an eight-gene CTB cluster, our phylogenomic analysis revealed gene collinearity adjacent to the established cluster in all CTB clusterharboring species. We demonstrate that the CTB cluster is larger than previously recognized and includes cercosporin facilitator protein, previously shown to be involved with cercosporin autoresistance, and four additional genes required for cercosporin biosynthesis, including the final pathway enzymes that install the unusual cercosporin methylenedioxy bridge. Lastly, we demonstrate production of cercosporin by Colletotrichum fioriniae, the first known cercosporin producer within this agriculturally important genus. Thus, our results provide insight into the intricate evolution and biology of a toxin critical to agriculture and broaden the production of cercosporin to another fungal genus containing many plant pathogens of important crops worldwide.

Original languageEnglish
Pages (from-to)E5459-E5466
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number24
DOIs
Publication statusPublished - 12 Jun 2018

Keywords

  • Cercospora
  • Cercosporin
  • Natural product
  • Perylenequinone
  • Secondary metabolism

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  • Research Output

    • 15 Citations
    • 1 Comment/Letter to the editor

    Erratum: Gene cluster conservation provides insight into cercosporin biosynthesis and extends production to the genus Colletotrichum

    De Jonge, R., Ebert, M. K., Huitt-Roehl, C. R., Pal, P., Suttle, J. C., Spanner, R. E., Neubauer, J. D., Jurick, W. M., Stott, K. A., Secor, G. A., Thomma, B. P. H. J., Van De Peer, Y., Townsend, C. A. & Bolton, M. D., 28 Aug 2018, In : Proceedings of the National Academy of Sciences of the United States of America. 115, 35, p. E8324

    Research output: Contribution to journalComment/Letter to the editorAcademic

    Open Access
  • Cite this

    de Jonge, R., Ebert, M. K., Huitt-Roehl, C. R., Pal, P., Suttle, J. C., Spanner, R. E., Neubauer, J. D., Jurick, W. M., Stott, K. A., Secor, G. A., Thomma, B. P. H. J., De Peer, Y. V., Townsend, C. A., & Bolton, M. D. (2018). Gene cluster conservation provides insight into cercosporin biosynthesis and extends production to the genus Colletotrichum. Proceedings of the National Academy of Sciences of the United States of America, 115(24), E5459-E5466. https://doi.org/10.1073/pnas.1712798115