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

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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 cluster-harboring 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.
Keywords
PHYLOGENETIC TREE SELECTION, BROWN LEAF-SPOT, PHOTOSENSITIZING TOXIN, POLYKETIDE SYNTHASE, FUNGAL VIRULENCE, SINGLET OXYGEN, NICOTIANAE, PATHOGEN, DISEASE, GENOME, natural product, perylenequinone, secondary metabolism, cercosporin, Cercospora

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MLA
de Jonge, Ronnie, et al. “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, vol. 115, no. 24, 2018, pp. E5459–66.
APA
de Jonge, R., Ebert, M. K., Huitt-Roehl, C. R., Pal, P., Suttle, J. C., Spanner, R. E., … 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.
Chicago author-date
Jonge, Ronnie de, Malaika K Ebert, Callie R Huitt-Roehl, Paramita Pal, Jeffrey C Suttle, Rebecca E Spanner, Jonathan D Neubauer, et al. 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): E5459–66.
Chicago author-date (all authors)
de Jonge, Ronnie, Malaika K Ebert, Callie R Huitt-Roehl, Paramita Pal, Jeffrey C Suttle, Rebecca E Spanner, Jonathan D Neubauer, Wayne M Jurick, II, Karina A Stott, Gary A Secor, Bart PHJ Thomma, Yves Van de Peer, Craig A Townsend, and Melvin D Bolton. 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.
Vancouver
1.
de Jonge R, Ebert MK, Huitt-Roehl CR, Pal P, Suttle JC, Spanner RE, et al. 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. 2018;115(24):E5459–66.
IEEE
[1]
R. de Jonge et al., “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, vol. 115, no. 24, pp. E5459–E5466, 2018.
@article{8567863,
  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 cluster-harboring 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.},
  author       = {de Jonge, Ronnie and Ebert, Malaika K and Huitt-Roehl, Callie R and Pal, Paramita and Suttle, Jeffrey C and Spanner, Rebecca E and Neubauer, Jonathan D and Jurick,, Wayne M, II and Stott, Karina A and Secor, Gary A and Thomma, Bart PHJ and Van de Peer, Yves and Townsend, Craig A and Bolton, Melvin D},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keywords     = {PHYLOGENETIC TREE SELECTION,BROWN LEAF-SPOT,PHOTOSENSITIZING TOXIN,POLYKETIDE SYNTHASE,FUNGAL VIRULENCE,SINGLET OXYGEN,NICOTIANAE,PATHOGEN,DISEASE,GENOME,natural product,perylenequinone,secondary metabolism,cercosporin,Cercospora},
  language     = {eng},
  number       = {24},
  pages        = {E5459--E5466},
  title        = {Gene cluster conservation provides insight into cercosporin biosynthesis and extends production to the genus Colletotrichum},
  url          = {http://dx.doi.org/10.1073/pnas.1712798115},
  volume       = {115},
  year         = {2018},
}

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