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United States Department of Agriculture

Agricultural Research Service

Research Project: Control of Toxic Endophytic Fungi with Bacterial Endophytes and Regulation of Bacterial Metabolites for Novel Uses in Food Safety

Location: Toxicology & Mycotoxin Research

Title: Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci)

Author
item Schardl, Christopher
item Young, Carolyn
item Hesse, Uljana
item Jaromczyk, Jerzy
item Farman, Mark
item Tudzynski, Paul
item Roe, Bruce
item Amyotte, Stefan
item An, Zhiqiang
item Andreeva, Kalina
item Arnaoudova, Elissaveta
item Bullock, Charles
item Calie, Patrick
item Charlton, Nikki
item Chen, Li
item Fleetwood, Damien
item Florea, Simona
item Guldener, Ulrich
item Harris, Daniel
item Haws, David
item Jaromczyk, Jolanta
item Johnson, Richard
item Khan, Anar
item Liu, Jinze
item Liu, Miao
item Machado, Caroline
item Moore, Neil
item Nagabhyru, Padmaja
item Oeser, Birgitt
item Pan, Juan
item Panaccione, Daniel
item Schmid, Jan
item Schweri, Kathryn
item Scott, Barry
item Sugawara, Koya
item Takach, Johanna
item Voisey, Christine
item Webb, Jennifer
item Wiseman, Jennifer
item Zeng, Zheng
item Cox, Murray
item Dinkins, Randy
item Glenn, Anthony - Tony
item Gordon, Anna
item Hollin, Walter
item Leistner, Eckhard
item Leuchtmann, Adrian
item Li, Chunjie
item Mace, Wade
item O'sullivan, Donal
item Steiner, Ulrike
item Tanaka, Eiji
item Wilson, Ella
item Yoshida, Ruriko

Submitted to: PLoS Genetics
Publication Type: Peer reviewed journal
Publication Acceptance Date: 12/31/2012
Publication Date: 2/28/2013
Publication URL: http://handle.nal.usda.gov/10113/55847
Citation: Schardl, C.L., Young, C.A., Hesse, U., Amyotte, S.G., Andreeva, K., et al. 2013. Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genetics. 9(2):e1003323. DOI:10.1371/journal.pgen.1003323.

Interpretive Summary: The fungal family Clavicipitaceae includes plant symbionts and pathogens that produce neurotropic alkaloids with diverse effects on vertebrate and invertebrate animals. For example, ergot alkaloids are historically linked to mass poisonings (St. Anthony's fire) and sociological effects such as the Salem witch trials and the drug culture (LSD is an ergoline derivative). Ergot alkaloids in various forms also have medical uses ranging from treatment of Parkinsonism to aiding childbirth. Among the plant-associated Clavicipitaceae, Epichloë and Neotyphodium species deploy an especially wide variety of protective alkaloids within four major chemical classes: ergot alkaloids, indole-diterpenes, lolines, and peramine. Here we describe a comparative analysis of gene clusters for biosynthesis of alkaloids and other secondary metabolites among the Clavicipitaceae. We sequenced genomes of 12 Epichloë/Neotyphodium species, two related plant symbionts, and three Claviceps species, and compared their alkaloid biosynthetic gene clusters and alkaloid profiles. The alkaloid loci tended to have conserved cores with genes that specify skeleton structures, flanked by more variable genes for chemical modifications that yield the various forms within each alkaloid class. The alkaloid loci of the Epichloë and Neotyphodium species were riddled with very large arrays of retroelement-derived repeats. Such repeat arrays facilitate gene rearrangements, deletions, duplications, and neofunctionalizations, suggesting that these species are under selection for alkaloid diversification, perhaps due to their highly variable life histories and plant-protective roles.

Technical Abstract: The fungal family Clavicipitaceae includes plant symbionts and pathogens that produce neurotropic alkaloids with diverse effects on vertebrate and invertebrate animals. For example, ergot alkaloids are historically linked to mass poisonings (St. Anthony's fire) and sociological effects such as the Salem witch trials and the drug culture (LSD is an ergoline derivative), whereas ergot alkaloids in various forms have medical uses ranging from treatment of Parkinsonism to aiding childbirth. Because of their chemical analogies to biogenic amines, alkaloids typically affect animal nervous systems and deter herbivory. Among the plant-associated Clavicipitaceae, the epichloae (Epichloë and Neotyphodium species) deploy an especially wide variety of protective alkaloids within four major chemical classes: ergot alkaloids, indole-diterpenes, lolines, and peramine. Epichloae also have an extraordinary variety of host-interactions, whereby some are pathogenic and contagious, others are mutualistic and vertically transmitted (heritable), and others exhibit both mutualistic and pathogenic characteristics. Here we describe a comparative analysis of gene clusters for biosynthesis of alkaloids and other secondary metabolites among the epichloae and other Clavicipitaceae. We sequenced genomes of 12 epichloae, two related plant symbionts, and three ergot fungi (Claviceps species), and compared their alkaloid gene clusters and alkaloid profiles. The alkaloid loci tended to have conserved cores with genes that specify skeleton structures, flanked by more variable genes for chemical modifications that yield the various forms within each alkaloid class. In stark contrast to the alkaloid loci in other Clavicipitaceae, and to most other secondary-metabolite (SM) gene clusters, the alkaloid loci of the epichloae were riddled with very large arrays of retroelement-derived repeats. Such repeat arrays facilitate gene rearrangements, deletions, duplications, and neofunctionalizations, suggesting that epichloae are under selection for alkaloid diversification, perhaps due to their highly variable life histories and plant-protective roles.

Last Modified: 8/24/2016
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