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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 and Mycotoxin Research

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

Authors
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
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: December 31, 2012
Publication Date: February 28, 2013
Repository 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: 10/25/2014
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