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

Author
item SCHARDL, CHRISTOPHER - University Of Kentucky
item YOUNG, CAROLYN - Samuel Roberts Noble Foundation, Inc
item HESSE, ULJANA - University Of The Western Cape
item JAROMCZYK, JERZY - University Of Kentucky
item FARMAN, MARK - University Of Kentucky
item TUDZYNSKI, PAUL - Wilhelms University
item ROE, BRUCE - University Of Oklahoma
item AMYOTTE, STEFAN - University Of Ottawa
item AN, ZHIQIANG - University Of Texas Health Science Center
item ANDREEVA, KALINA - University Of California
item ARNAOUDOVA, ELISSAVETA - University Of Kentucky
item BULLOCK, CHARLES - University Of Kentucky
item CALIE, PATRICK - Eastern Kentucky University
item CHARLTON, NIKKI - Samuel Roberts Noble Foundation, Inc
item CHEN, LI - Non ARS Employee
item FLEETWOOD, DAMIEN - Agresearch
item FLOREA, SIMONA - University Of Kentucky
item GULDENER, ULRICH - Institute For Bioinformatics - Germany
item HARRIS, DANIEL - University Of Kentucky
item HAWS, DAVID - University Of Kentucky
item JAROMCZYK, JOLANTA - University Of Kentucky
item JOHNSON, RICHARD - Agresearch
item KHAN, ANAR - Agresearch
item LIU, JINZE - University Of Kentucky
item Liu, Miao
item MACHADO, CAROLINE - Indiana University
item MOORE, NEIL - University Of Kentucky
item NAGABHYRU, PADMAJA - University Of Kentucky
item OESER, BIRGITT - Wilhelms University
item PAN, JUAN - University Of Kentucky
item PANACCIONE, DANIEL - West Virginia University
item SCHMID, JAN - Massey University
item SCHWERI, KATHRYN - North Carolina State University
item SCOTT, BARRY - Massey University
item SUGAWARA, KOYA - National Agricultural Research Organization - Japan (NARO)
item TAKACH, JOHANNA - Samuel Roberts Noble Foundation, Inc
item VOISEY, CHRISTINE - Agresearch
item WEBB, JENNIFER - University Of Kentucky
item WISEMAN, JENNIFER - Life Technologies Corporation
item ZENG, ZHENG - University Of Kentucky
item COX, MURRAY - Massey University
item Dinkins, Randy
item Glenn, Anthony - Tony
item GORDON, ANNA - National Institute Of Agricultural Botany (NIAB)
item HOLLIN, WALTER - University Of Kentucky
item LEISTNER, ECKHARD
item LEUCHTMANN, ADRIAN - Eth Zurich
item LI, CHUNJIE - Lanzhou University
item MACE, WADE - Agresearch
item O'SULLIVAN, DONAL - National Institute Of Agricultural Botany (NIAB)
item STEINER, ULRIKE
item TANAKA, EIJI - Ishikawa Prefectural University
item WILSON, ELLA - Non ARS Employee
item YOSHIDA, RURIKO - University Of Kentucky

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/31/2012
Publication Date: 2/28/2013
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.