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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 AMYOTTE, STEFAN - University Of Ottawa
item ANDREEVA, KALINA - University Of California
item CALIE, PATRICK - Eastern Kentucky University
item FLEETWOOD, DAMIEN - Agresearch
item HAWS, DAVID - University Of Kentucky
item MOORE, NEIL - University Of Kentucky
item OESER, BIRGITT - University Of Munster
item PANACCIONE, DANIEL - West Virginia University
item SCHWERI, KATHRYN - North Carolina State University
item VOISEY, CHRISTINE - Agresearch
item FARMAN, MARK - University Of Kentucky
item JAROMCZYK, JERZY - University Of Kentucky
item ROE, BRUCE - University Of Oklahoma
item O'SULLIVAN, DONAL - National Institute Of Agricultural Botany (NIAB)
item SCOTT, BARRY - Massey University
item TUDZYNSKI, PAUL - University Of Munster
item AN, ZHIQIANG - University Of Texas Health Science Center
item ARNAOUDOVA, ELISSAVETA - University Of Kentucky
item BULLOCK, CHARLES - University Of Kentucky
item CHARLTON, NIKKI - Samuel Roberts Noble Foundation, Inc
item CHEN, LI - University Of Kentucky
item COX, MURRAY - Massey University
item Dinkins, Randy
item FLOREA, SIMONA - University Of Kentucky
item Glenn, Anthony - Tony
item GORDON, ANNA - National Institute Of Agricultural Botany (NIAB)
item GULDENER, ULRICH - Institute For Bioinformatics - Germany
item HARRIS, DANIEL - University Of Kentucky
item HOLLIN, WALTER - University Of Kentucky
item JAROMCZYK, JOLANTA - University Of Kentucky
item JOHNSON, RICHARD - Agresearch
item KHAN, ANAR - Agresearch
item LEISTNER, ECKHARD - Universitat Bonn
item LEUCHTMANN, ADRIAN - Eth Zurich
item LI, CHUNJIE - Lanzhou University
item LIU, JINGE - University Of Kentucky
item LIU, JINZE - University Of Kentucky
item LIU, MIAO - University Of Kentucky
item MACE, WADE - Agresearch
item MACHADO, CAROLINE - Indiana University
item NAGABHYRU, PADMAJA - University Of Kentucky
item PAN, JUAN - University Of Kentucky
item SCHMID, JAN - Massey University
item SUGAWARA, KOYA - National Agricultural Research Organization - Japan (NARO)
item STEINER, ULRIKE - Universitat Bonn
item TAKACH, JOHANNA - Samuel Roberts Noble Foundation, Inc
item TANAKA, EIJI - Ishikawa Prefectural University
item WEBB, JENNIFER - University Of Kentucky
item WILSON, ELLA - University Of North Carolina
item WISEMAN, JENNIFER - Life Technologies Corporation
item YOSHIDA, RURIKO - University Of Kentucky
item ZENG, SHENG - 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., Calie, P.J., Fleetwood, D.J., Haws, D.C., Moore, N., Oeser, B., Panaccione, D.G., Schweri, K.K., Voisey, C.R., Farman, M.L., Jaromczyk, J.W., Roe, B.A., O'Sullivan, D.M., Scott, B., Tudzynski, P., An, Z., Arnaoudova, E., Bullock, C.T., Charlton, N.D., Chen, L., Cox, M., Dinkins, R.D., Florea, S., Glenn, A.E., Gordon, A., Guldener, U., Harris, D.R., Hollin, W., Jaromczyk, J., Johnson, R.D., Khan, A.K., Leistner, E., Leuchtmann, A., Li, C., Liu, J., Liu, J., Liu, M., Mace, W., Machado, C., Nagabhyru, P., Pan, J., Schmid, J., Sugawara, K., Steiner, U., Takach, J.E., Tanaka, E., Webb, J.S., Wilson, E., Wiseman, J., Yoshida, R., Zeng, S. 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 parasites that produce several potent psychoactive and bioprotective alkaloids. The family includes grass-symbiotic epichloae (Epichloë and Neotyphodium species), which have highly diverse chemotypes with four distinct classes of anti-insect and anti-mammalian alkaloids. Epichloae also vary widely in host-interactions, some being pathogenic and contagious, and others being mutualistic and vertically transmitted (seed-borne). We sequenced genomes of seven epichloae, two related symbionts, and three ergot fungi, and compared their alkaloid gene clusters. The clusters tend to have conserved cores that specify the alkaloid skeleton structures, and peripheral genes for variations affecting pharmacological specificities. In contrast to most secondary metabolite gene clusters, the alkaloid loci have large retroelement-derived repeat-arrays, especially in the epichloae. Such repeats can facilitate gene rearrangements, deletions, duplications and neofunctionalization, suggesting that epichloae 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 parasites that produce several potent psychoactive and bioprotective alkaloids. The family includes grass-symbiotic epichloae (Epichloë and Neotyphodium species), which have highly diverse chemotypes with four distinct classes of anti-insect and anti-mammalian alkaloids. Epichloae also vary widely in host-interactions, some being pathogenic and contagious, and others being mutualistic and vertically transmitted (seed-borne). We sequenced genomes of seven epichloae, two related symbionts, and three ergot fungi, and compared their alkaloid gene clusters. The clusters tend to have conserved cores that specify the alkaloid skeleton structures, and peripheral genes for variations affecting pharmacological specificities. In contrast to most secondary metabolite gene clusters, the alkaloid loci have large retroelement-derived repeat-arrays, especially in the epichloae. Such repeats can facilitate gene rearrangements, deletions, duplications and neofunctionalization, suggesting that epichloae are under selection for alkaloid diversification, perhaps due to their highly variable life histories and protective roles.