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United States Department of Agriculture

Agricultural Research Service

Research Project: FORAGE SYSTEMS FOR SUSTAINABLE ANIMAL PRODUCTION IN THE MID-SOUTH

Location: Forage-Animal Production 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 Amyotte, Stefan -
item Andreeva, Kalina -
item Calie, Patrick -
item Fleetwood, Damien -
item Haws, David -
item Moore, Neil -
item Oeser, Birgitt -
item Panaccione, Daniel -
item Schweri, Kathryn -
item Voisey, Christine -
item Farman, Mark -
item Jaromczyk, Jerzy -
item Roe, Bruce -
item O'Sullivan, Donal -
item Scott, Barry -
item Tudzynski, Paul -
item An, Zhiqiang -
item Arnaoudova, Elissaveta -
item Bullock, Charles -
item Charlton, Nikki -
item Chen, Li -
item Cox, Murray -
item DINKINS, RANDY
item Florea, Simona -
item GLENN, ANTHONY
item Gordon, Anna -
item Guldener, Ulrich -
item Harris, Daniel -
item Hollin, Walter -
item Jaromczyk, Jolanta -
item Johnson, Richard -
item Khan, Anar -
item Leistner, Eckhard -
item Leuchtmann, Adrian -
item Li, Chunjie -
item Liu, Jinge -
item Liu, Jinze -
item Liu, Miao -
item Mace, Wade -
item Machado, Caroline -
item Nagabhyru, Padmaja -
item Pan, Juan -
item Schmid, Jan -
item Sugawara, Koya -
item Steiner, Ulrike -
item Takach, Johanna -
item Tanaka, Eiji -
item Webb, Jennifer -
item Wilson, Ella -
item Wiseman, Jennifer -
item Yoshida, Ruriko -
item Zeng, Sheng -

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: December 31, 2012
Publication Date: February 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.

Last Modified: 9/10/2014