TY - JOUR
T1 - Plant-Symbiotic Fungi as Chemical Engineers
T2 - Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci
AU - Schardl, Christopher L.
AU - Young, Carolyn A.
AU - Hesse, Uljana
AU - Amyotte, Stefan G.
AU - Andreeva, Kalina
AU - Calie, Patrick J.
AU - Fleetwood, Damien J.
AU - Haws, David C.
AU - Moore, Neil
AU - Oeser, Birgitt
AU - Panaccione, Daniel G.
AU - Schweri, Kathryn K.
AU - Voisey, Christine R.
AU - Farman, Mark L.
AU - Jaromczyk, Jerzy W.
AU - Roe, Bruce A.
AU - O'Sullivan, Donal M.
AU - Scott, Barry
AU - Tudzynski, Paul
AU - An, Zhiqiang
AU - Arnaoudova, Elissaveta G.
AU - Bullock, Charles T.
AU - Charlton, Nikki D.
AU - Chen, Li
AU - Cox, Murray
AU - Dinkins, Randy D.
AU - Florea, Simona
AU - Glenn, Anthony E.
AU - Gordon, Anna
AU - Güldener, Ulrich
AU - Harris, Daniel R.
AU - Hollin, Walter
AU - Jaromczyk, Jolanta
AU - Johnson, Richard D.
AU - Khan, Anar K.
AU - Leistner, Eckhard
AU - Leuchtmann, Adrian
AU - Li, Chunjie
AU - Liu, Jin Ge
AU - Liu, Jinze
AU - Liu, Miao
AU - Mace, Wade
AU - Machado, Caroline
AU - Nagabhyru, Padmaja
AU - Pan, Juan
AU - Schmid, Jan
AU - Sugawara, Koya
AU - Steiner, Ulrike
AU - Takach, Johanna E.
AU - Tanaka, Eiji
AU - Webb, Jennifer S.
AU - Wilson, Ella V.
AU - Wiseman, Jennifer L.
AU - Yoshida, Ruriko
AU - Zeng, Zheng
N1 - Funding Information:
We thank Richard M. Higashi and Teresa W. M. Fan of the University of Louisville Center for Regulatory and Environmental Analytical Metabolomics (supported by NSF EPSCoR grant EPS-0447479), together with Jerome R. Faulkner, University of Kentucky, and for identification of 1-acetamidopyrrolizidine; Abbe Kesterson and Alfred D. Byrd of the University of Kentucky Advanced Genetic Technologies Center for assistance in DNA sequencing; and John May of the University of Kentucky Environmental Research Training Laboratories for assistance in loline alkaloid analysis. This is publication number 13-12-004 of the Kentucky Agricultural Experiment Station, published with approval of the director.
PY - 2013/2
Y1 - 2013/2
N2 - The fungal family Clavicipitaceae includes plant symbionts and parasites that produce several psychoactive and bioprotective alkaloids. The family includes grass symbionts in the epichloae clade (Epichloë and Neotyphodium species), which are extraordinarily diverse both in their host interactions and in their alkaloid profiles. Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some-including the infamous ergot alkaloids-have potent effects on mammals. The exceptional chemotypic diversity of the epichloae may relate to their broad range of host interactions, whereby some are pathogenic and contagious, others are mutualistic and vertically transmitted (seed-borne), and still others vary in pathogenic or mutualistic behavior. We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids. Results indicated a strong tendency for alkaloid loci to have conserved cores that specify the skeleton structures and peripheral genes that determine chemical variations that are known to affect their pharmacological specificities. Generally, gene locations in cluster peripheries positioned them near to transposon-derived, AT-rich repeat blocks, which were probably involved in gene losses, duplications, and neofunctionalizations. The alkaloid loci in the epichloae had unusual structures riddled with large, complex, and dynamic repeat blocks. This feature was not reflective of overall differences in repeat contents in the genomes, nor was it characteristic of most other specialized metabolism loci. The organization and dynamics of alkaloid loci and abundant repeat blocks in the epichloae suggested that these fungi are under selection for alkaloid diversification. We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses.
AB - The fungal family Clavicipitaceae includes plant symbionts and parasites that produce several psychoactive and bioprotective alkaloids. The family includes grass symbionts in the epichloae clade (Epichloë and Neotyphodium species), which are extraordinarily diverse both in their host interactions and in their alkaloid profiles. Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some-including the infamous ergot alkaloids-have potent effects on mammals. The exceptional chemotypic diversity of the epichloae may relate to their broad range of host interactions, whereby some are pathogenic and contagious, others are mutualistic and vertically transmitted (seed-borne), and still others vary in pathogenic or mutualistic behavior. We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids. Results indicated a strong tendency for alkaloid loci to have conserved cores that specify the skeleton structures and peripheral genes that determine chemical variations that are known to affect their pharmacological specificities. Generally, gene locations in cluster peripheries positioned them near to transposon-derived, AT-rich repeat blocks, which were probably involved in gene losses, duplications, and neofunctionalizations. The alkaloid loci in the epichloae had unusual structures riddled with large, complex, and dynamic repeat blocks. This feature was not reflective of overall differences in repeat contents in the genomes, nor was it characteristic of most other specialized metabolism loci. The organization and dynamics of alkaloid loci and abundant repeat blocks in the epichloae suggested that these fungi are under selection for alkaloid diversification. We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses.
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U2 - 10.1371/journal.pgen.1003323
DO - 10.1371/journal.pgen.1003323
M3 - Article
C2 - 23468653
AN - SCOPUS:84874772540
SN - 1553-7390
VL - 9
JO - PLoS Genetics
JF - PLoS Genetics
IS - 2
M1 - e1003323
ER -
