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


ABSTRACT: 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.

SUBMITTER: Schardl CL 

PROVIDER: S-EPMC3585121 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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

Schardl Christopher L CL   Young Carolyn A CA   Hesse Uljana U   Amyotte Stefan G SG   Andreeva Kalina K   Calie Patrick J PJ   Fleetwood Damien J DJ   Haws David C DC   Moore Neil N   Oeser Birgitt B   Panaccione Daniel G DG   Schweri Kathryn K KK   Voisey Christine R CR   Farman Mark L ML   Jaromczyk Jerzy W JW   Roe Bruce A BA   O'Sullivan Donal M DM   Scott Barry B   Tudzynski Paul P   An Zhiqiang Z   Arnaoudova Elissaveta G EG   Bullock Charles T CT   Charlton Nikki D ND   Chen Li L   Cox Murray M   Dinkins Randy D RD   Florea Simona S   Glenn Anthony E AE   Gordon Anna A   Güldener Ulrich U   Harris Daniel R DR   Hollin Walter W   Jaromczyk Jolanta J   Johnson Richard D RD   Khan Anar K AK   Leistner Eckhard E   Leuchtmann Adrian A   Li Chunjie C   Liu JinGe J   Liu Jinze J   Liu Miao M   Mace Wade W   Machado Caroline C   Nagabhyru Padmaja P   Pan Juan J   Schmid Jan J   Sugawara Koya K   Steiner Ulrike U   Takach Johanna E JE   Tanaka Eiji E   Webb Jennifer S JS   Wilson Ella V EV   Wiseman Jennifer L JL   Yoshida Ruriko R   Zeng Zheng Z  

PLoS genetics 20130228 2


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 exce  ...[more]

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