Plant-Symbiotic Fungi as Chemical Engineers: Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci

Christopher L. Schardl, Carolyn A. Young, Uljana Hesse, Stefan G. Amyotte, Kalina Andreeva, Patrick J. Calie, Damien J. Fleetwood, David C. Haws, Neil Moore, Birgitt Oeser, Daniel G. Panaccione, Kathryn K. Schweri, Christine R. Voisey, Mark L. Farman, Jerzy W. Jaromczyk, Bruce A. Roe, Donal M. O'Sullivan, Barry Scott, Paul Tudzynski, Zhiqiang AnElissaveta G. Arnaoudova, Charles T. Bullock, Nikki D. Charlton, Li Chen, Murray Cox, Randy D. Dinkins, Simona Florea, Anthony E. Glenn, Anna Gordon, Ulrich Güldener, Daniel R. Harris, Walter Hollin, Jolanta Jaromczyk, Richard D. Johnson, Anar K. Khan, Eckhard Leistner, Adrian Leuchtmann, Chunjie Li, Jin Ge Liu, Jinze Liu, Miao Liu, Wade Mace, Caroline Machado, Padmaja Nagabhyru, Juan Pan, Jan Schmid, Koya Sugawara, Ulrike Steiner, Johanna E. Takach, Eiji Tanaka, Jennifer S. Webb, Ella V. Wilson, Jennifer L. Wiseman, Ruriko Yoshida, Zheng Zeng

Research output: Contribution to journalArticlepeer-review

297 Scopus citations

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.

Original languageEnglish
Article numbere1003323
JournalPLoS Genetics
Volume9
Issue number2
DOIs
StatePublished - Feb 2013

Bibliographical note

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.

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

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