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PMID: 23468653 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

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

PLoS genetics ·Vol. 9 ·No. 2 ·2013-00-00 ·Pages e1003323

Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ, Fleetwood DJ, Haws DC, Moore N, Oeser B, Panaccione DG, Schweri KK, Voisey CR, Farman ML, Jaromczyk JW, Roe BA, O'Sullivan DM, Scott B, Tudzynski P, An Z, Arnaoudova EG, Bullock CT, Charlton ND, Chen L, Cox M, Dinkins RD, Florea S, Glenn AE, Gordon A, Güldener U, Harris DR, Hollin W, Jaromczyk J, Johnson RD, Khan AK, 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 JE, Tanaka E, Webb JS, Wilson EV, Wiseman JL, Yoshida R, Zeng Z

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.

MeSH Terms
Alkaloids/chemistry,classification,genetics,metabolism Claviceps/genetics,metabolism,pathogenicity Epichloe/genetics,metabolism,pathogenicity Ergot Alkaloids/genetics,metabolism Gene Expression Regulation, Fungal Hypocreales/genetics,metabolism Neotyphodium Poaceae/genetics,metabolism,parasitology Selection, Genetic Symbiosis/genetics
Chemicals
Alkaloids Ergot Alkaloids
Authors & Affiliations
55 authors, click to expand affiliations / ORCID
Schardl Christopher L
Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, USA. [email protected]
Young Carolyn A
Hesse Uljana
Amyotte Stefan G
Andreeva Kalina
Calie Patrick J
Fleetwood Damien J
Haws David C
Moore Neil
Oeser Birgitt
Panaccione Daniel G
Schweri Kathryn K
Voisey Christine R
Farman Mark L
Jaromczyk Jerzy W
Roe Bruce A
O'Sullivan Donal M
Scott Barry
Tudzynski Paul
An Zhiqiang
Arnaoudova Elissaveta G
Bullock Charles T
Charlton Nikki D
Chen Li
Cox Murray
Dinkins Randy D
Florea Simona
Glenn Anthony E
Gordon Anna
Güldener Ulrich
Harris Daniel R
Hollin Walter
Jaromczyk Jolanta
Johnson Richard D
Khan Anar K
Leistner Eckhard
Leuchtmann Adrian
Li Chunjie
Liu JinGe
Liu Jinze
Liu Miao
Mace Wade
Machado Caroline
Nagabhyru Padmaja
Pan Juan
Schmid Jan
Sugawara Koya
Steiner Ulrike
Takach Johanna E
Tanaka Eiji
Webb Jennifer S
Wilson Ella V
Wiseman Jennifer L
Yoshida Ruriko
Zeng Zheng
Conflict of Interest

The authors have declared that no competing interests exist.

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Article Info
Journal
PLoS genetics
Abbr.
PLoS Genet
ISSN
1553-7404
DOI
10.1371/journal.pgen.1003323
Email
[email protected]
Published
2013-00-00
Epub
2013-00-28
Pages
e1003323
Language
English
Region
United States
NLM ID
101239074
PMCID
PMC3585121
Subset
IM
Grants
NCRR NIH HHS · P20 RR016481 · United States
Biotechnology and Biological Sciences Research Council · BB/G020418/1 · United Kingdom
NCRR NIH HHS · 2 P20 RR-16481 · United States
NIGMS NIH HHS · R01GM086888 · United States
NHGRI NIH HHS · R01 HG006272 · United States
NIGMS NIH HHS · R01 GM086888 · United States
External Links
PubMed source DOI: 10.1371/journal.pgen.1003323 PMC Full Text View journal details
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