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

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 - PLoS Genet. (2013)

Bottom Line: Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some-including the infamous ergot alkaloids-have potent effects on mammals.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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, USA. Schardl@uky.edu

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.

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Fine-mapping of repeats in two regions of the EAS clusters of epichloae.(A) The easE-easF-easG regions. (B) The dmaW-cloA-easC-easD regions. Genes are colored as in Figure 6. AT-rich repeats are in gray, and named or numbered to indicate relationships between repeats in the different species. MITEs are indicated by labeled vertical black bars. In some cases, the gene cluster orientation is different from those shown in Figure 6 to facilitate gene alignment. The Waru element is an autonomous parent element of MITE 8m.
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pgen-1003323-g011: Fine-mapping of repeats in two regions of the EAS clusters of epichloae.(A) The easE-easF-easG regions. (B) The dmaW-cloA-easC-easD regions. Genes are colored as in Figure 6. AT-rich repeats are in gray, and named or numbered to indicate relationships between repeats in the different species. MITEs are indicated by labeled vertical black bars. In some cases, the gene cluster orientation is different from those shown in Figure 6 to facilitate gene alignment. The Waru element is an autonomous parent element of MITE 8m.

Mentions: The EAS and IDT clusters of Claviceps species, P. ipomoeae and A. take had very little repeat DNA within them, although repeat blocks flanked the EAS clusters of C. fusiformis PRL 1980 and C. paspali RRC-1481 (Figure 6, Figure 7). These Claviceps strains had lost or inactivated one (C. paspali) or all (C. fusiformis) lysergyl peptide synthetase (lps) genes at the cluster periphery, but the conserved-gene cores of their EAS and IDT clusters remained nearly free of repeat sequences. In contrast, the epichloae all had long blocks of repeat sequences associated with their alkaloid gene loci, and (except for the EAS loci of E818, which were divided by a telomere) all EAS and IDT loci of epichloae were broken up further into subclusters by such long repeat blocks. Even within subclusters a large number of MITE insertions were evident in intergenic regions (Figure 11).


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

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 - PLoS Genet. (2013)

Fine-mapping of repeats in two regions of the EAS clusters of epichloae.(A) The easE-easF-easG regions. (B) The dmaW-cloA-easC-easD regions. Genes are colored as in Figure 6. AT-rich repeats are in gray, and named or numbered to indicate relationships between repeats in the different species. MITEs are indicated by labeled vertical black bars. In some cases, the gene cluster orientation is different from those shown in Figure 6 to facilitate gene alignment. The Waru element is an autonomous parent element of MITE 8m.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3585121&req=5

pgen-1003323-g011: Fine-mapping of repeats in two regions of the EAS clusters of epichloae.(A) The easE-easF-easG regions. (B) The dmaW-cloA-easC-easD regions. Genes are colored as in Figure 6. AT-rich repeats are in gray, and named or numbered to indicate relationships between repeats in the different species. MITEs are indicated by labeled vertical black bars. In some cases, the gene cluster orientation is different from those shown in Figure 6 to facilitate gene alignment. The Waru element is an autonomous parent element of MITE 8m.
Mentions: The EAS and IDT clusters of Claviceps species, P. ipomoeae and A. take had very little repeat DNA within them, although repeat blocks flanked the EAS clusters of C. fusiformis PRL 1980 and C. paspali RRC-1481 (Figure 6, Figure 7). These Claviceps strains had lost or inactivated one (C. paspali) or all (C. fusiformis) lysergyl peptide synthetase (lps) genes at the cluster periphery, but the conserved-gene cores of their EAS and IDT clusters remained nearly free of repeat sequences. In contrast, the epichloae all had long blocks of repeat sequences associated with their alkaloid gene loci, and (except for the EAS loci of E818, which were divided by a telomere) all EAS and IDT loci of epichloae were broken up further into subclusters by such long repeat blocks. Even within subclusters a large number of MITE insertions were evident in intergenic regions (Figure 11).

Bottom Line: Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some-including the infamous ergot alkaloids-have potent effects on mammals.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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, University of Kentucky, Lexington, Kentucky, USA. Schardl@uky.edu

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.

Show MeSH
Related in: MedlinePlus