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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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Peramine biosynthesis loci (PER) in epichloae and the homologous loci in other Clavicipitaceae.On each map perA is color-coded blue for a complete gene and as an open box for perA-ΔR*. Domains of perA are indicated as A (adenylation), T (thiolation), C (condensation), M (N-methylation) and R* (reduction). Subscripts indicate postulated specificity of adenylation domains for 1-pyrroline-5-carboxylate (AP) and arginine (AR) [16]. Other features are indicated as in Figure 7.
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pgen-1003323-g010: Peramine biosynthesis loci (PER) in epichloae and the homologous loci in other Clavicipitaceae.On each map perA is color-coded blue for a complete gene and as an open box for perA-ΔR*. Domains of perA are indicated as A (adenylation), T (thiolation), C (condensation), M (N-methylation) and R* (reduction). Subscripts indicate postulated specificity of adenylation domains for 1-pyrroline-5-carboxylate (AP) and arginine (AR) [16]. Other features are indicated as in Figure 7.

Mentions: As was the case for the other alkaloid loci, the peramine (PER) locus was variable, containing the entire multifunctional perA gene in the peramine producers, no perA gene, or a partially deleted perA gene designated perA-ΔR* (Figure 10). The complete gene encodes a multifunctional protein with peptide synthetase, methyltransferase and reductase domains that together may be sufficient for synthesis of peramine [16]. The PER locus in E. festucae E2368 and E. typhina E5819 shared identical deletions of the C-terminal reductase domain. Nevertheless, perA-ΔR* was expressed in E2368, raising the possibility that this form also encodes a multifunctional protein, which may participate in the biosynthesis of a metabolite related to peramine if an appropriate thioesterase, condensation, cyclization or reduction domain is provided in trans.


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)

Peramine biosynthesis loci (PER) in epichloae and the homologous loci in other Clavicipitaceae.On each map perA is color-coded blue for a complete gene and as an open box for perA-ΔR*. Domains of perA are indicated as A (adenylation), T (thiolation), C (condensation), M (N-methylation) and R* (reduction). Subscripts indicate postulated specificity of adenylation domains for 1-pyrroline-5-carboxylate (AP) and arginine (AR) [16]. Other features are indicated as in Figure 7.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1003323-g010: Peramine biosynthesis loci (PER) in epichloae and the homologous loci in other Clavicipitaceae.On each map perA is color-coded blue for a complete gene and as an open box for perA-ΔR*. Domains of perA are indicated as A (adenylation), T (thiolation), C (condensation), M (N-methylation) and R* (reduction). Subscripts indicate postulated specificity of adenylation domains for 1-pyrroline-5-carboxylate (AP) and arginine (AR) [16]. Other features are indicated as in Figure 7.
Mentions: As was the case for the other alkaloid loci, the peramine (PER) locus was variable, containing the entire multifunctional perA gene in the peramine producers, no perA gene, or a partially deleted perA gene designated perA-ΔR* (Figure 10). The complete gene encodes a multifunctional protein with peptide synthetase, methyltransferase and reductase domains that together may be sufficient for synthesis of peramine [16]. The PER locus in E. festucae E2368 and E. typhina E5819 shared identical deletions of the C-terminal reductase domain. Nevertheless, perA-ΔR* was expressed in E2368, raising the possibility that this form also encodes a multifunctional protein, which may participate in the biosynthesis of a metabolite related to peramine if an appropriate thioesterase, condensation, cyclization or reduction domain is provided in trans.

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