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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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Structures of the ergot alkaloid biosynthesis loci (EAS) in sequenced genomes.Tracks from top to bottom of each map represent the following: genes, repeats, MITEs, and graphs of AT (red) and GC (blue) contents. Each gene is represented by one or more boxes representing the coding sequences in exons, and an arrow indicating the direction of transcription. Double-slash marks (//) indicate sequence gaps within scaffolds of the assembled E. festucae genome sequences. Closed circles indicate telomeres, and distances from the telomere on the E. festucae map are indicated in kilobasepairs (kb). Cyan bars beneath each map represent repeat sequences, and are labeled with names or numbers to indicate relationships between repeats in the different species. Vertical bars beneath the repeat maps indicate MITEs. Gene names are abbreviated A through P for easA through easP, W for dmaW, and clo for cloA. Genes for synthesis of the ergoline ring system (skeleton) are shown in dark blue for the steps to chanoclavine-I (W, F, E, and C), and in light blue (D, A, and G) for steps to agroclavine. Genes for subsequent chemical decorations are shown in red (clo, H, O, P, lpsA, lpsB, and lpsC). Identifiable genes flanking the clusters are indicated in gray, and unfilled arrows indicate pseudogenes. The major pathway end-products for each strain are listed below each species name, abbreviated as indicated in Figure 2, and in bold for those confirmed in this study. Note that LAH is a reported product of C. paspali, but the sequenced strain is predicted not to synthesize it due to a defective easE gene.
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pgen-1003323-g006: Structures of the ergot alkaloid biosynthesis loci (EAS) in sequenced genomes.Tracks from top to bottom of each map represent the following: genes, repeats, MITEs, and graphs of AT (red) and GC (blue) contents. Each gene is represented by one or more boxes representing the coding sequences in exons, and an arrow indicating the direction of transcription. Double-slash marks (//) indicate sequence gaps within scaffolds of the assembled E. festucae genome sequences. Closed circles indicate telomeres, and distances from the telomere on the E. festucae map are indicated in kilobasepairs (kb). Cyan bars beneath each map represent repeat sequences, and are labeled with names or numbers to indicate relationships between repeats in the different species. Vertical bars beneath the repeat maps indicate MITEs. Gene names are abbreviated A through P for easA through easP, W for dmaW, and clo for cloA. Genes for synthesis of the ergoline ring system (skeleton) are shown in dark blue for the steps to chanoclavine-I (W, F, E, and C), and in light blue (D, A, and G) for steps to agroclavine. Genes for subsequent chemical decorations are shown in red (clo, H, O, P, lpsA, lpsB, and lpsC). Identifiable genes flanking the clusters are indicated in gray, and unfilled arrows indicate pseudogenes. The major pathway end-products for each strain are listed below each species name, abbreviated as indicated in Figure 2, and in bold for those confirmed in this study. Note that LAH is a reported product of C. paspali, but the sequenced strain is predicted not to synthesize it due to a defective easE gene.

Mentions: In the scaffolded assemblies of the C. purpurea and E. festucae Fl1 genomes, and the scaffolded E2368 assembly of 2010-06, the EAS genes were clustered within individual supercontigs (Figure 6). Also in the assemblies of C. fusiformis, C. paspali and P. ipomoeae genomes functional EAS genes were contained in single contigs. Other non-scaffolded assemblies had EAS genes in two or three contigs, but only in the case of E818 were the EAS genes unequivocally separated in two separate clusters. Long-range physical mapping of the EAS genes of E2368 confirmed that they were clustered (Figure S2).


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)

Structures of the ergot alkaloid biosynthesis loci (EAS) in sequenced genomes.Tracks from top to bottom of each map represent the following: genes, repeats, MITEs, and graphs of AT (red) and GC (blue) contents. Each gene is represented by one or more boxes representing the coding sequences in exons, and an arrow indicating the direction of transcription. Double-slash marks (//) indicate sequence gaps within scaffolds of the assembled E. festucae genome sequences. Closed circles indicate telomeres, and distances from the telomere on the E. festucae map are indicated in kilobasepairs (kb). Cyan bars beneath each map represent repeat sequences, and are labeled with names or numbers to indicate relationships between repeats in the different species. Vertical bars beneath the repeat maps indicate MITEs. Gene names are abbreviated A through P for easA through easP, W for dmaW, and clo for cloA. Genes for synthesis of the ergoline ring system (skeleton) are shown in dark blue for the steps to chanoclavine-I (W, F, E, and C), and in light blue (D, A, and G) for steps to agroclavine. Genes for subsequent chemical decorations are shown in red (clo, H, O, P, lpsA, lpsB, and lpsC). Identifiable genes flanking the clusters are indicated in gray, and unfilled arrows indicate pseudogenes. The major pathway end-products for each strain are listed below each species name, abbreviated as indicated in Figure 2, and in bold for those confirmed in this study. Note that LAH is a reported product of C. paspali, but the sequenced strain is predicted not to synthesize it due to a defective easE gene.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1003323-g006: Structures of the ergot alkaloid biosynthesis loci (EAS) in sequenced genomes.Tracks from top to bottom of each map represent the following: genes, repeats, MITEs, and graphs of AT (red) and GC (blue) contents. Each gene is represented by one or more boxes representing the coding sequences in exons, and an arrow indicating the direction of transcription. Double-slash marks (//) indicate sequence gaps within scaffolds of the assembled E. festucae genome sequences. Closed circles indicate telomeres, and distances from the telomere on the E. festucae map are indicated in kilobasepairs (kb). Cyan bars beneath each map represent repeat sequences, and are labeled with names or numbers to indicate relationships between repeats in the different species. Vertical bars beneath the repeat maps indicate MITEs. Gene names are abbreviated A through P for easA through easP, W for dmaW, and clo for cloA. Genes for synthesis of the ergoline ring system (skeleton) are shown in dark blue for the steps to chanoclavine-I (W, F, E, and C), and in light blue (D, A, and G) for steps to agroclavine. Genes for subsequent chemical decorations are shown in red (clo, H, O, P, lpsA, lpsB, and lpsC). Identifiable genes flanking the clusters are indicated in gray, and unfilled arrows indicate pseudogenes. The major pathway end-products for each strain are listed below each species name, abbreviated as indicated in Figure 2, and in bold for those confirmed in this study. Note that LAH is a reported product of C. paspali, but the sequenced strain is predicted not to synthesize it due to a defective easE gene.
Mentions: In the scaffolded assemblies of the C. purpurea and E. festucae Fl1 genomes, and the scaffolded E2368 assembly of 2010-06, the EAS genes were clustered within individual supercontigs (Figure 6). Also in the assemblies of C. fusiformis, C. paspali and P. ipomoeae genomes functional EAS genes were contained in single contigs. Other non-scaffolded assemblies had EAS genes in two or three contigs, but only in the case of E818 were the EAS genes unequivocally separated in two separate clusters. Long-range physical mapping of the EAS genes of E2368 confirmed that they were clustered (Figure S2).

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