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Genetics, genomics and evolution of ergot alkaloid diversity.

Young CA, Schardl CL, Panaccione DG, Florea S, Takach JE, Charlton ND, Moore N, Webb JS, Jaromczyk J - Toxins (Basel) (2015)

Bottom Line: The chromosome ends appear to be particularly effective engines for gene gains, losses and rearrangements, but not necessarily for neofunctionalization.Changes in gene expression could lead to accumulation of various pathway intermediates and affect levels of different ergot alkaloids.The huge structural diversity of ergot alkaloids probably represents adaptations to a wide variety of ecological situations by affecting the biological spectra and mechanisms of defense against herbivores, as evidenced by the diverse pharmacological effects of ergot alkaloids used in medicine.

View Article: PubMed Central - PubMed

Affiliation: Forage Improvement Division, The Samuel Roberts Noble Foundation, Ardmore, OK 73401, USA. cayoung@noble.org.

ABSTRACT
The ergot alkaloid biosynthesis system has become an excellent model to study evolutionary diversification of specialized (secondary) metabolites. This is a very diverse class of alkaloids with various neurotropic activities, produced by fungi in several orders of the phylum Ascomycota, including plant pathogens and protective plant symbionts in the family Clavicipitaceae. Results of comparative genomics and phylogenomic analyses reveal multiple examples of three evolutionary processes that have generated ergot-alkaloid diversity: gene gains, gene losses, and gene sequence changes that have led to altered substrates or product specificities of the enzymes that they encode (neofunctionalization). The chromosome ends appear to be particularly effective engines for gene gains, losses and rearrangements, but not necessarily for neofunctionalization. Changes in gene expression could lead to accumulation of various pathway intermediates and affect levels of different ergot alkaloids. Genetic alterations associated with interspecific hybrids of Epichloë species suggest that such variation is also selectively favored. The huge structural diversity of ergot alkaloids probably represents adaptations to a wide variety of ecological situations by affecting the biological spectra and mechanisms of defense against herbivores, as evidenced by the diverse pharmacological effects of ergot alkaloids used in medicine.

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Phylogeny of dmaW genes of Epichloë strains. The phylogenetic tree was inferred by maximum likelihood on a nucleotide alignment of coding sequences. Methods are as in Figure 3. The dmaW alleles are distinguished in hybrids that possess more than one copy with a letter that refers to the ancestral progenitor (a = E. amarillans, b = E. baconii-related Lolium associated Epichloë subclade, e = E. elymi, f = E. festucae, m = E. mollis-related and p = E. typhina subsp. poae. The dmaW gene of E. inebrians has been omitted in this analysis because the gene and EAS locus is more similar to that of P. ipomoeae than to those of other Epichloë species (see Figure 3).
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toxins-07-01273-f008: Phylogeny of dmaW genes of Epichloë strains. The phylogenetic tree was inferred by maximum likelihood on a nucleotide alignment of coding sequences. Methods are as in Figure 3. The dmaW alleles are distinguished in hybrids that possess more than one copy with a letter that refers to the ancestral progenitor (a = E. amarillans, b = E. baconii-related Lolium associated Epichloë subclade, e = E. elymi, f = E. festucae, m = E. mollis-related and p = E. typhina subsp. poae. The dmaW gene of E. inebrians has been omitted in this analysis because the gene and EAS locus is more similar to that of P. ipomoeae than to those of other Epichloë species (see Figure 3).

Mentions: Compared to sexual strains or other haploids, the hybrid Epichloë species have a greater potential to contain EAS genes because each of the ancestors contributes genetic information. In addition, variations of the EAS locus within a hybrid can be due to copy number or differences within the inherited EAS cluster (EASCC vs EASERP clusters). Some, but not all isolates from the hybrid species, Epichloë canadensis, E. coenophiala, and E. sp. FaTG-2, contain two EAS copies (Figure 8). The E. canadensis isolate e4815 contains two EAS clusters—EASERP for ERV and EASCC—that are representative of the two contributing ancestors, E. amarillans and E. elymi, respectively. In contrast, E. canadensis isolate CWR34 contains a single EASCC cluster, contributed by its E. elymi ancestor. Mating-type gene differences between E. canadensis isolates e4815 and CWR34 clearly indicate that they are the result of independent hybridizations, but it is unclear if CWR34 subsequently lost the E. amarillans EAS cluster, or if its particular ancestral strain of E. amarillans lacked EAS genes.


Genetics, genomics and evolution of ergot alkaloid diversity.

Young CA, Schardl CL, Panaccione DG, Florea S, Takach JE, Charlton ND, Moore N, Webb JS, Jaromczyk J - Toxins (Basel) (2015)

Phylogeny of dmaW genes of Epichloë strains. The phylogenetic tree was inferred by maximum likelihood on a nucleotide alignment of coding sequences. Methods are as in Figure 3. The dmaW alleles are distinguished in hybrids that possess more than one copy with a letter that refers to the ancestral progenitor (a = E. amarillans, b = E. baconii-related Lolium associated Epichloë subclade, e = E. elymi, f = E. festucae, m = E. mollis-related and p = E. typhina subsp. poae. The dmaW gene of E. inebrians has been omitted in this analysis because the gene and EAS locus is more similar to that of P. ipomoeae than to those of other Epichloë species (see Figure 3).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4417967&req=5

toxins-07-01273-f008: Phylogeny of dmaW genes of Epichloë strains. The phylogenetic tree was inferred by maximum likelihood on a nucleotide alignment of coding sequences. Methods are as in Figure 3. The dmaW alleles are distinguished in hybrids that possess more than one copy with a letter that refers to the ancestral progenitor (a = E. amarillans, b = E. baconii-related Lolium associated Epichloë subclade, e = E. elymi, f = E. festucae, m = E. mollis-related and p = E. typhina subsp. poae. The dmaW gene of E. inebrians has been omitted in this analysis because the gene and EAS locus is more similar to that of P. ipomoeae than to those of other Epichloë species (see Figure 3).
Mentions: Compared to sexual strains or other haploids, the hybrid Epichloë species have a greater potential to contain EAS genes because each of the ancestors contributes genetic information. In addition, variations of the EAS locus within a hybrid can be due to copy number or differences within the inherited EAS cluster (EASCC vs EASERP clusters). Some, but not all isolates from the hybrid species, Epichloë canadensis, E. coenophiala, and E. sp. FaTG-2, contain two EAS copies (Figure 8). The E. canadensis isolate e4815 contains two EAS clusters—EASERP for ERV and EASCC—that are representative of the two contributing ancestors, E. amarillans and E. elymi, respectively. In contrast, E. canadensis isolate CWR34 contains a single EASCC cluster, contributed by its E. elymi ancestor. Mating-type gene differences between E. canadensis isolates e4815 and CWR34 clearly indicate that they are the result of independent hybridizations, but it is unclear if CWR34 subsequently lost the E. amarillans EAS cluster, or if its particular ancestral strain of E. amarillans lacked EAS genes.

Bottom Line: The chromosome ends appear to be particularly effective engines for gene gains, losses and rearrangements, but not necessarily for neofunctionalization.Changes in gene expression could lead to accumulation of various pathway intermediates and affect levels of different ergot alkaloids.The huge structural diversity of ergot alkaloids probably represents adaptations to a wide variety of ecological situations by affecting the biological spectra and mechanisms of defense against herbivores, as evidenced by the diverse pharmacological effects of ergot alkaloids used in medicine.

View Article: PubMed Central - PubMed

Affiliation: Forage Improvement Division, The Samuel Roberts Noble Foundation, Ardmore, OK 73401, USA. cayoung@noble.org.

ABSTRACT
The ergot alkaloid biosynthesis system has become an excellent model to study evolutionary diversification of specialized (secondary) metabolites. This is a very diverse class of alkaloids with various neurotropic activities, produced by fungi in several orders of the phylum Ascomycota, including plant pathogens and protective plant symbionts in the family Clavicipitaceae. Results of comparative genomics and phylogenomic analyses reveal multiple examples of three evolutionary processes that have generated ergot-alkaloid diversity: gene gains, gene losses, and gene sequence changes that have led to altered substrates or product specificities of the enzymes that they encode (neofunctionalization). The chromosome ends appear to be particularly effective engines for gene gains, losses and rearrangements, but not necessarily for neofunctionalization. Changes in gene expression could lead to accumulation of various pathway intermediates and affect levels of different ergot alkaloids. Genetic alterations associated with interspecific hybrids of Epichloë species suggest that such variation is also selectively favored. The huge structural diversity of ergot alkaloids probably represents adaptations to a wide variety of ecological situations by affecting the biological spectra and mechanisms of defense against herbivores, as evidenced by the diverse pharmacological effects of ergot alkaloids used in medicine.

Show MeSH