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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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Remaining EAS genes and pseudogenes after independent losses in two E. bromicola isolates, AL0434 and AL0426/2. The AT-GC DNA contents are shown under the maps. Pseudogenes are represented by Ψ.
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toxins-07-01273-f007: Remaining EAS genes and pseudogenes after independent losses in two E. bromicola isolates, AL0434 and AL0426/2. The AT-GC DNA contents are shown under the maps. Pseudogenes are represented by Ψ.

Mentions: Pseudogenes and gene remnants have been identified within or adjacent to many of the described EAS clusters within the Clavicipitaceae. Most Epichloë species that are unable to produce ergot alkaloids lack functional EAS genes or only retain remnants of some EAS genes. For example, a remnant lpsA sequence is present in the genome sequences of E. amarillans strain E57, E. bromicola strain AL0434, and Epichloë coenophiala strains e4509, AR542 and AR584. Typically these lpsA remnants have multiple frameshifts, stop codons or both, and are flanked or even disrupted by AT-rich repeat sequences; or, in the case of E57, the gene is truncated at the telomere [24]. In comparison to E. bromicola strain AL0434, which has only an lpsA remnant, strain AL0426/2 has retained a greater number of EAS genes (Figure 7). The E. bromicola AL0426/2 genome assembly (www.endophyte.uky.edu) contains lpsB, easE, easF and easG (contig 634), but easE is a pseudogene in which part of the coding sequence is missing. Since dmaW and easC are also missing, the AL0426/2 isolate is not expected to produce ergot alkaloids. The identification of two independent EAS gene loss events in E. bromicola (strains AL0434 and AL0426/2) suggests that this species may have greater EAS diversity than is currently recognized, but E. bromicola strains capable of producing ergot alkaloids have not yet been identified [61].


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)

Remaining EAS genes and pseudogenes after independent losses in two E. bromicola isolates, AL0434 and AL0426/2. The AT-GC DNA contents are shown under the maps. Pseudogenes are represented by Ψ.
© Copyright Policy
Related In: Results  -  Collection

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

toxins-07-01273-f007: Remaining EAS genes and pseudogenes after independent losses in two E. bromicola isolates, AL0434 and AL0426/2. The AT-GC DNA contents are shown under the maps. Pseudogenes are represented by Ψ.
Mentions: Pseudogenes and gene remnants have been identified within or adjacent to many of the described EAS clusters within the Clavicipitaceae. Most Epichloë species that are unable to produce ergot alkaloids lack functional EAS genes or only retain remnants of some EAS genes. For example, a remnant lpsA sequence is present in the genome sequences of E. amarillans strain E57, E. bromicola strain AL0434, and Epichloë coenophiala strains e4509, AR542 and AR584. Typically these lpsA remnants have multiple frameshifts, stop codons or both, and are flanked or even disrupted by AT-rich repeat sequences; or, in the case of E57, the gene is truncated at the telomere [24]. In comparison to E. bromicola strain AL0434, which has only an lpsA remnant, strain AL0426/2 has retained a greater number of EAS genes (Figure 7). The E. bromicola AL0426/2 genome assembly (www.endophyte.uky.edu) contains lpsB, easE, easF and easG (contig 634), but easE is a pseudogene in which part of the coding sequence is missing. Since dmaW and easC are also missing, the AL0426/2 isolate is not expected to produce ergot alkaloids. The identification of two independent EAS gene loss events in E. bromicola (strains AL0434 and AL0426/2) suggests that this species may have greater EAS diversity than is currently recognized, but E. bromicola strains capable of producing ergot alkaloids have not yet been identified [61].

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