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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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Structures of representative EAS loci showing synteny of EAS genes between species. Genes are colored to represent the stage of the pathway for the encoded product (see Figure 1 and Figure 2). Pseudogenes are represented by Ψ and white-filled arrows. Gray polygons link orthologous genes and gene blocks but are not meant to imply particular phylogenetic relationships. The EAS crown clade includes clusters from At. hypoxylon, B. obtecta, C. purpurea, C. fusiformis and P. ipomoeae.
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toxins-07-01273-f010: Structures of representative EAS loci showing synteny of EAS genes between species. Genes are colored to represent the stage of the pathway for the encoded product (see Figure 1 and Figure 2). Pseudogenes are represented by Ψ and white-filled arrows. Gray polygons link orthologous genes and gene blocks but are not meant to imply particular phylogenetic relationships. The EAS crown clade includes clusters from At. hypoxylon, B. obtecta, C. purpurea, C. fusiformis and P. ipomoeae.

Mentions: Although functional EAS genes are always clustered, they are not always in a single cluster, arrangements of the genes are not highly conserved, and locations of the clusters can vary, some being subterminal (near chromosome ends), and others being internal and flanked on both sides by long regions rich in housekeeping genes (Figure 10). With the exception of the Epichloë species (discussed below), the degree of divergence in EAS gene arrangements, gene contents, and the pathway end-products generally relates to the degree of divergence between species. Thus, it is unsurprising that the EAS cluster arrangements and gene contents differ greatly in comparison of N. fumigata to the Clavicipitaceae. A surprisingly consistent feature is the arrangement and close linkage of easE and easF in all except E. elymi E56; even their Ar. benhamiae orthologues, respectively designated ARB_4648 and ARB_4647, are adjacent but arranged tail to tail [18]. However, EAS gene arrangements and orientations are very similar in what we will call the “crown EAS clade” (Figure 3): Metarhizium spp. (including Metarhizium acridum, which is not shown), P. ipomoeae, B. obtecta, At. hypoxylon, Claviceps spp. and E. inebrians. Differences within the crown EAS clade were as follows: (1) an inversion of lpsB-easA segment in C. fusiformis relative to the others; (2) separation of the easH-lpsA segment from others in B. obtecta, due to an event that (based on remnant genes) occurred in a common ancestor of B. obtecta and At. hypoxylon; (3) breakage of the cluster in E. inebrians by a telomere introduced immediately downstream of cloA; and (4) several gene losses or inactivations that have resulted in changes in ergot alkaloid profiles, as discussed above.


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)

Structures of representative EAS loci showing synteny of EAS genes between species. Genes are colored to represent the stage of the pathway for the encoded product (see Figure 1 and Figure 2). Pseudogenes are represented by Ψ and white-filled arrows. Gray polygons link orthologous genes and gene blocks but are not meant to imply particular phylogenetic relationships. The EAS crown clade includes clusters from At. hypoxylon, B. obtecta, C. purpurea, C. fusiformis and P. ipomoeae.
© Copyright Policy
Related In: Results  -  Collection

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

toxins-07-01273-f010: Structures of representative EAS loci showing synteny of EAS genes between species. Genes are colored to represent the stage of the pathway for the encoded product (see Figure 1 and Figure 2). Pseudogenes are represented by Ψ and white-filled arrows. Gray polygons link orthologous genes and gene blocks but are not meant to imply particular phylogenetic relationships. The EAS crown clade includes clusters from At. hypoxylon, B. obtecta, C. purpurea, C. fusiformis and P. ipomoeae.
Mentions: Although functional EAS genes are always clustered, they are not always in a single cluster, arrangements of the genes are not highly conserved, and locations of the clusters can vary, some being subterminal (near chromosome ends), and others being internal and flanked on both sides by long regions rich in housekeeping genes (Figure 10). With the exception of the Epichloë species (discussed below), the degree of divergence in EAS gene arrangements, gene contents, and the pathway end-products generally relates to the degree of divergence between species. Thus, it is unsurprising that the EAS cluster arrangements and gene contents differ greatly in comparison of N. fumigata to the Clavicipitaceae. A surprisingly consistent feature is the arrangement and close linkage of easE and easF in all except E. elymi E56; even their Ar. benhamiae orthologues, respectively designated ARB_4648 and ARB_4647, are adjacent but arranged tail to tail [18]. However, EAS gene arrangements and orientations are very similar in what we will call the “crown EAS clade” (Figure 3): Metarhizium spp. (including Metarhizium acridum, which is not shown), P. ipomoeae, B. obtecta, At. hypoxylon, Claviceps spp. and E. inebrians. Differences within the crown EAS clade were as follows: (1) an inversion of lpsB-easA segment in C. fusiformis relative to the others; (2) separation of the easH-lpsA segment from others in B. obtecta, due to an event that (based on remnant genes) occurred in a common ancestor of B. obtecta and At. hypoxylon; (3) breakage of the cluster in E. inebrians by a telomere introduced immediately downstream of cloA; and (4) several gene losses or inactivations that have resulted in changes in ergot alkaloid profiles, as discussed above.

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