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Diversification of the C-TERMINALLY ENCODED PEPTIDE (CEP) gene family in angiosperms, and evolution of plant-family specific CEP genes.

Ogilvie HA, Imin N, Djordjevic MA - BMC Genomics (2014)

Bottom Line: Using a motif-based system developed for this study to identify canonical CEP peptide domains, a total of 916 CEP genes and 1,223 CEP domains were found in angiosperms and for the first time in gymnosperms.Both CEP genes and domains were found to have diversified in angiosperms, particularly in the Poaceae and Solanaceae plant families.Multispecies orthologous relationships were determined for 22% of identified CEP genes, and further analysis of those groups found selective constraints upon residues within the CEP peptide and within the previously little-characterized variable region.

View Article: PubMed Central - PubMed

Affiliation: Research School of Biology, The Australian National University, Canberra ACT 0200, Australia. huw.ogilvie@anu.edu.au.

ABSTRACT

Background: Small, secreted signaling peptides work in parallel with phytohormones to control important aspects of plant growth and development. Genes from the C-TERMINALLY ENCODED PEPTIDE (CEP) family produce such peptides which negatively regulate plant growth, especially under stress, and affect other important developmental processes. To illuminate how the CEP gene family has evolved within the plant kingdom, including its emergence, diversification and variation between lineages, a comprehensive survey was undertaken to identify and characterize CEP genes in 106 plant genomes.

Results: Using a motif-based system developed for this study to identify canonical CEP peptide domains, a total of 916 CEP genes and 1,223 CEP domains were found in angiosperms and for the first time in gymnosperms. This defines a narrow band for the emergence of CEP genes in plants, from the divergence of lycophytes to the angiosperm/gymnosperm split. Both CEP genes and domains were found to have diversified in angiosperms, particularly in the Poaceae and Solanaceae plant families. Multispecies orthologous relationships were determined for 22% of identified CEP genes, and further analysis of those groups found selective constraints upon residues within the CEP peptide and within the previously little-characterized variable region. An examination of public Oryza sativa RNA-Seq datasets revealed an expression pattern that links OsCEP5 and OsCEP6 to panicle development and flowering, and CEP gene trees reveal these emerged from a duplication event associated with the Poaceae plant family.

Conclusions: The characterization of the plant-family specific CEP genes OsCEP5 and OsCEP6, the association of CEP genes with angiosperm-specific development processes like panicle development, and the diversification of CEP genes in angiosperms provides further support for the hypothesis that CEP genes have been integral to the evolution of novel traits within the angiosperm lineage. Beyond these findings, the comprehensive set of CEP genes and their properties reported here will be a resource for future research on CEP genes and peptides.

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A comparison of CEP gene (A) and CEP domain (B) sequence diversity between seed plant families. These density plots of sequence diversity graph the distributions of pairwise genetic distances of CEP genes and domains within a single organism, aggregated by plant family. Genetic distances were calculated based on the AA sequences, using a maximum likelihood estimation. Tukey’s test reveals that both CEP gene and domain sequence diversity is significantly greater in all angiosperm families than in the gymnosperm family Pinaceae (P < 0.001). Additionally, the CEP gene and domain sequence diversity of Poaceae and Solanaceae are significantly (P < 0.05) greater than in other angiosperm families.
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Fig2: A comparison of CEP gene (A) and CEP domain (B) sequence diversity between seed plant families. These density plots of sequence diversity graph the distributions of pairwise genetic distances of CEP genes and domains within a single organism, aggregated by plant family. Genetic distances were calculated based on the AA sequences, using a maximum likelihood estimation. Tukey’s test reveals that both CEP gene and domain sequence diversity is significantly greater in all angiosperm families than in the gymnosperm family Pinaceae (P < 0.001). Additionally, the CEP gene and domain sequence diversity of Poaceae and Solanaceae are significantly (P < 0.05) greater than in other angiosperm families.

Mentions: For both CEP genes and CEP domains, all five well-represented angiosperm families featured significantly (P < 0.001) more sequence diversity than Pinaceae. Intriguingly, the CEP gene and CEP domain sequence diversity of Solanaceae (within the eudicot and asterid clades) and Poaceae (within the monocot clade) were both significantly (P < 0.05) greater than Brassicaceae, Fabaceae or Rosaceae (Figure 2). Solanaceae and Poaceae do not share a common ancestor to the exclusion of the other well-represented families [21], so this pattern must require either independent increases in CEP sequence diversity in the Solanaceae and Poaceae lineages, or a loss of sequence diversity in the rosid clade which includes the other well-represented angiosperm plant families.Figure 2


Diversification of the C-TERMINALLY ENCODED PEPTIDE (CEP) gene family in angiosperms, and evolution of plant-family specific CEP genes.

Ogilvie HA, Imin N, Djordjevic MA - BMC Genomics (2014)

A comparison of CEP gene (A) and CEP domain (B) sequence diversity between seed plant families. These density plots of sequence diversity graph the distributions of pairwise genetic distances of CEP genes and domains within a single organism, aggregated by plant family. Genetic distances were calculated based on the AA sequences, using a maximum likelihood estimation. Tukey’s test reveals that both CEP gene and domain sequence diversity is significantly greater in all angiosperm families than in the gymnosperm family Pinaceae (P < 0.001). Additionally, the CEP gene and domain sequence diversity of Poaceae and Solanaceae are significantly (P < 0.05) greater than in other angiosperm families.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4197245&req=5

Fig2: A comparison of CEP gene (A) and CEP domain (B) sequence diversity between seed plant families. These density plots of sequence diversity graph the distributions of pairwise genetic distances of CEP genes and domains within a single organism, aggregated by plant family. Genetic distances were calculated based on the AA sequences, using a maximum likelihood estimation. Tukey’s test reveals that both CEP gene and domain sequence diversity is significantly greater in all angiosperm families than in the gymnosperm family Pinaceae (P < 0.001). Additionally, the CEP gene and domain sequence diversity of Poaceae and Solanaceae are significantly (P < 0.05) greater than in other angiosperm families.
Mentions: For both CEP genes and CEP domains, all five well-represented angiosperm families featured significantly (P < 0.001) more sequence diversity than Pinaceae. Intriguingly, the CEP gene and CEP domain sequence diversity of Solanaceae (within the eudicot and asterid clades) and Poaceae (within the monocot clade) were both significantly (P < 0.05) greater than Brassicaceae, Fabaceae or Rosaceae (Figure 2). Solanaceae and Poaceae do not share a common ancestor to the exclusion of the other well-represented families [21], so this pattern must require either independent increases in CEP sequence diversity in the Solanaceae and Poaceae lineages, or a loss of sequence diversity in the rosid clade which includes the other well-represented angiosperm plant families.Figure 2

Bottom Line: Using a motif-based system developed for this study to identify canonical CEP peptide domains, a total of 916 CEP genes and 1,223 CEP domains were found in angiosperms and for the first time in gymnosperms.Both CEP genes and domains were found to have diversified in angiosperms, particularly in the Poaceae and Solanaceae plant families.Multispecies orthologous relationships were determined for 22% of identified CEP genes, and further analysis of those groups found selective constraints upon residues within the CEP peptide and within the previously little-characterized variable region.

View Article: PubMed Central - PubMed

Affiliation: Research School of Biology, The Australian National University, Canberra ACT 0200, Australia. huw.ogilvie@anu.edu.au.

ABSTRACT

Background: Small, secreted signaling peptides work in parallel with phytohormones to control important aspects of plant growth and development. Genes from the C-TERMINALLY ENCODED PEPTIDE (CEP) family produce such peptides which negatively regulate plant growth, especially under stress, and affect other important developmental processes. To illuminate how the CEP gene family has evolved within the plant kingdom, including its emergence, diversification and variation between lineages, a comprehensive survey was undertaken to identify and characterize CEP genes in 106 plant genomes.

Results: Using a motif-based system developed for this study to identify canonical CEP peptide domains, a total of 916 CEP genes and 1,223 CEP domains were found in angiosperms and for the first time in gymnosperms. This defines a narrow band for the emergence of CEP genes in plants, from the divergence of lycophytes to the angiosperm/gymnosperm split. Both CEP genes and domains were found to have diversified in angiosperms, particularly in the Poaceae and Solanaceae plant families. Multispecies orthologous relationships were determined for 22% of identified CEP genes, and further analysis of those groups found selective constraints upon residues within the CEP peptide and within the previously little-characterized variable region. An examination of public Oryza sativa RNA-Seq datasets revealed an expression pattern that links OsCEP5 and OsCEP6 to panicle development and flowering, and CEP gene trees reveal these emerged from a duplication event associated with the Poaceae plant family.

Conclusions: The characterization of the plant-family specific CEP genes OsCEP5 and OsCEP6, the association of CEP genes with angiosperm-specific development processes like panicle development, and the diversification of CEP genes in angiosperms provides further support for the hypothesis that CEP genes have been integral to the evolution of novel traits within the angiosperm lineage. Beyond these findings, the comprehensive set of CEP genes and their properties reported here will be a resource for future research on CEP genes and peptides.

Show MeSH