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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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dN/dSratios of selection pressure across the amino acid sequences of exemplary orthologous groups of CEP genes. dN/dS means (black line) and 95% HPD intervals (blue ribbon) were calculated for orthologous groups of CEP genes. Orthologous groups were chosen from a diverse range of angiosperm families: group 3 from Rosaceae (A), group 4 from Fabaceae (B), group 8 from Solanaceae (C), group 10 from the sister families Brassicaceae and Cleomaceae (D) and group 28 from Poaceae (E). The entire coding region was analyzed, including the NSS (light red), variable region (grey), CEP domain (blue) and C-terminal extension (green). Significantly constrained residues (upper HPD limit < 1) are highlighted in bold. Conserved motifs within the variable region and related motifs in the CEP domain are underlined.
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Fig4: dN/dSratios of selection pressure across the amino acid sequences of exemplary orthologous groups of CEP genes. dN/dS means (black line) and 95% HPD intervals (blue ribbon) were calculated for orthologous groups of CEP genes. Orthologous groups were chosen from a diverse range of angiosperm families: group 3 from Rosaceae (A), group 4 from Fabaceae (B), group 8 from Solanaceae (C), group 10 from the sister families Brassicaceae and Cleomaceae (D) and group 28 from Poaceae (E). The entire coding region was analyzed, including the NSS (light red), variable region (grey), CEP domain (blue) and C-terminal extension (green). Significantly constrained residues (upper HPD limit < 1) are highlighted in bold. Conserved motifs within the variable region and related motifs in the CEP domain are underlined.

Mentions: To identify any residues in the CEP prepropeptide that are under negative selection, ratios of non-synonymous to synonymous substitutions (dN/dS) were estimated for all residues of all orthologous groups (Additional file 3). Ratios below 1 indicate a selective constraint at that position, favoring specific AAs [25]. One exemplary orthologous group was selected from each well-represented angiosperm plant family. Significantly constrained residues were found across the CEP coding region in each exemplary group, including within the NSS (light red), variable region (grey), CEP domain (blue) and C-terminal extension (green) (Figure 4).Figure 4


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)

dN/dSratios of selection pressure across the amino acid sequences of exemplary orthologous groups of CEP genes. dN/dS means (black line) and 95% HPD intervals (blue ribbon) were calculated for orthologous groups of CEP genes. Orthologous groups were chosen from a diverse range of angiosperm families: group 3 from Rosaceae (A), group 4 from Fabaceae (B), group 8 from Solanaceae (C), group 10 from the sister families Brassicaceae and Cleomaceae (D) and group 28 from Poaceae (E). The entire coding region was analyzed, including the NSS (light red), variable region (grey), CEP domain (blue) and C-terminal extension (green). Significantly constrained residues (upper HPD limit < 1) are highlighted in bold. Conserved motifs within the variable region and related motifs in the CEP domain are underlined.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig4: dN/dSratios of selection pressure across the amino acid sequences of exemplary orthologous groups of CEP genes. dN/dS means (black line) and 95% HPD intervals (blue ribbon) were calculated for orthologous groups of CEP genes. Orthologous groups were chosen from a diverse range of angiosperm families: group 3 from Rosaceae (A), group 4 from Fabaceae (B), group 8 from Solanaceae (C), group 10 from the sister families Brassicaceae and Cleomaceae (D) and group 28 from Poaceae (E). The entire coding region was analyzed, including the NSS (light red), variable region (grey), CEP domain (blue) and C-terminal extension (green). Significantly constrained residues (upper HPD limit < 1) are highlighted in bold. Conserved motifs within the variable region and related motifs in the CEP domain are underlined.
Mentions: To identify any residues in the CEP prepropeptide that are under negative selection, ratios of non-synonymous to synonymous substitutions (dN/dS) were estimated for all residues of all orthologous groups (Additional file 3). Ratios below 1 indicate a selective constraint at that position, favoring specific AAs [25]. One exemplary orthologous group was selected from each well-represented angiosperm plant family. Significantly constrained residues were found across the CEP coding region in each exemplary group, including within the NSS (light red), variable region (grey), CEP domain (blue) and C-terminal extension (green) (Figure 4).Figure 4

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