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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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Maximum GC content at each residue of the CEP domain in plant families. These sequence logos are based on weighted CEP domain sequences identified in the genomes of the plant families Brassicaceae (A), Fabaceae (B), Pinaceae (C), Poaceae (D), Rosaceae (E) and Solanaceae (F). AAs are colored by the maximum number of guanine and/or cytosine residues in the codons that encode each AA; 3 (green), 2 (orange) or 1 (red). All AAs are represented as standard, single-letter abbreviations [22].
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Fig6: Maximum GC content at each residue of the CEP domain in plant families. These sequence logos are based on weighted CEP domain sequences identified in the genomes of the plant families Brassicaceae (A), Fabaceae (B), Pinaceae (C), Poaceae (D), Rosaceae (E) and Solanaceae (F). AAs are colored by the maximum number of guanine and/or cytosine residues in the codons that encode each AA; 3 (green), 2 (orange) or 1 (red). All AAs are represented as standard, single-letter abbreviations [22].

Mentions: The distributions of AAs at position 2 of the Poaceae and Solanaceae CEP domains (Figure 6) is consistent with the stark difference in GC content between CEP genes from those plant families. The most common AAs at this position in Poaceae – valine, serine, glycine and threonine – can be encoded using GC rich codons containing two or three guanine or cytosine nucleotides (Figure 6D). In contrast to this, the most common AAs at this position in Solanaceae – phenylalanine, tyrosine, lysine and isoleucine – can only be encoded using GC poor codons containing zero or one guanine or cytosine nucleotides (Figure 6F). However in position 13, where a selective constraint was often observed (Figure 4), the most common AA for both Poaceae and Solanaceae CEP domains was isoleucine, which utilizes GC poor codons (Figure 6D and Figure 6F).Figure 5


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)

Maximum GC content at each residue of the CEP domain in plant families. These sequence logos are based on weighted CEP domain sequences identified in the genomes of the plant families Brassicaceae (A), Fabaceae (B), Pinaceae (C), Poaceae (D), Rosaceae (E) and Solanaceae (F). AAs are colored by the maximum number of guanine and/or cytosine residues in the codons that encode each AA; 3 (green), 2 (orange) or 1 (red). All AAs are represented as standard, single-letter abbreviations [22].
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: Maximum GC content at each residue of the CEP domain in plant families. These sequence logos are based on weighted CEP domain sequences identified in the genomes of the plant families Brassicaceae (A), Fabaceae (B), Pinaceae (C), Poaceae (D), Rosaceae (E) and Solanaceae (F). AAs are colored by the maximum number of guanine and/or cytosine residues in the codons that encode each AA; 3 (green), 2 (orange) or 1 (red). All AAs are represented as standard, single-letter abbreviations [22].
Mentions: The distributions of AAs at position 2 of the Poaceae and Solanaceae CEP domains (Figure 6) is consistent with the stark difference in GC content between CEP genes from those plant families. The most common AAs at this position in Poaceae – valine, serine, glycine and threonine – can be encoded using GC rich codons containing two or three guanine or cytosine nucleotides (Figure 6D). In contrast to this, the most common AAs at this position in Solanaceae – phenylalanine, tyrosine, lysine and isoleucine – can only be encoded using GC poor codons containing zero or one guanine or cytosine nucleotides (Figure 6F). However in position 13, where a selective constraint was often observed (Figure 4), the most common AA for both Poaceae and Solanaceae CEP domains was isoleucine, which utilizes GC poor codons (Figure 6D and Figure 6F).Figure 5

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