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Separate introns gained within short and long soluble peridinin-chlorophyll a-protein genes during radiation of Symbiodinium (Dinophyceae) clade A and B lineages.

Reichman JR, Vize PD - PLoS ONE (2014)

Bottom Line: The clade A short sPCP intron was either gained by S. microadriaticum or possibly by the ancestor of Symbiodinium types A/A1, A3, A4 and A5.The timing of short sPCP intron gain in Symbiodinium clade A is less certain.But, all sPCP introns were gained after fusion of ancestral short sPCP genes, which we confirm as occurring once in dinoflagellate evolution.

View Article: PubMed Central - PubMed

Affiliation: US Environmental Protection Agency, Western Ecology Division, Corvallis, Oregon, United States of America; Oregon State University, Department of Botany and Plant Pathology, Corvallis, Oregon, United States of America.

ABSTRACT
Here we document introns in two Symbiodinium clades that were most likely gained following divergence of this genus from other peridinin-containing dinoflagellate lineages. Soluble peridinin-chlorophyll a-proteins (sPCP) occur in short and long forms in different species. Duplication and fusion of short sPCP genes produced long sPCP genes. All short and long sPCP genes characterized to date, including those from free living species and Symbiodinium sp. 203 (clade C/type C2) are intronless. However, we observed that long sPCP genes from two Caribbean Symbiodinium clade B isolates each contained two introns. To test the hypothesis that introns were gained during radiation of clade B, we compared sPCP genomic and cDNA sequences from 13 additional distinct Caribbean and Pacific Symbiodinium clade A, B, and F isolates. Long sPCP genes from all clade B/B1 and B/B19 descendants contain orthologs of both introns. Short sPCP genes from S. pilosum (A/A2) and S. muscatinei (B/B4) plus long sPCP genes from S. microadriaticum (A/A1) and S. kawagutii (F/F1) are intronless. Short sPCP genes of S. microadriaticum have a third unique intron. Symbiodinium clade B long sPCP sequences are useful for assessing divergence among B1 and B19 descendants. Phylogenetic analyses of coding sequences from four dinoflagellate orders indicate that introns were gained independently during radiation of Symbiodinium clades A and B. Long sPCP introns were present in the most recent common ancestor of Symbiodinium clade B core types B1 and B19, which apparently diverged sometime during the Miocene. The clade A short sPCP intron was either gained by S. microadriaticum or possibly by the ancestor of Symbiodinium types A/A1, A3, A4 and A5. The timing of short sPCP intron gain in Symbiodinium clade A is less certain. But, all sPCP introns were gained after fusion of ancestral short sPCP genes, which we confirm as occurring once in dinoflagellate evolution.

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Phylogenies of Symbiodinium clade B long sPCP cassette sequences.(A) Maximum likelihood tree of all non-chimeric clones. (B) Most parsimonious tree of most frequently recovered non-chimeric clones. Branch lengths for the most parsimonious tree are shown above the branches. Support values >70% based on +1000 bootstrap trees are shown in parentheses. Support values for minor branches of the maximum likelihood tree are not displayed. Blue squares = B/B1/B184; Green circles = B/B2/B224 (descendant of B/B19); Orange circles = B/B19/B211. The positions of Dstok28 and Dstrig102 are underlined in red. The topologies of both trees are congruent with each other.
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pone-0110608-g003: Phylogenies of Symbiodinium clade B long sPCP cassette sequences.(A) Maximum likelihood tree of all non-chimeric clones. (B) Most parsimonious tree of most frequently recovered non-chimeric clones. Branch lengths for the most parsimonious tree are shown above the branches. Support values >70% based on +1000 bootstrap trees are shown in parentheses. Support values for minor branches of the maximum likelihood tree are not displayed. Blue squares = B/B1/B184; Green circles = B/B2/B224 (descendant of B/B19); Orange circles = B/B19/B211. The positions of Dstok28 and Dstrig102 are underlined in red. The topologies of both trees are congruent with each other.

Mentions: Phylogenetic trees of clade B long sPCP gene sequences (including all exons and introns) are presented in Figure 3. Maximum likelihood relationships among all 138 non-chimeric clones were inferred with SATé (Figure 3A). Subclades containing sequences from B/B1/B184, B/B19/B211 and B/B2/B224 types were resolved from each other with 100% bootstrap support in each case. Branches for individual Dstok28 clones were interdigitated among those from B/B1/B184 isolates Ap1, FLAp2-10AB, Pe, S. minutum Pd, SSPe and Zp. A Dstrig102 subclade with 80% bootstrap support was placed as sister to a comingled group of S. psygmophilum HIAp and S. psygmophilum PurPflex (B/B2/B224) sequences.


Separate introns gained within short and long soluble peridinin-chlorophyll a-protein genes during radiation of Symbiodinium (Dinophyceae) clade A and B lineages.

Reichman JR, Vize PD - PLoS ONE (2014)

Phylogenies of Symbiodinium clade B long sPCP cassette sequences.(A) Maximum likelihood tree of all non-chimeric clones. (B) Most parsimonious tree of most frequently recovered non-chimeric clones. Branch lengths for the most parsimonious tree are shown above the branches. Support values >70% based on +1000 bootstrap trees are shown in parentheses. Support values for minor branches of the maximum likelihood tree are not displayed. Blue squares = B/B1/B184; Green circles = B/B2/B224 (descendant of B/B19); Orange circles = B/B19/B211. The positions of Dstok28 and Dstrig102 are underlined in red. The topologies of both trees are congruent with each other.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4201569&req=5

pone-0110608-g003: Phylogenies of Symbiodinium clade B long sPCP cassette sequences.(A) Maximum likelihood tree of all non-chimeric clones. (B) Most parsimonious tree of most frequently recovered non-chimeric clones. Branch lengths for the most parsimonious tree are shown above the branches. Support values >70% based on +1000 bootstrap trees are shown in parentheses. Support values for minor branches of the maximum likelihood tree are not displayed. Blue squares = B/B1/B184; Green circles = B/B2/B224 (descendant of B/B19); Orange circles = B/B19/B211. The positions of Dstok28 and Dstrig102 are underlined in red. The topologies of both trees are congruent with each other.
Mentions: Phylogenetic trees of clade B long sPCP gene sequences (including all exons and introns) are presented in Figure 3. Maximum likelihood relationships among all 138 non-chimeric clones were inferred with SATé (Figure 3A). Subclades containing sequences from B/B1/B184, B/B19/B211 and B/B2/B224 types were resolved from each other with 100% bootstrap support in each case. Branches for individual Dstok28 clones were interdigitated among those from B/B1/B184 isolates Ap1, FLAp2-10AB, Pe, S. minutum Pd, SSPe and Zp. A Dstrig102 subclade with 80% bootstrap support was placed as sister to a comingled group of S. psygmophilum HIAp and S. psygmophilum PurPflex (B/B2/B224) sequences.

Bottom Line: The clade A short sPCP intron was either gained by S. microadriaticum or possibly by the ancestor of Symbiodinium types A/A1, A3, A4 and A5.The timing of short sPCP intron gain in Symbiodinium clade A is less certain.But, all sPCP introns were gained after fusion of ancestral short sPCP genes, which we confirm as occurring once in dinoflagellate evolution.

View Article: PubMed Central - PubMed

Affiliation: US Environmental Protection Agency, Western Ecology Division, Corvallis, Oregon, United States of America; Oregon State University, Department of Botany and Plant Pathology, Corvallis, Oregon, United States of America.

ABSTRACT
Here we document introns in two Symbiodinium clades that were most likely gained following divergence of this genus from other peridinin-containing dinoflagellate lineages. Soluble peridinin-chlorophyll a-proteins (sPCP) occur in short and long forms in different species. Duplication and fusion of short sPCP genes produced long sPCP genes. All short and long sPCP genes characterized to date, including those from free living species and Symbiodinium sp. 203 (clade C/type C2) are intronless. However, we observed that long sPCP genes from two Caribbean Symbiodinium clade B isolates each contained two introns. To test the hypothesis that introns were gained during radiation of clade B, we compared sPCP genomic and cDNA sequences from 13 additional distinct Caribbean and Pacific Symbiodinium clade A, B, and F isolates. Long sPCP genes from all clade B/B1 and B/B19 descendants contain orthologs of both introns. Short sPCP genes from S. pilosum (A/A2) and S. muscatinei (B/B4) plus long sPCP genes from S. microadriaticum (A/A1) and S. kawagutii (F/F1) are intronless. Short sPCP genes of S. microadriaticum have a third unique intron. Symbiodinium clade B long sPCP sequences are useful for assessing divergence among B1 and B19 descendants. Phylogenetic analyses of coding sequences from four dinoflagellate orders indicate that introns were gained independently during radiation of Symbiodinium clades A and B. Long sPCP introns were present in the most recent common ancestor of Symbiodinium clade B core types B1 and B19, which apparently diverged sometime during the Miocene. The clade A short sPCP intron was either gained by S. microadriaticum or possibly by the ancestor of Symbiodinium types A/A1, A3, A4 and A5. The timing of short sPCP intron gain in Symbiodinium clade A is less certain. But, all sPCP introns were gained after fusion of ancestral short sPCP genes, which we confirm as occurring once in dinoflagellate evolution.

Show MeSH
Related in: MedlinePlus