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PLoS One
2014 Oct 17;910:e110608. doi: 10.1371/journal.pone.0110608.
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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.
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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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Figure 2. Maps showing the organization of Symbiodinium sPCP tandem genes containing introns and the corresponding cDNAs.(A) Long sPCP genes from clade B/B1 and B19 descendant isolates contained two introns. The CDS identified in genomic and cDNA clones was â¼1.1 kb. (B) Short sPCP genes from S. microadriaticum (clade A/A1) had one intron and the CDS was â¼600 bp.
Figure 3. 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 squaresâ=âB/B1/B184; Green circlesâ=âB/B2/B224 (descendant of B/B19); Orange circlesâ=âB/B19/B211. The positions of Dstok28 and Dstrig102 are underlined in red. The topologies of both trees are congruent with each other.
Figure 4. Phylogenies of long and short sPCP coding sequences (excluding introns) from four dinoflagellate orders.(A) Most parsimonious tree for long sPCP CDS data from the Suessiales, Gonyaulacales and Gynnodiniales. (B) Most parsimonious tree for short sPCP CDS from the Suessiales and Peridiniales. Branch lengths are shown above the branches. Support values >50% based on +1000 bootstrap trees are shown in parentheses below branches. Double inverted trianglesâ=âthe long sPCP branch leading to Symbiodinium clade B sequences, each of which contained two introns. Single inverted triangleâ=âthe short sPCP branch for the S. microadriaticum sequence that had a single intron. (C) Long sPCP tree redrawn to indicate possibility of ancient introns present in the most recent common ancestor of Suessiales, Gonyaulacales and Gynnodiniales. Vertical barâ=âloss of an intron on an ascending branch required to explain the data. (D) Short sPCP tree redrawn to indicate possibility of an ancient intron present in the most recent common ancestor of Suessiales and Peridinales. Required losses on ascending branches are indicated as before.
Figure 5. Phylogeny of short and long sPCP predicted amino acid sequences from four dinoflagellate orders.The most parsimonious tree shows unambiguous resolution of short and long sPCP sister clades. Branch lengths are shown above the branches. Support values >70% based on +1000 bootstrap trees are shown in parentheses below branches. The long sPCP genes were produced from fusion of duplicated short sPCP genes that occurred once early during the evolution of peridinin-containing dinoflagellates. Thereafter, short and long sPCP genes and corresponding polypeptides diverged.
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Correction: Separate Introns Gained within Short and Long Soluble Peridinin-Chlorophyll a-Protein Genes during Radiation of Symbiodinium (Dinophyceae) Clade A and B Lineages.
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