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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 ∼1.1 kb. (B) Short sPCP genes from S. microadriaticum (clade A/A1) had one intron and the CDS was ∼600 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 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.
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 triangles = the long sPCP branch leading to Symbiodinium clade B sequences, each of which contained two introns. Single inverted triangle = the 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 bar = loss 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.
,
Correction: Separate Introns Gained within Short and Long Soluble Peridinin-Chlorophyll a-Protein Genes during Radiation of Symbiodinium (Dinophyceae) Clade A and B Lineages.
2015, Pubmed
,
Correction: Separate Introns Gained within Short and Long Soluble Peridinin-Chlorophyll a-Protein Genes during Radiation of Symbiodinium (Dinophyceae) Clade A and B Lineages.
2015,
Pubmed Babenko,
Prevalence of intron gain over intron loss in the evolution of paralogous gene families.
2004,
Pubmed Bachvaroff,
Dinoflagellate expressed sequence tag data indicate massive transfer of chloroplast genes to the nuclear genome.
2004,
Pubmed Bachvaroff,
From stop to start: tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae.
2008,
Pubmed Basu,
Evolutionary dynamics of introns in plastid-derived genes in plants: saturation nearly reached but slow intron gain continues.
2008,
Pubmed Bendtsen,
Improved prediction of signal peptides: SignalP 3.0.
2004,
Pubmed Bradley,
Recombinant DNA sequences generated by PCR amplification.
1997,
Pubmed Buratti,
DBASS3 and DBASS5: databases of aberrant 3'- and 5'-splice sites.
2011,
Pubmed Coffroth,
Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium.
2005,
Pubmed Csurös,
Extremely intron-rich genes in the alveolate ancestors inferred with a flexible maximum-likelihood approach.
2008,
Pubmed Dibb,
Evidence that introns arose at proto-splice sites.
1989,
Pubmed Durnford,
A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution.
1999,
Pubmed Felsenstein,
Evolutionary trees from DNA sequences: a maximum likelihood approach.
1981,
Pubmed Finney,
The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium.
2010,
Pubmed GUILLARD,
Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran.
1962,
Pubmed Hasegawa,
Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.
1985,
Pubmed Haxo,
Peridinin-Chlorophyll a Proteins of the Dinoflagellate Amphidinium carterae (Plymouth 450).
1976,
Pubmed Hiller,
The 15-kDa forms of the apo-peridinin-chlorophyll a protein (PCP) in dinoflagellates show high identity with the apo-32 kDa PCP forms, and have similar N-terminal leaders and gene arrangements.
2001,
Pubmed Hofmann,
Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae.
1996,
Pubmed Huber,
Bellerophon: a program to detect chimeric sequences in multiple sequence alignments.
2004,
Pubmed Jeffares,
The biology of intron gain and loss.
2006,
Pubmed Kapustin,
Cryptic splice sites and split genes.
2011,
Pubmed Kimura,
A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.
1980,
Pubmed Kuzoff,
The phylogenetic potential of entire 26S rDNA sequences in plants.
1998,
Pubmed Lajeunesse,
A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria.
2012,
Pubmed Lajeunesse,
Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt).
2000,
Pubmed Lajeunesse,
"Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition.
2005,
Pubmed LaJeunesse,
Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance.
2010,
Pubmed Le,
Structure and organization of the peridinin-chlorophyll a-binding protein gene in Gonyaulax polyedra.
1997,
Pubmed Liu,
Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees.
2009,
Pubmed Liu,
Primary and secondary structure of dinoflagellate U5 small nuclear RNA.
1984,
Pubmed Logsdon,
Molecular evolution: recent cases of spliceosomal intron gain?
,
Pubmed Logsdon,
The recent origins of spliceosomal introns revisited.
1998,
Pubmed Matsumoto,
A deviant genetic code in the green alga-derived plastid in the dinoflagellate Lepidodinium chlorophorum.
2011,
Pubmed Nielsen,
Patterns of intron gain and loss in fungi.
2004,
Pubmed Norris,
Nucleotide sequence of a cDNA clone encoding the precursor of the peridinin-chlorophyll a-binding protein from the dinoflagellate Symbiodinium sp.
1994,
Pubmed Okamoto,
Members of a dinoflagellate luciferase gene family differ in synonymous substitution rates.
2001,
Pubmed Patron,
Complex protein targeting to dinoflagellate plastids.
2005,
Pubmed Pettay,
Microsatellite loci for assessing genetic diversity, dispersal and clonality of coral symbionts in 'stress-tolerant' clade D Symbiodinium.
2009,
Pubmed Pochon,
Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium.
2006,
Pubmed Pochon,
A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i.
2010,
Pubmed Posada,
MODELTEST: testing the model of DNA substitution.
1998,
Pubmed Prézelin,
Purification and characterization of peridinin-chlorophyll a-proteins from the marine dinoflagellates Glenodinium sp. and Gonyaulax polyedra.
1976,
Pubmed Qiu,
The evolutionary gain of spliceosomal introns: sequence and phase preferences.
2004,
Pubmed Reddy,
Isolation and partial characterization of dinoflagellate U1-U6 small RNAs homologous to rat U small nuclear RNAs.
1983,
Pubmed Reichman,
PCP gene family in Symbiodinium from Hippopus hippopus: low levels of concerted evolution, isoform diversity, and spectral tuning of chromophores.
2003,
Pubmed
,
Xenbase Rogozin,
Remarkable interkingdom conservation of intron positions and massive, lineage-specific intron loss and gain in eukaryotic evolution.
2003,
Pubmed Rowan,
A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses.
1991,
Pubmed Rowan,
Intraspecific diversity and ecological zonation in coral-algal symbiosis.
1995,
Pubmed Rowan,
Ribosomal RNA sequences and the diversity of symbiotic dinoflagellates (zooxanthellae).
1992,
Pubmed Rowan,
Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family.
1996,
Pubmed Roy,
Rates of intron loss and gain: implications for early eukaryotic evolution.
2005,
Pubmed Sadusky,
Exon junction sequences as cryptic splice sites: implications for intron origin.
2004,
Pubmed Santos,
Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean.
2004,
Pubmed Santos,
Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S)-ribosomal DNA sequences.
2003,
Pubmed Santos,
Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium freudenthal are haploid.
2003,
Pubmed Santos,
Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences.
2002,
Pubmed Sharples,
Two distinct forms of the peridinin-chlorophyll a-protein from Amphidinium carterae.
1996,
Pubmed Shoguchi,
Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure.
2013,
Pubmed Siegelman,
Peridnin-chlorophyll a-proteins of dinoflagellate algae.
,
Pubmed Simmons,
Gaps as characters in sequence-based phylogenetic analyses.
2000,
Pubmed Stamatakis,
RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees.
2005,
Pubmed Stoltzfus,
Molecular evolution: introns fall into place.
2004,
Pubmed Thornhill,
Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates.
2007,
Pubmed Tomita,
Introns and reading frames: correlation between splicing sites and their codon positions.
1996,
Pubmed Tordai,
Insertion of spliceosomal introns in proto-splice sites: the case of secretory signal peptides.
2004,
Pubmed Triplett,
Characterization of two full-length cDNA sequences encoding for apoproteins of peridinin-chlorophyll a-protein (PCP) complexes.
1993,
Pubmed Voolstra,
Evolutionary analysis of orthologous cDNA sequences from cultured and symbiotic dinoflagellate symbionts of reef-building corals (Dinophyceae: Symbiodinium).
2009,
Pubmed Wilcox,
Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: morphology does not recapitulate phylogeny.
1998,
Pubmed
