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

Jay R Reichman,Peter D Vize,Bernd Schierwater

doi:10.1371/journal.pone.0110608

Jay R Reichman, Peter D Vize + Show 1 more

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https://doi.org/10.1371/journal.pone.0110608

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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.

Highlights

Spliceosomal introns are present in all known eukaryotic genomes, yet the density of introns is highly variable across lineages [1]
The similarity of N-terminal and C-terminal domains of long soluble peridinin-chlorophyll a-proteins (sPCP) is the result of a pseudo-axis of symmetry in their amino acid sequences, which indicates that dinoflagellate long sPCP genes arose via duplication and fusion of short sPCP genes [53,54,56,64]
Nuclear large subunit rDNA sequences from Dstok28 and Dstrig102 were used for preliminary identification of these samples, both of which most closely matched Symbiodinium clade B accessions in GenBank

Summary

Introduction

Spliceosomal introns are present in all known eukaryotic genomes, yet the density of introns is highly variable across lineages [1]. Mature long sPCP apoproteins contain paired domains that do resemble each other and short sPCPs. The similarity of N-terminal and C-terminal domains of long sPCPs is the result of a pseudo-axis of symmetry in their amino acid sequences, which indicates that dinoflagellate long sPCP genes arose via duplication and fusion of short sPCP genes [53,54,56,64]. The ecological and evolutionary reasons for the distribution remain obscure but it is possible that fusion of short sPCP genes happened more than once Another point regarding sPCP gene evolution is that both classes of apoproteins are encoded by tandem arrays of nuclear genes that vary in terms of copy number and heterogeneity across dinoflagellate lineages. Variation within sPCP gene families is the primary source of sPCP isoform diversity [54,55,56,57]

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