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Spliced leader RNAs, mitochondrial gene frameshifts and multi-protein phylogeny expand support for the genus Perkinsus as a unique group of alveolates.

Zhang H, Campbell DA, Sturm NR, Dungan CF, Lin S - PLoS ONE (2011)

Bottom Line: In contrast to the canonical 22-nt SL found in dinoflagellates (DinoSL), P. marinus has a shorter (21-nt) and a longer (22-nt) SL with slightly different sequences than DinoSL.The major SL RNA transcripts range in size between 80-83 nt in P. marinus, and ∼ 83 nt in P. chesapeaki, significantly larger than the typical ≤ 56-nt dinoflagellate SL RNA.These results, along with the presence of the numerous uncharacterized 'marine alveolate group I' and Perkinsus-like lineages separating perkinsids from core dinoflagellates, expand support for the affiliation of the genus Perkinsus with an independent lineage (Perkinsozoa) positioned between the phyla of Apicomplexa and Dinoflagellata.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Sciences, University of Connecticut, Groton, Connecticut, United States of America. huan.zhang@uconn.edu

ABSTRACT
The genus Perkinsus occupies a precarious phylogenetic position. To gain a better understanding of the relationship between perkinsids, dinoflagellates and other alveolates, we analyzed the nuclear-encoded spliced-leader (SL) RNA and mitochondrial genes, intron prevalence, and multi-protein phylogenies. In contrast to the canonical 22-nt SL found in dinoflagellates (DinoSL), P. marinus has a shorter (21-nt) and a longer (22-nt) SL with slightly different sequences than DinoSL. The major SL RNA transcripts range in size between 80-83 nt in P. marinus, and ∼ 83 nt in P. chesapeaki, significantly larger than the typical ≤ 56-nt dinoflagellate SL RNA. In most of the phylogenetic trees based on 41 predicted protein sequences, P. marinus branched at the base of the dinoflagellate clade that included the ancient taxa Oxyrrhis and Amoebophrya, sister to the clade of apicomplexans, and in some cases clustered with apicomplexans as a sister to the dinoflagellate clade. Of 104 Perkinsus spp. genes examined 69.2% had introns, a higher intron prevalence than in dinoflagellates. Examination of Perkinsus spp. mitochondrial cytochrome B and cytochrome C oxidase subunit I genes and their cDNAs revealed no mRNA editing, but these transcripts can only be translated when frameshifts are introduced at every AGG and CCC codon as if AGGY codes for glycine and CCCCU for proline. These results, along with the presence of the numerous uncharacterized 'marine alveolate group I' and Perkinsus-like lineages separating perkinsids from core dinoflagellates, expand support for the affiliation of the genus Perkinsus with an independent lineage (Perkinsozoa) positioned between the phyla of Apicomplexa and Dinoflagellata.

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Phylogenetic affiliation of Perkinsus marinus with apicomplexan based on three histone proteins.Histone H2B(A), H3 (B), and H4 (C) consensus trees with support from NJ (bootstrap, only >70% are shown), ML (aLRT), and MB (posterior probability). Brackets indicate clades of apicomplexans (AP), dinoflagellates (DI) and ciliates (CI).
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pone-0019933-g009: Phylogenetic affiliation of Perkinsus marinus with apicomplexan based on three histone proteins.Histone H2B(A), H3 (B), and H4 (C) consensus trees with support from NJ (bootstrap, only >70% are shown), ML (aLRT), and MB (posterior probability). Brackets indicate clades of apicomplexans (AP), dinoflagellates (DI) and ciliates (CI).

Mentions: Multiple sequences were obtained for each of the P. marinus histones; in most of the phylogenetic trees, these sequences clustered together and allied with apicomplexans except for the H3 tree, in which one P. marinus H3 grouped with the apicomplexan Toxoplasma gondii, the other with dinoflagellate/ciliate clade (Figures 8, 9). Histone 2A in many organisms has acquired an isoform referred to as H2A.X. In both dinoflagellates and P. marinus, H2A.X seems to be the dominant, if not the only, form. The homolog retrieved from the P. marinus genome was clustered with H2A.X in the clade of apicomplexans (Figure 8).


Spliced leader RNAs, mitochondrial gene frameshifts and multi-protein phylogeny expand support for the genus Perkinsus as a unique group of alveolates.

Zhang H, Campbell DA, Sturm NR, Dungan CF, Lin S - PLoS ONE (2011)

Phylogenetic affiliation of Perkinsus marinus with apicomplexan based on three histone proteins.Histone H2B(A), H3 (B), and H4 (C) consensus trees with support from NJ (bootstrap, only >70% are shown), ML (aLRT), and MB (posterior probability). Brackets indicate clades of apicomplexans (AP), dinoflagellates (DI) and ciliates (CI).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3101222&req=5

pone-0019933-g009: Phylogenetic affiliation of Perkinsus marinus with apicomplexan based on three histone proteins.Histone H2B(A), H3 (B), and H4 (C) consensus trees with support from NJ (bootstrap, only >70% are shown), ML (aLRT), and MB (posterior probability). Brackets indicate clades of apicomplexans (AP), dinoflagellates (DI) and ciliates (CI).
Mentions: Multiple sequences were obtained for each of the P. marinus histones; in most of the phylogenetic trees, these sequences clustered together and allied with apicomplexans except for the H3 tree, in which one P. marinus H3 grouped with the apicomplexan Toxoplasma gondii, the other with dinoflagellate/ciliate clade (Figures 8, 9). Histone 2A in many organisms has acquired an isoform referred to as H2A.X. In both dinoflagellates and P. marinus, H2A.X seems to be the dominant, if not the only, form. The homolog retrieved from the P. marinus genome was clustered with H2A.X in the clade of apicomplexans (Figure 8).

Bottom Line: In contrast to the canonical 22-nt SL found in dinoflagellates (DinoSL), P. marinus has a shorter (21-nt) and a longer (22-nt) SL with slightly different sequences than DinoSL.The major SL RNA transcripts range in size between 80-83 nt in P. marinus, and ∼ 83 nt in P. chesapeaki, significantly larger than the typical ≤ 56-nt dinoflagellate SL RNA.These results, along with the presence of the numerous uncharacterized 'marine alveolate group I' and Perkinsus-like lineages separating perkinsids from core dinoflagellates, expand support for the affiliation of the genus Perkinsus with an independent lineage (Perkinsozoa) positioned between the phyla of Apicomplexa and Dinoflagellata.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Sciences, University of Connecticut, Groton, Connecticut, United States of America. huan.zhang@uconn.edu

ABSTRACT
The genus Perkinsus occupies a precarious phylogenetic position. To gain a better understanding of the relationship between perkinsids, dinoflagellates and other alveolates, we analyzed the nuclear-encoded spliced-leader (SL) RNA and mitochondrial genes, intron prevalence, and multi-protein phylogenies. In contrast to the canonical 22-nt SL found in dinoflagellates (DinoSL), P. marinus has a shorter (21-nt) and a longer (22-nt) SL with slightly different sequences than DinoSL. The major SL RNA transcripts range in size between 80-83 nt in P. marinus, and ∼ 83 nt in P. chesapeaki, significantly larger than the typical ≤ 56-nt dinoflagellate SL RNA. In most of the phylogenetic trees based on 41 predicted protein sequences, P. marinus branched at the base of the dinoflagellate clade that included the ancient taxa Oxyrrhis and Amoebophrya, sister to the clade of apicomplexans, and in some cases clustered with apicomplexans as a sister to the dinoflagellate clade. Of 104 Perkinsus spp. genes examined 69.2% had introns, a higher intron prevalence than in dinoflagellates. Examination of Perkinsus spp. mitochondrial cytochrome B and cytochrome C oxidase subunit I genes and their cDNAs revealed no mRNA editing, but these transcripts can only be translated when frameshifts are introduced at every AGG and CCC codon as if AGGY codes for glycine and CCCCU for proline. These results, along with the presence of the numerous uncharacterized 'marine alveolate group I' and Perkinsus-like lineages separating perkinsids from core dinoflagellates, expand support for the affiliation of the genus Perkinsus with an independent lineage (Perkinsozoa) positioned between the phyla of Apicomplexa and Dinoflagellata.

Show MeSH