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Evolutionary history of selenocysteine incorporation from the perspective of SECIS binding proteins.

Donovan J, Copeland PR - BMC Evol. Biol. (2009)

Bottom Line: In addition, we describe the emergence of a motif upstream of the SBP2 RNA binding domain that shares significant similarity with a motif within the pseudouridine synthase Cbf5.Our analysis suggests that SECIS binding proteins arose once in evolution but diverged significantly in multiple lineages.In addition, likely due to a gene duplication event in the early vertebrate lineage, SBP2 and SBP2L are paralogous in vertebrates.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular Genetics, Microbiology, and Immunology, Graduate School of Biomedical Sciences, University of Medicine and Dentistry of New Jersey - Robert Wood Johnson Medical School, Piscataway, NJ, USA. donovaje@umdnj.edu

ABSTRACT

Background: The co-translational incorporation of selenocysteine into nascent polypeptides by recoding the UGA stop codon occurs in all domains of life. In eukaryotes, this event requires at least three specific factors: SECIS binding protein 2 (SBP2), a specific translation elongation factor (eEFSec), selenocysteinyl tRNA, and a cis-acting selenocysteine insertion sequence (SECIS) element in selenoprotein mRNAs. While the phylogenetic relationships of selenoprotein families and the evolution of selenocysteine usage are well documented, the evolutionary history of SECIS binding proteins has not been explored.

Results: In this report we present a phylogeny of the eukaryotic SECIS binding protein family which includes SBP2 and a related protein we herein term SBP2L. Here we show that SBP2L is an SBP2 paralogue in vertebrates and is the only form of SECIS binding protein in invertebrate deuterostomes, suggesting a key role in Sec incorporation in these organisms, but an SBP2/SBP2L fusion protein is unable to support Sec incorporation in vitro. An in-depth phylogenetic analysis of the conserved L7Ae RNA binding domain suggests an ancestral relationship with ribosomal protein L30. In addition, we describe the emergence of a motif upstream of the SBP2 RNA binding domain that shares significant similarity with a motif within the pseudouridine synthase Cbf5.

Conclusion: Our analysis suggests that SECIS binding proteins arose once in evolution but diverged significantly in multiple lineages. In addition, likely due to a gene duplication event in the early vertebrate lineage, SBP2 and SBP2L are paralogous in vertebrates.

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Aedes aegypti SBP2 is coded by two genes. (A) Multiple sequence alignment of insect SBP2 from the indicated species. Residues were colored using JalView based on BLOSUM62 score. The black line above the alignment denotes EST coverage of residues in the predicted A. aegypti SID peptide that are in an EST corresponding to the A. aegypti RBD. (B) Maximum likelihood tree of the insect SBP2 sequences used in panel A. In order to build the tree, the A. aegypti SID and RBD sequences were combined into one sequence file. (C) The genomic contexts of SBP2 from A. aegypti and C. quinquefasciatus and D. melanogaster were ascertained from Entrez Gene at NCBI. Arrows indicate gene orientation and gene names are as indicated.
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Figure 9: Aedes aegypti SBP2 is coded by two genes. (A) Multiple sequence alignment of insect SBP2 from the indicated species. Residues were colored using JalView based on BLOSUM62 score. The black line above the alignment denotes EST coverage of residues in the predicted A. aegypti SID peptide that are in an EST corresponding to the A. aegypti RBD. (B) Maximum likelihood tree of the insect SBP2 sequences used in panel A. In order to build the tree, the A. aegypti SID and RBD sequences were combined into one sequence file. (C) The genomic contexts of SBP2 from A. aegypti and C. quinquefasciatus and D. melanogaster were ascertained from Entrez Gene at NCBI. Arrows indicate gene orientation and gene names are as indicated.

Mentions: Chapple and Guigó recently investigated evolutionary relationships of insect selenoproteins and Sec incorporation factors [7]. In that work, a multiple sequence alignment of insect SBP2 showed that Aedes aegypti SBP2 contains an RNA binding domain but apparently lacks a Sec incorporation domain. This is striking as SBP2 from other insects, including the mosquitoes A. gambiae and Culex quinquefasciatus, contain a Sec incorporation domain [7]. We therefore performed a BLASTp search with default parameters but limited to A. aegypti (taxid: 7159) using C. quinquefasciatus SBP2 as a query. This search yielded the previously identified A. aegypti SBP2 RBD [7] and A. aegypti hypothetical protein AaeL_AAEL008122 (Expect = 7e-85; hereafter A. aegypti SID) which has 66% identity and 76% similarity to C. quinquefasciatus SBP23-275, suggesting that the SID is encoded by a separate gene in A. aegypti. A BLASTp search against A. aegypti using the SID of rat SBP2 (aa 504-530) as a query also identified the A. aegypti SID (Expect = 1e-04). A multiple sequence alignment of representative insect SID and RBD sequences is shown in Figure 9A. Phylogenetic inference of insect SBP2 using the WAG substitution model in PhyML placed A. aegypti SBP2 with that of other mosquitoes with strong bootstrap support (Figure 9B).


Evolutionary history of selenocysteine incorporation from the perspective of SECIS binding proteins.

Donovan J, Copeland PR - BMC Evol. Biol. (2009)

Aedes aegypti SBP2 is coded by two genes. (A) Multiple sequence alignment of insect SBP2 from the indicated species. Residues were colored using JalView based on BLOSUM62 score. The black line above the alignment denotes EST coverage of residues in the predicted A. aegypti SID peptide that are in an EST corresponding to the A. aegypti RBD. (B) Maximum likelihood tree of the insect SBP2 sequences used in panel A. In order to build the tree, the A. aegypti SID and RBD sequences were combined into one sequence file. (C) The genomic contexts of SBP2 from A. aegypti and C. quinquefasciatus and D. melanogaster were ascertained from Entrez Gene at NCBI. Arrows indicate gene orientation and gene names are as indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2746813&req=5

Figure 9: Aedes aegypti SBP2 is coded by two genes. (A) Multiple sequence alignment of insect SBP2 from the indicated species. Residues were colored using JalView based on BLOSUM62 score. The black line above the alignment denotes EST coverage of residues in the predicted A. aegypti SID peptide that are in an EST corresponding to the A. aegypti RBD. (B) Maximum likelihood tree of the insect SBP2 sequences used in panel A. In order to build the tree, the A. aegypti SID and RBD sequences were combined into one sequence file. (C) The genomic contexts of SBP2 from A. aegypti and C. quinquefasciatus and D. melanogaster were ascertained from Entrez Gene at NCBI. Arrows indicate gene orientation and gene names are as indicated.
Mentions: Chapple and Guigó recently investigated evolutionary relationships of insect selenoproteins and Sec incorporation factors [7]. In that work, a multiple sequence alignment of insect SBP2 showed that Aedes aegypti SBP2 contains an RNA binding domain but apparently lacks a Sec incorporation domain. This is striking as SBP2 from other insects, including the mosquitoes A. gambiae and Culex quinquefasciatus, contain a Sec incorporation domain [7]. We therefore performed a BLASTp search with default parameters but limited to A. aegypti (taxid: 7159) using C. quinquefasciatus SBP2 as a query. This search yielded the previously identified A. aegypti SBP2 RBD [7] and A. aegypti hypothetical protein AaeL_AAEL008122 (Expect = 7e-85; hereafter A. aegypti SID) which has 66% identity and 76% similarity to C. quinquefasciatus SBP23-275, suggesting that the SID is encoded by a separate gene in A. aegypti. A BLASTp search against A. aegypti using the SID of rat SBP2 (aa 504-530) as a query also identified the A. aegypti SID (Expect = 1e-04). A multiple sequence alignment of representative insect SID and RBD sequences is shown in Figure 9A. Phylogenetic inference of insect SBP2 using the WAG substitution model in PhyML placed A. aegypti SBP2 with that of other mosquitoes with strong bootstrap support (Figure 9B).

Bottom Line: In addition, we describe the emergence of a motif upstream of the SBP2 RNA binding domain that shares significant similarity with a motif within the pseudouridine synthase Cbf5.Our analysis suggests that SECIS binding proteins arose once in evolution but diverged significantly in multiple lineages.In addition, likely due to a gene duplication event in the early vertebrate lineage, SBP2 and SBP2L are paralogous in vertebrates.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular Genetics, Microbiology, and Immunology, Graduate School of Biomedical Sciences, University of Medicine and Dentistry of New Jersey - Robert Wood Johnson Medical School, Piscataway, NJ, USA. donovaje@umdnj.edu

ABSTRACT

Background: The co-translational incorporation of selenocysteine into nascent polypeptides by recoding the UGA stop codon occurs in all domains of life. In eukaryotes, this event requires at least three specific factors: SECIS binding protein 2 (SBP2), a specific translation elongation factor (eEFSec), selenocysteinyl tRNA, and a cis-acting selenocysteine insertion sequence (SECIS) element in selenoprotein mRNAs. While the phylogenetic relationships of selenoprotein families and the evolution of selenocysteine usage are well documented, the evolutionary history of SECIS binding proteins has not been explored.

Results: In this report we present a phylogeny of the eukaryotic SECIS binding protein family which includes SBP2 and a related protein we herein term SBP2L. Here we show that SBP2L is an SBP2 paralogue in vertebrates and is the only form of SECIS binding protein in invertebrate deuterostomes, suggesting a key role in Sec incorporation in these organisms, but an SBP2/SBP2L fusion protein is unable to support Sec incorporation in vitro. An in-depth phylogenetic analysis of the conserved L7Ae RNA binding domain suggests an ancestral relationship with ribosomal protein L30. In addition, we describe the emergence of a motif upstream of the SBP2 RNA binding domain that shares significant similarity with a motif within the pseudouridine synthase Cbf5.

Conclusion: Our analysis suggests that SECIS binding proteins arose once in evolution but diverged significantly in multiple lineages. In addition, likely due to a gene duplication event in the early vertebrate lineage, SBP2 and SBP2L are paralogous in vertebrates.

Show MeSH
Related in: MedlinePlus