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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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Convergence of a short motif in Cbf5 and SECIS binding proteins. Maximum likelihood tree of Cbf5 and SECIS binding proteins inferred using PhyML with 1000 bootstraps. Bootstrap values below 0.5 are not show. The alignment used to generate the tree is shown to the right.
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Figure 8: Convergence of a short motif in Cbf5 and SECIS binding proteins. Maximum likelihood tree of Cbf5 and SECIS binding proteins inferred using PhyML with 1000 bootstraps. Bootstrap values below 0.5 are not show. The alignment used to generate the tree is shown to the right.

Mentions: Caban and colleagues recently performed structure/function studies on the SBP2 RNA binding domain including its L7Ae motif [13]. In this work they noted that SBP2 residues in the region of RFQDR654-658 N-terminal to the L7Ae core were required for Sec incorporation but not SECIS element or ribosome binding. Interestingly, these residues are not conserved among the various subgroups of the L7Ae superfamily. Accordingly, we sought to determine whether or not this motif and residues in its vicinity had a discernible relative. A BLASTp search against the Protein Data Bank with relaxed settings and rat SBP2 as a query expectedly yielded hits of various L7Ae family members. However, this search also produced a hit for Methanococcus jannaschii Cbf5, the H/ACA sRNA guided pseudouridylate synthase [[26], reviewed in [27]]. Querying the CDD with rat SBP2 and relaxed settings (Expect Threshold = 10) also yielded a hit against Cbf5 (Expect = 2.3). This corresponded to rat SBP2642-666 and and Pyrococcus horikoshii Cbf5125-150. In addition, PSI-BLAST using full length rat SBP2 as the initial query independently led to the identification of Cbf5 as a potential relative (data not shown). Notably, the only region of significant similarity is that between RFQDR654-658 and the universally conserved Gly residue in the L7Ae RNA binding motif (G676). Figure 8 shows a multiple sequence alignment and phylogenetic tree illustrating the relationship between the Cbf5 and SBP2. The conservation of this region among the Cbf5 group from archaea to mammals is quite high with strong clade support, but the highest level of conservation is between archaeal Cbf5 and vertebrate SBP2. The substantial divergence between the Cbf5 motif and that observed in SBP2 from unicellular eukaryotes and protostomes and the short length of the motif suggests that it may have arisen as a result of convergent evolution.


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

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

Convergence of a short motif in Cbf5 and SECIS binding proteins. Maximum likelihood tree of Cbf5 and SECIS binding proteins inferred using PhyML with 1000 bootstraps. Bootstrap values below 0.5 are not show. The alignment used to generate the tree is shown to the right.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Convergence of a short motif in Cbf5 and SECIS binding proteins. Maximum likelihood tree of Cbf5 and SECIS binding proteins inferred using PhyML with 1000 bootstraps. Bootstrap values below 0.5 are not show. The alignment used to generate the tree is shown to the right.
Mentions: Caban and colleagues recently performed structure/function studies on the SBP2 RNA binding domain including its L7Ae motif [13]. In this work they noted that SBP2 residues in the region of RFQDR654-658 N-terminal to the L7Ae core were required for Sec incorporation but not SECIS element or ribosome binding. Interestingly, these residues are not conserved among the various subgroups of the L7Ae superfamily. Accordingly, we sought to determine whether or not this motif and residues in its vicinity had a discernible relative. A BLASTp search against the Protein Data Bank with relaxed settings and rat SBP2 as a query expectedly yielded hits of various L7Ae family members. However, this search also produced a hit for Methanococcus jannaschii Cbf5, the H/ACA sRNA guided pseudouridylate synthase [[26], reviewed in [27]]. Querying the CDD with rat SBP2 and relaxed settings (Expect Threshold = 10) also yielded a hit against Cbf5 (Expect = 2.3). This corresponded to rat SBP2642-666 and and Pyrococcus horikoshii Cbf5125-150. In addition, PSI-BLAST using full length rat SBP2 as the initial query independently led to the identification of Cbf5 as a potential relative (data not shown). Notably, the only region of significant similarity is that between RFQDR654-658 and the universally conserved Gly residue in the L7Ae RNA binding motif (G676). Figure 8 shows a multiple sequence alignment and phylogenetic tree illustrating the relationship between the Cbf5 and SBP2. The conservation of this region among the Cbf5 group from archaea to mammals is quite high with strong clade support, but the highest level of conservation is between archaeal Cbf5 and vertebrate SBP2. The substantial divergence between the Cbf5 motif and that observed in SBP2 from unicellular eukaryotes and protostomes and the short length of the motif suggests that it may have arisen as a result of convergent evolution.

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