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Evolution of selenoproteins in the metazoan.

Jiang L, Ni J, Liu Q - BMC Genomics (2012)

Bottom Line: Amphioxus was found to have the most abundant and variant selenoproteins of any animal currently characterized, including a special selenoprotein P (SelP) possessing 3 repeated Trx-like domains and Sec residues in the N-terminal and 2 Sec residues in the C-terminal.During evolutionary history, only a few new selenoproteins have emerged and few were lost.Furthermore, the massive loss of selenoproteins in nematodes and insects likely occurred independently in isolated partial evolutionary branches.

View Article: PubMed Central - HTML - PubMed

Affiliation: College of Life Sciences, Shenzhen University, Shenzhen, 518060, Guangdong Province, PR, China.

ABSTRACT

Background: The selenocysteine (Sec) containing proteins, selenoproteins, are an important group of proteins present throughout all 3 kingdoms of life. With the rapid progression of selenoprotein research in the post-genomic era, application of bioinformatics methods to the identification of selenoproteins in newly sequenced species has become increasingly important. Although selenoproteins in human and other vertebrates have been investigated, studies of primitive invertebrate selenoproteomes are rarely reported outside of insects and nematodes.

Result: A more integrated view of selenoprotein evolution was constructed using several representative species from different evolutionary eras. Using a SelGenAmic-based selenoprotein identification method, 178 selenoprotein genes were identified in 6 invertebrates: Amphimedon queenslandica, Trichoplax adhaerens, Nematostella vectensis, Lottia gigantean, Capitella teleta, and Branchiostoma floridae. Amphioxus was found to have the most abundant and variant selenoproteins of any animal currently characterized, including a special selenoprotein P (SelP) possessing 3 repeated Trx-like domains and Sec residues in the N-terminal and 2 Sec residues in the C-terminal. This gene structure suggests the existence of two different strategies for extension of Sec numbers in SelP for the preservation and transportation of selenium. In addition, novel eukaryotic AphC-like selenoproteins were identified in sponges.

Conclusion: Comparison of various animal species suggests that even the most primitive animals possess a selenoproteome range and variety similar to humans. During evolutionary history, only a few new selenoproteins have emerged and few were lost. Furthermore, the massive loss of selenoproteins in nematodes and insects likely occurred independently in isolated partial evolutionary branches.

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Gene structures of Branchiostoma floridae DIs and  Trichoplax adhaerens DIs. A. Gene clusters of Bf.DI_a, Bf.DI_b and Bf.DI_c. The schematic position (under the coordinate) of Bf.DI_b indicates that this gene is on the minus strand. Two strong SECIS elements are located downstream of Bf.DI_b. B. Gene cluster of 6 Ta DIs. Ta.DI_h, Ta.DI_i and Ta.DI_j on the minus strand. A strong SECIS element is located downstream of each of Ta.DI_g, Ta.DI_i and Ta.DI_j.
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Figure 5: Gene structures of Branchiostoma floridae DIs and Trichoplax adhaerens DIs. A. Gene clusters of Bf.DI_a, Bf.DI_b and Bf.DI_c. The schematic position (under the coordinate) of Bf.DI_b indicates that this gene is on the minus strand. Two strong SECIS elements are located downstream of Bf.DI_b. B. Gene cluster of 6 Ta DIs. Ta.DI_h, Ta.DI_i and Ta.DI_j on the minus strand. A strong SECIS element is located downstream of each of Ta.DI_g, Ta.DI_i and Ta.DI_j.

Mentions: The gene cluster of Bf.SelP_a and 3NSelP was not the only cluster observed in invertebrate selenoproteins. The most significant amount of gene clusters occurred in the iodothyronine deiodinase (DI) family. In the eukaryotic kingdom, almost all DI proteins were found in multicellular animals. Especially in vertebrates, all animals reportedly included selenoproteins containing DI. In the current study, no DI was found in Amphimedon queenslandica, and only Cys-form DI genes were found in Nematostella vectensis. The clustering duplication of DI was found in Branchiostoma floridae, Trichoplax adhaerens, and Lottia gigantea. In some of these clusters, 3 or more duplicated genes were tandemly locate in one genome sequence. As seen in Figure 5A, the genes Bf.DI_a, Bf.DI_b, and Bf.DI_c constitute a cluster in which Bf.DI_a and Bf.DI_c are located in the positive strand, while Bf.DI_b is located in the minus strand. Interestingly, 2 strong SECIS elements are located downstream of Bf.DI_b. (Another rare 2 SECIS element containing gene is Nv.Gpx_a found in Nematostella vectensis, as shown in Additional file1: Figure S1 and Figure S3). One of these SECIS elements, however, was not necessary for DI, which possesses only the one TGA codon required for read-through. Because this element appears to serve no current function, future evolutions of this cluster may exhibit loss of the additional SECIS elements. Gene duplication, recombination, and divergence are the main force of genetic evolution[34], and thus clusters consisting of similar genes can be seen as a record of evolutionary events. The 2 SECIS elements of Bf2DI are potentially a result of nonreciprocal recombination during duplication, wherein the DNA sequence including the SECIS elements was copied more times than other sections. The largest gene cluster was found in the Trichoplax adhaerens, where 6 DI genes were located tandemly in different strands (Figure 5B). Notably, not all of the genes in this cluster possessed a SECIS element. Only 3 strong SECIS elements were found in the 3 intergenic regions among the middle 4 genes of this cluster.


Evolution of selenoproteins in the metazoan.

Jiang L, Ni J, Liu Q - BMC Genomics (2012)

Gene structures of Branchiostoma floridae DIs and  Trichoplax adhaerens DIs. A. Gene clusters of Bf.DI_a, Bf.DI_b and Bf.DI_c. The schematic position (under the coordinate) of Bf.DI_b indicates that this gene is on the minus strand. Two strong SECIS elements are located downstream of Bf.DI_b. B. Gene cluster of 6 Ta DIs. Ta.DI_h, Ta.DI_i and Ta.DI_j on the minus strand. A strong SECIS element is located downstream of each of Ta.DI_g, Ta.DI_i and Ta.DI_j.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3473315&req=5

Figure 5: Gene structures of Branchiostoma floridae DIs and Trichoplax adhaerens DIs. A. Gene clusters of Bf.DI_a, Bf.DI_b and Bf.DI_c. The schematic position (under the coordinate) of Bf.DI_b indicates that this gene is on the minus strand. Two strong SECIS elements are located downstream of Bf.DI_b. B. Gene cluster of 6 Ta DIs. Ta.DI_h, Ta.DI_i and Ta.DI_j on the minus strand. A strong SECIS element is located downstream of each of Ta.DI_g, Ta.DI_i and Ta.DI_j.
Mentions: The gene cluster of Bf.SelP_a and 3NSelP was not the only cluster observed in invertebrate selenoproteins. The most significant amount of gene clusters occurred in the iodothyronine deiodinase (DI) family. In the eukaryotic kingdom, almost all DI proteins were found in multicellular animals. Especially in vertebrates, all animals reportedly included selenoproteins containing DI. In the current study, no DI was found in Amphimedon queenslandica, and only Cys-form DI genes were found in Nematostella vectensis. The clustering duplication of DI was found in Branchiostoma floridae, Trichoplax adhaerens, and Lottia gigantea. In some of these clusters, 3 or more duplicated genes were tandemly locate in one genome sequence. As seen in Figure 5A, the genes Bf.DI_a, Bf.DI_b, and Bf.DI_c constitute a cluster in which Bf.DI_a and Bf.DI_c are located in the positive strand, while Bf.DI_b is located in the minus strand. Interestingly, 2 strong SECIS elements are located downstream of Bf.DI_b. (Another rare 2 SECIS element containing gene is Nv.Gpx_a found in Nematostella vectensis, as shown in Additional file1: Figure S1 and Figure S3). One of these SECIS elements, however, was not necessary for DI, which possesses only the one TGA codon required for read-through. Because this element appears to serve no current function, future evolutions of this cluster may exhibit loss of the additional SECIS elements. Gene duplication, recombination, and divergence are the main force of genetic evolution[34], and thus clusters consisting of similar genes can be seen as a record of evolutionary events. The 2 SECIS elements of Bf2DI are potentially a result of nonreciprocal recombination during duplication, wherein the DNA sequence including the SECIS elements was copied more times than other sections. The largest gene cluster was found in the Trichoplax adhaerens, where 6 DI genes were located tandemly in different strands (Figure 5B). Notably, not all of the genes in this cluster possessed a SECIS element. Only 3 strong SECIS elements were found in the 3 intergenic regions among the middle 4 genes of this cluster.

Bottom Line: Amphioxus was found to have the most abundant and variant selenoproteins of any animal currently characterized, including a special selenoprotein P (SelP) possessing 3 repeated Trx-like domains and Sec residues in the N-terminal and 2 Sec residues in the C-terminal.During evolutionary history, only a few new selenoproteins have emerged and few were lost.Furthermore, the massive loss of selenoproteins in nematodes and insects likely occurred independently in isolated partial evolutionary branches.

View Article: PubMed Central - HTML - PubMed

Affiliation: College of Life Sciences, Shenzhen University, Shenzhen, 518060, Guangdong Province, PR, China.

ABSTRACT

Background: The selenocysteine (Sec) containing proteins, selenoproteins, are an important group of proteins present throughout all 3 kingdoms of life. With the rapid progression of selenoprotein research in the post-genomic era, application of bioinformatics methods to the identification of selenoproteins in newly sequenced species has become increasingly important. Although selenoproteins in human and other vertebrates have been investigated, studies of primitive invertebrate selenoproteomes are rarely reported outside of insects and nematodes.

Result: A more integrated view of selenoprotein evolution was constructed using several representative species from different evolutionary eras. Using a SelGenAmic-based selenoprotein identification method, 178 selenoprotein genes were identified in 6 invertebrates: Amphimedon queenslandica, Trichoplax adhaerens, Nematostella vectensis, Lottia gigantean, Capitella teleta, and Branchiostoma floridae. Amphioxus was found to have the most abundant and variant selenoproteins of any animal currently characterized, including a special selenoprotein P (SelP) possessing 3 repeated Trx-like domains and Sec residues in the N-terminal and 2 Sec residues in the C-terminal. This gene structure suggests the existence of two different strategies for extension of Sec numbers in SelP for the preservation and transportation of selenium. In addition, novel eukaryotic AphC-like selenoproteins were identified in sponges.

Conclusion: Comparison of various animal species suggests that even the most primitive animals possess a selenoproteome range and variety similar to humans. During evolutionary history, only a few new selenoproteins have emerged and few were lost. Furthermore, the massive loss of selenoproteins in nematodes and insects likely occurred independently in isolated partial evolutionary branches.

Show MeSH
Related in: MedlinePlus