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Gene conversion and purifying selection of a placenta-specific ERV-V envelope gene during simian evolution.

Kjeldbjerg AL, Villesen P, Aagaard L, Pedersen FS - BMC Evol. Biol. (2008)

Bottom Line: The ENVV2 gene is preserved with an intact reading frame during simian evolution, but none of the ENVV genes are found in the prosimian species tested.This is the first case of gene conversion involving long open reading frames in HERVs.Together with the placenta-specific expression of the human and baboon ENVV1 and ENVV2 envelope genes, these data provide strong evidence of a beneficial role for the host.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular Biology, University of Aarhus, DK-8000 Aarhus C, Denmark. alk@mb.au.dk

ABSTRACT

Background: Most human endogenous retroviruses (HERVs) invaded our genome at least 25 million years ago. The majority of the viral genes are degenerated, since no selection preserves them within the genome. However, a few intact and very old HERV genes exist, and likely are beneficial for the host. We here address evolutionary aspects of two HERV-V envelope genes, ENVV1 and ENVV2, located in tandem and containing a long open reading frame.

Results: The ENVV2 gene is preserved with an intact reading frame during simian evolution, but none of the ENVV genes are found in the prosimian species tested. While we observe many transposon insertions in the gag and pol regions of the ERV-V2 provirus, the ENVV2 genes have escaped transposon crossfire in all species tested. Additional analysis of nucleotide substitutions provides further strong evidence of purifying selection on the ENVV2 gene during primate evolution. The other copy, ENVV1, seems to be involved in gene conversion of the major part of the envelope. Furthermore, ENVV1 and ENVV2 show placenta-specific expression in human and a baboon species.

Conclusion: Our analyses show that ERV-V entered our genome after the split between simian and prosimian primates. Subsequent purifying selection and gene conversion have preserved two copies of the ENVV envelope gene in most species. This is the first case of gene conversion involving long open reading frames in HERVs. Together with the placenta-specific expression of the human and baboon ENVV1 and ENVV2 envelope genes, these data provide strong evidence of a beneficial role for the host.

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ENVV2 annotation. Annotation of the human HERV-V2 locus showing the high content of SINE elements in this region. Gag, pol and env tBLASTn hits are indicated by red, green and blue, predicted LTR regions (yellow). The region undergoing gene conversion is indicated by vertical dashed lines (see text). Splice donor site and poly A signal are predicted sites.
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Figure 5: ENVV2 annotation. Annotation of the human HERV-V2 locus showing the high content of SINE elements in this region. Gag, pol and env tBLASTn hits are indicated by red, green and blue, predicted LTR regions (yellow). The region undergoing gene conversion is indicated by vertical dashed lines (see text). Splice donor site and poly A signal are predicted sites.

Mentions: The HERV-V2 locus contains eight SINE elements all located closely outside ENVV2, both inside and between gag and pol fragments (Figure 5). Assuming a random distribution of SINE elements within the HERV-V2 locus (i.e. assuming no selection on the ENVV2 region), the probability of observing the 8 SINE elements outside and 0 SINE elements inside the ENVV2 gene is significant (P = 0.048), indicating that the ENVV2 gene has survived transposon crossfire.


Gene conversion and purifying selection of a placenta-specific ERV-V envelope gene during simian evolution.

Kjeldbjerg AL, Villesen P, Aagaard L, Pedersen FS - BMC Evol. Biol. (2008)

ENVV2 annotation. Annotation of the human HERV-V2 locus showing the high content of SINE elements in this region. Gag, pol and env tBLASTn hits are indicated by red, green and blue, predicted LTR regions (yellow). The region undergoing gene conversion is indicated by vertical dashed lines (see text). Splice donor site and poly A signal are predicted sites.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2567338&req=5

Figure 5: ENVV2 annotation. Annotation of the human HERV-V2 locus showing the high content of SINE elements in this region. Gag, pol and env tBLASTn hits are indicated by red, green and blue, predicted LTR regions (yellow). The region undergoing gene conversion is indicated by vertical dashed lines (see text). Splice donor site and poly A signal are predicted sites.
Mentions: The HERV-V2 locus contains eight SINE elements all located closely outside ENVV2, both inside and between gag and pol fragments (Figure 5). Assuming a random distribution of SINE elements within the HERV-V2 locus (i.e. assuming no selection on the ENVV2 region), the probability of observing the 8 SINE elements outside and 0 SINE elements inside the ENVV2 gene is significant (P = 0.048), indicating that the ENVV2 gene has survived transposon crossfire.

Bottom Line: The ENVV2 gene is preserved with an intact reading frame during simian evolution, but none of the ENVV genes are found in the prosimian species tested.This is the first case of gene conversion involving long open reading frames in HERVs.Together with the placenta-specific expression of the human and baboon ENVV1 and ENVV2 envelope genes, these data provide strong evidence of a beneficial role for the host.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular Biology, University of Aarhus, DK-8000 Aarhus C, Denmark. alk@mb.au.dk

ABSTRACT

Background: Most human endogenous retroviruses (HERVs) invaded our genome at least 25 million years ago. The majority of the viral genes are degenerated, since no selection preserves them within the genome. However, a few intact and very old HERV genes exist, and likely are beneficial for the host. We here address evolutionary aspects of two HERV-V envelope genes, ENVV1 and ENVV2, located in tandem and containing a long open reading frame.

Results: The ENVV2 gene is preserved with an intact reading frame during simian evolution, but none of the ENVV genes are found in the prosimian species tested. While we observe many transposon insertions in the gag and pol regions of the ERV-V2 provirus, the ENVV2 genes have escaped transposon crossfire in all species tested. Additional analysis of nucleotide substitutions provides further strong evidence of purifying selection on the ENVV2 gene during primate evolution. The other copy, ENVV1, seems to be involved in gene conversion of the major part of the envelope. Furthermore, ENVV1 and ENVV2 show placenta-specific expression in human and a baboon species.

Conclusion: Our analyses show that ERV-V entered our genome after the split between simian and prosimian primates. Subsequent purifying selection and gene conversion have preserved two copies of the ENVV envelope gene in most species. This is the first case of gene conversion involving long open reading frames in HERVs. Together with the placenta-specific expression of the human and baboon ENVV1 and ENVV2 envelope genes, these data provide strong evidence of a beneficial role for the host.

Show MeSH
Related in: MedlinePlus