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Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes.

Liu H, Fu Y, Li B, Yu X, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D - BMC Evol. Biol. (2011)

Bottom Line: In eukaryotes, retroviruses, which can integrate into host genome as an obligate step in their replication strategy, comprise approximately 8% of the human genome.We conclude that the replication initiation protein (Rep)-related sequences of geminiviruses, nanoviruses and circoviruses have been frequently transferred to a broad range of eukaryotic species, including plants, fungi, animals and protists.Some of the transferred viral genes were conserved and expressed, suggesting that these genes have been coopted to assume cellular functions in the host genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, Hubei Province, P R China.

ABSTRACT

Background: In addition to vertical transmission, organisms can also acquire genes from other distantly related species or from their extra-chromosomal elements (plasmids and viruses) via horizontal gene transfer (HGT). It has been suggested that phages represent substantial forces in prokaryotic evolution. In eukaryotes, retroviruses, which can integrate into host genome as an obligate step in their replication strategy, comprise approximately 8% of the human genome. Unlike retroviruses, few members of other virus families are known to transfer genes to host genomes.

Results: Here we performed a systematic search for sequences related to circular single-stranded DNA (ssDNA) viruses in publicly available eukaryotic genome databases followed by comprehensive phylogenetic analysis. We conclude that the replication initiation protein (Rep)-related sequences of geminiviruses, nanoviruses and circoviruses have been frequently transferred to a broad range of eukaryotic species, including plants, fungi, animals and protists. Some of the transferred viral genes were conserved and expressed, suggesting that these genes have been coopted to assume cellular functions in the host genomes. We also identified geminivirus-like and parvovirus-like transposable elements in genomes of fungi and lower animals, respectively, and thereby provide direct evidence that eukaryotic transposons could derive from ssDNA viruses.

Conclusions: Our discovery extends the host range of circular ssDNA viruses and sheds light on the origin and evolution of these viruses. It also suggests that ssDNA viruses act as an unforeseen source of genetic innovation in their hosts.

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Genomic comparisons showing the endogenous viral sequences inserted into coding regions of host genes. Rectangular boxes with arrowheads indicate genes (Red, viral Rep-like genes; blue, host genes). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) identity scores are indicated.
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Figure 3: Genomic comparisons showing the endogenous viral sequences inserted into coding regions of host genes. Rectangular boxes with arrowheads indicate genes (Red, viral Rep-like genes; blue, host genes). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) identity scores are indicated.

Mentions: Compared to related exogenous viral genes, some endogenous virus-like sequences are full-length or near full-length genes while many others comprise only gene fragments. Despite pronounced sequence divergence, the conserved motifs of Rep protein can still be easily found in putative protein sequences of endogenous virus-like genes (see Additional file 1: Figure S2 and S3). The endogenous viral sequences are generally interspersed within non-coding regions of host genomes but several were found to be inserted into the coding regions of host genes or transposons (Figure 3). This finding suggests that these viral sequences have influenced host genome evolution through gene disruption.


Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes.

Liu H, Fu Y, Li B, Yu X, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D - BMC Evol. Biol. (2011)

Genomic comparisons showing the endogenous viral sequences inserted into coding regions of host genes. Rectangular boxes with arrowheads indicate genes (Red, viral Rep-like genes; blue, host genes). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) identity scores are indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3198968&req=5

Figure 3: Genomic comparisons showing the endogenous viral sequences inserted into coding regions of host genes. Rectangular boxes with arrowheads indicate genes (Red, viral Rep-like genes; blue, host genes). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) identity scores are indicated.
Mentions: Compared to related exogenous viral genes, some endogenous virus-like sequences are full-length or near full-length genes while many others comprise only gene fragments. Despite pronounced sequence divergence, the conserved motifs of Rep protein can still be easily found in putative protein sequences of endogenous virus-like genes (see Additional file 1: Figure S2 and S3). The endogenous viral sequences are generally interspersed within non-coding regions of host genomes but several were found to be inserted into the coding regions of host genes or transposons (Figure 3). This finding suggests that these viral sequences have influenced host genome evolution through gene disruption.

Bottom Line: In eukaryotes, retroviruses, which can integrate into host genome as an obligate step in their replication strategy, comprise approximately 8% of the human genome.We conclude that the replication initiation protein (Rep)-related sequences of geminiviruses, nanoviruses and circoviruses have been frequently transferred to a broad range of eukaryotic species, including plants, fungi, animals and protists.Some of the transferred viral genes were conserved and expressed, suggesting that these genes have been coopted to assume cellular functions in the host genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, Hubei Province, P R China.

ABSTRACT

Background: In addition to vertical transmission, organisms can also acquire genes from other distantly related species or from their extra-chromosomal elements (plasmids and viruses) via horizontal gene transfer (HGT). It has been suggested that phages represent substantial forces in prokaryotic evolution. In eukaryotes, retroviruses, which can integrate into host genome as an obligate step in their replication strategy, comprise approximately 8% of the human genome. Unlike retroviruses, few members of other virus families are known to transfer genes to host genomes.

Results: Here we performed a systematic search for sequences related to circular single-stranded DNA (ssDNA) viruses in publicly available eukaryotic genome databases followed by comprehensive phylogenetic analysis. We conclude that the replication initiation protein (Rep)-related sequences of geminiviruses, nanoviruses and circoviruses have been frequently transferred to a broad range of eukaryotic species, including plants, fungi, animals and protists. Some of the transferred viral genes were conserved and expressed, suggesting that these genes have been coopted to assume cellular functions in the host genomes. We also identified geminivirus-like and parvovirus-like transposable elements in genomes of fungi and lower animals, respectively, and thereby provide direct evidence that eukaryotic transposons could derive from ssDNA viruses.

Conclusions: Our discovery extends the host range of circular ssDNA viruses and sheds light on the origin and evolution of these viruses. It also suggests that ssDNA viruses act as an unforeseen source of genetic innovation in their hosts.

Show MeSH
Related in: MedlinePlus