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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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Related in: MedlinePlus

Genomic organization of ssDNA virus-like transposons in fungi (A) and lower eukaryotes (B). (A) The genomic organization of geminivirus-like transposon in Tuber melanosporum. Arrowhead boxes indicate ORFs (orange, Rep-like gene; blue, transposase gene). The black vertical lines in the arrowhead boxes indicate stop codons. Green rectangular box indicates microsatellite sequence. The sequence of terminal inverted repeat (TIR) is shown at the top to the right. (B) The genomic organization and comparison of parvovirus-like transposon with related exogenous planaria virus. Yellow arrowhead boxes indicate Rep-like ORFs. Swallow tails indicate terminal inverted repeats (TIRs). The annotated ORF names are indicated. Purple rectangular boxes indicate protein domains and the domain family names are shown: Parvo_NS1, Parvovirus non-structural protein NS1 (pfam01057); Parvo_coat_N, Parvovirus coat protein VP1 (pfam08398); PPV_E1_C, Papillomavirus helicase (pfam00519). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) or amino acid (aa) identity are indicated. The Planaria asexual strain-specific virus-like element has not been found to integrate in the host genome.
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Figure 5: Genomic organization of ssDNA virus-like transposons in fungi (A) and lower eukaryotes (B). (A) The genomic organization of geminivirus-like transposon in Tuber melanosporum. Arrowhead boxes indicate ORFs (orange, Rep-like gene; blue, transposase gene). The black vertical lines in the arrowhead boxes indicate stop codons. Green rectangular box indicates microsatellite sequence. The sequence of terminal inverted repeat (TIR) is shown at the top to the right. (B) The genomic organization and comparison of parvovirus-like transposon with related exogenous planaria virus. Yellow arrowhead boxes indicate Rep-like ORFs. Swallow tails indicate terminal inverted repeats (TIRs). The annotated ORF names are indicated. Purple rectangular boxes indicate protein domains and the domain family names are shown: Parvo_NS1, Parvovirus non-structural protein NS1 (pfam01057); Parvo_coat_N, Parvovirus coat protein VP1 (pfam08398); PPV_E1_C, Papillomavirus helicase (pfam00519). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) or amino acid (aa) identity are indicated. The Planaria asexual strain-specific virus-like element has not been found to integrate in the host genome.

Mentions: There are 42 geminivirus-like Rep genes or remnants interspersed in the genome of Perigord black truffle (Tuber melanosporum), an ectomycorrhizal fungus. All but one are most closely related to each other and formed a distinct clade (Figure 4). They share high (> 95%) nucleotide sequence identities with each other and thus allow us to reconstruct a consensus sequence. The reconstructed copy contains one interrupted Rep-like open reading frame (ORF), two transposase ORFs (one is interrupted and the other is truncated), and one microsatellite sequence (Figure 5A). It also contains 37-bp terminal inverted repeats (TIRs) but no obvious target site duplications (TSDs). It is most likely that this copy represents a novel transposon related to geminivirus identified in a eukaryotic genome. The genetic distances among these transposable repeats are very short suggesting that the transposons have undergone recent large-scale amplification in the host genome.


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 organization of ssDNA virus-like transposons in fungi (A) and lower eukaryotes (B). (A) The genomic organization of geminivirus-like transposon in Tuber melanosporum. Arrowhead boxes indicate ORFs (orange, Rep-like gene; blue, transposase gene). The black vertical lines in the arrowhead boxes indicate stop codons. Green rectangular box indicates microsatellite sequence. The sequence of terminal inverted repeat (TIR) is shown at the top to the right. (B) The genomic organization and comparison of parvovirus-like transposon with related exogenous planaria virus. Yellow arrowhead boxes indicate Rep-like ORFs. Swallow tails indicate terminal inverted repeats (TIRs). The annotated ORF names are indicated. Purple rectangular boxes indicate protein domains and the domain family names are shown: Parvo_NS1, Parvovirus non-structural protein NS1 (pfam01057); Parvo_coat_N, Parvovirus coat protein VP1 (pfam08398); PPV_E1_C, Papillomavirus helicase (pfam00519). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) or amino acid (aa) identity are indicated. The Planaria asexual strain-specific virus-like element has not been found to integrate in the host genome.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Genomic organization of ssDNA virus-like transposons in fungi (A) and lower eukaryotes (B). (A) The genomic organization of geminivirus-like transposon in Tuber melanosporum. Arrowhead boxes indicate ORFs (orange, Rep-like gene; blue, transposase gene). The black vertical lines in the arrowhead boxes indicate stop codons. Green rectangular box indicates microsatellite sequence. The sequence of terminal inverted repeat (TIR) is shown at the top to the right. (B) The genomic organization and comparison of parvovirus-like transposon with related exogenous planaria virus. Yellow arrowhead boxes indicate Rep-like ORFs. Swallow tails indicate terminal inverted repeats (TIRs). The annotated ORF names are indicated. Purple rectangular boxes indicate protein domains and the domain family names are shown: Parvo_NS1, Parvovirus non-structural protein NS1 (pfam01057); Parvo_coat_N, Parvovirus coat protein VP1 (pfam08398); PPV_E1_C, Papillomavirus helicase (pfam00519). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) or amino acid (aa) identity are indicated. The Planaria asexual strain-specific virus-like element has not been found to integrate in the host genome.
Mentions: There are 42 geminivirus-like Rep genes or remnants interspersed in the genome of Perigord black truffle (Tuber melanosporum), an ectomycorrhizal fungus. All but one are most closely related to each other and formed a distinct clade (Figure 4). They share high (> 95%) nucleotide sequence identities with each other and thus allow us to reconstruct a consensus sequence. The reconstructed copy contains one interrupted Rep-like open reading frame (ORF), two transposase ORFs (one is interrupted and the other is truncated), and one microsatellite sequence (Figure 5A). It also contains 37-bp terminal inverted repeats (TIRs) but no obvious target site duplications (TSDs). It is most likely that this copy represents a novel transposon related to geminivirus identified in a eukaryotic genome. The genetic distances among these transposable repeats are very short suggesting that the transposons have undergone recent large-scale amplification in the host genome.

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