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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

Integrated plasmid or virus-like genes in Phytophthora sp. (A) and Giardia intestinalis (B). Arrowhead boxes indicate ORFs (orange, Rep-like genes; other colors, unknown genes). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) or amino acid (aa) identity are indicated. The annotated ORF names or accession numbers are indicated. ψ, interrupted ORF.
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Figure 1: Integrated plasmid or virus-like genes in Phytophthora sp. (A) and Giardia intestinalis (B). Arrowhead boxes indicate ORFs (orange, Rep-like genes; other colors, unknown genes). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) or amino acid (aa) identity are indicated. The annotated ORF names or accession numbers are indicated. ψ, interrupted ORF.

Mentions: One apparently truncated Rep-like protein from the mitochondrion of oomycete Phytophthora sojae [35] contained Gemini_AL1 domain. Interestingly, we also found its coordinates in mitochondrion type II haplotypes of P. infestans [36] (Figure 1A), which has not been identified in previous reports. The mitochondrial regions containing the Rep-like sequences were absent in mitochondrion of P. ramorum and the type I haplotypes of P. infestans [36]. In addition, they are most closely related to the Reps of plasmids from the red algae Porphyra tenera [37]. These findings suggest that the Rep-like sequences are most likely derived from an integrated plasmid. Two circovirus Rep-related sequences have been found in the genome of canarypox virus [38] but not in other poxviruses, thus suggesting that they were acquired horizontally.


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)

Integrated plasmid or virus-like genes in Phytophthora sp. (A) and Giardia intestinalis (B). Arrowhead boxes indicate ORFs (orange, Rep-like genes; other colors, unknown genes). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) or amino acid (aa) identity are indicated. The annotated ORF names or accession numbers are indicated. ψ, interrupted ORF.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Integrated plasmid or virus-like genes in Phytophthora sp. (A) and Giardia intestinalis (B). Arrowhead boxes indicate ORFs (orange, Rep-like genes; other colors, unknown genes). Gray sectors connect corresponding homologous regions and the % nucleotide (nt) or amino acid (aa) identity are indicated. The annotated ORF names or accession numbers are indicated. ψ, interrupted ORF.
Mentions: One apparently truncated Rep-like protein from the mitochondrion of oomycete Phytophthora sojae [35] contained Gemini_AL1 domain. Interestingly, we also found its coordinates in mitochondrion type II haplotypes of P. infestans [36] (Figure 1A), which has not been identified in previous reports. The mitochondrial regions containing the Rep-like sequences were absent in mitochondrion of P. ramorum and the type I haplotypes of P. infestans [36]. In addition, they are most closely related to the Reps of plasmids from the red algae Porphyra tenera [37]. These findings suggest that the Rep-like sequences are most likely derived from an integrated plasmid. Two circovirus Rep-related sequences have been found in the genome of canarypox virus [38] but not in other poxviruses, thus suggesting that they were acquired horizontally.

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