title: Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes.
abstract: Horizontal gene transfer commonly occurs from cells to viruses but rarely occurs from viruses to their host cells, with the exception of retroviruses and some DNA viruses. However, extensive sequence similarity searches in public genome databases for various organisms showed that the capsid protein and RNA-dependent RNA polymerase genes from totiviruses and partitiviruses have widespread homologs in the nuclear genomes of eukaryotic organisms, including plants, arthropods, fungi, nematodes, and protozoa. PCR amplification and sequencing as well as comparative evidence of junction coverage between virus and host sequences support the conclusion that these viral homologs are real and occur in eukaryotic genomes. Sequence comparison and phylogenetic analysis suggest that these genes were likely transferred horizontally from viruses to eukaryotic genomes. Furthermore, we present evidence showing that some of the transferred genes are conserved and expressed in eukaryotic organisms and suggesting that these viral genes are also functional in the recipient genomes. Our findings imply that horizontal transfer of double-stranded RNA viral genes is widespread among eukaryotes and may give rise to functionally important new genes, thus entailing that RNA viruses may play significant roles in the evolution of eukaryotes.
authors.affiliation: College of Plant Science and Technology, Huazhong Agricultural University, Hubei Province, People's Republic of China.
authors.forename: Huiquan
authors.initials: H
authors.lastname: Liu
authors.forename: Yanping
authors.initials: Y
authors.lastname: Fu
authors.forename: Daohong
authors.initials: D
authors.lastname: Jiang
authors.forename: Guoqing
authors.initials: G
authors.lastname: Li
authors.forename: Jiatao
authors.initials: J
authors.lastname: Xie
authors.forename: Jiasen
authors.initials: J
authors.lastname: Cheng
authors.forename: Youliang
authors.initials: Y
authors.lastname: Peng
authors.forename: Said A
authors.initials: SA
authors.lastname: Ghabrial
authors.forename: Xianhong
authors.initials: X
authors.lastname: Yi
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D002467:Cell Nucleus / Q000235:genetics / Q000821:virology*; D056890:Eukaryota / Q000235:genetics* / Q000821:virology*; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D016678:Genome; D008969:Molecular Sequence Data; D010802:Phylogeny; D010944:Plants / Q000235:genetics / Q000821:virology; D012328:RNA Viruses / Q000145:classification / Q000235:genetics* / Q000502:physiology; D012330:RNA, Double-Stranded / Q000235:genetics; D012367:RNA, Viral / Q000235:genetics; D016415:Sequence Alignment
chemical_list: D012330:RNA, Double-Stranded; D012367:RNA, Viral
references.citation: Nat Rev Microbiol. 2009 Apr;7(4):306-11
references.pmid: 19270719
references.citation: Virology. 2005 Feb 20;332(2):614-22
references.pmid: 15680426
references.citation: Genome Res. 2009 Aug;19(8):1441-9
references.pmid: 19451591
references.citation: Biol Direct. 2009 Jun 26;4:21
references.pmid: 19558678
references.citation: Nature. 1997 Nov 20;390(6657):298-301
references.pmid: 9384383
references.citation: BMC Biol. 2009 Dec 18;7:88
references.pmid: 20021636
references.citation: Nature. 1996 Oct 17;383(6601):644-6
references.pmid: 8857544
references.citation: Ann N Y Acad Sci. 2009 Oct;1178:194-232
references.pmid: 19845639
references.citation: Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):759-64
references.pmid: 8570630
references.citation: Nature. 1989 Jul 13;340(6229):156-7
references.pmid: 2544809
references.citation: Mol Microbiol. 2000 Jan;35(1):1-5
references.pmid: 10632872
references.citation: Eukaryot Cell. 2009 Oct;8(10):1521-31
references.pmid: 19666779
references.citation: Virus Genes. 1998;16(1):119-31
references.pmid: 9562896
references.citation: Bioessays. 2009 Nov;31(11):1201-10
references.pmid: 19795412
references.citation: BMC Evol Biol. 2008 Feb 27;8:67
references.pmid: 18304319
references.citation: Cold Spring Harb Symp Quant Biol. 1984;49:321-8
references.pmid: 6099243
references.citation: Arch Virol. 2007;152(8):1477-88
references.pmid: 17533556
references.citation: Biol Direct. 2009 Sep 02;4:32
references.pmid: 19725947
references.citation: BMC Evol Biol. 2008 Jan 18;8:12
references.pmid: 18205905
references.citation: Microbiol Rev. 1996 Mar;60(1):250-65
references.pmid: 8852903
references.citation: Nat Rev Microbiol. 2005 Jun;3(6):504-10
references.pmid: 15886693
references.citation: Trends Plant Sci. 2004 Feb;9(2):60-1
references.pmid: 15106587
references.citation: Mol Cell. 1999 Nov;4(5):873-81
references.pmid: 10619034
references.citation: Nature. 2003 Jun 12;423(6941):760-2
references.pmid: 12802336
references.citation: Res Microbiol. 2003 May;154(4):237-43
references.pmid: 12798227
references.citation: BMC Biol. 2010 Jan 12;8:2
references.pmid: 20067611
references.citation: J Exp Bot. 2005 Jan;56(409):1-14
references.pmid: 15557293
references.citation: Nat Rev Microbiol. 2008 Dec;6(12):925-39
references.pmid: 18997823
references.citation: Plant J. 2003 Aug;35(4):523-34
references.pmid: 12904214
references.citation: Syst Biol. 2003 Oct;52(5):696-704
references.pmid: 14530136
references.citation: Mol Plant Microbe Interact. 2005 Oct;18(10):1069-80
references.pmid: 16255246
references.citation: Philos Trans R Soc Lond B Biol Sci. 2008 Dec 27;363(1512):3965-76
references.pmid: 18852096
references.citation: BMC Evol Biol. 2010 Jun 22;10:193
references.pmid: 20569424
references.citation: Annu Rev Phytopathol. 2000 Sep;38:293-324
references.pmid: 11701845
references.citation: Heredity (Edinb). 2000 Aug;85 ( Pt 2):101-6
references.pmid: 11012710
references.citation: Bioinformatics. 2005 Dec 15;21(24):4338-47
references.pmid: 16234323
references.citation: Virus Res. 2006 Apr;117(1):5-16
references.pmid: 16476498
references.citation: Virus Res. 2006 Apr;117(1):1-4
references.pmid: 16497406
references.citation: J R Soc Med. 2004 Dec;97(12):560-5
references.pmid: 15574851
references.citation: J R Soc Med. 2009 Aug;102(8):324-31
references.pmid: 19679734
references.citation: Nat Rev Genet. 2008 May;9(5):411-2; author reply 414
references.pmid: 18421312
references.citation: Nat Rev Genet. 2003 Jan;4(1):50-60
references.pmid: 12509753
references.citation: Virology. 2007 Jun 5;362(2):342-9
references.pmid: 17275871
references.citation: Bioinformatics. 2007 May 1;23(9):1073-9
references.pmid: 17332019
references.citation: Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6261-5
references.pmid: 17384150
references.citation: Annu Rev Phytopathol. 2009;47:353-84
references.pmid: 19400634
references.citation: BMC Bioinformatics. 2006 Oct 25;7:474
references.pmid: 17064419
references.citation: Genome Biol. 2006;7(6):110
references.pmid: 16787527
references.citation: Trends Genet. 1998 Jun;14(6):220-1
references.pmid: 9635404
references.citation: Nat Rev Microbiol. 2006 May;4(5):371-82
references.pmid: 16582931
references.citation: Nature. 2010 Jan 7;463(7277):84-7
references.pmid: 20054395
references.citation: Curr Opin Immunol. 2008 Feb;20(1):10-6
references.pmid: 18206360
references.citation: Science. 2005 May 20;308(5725):1114; author reply 1114
references.pmid: 15905382
references.citation: Science. 2009 Jan 16;323(5912):393-6
references.pmid: 19150848
references.citation: Nat Immunol. 2006 Feb;7(2):131-7
references.pmid: 16424890
references.citation: Nature. 1999 Nov 4;402(6757):96-100
references.pmid: 10573425
references.citation: Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2192-7
references.pmid: 10051617
references.citation: Syst Biol. 2006 Aug;55(4):539-52
references.pmid: 16785212
references.citation: Arch Virol. 2009;154(2):373-9
references.pmid: 19107323
references.citation: Virus Res. 2006 Apr;117(1):38-51
references.pmid: 16529837