Widespread Endogenization of Genome Sequences of Non-Retroviral RNA Viruses into Plant Genomes

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Non-retroviral RNA virus sequences (NRVSs) have been found in the chromosomes of vertebrates and fungi, but not plants. Here we report similarly endogenized NRVSs derived from plus-, negative-, and double-stranded RNA viruses in plant chromosomes. These sequences were found by searching public genomic sequence databases, and, importantly, most NRVSs were subsequently detected by direct molecular analyses of plant DNAs. The most widespread NRVSs were related to the coat protein (CP) genes of the family Partitiviridae which have bisegmented dsRNA genomes, and included plant- and fungus-infecting members. The CP of a novel fungal virus (Rosellinia necatrix partitivirus 2, RnPV2) had the greatest sequence similarity to Arabidopsis thaliana ILR2, which is thought to regulate the activities of the phytohormone auxin, indole-3-acetic acid (IAA). Furthermore, partitivirus CP-like sequences much more closely related to plant partitiviruses than to RnPV2 were identified in a wide range of plant species. In addition, the nucleocapsid protein genes of cytorhabdoviruses and varicosaviruses were found in species of over 9 plant families, including Brassicaceae and Solanaceae. A replicase-like sequence of a betaflexivirus was identified in the cucumber genome. The pattern of occurrence of NRVSs and the phylogenetic analyses of NRVSs and related viruses indicate that multiple independent integrations into many plant lineages may have occurred. For example, one of the NRVSs was retained in Ar. thaliana but not in Ar. lyrata or other related Camelina species, whereas another NRVS displayed the reverse pattern. Our study has shown that single- and double-stranded RNA viral sequences are widespread in plant genomes, and shows the potential of genome integrated NRVSs to contribute to resolve unclear phylogenetic relationships of plant species.

Vyšlo v časopise: Widespread Endogenization of Genome Sequences of Non-Retroviral RNA Viruses into Plant Genomes. PLoS Pathog 7(7): e32767. doi:10.1371/journal.ppat.1002146
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002146

Souhrn

Zdroje

1. GorbalenyaAE 1992 Host-related sequences in RNA viral genomes. Semin Virol 3 359 371

2. MeyersGRumenapfTThielHJ 1989 Ubiquitin in a togavirus. Nature 341 491

3. MayoMAJollyCA 1991 The 5′-terminal sequence of potato leafroll virus RNA: evidence of recombination between virus and host RNA. J Gen Virol 72 2591 2595

4. AgranovskyAABoykoVPKarasevAVKooninEVDoljaVV 1991 Putative 65 kDa protein of beet yellows closterovirus is a homologue of HSP70 heat shock proteins. J Mol Biol 217 603 610

5. DoljaVVKreuzeJFValkonenJP 2006 Comparative and functional genomics of closteroviruses. Virus Res 117 38 51

6. BertschCBeuveMDoljaVVWirthMPelsyF 2009 Retention of the virus-derived sequences in the nuclear genome of grapevine as a potential pathway to virus resistance. Biol Direct 4 21

7. GayralPNoa-CarrazanaJCLescotMLheureuxFLockhartBE 2008 A single Banana streak virus integration event in the banana genome as the origin of infectious endogenous pararetrovirus. J Virol 82 6697 6710

8. Richert-PoggelerKRNoreenFSchwarzacherTHarperGHohnT 2003 Induction of infectious petunia vein clearing (pararetro) virus from endogenous provirus in petunia. EMBO J 22 4836 4845

9. KuniiMKandaMNaganoHUyedaIKishimaY 2004 Reconstruction of putative DNA virus from endogenous rice tungro bacilliform virus-like sequences in the rice genome: implications for integration and evolution. BMC Genomics 5 80

10. GeukingMBWeberJDewannieuxMGorelikEHeidmannT 2009 Recombination of retrotransposon and exogenous RNA virus results in nonretroviral cDNA integration. Science 323 393 396

11. HorieMHondaTSuzukiYKobayashiYDaitoT 2010 Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463 84 87

12. BelyiVALevineAJSkalkaAM 2010 Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog 6 e1001030

13. KatzourakisAGiffordRJ 2010 Endogenous viral elements in animal genomes. PLoS Genet 6 e1001191

14. TaylorDJLeachRWBruennJ 2010 Filoviruses are ancient and integrated into mammalian genomes. BMC Evol Biol 10 193

15. KooninEV 2010 Taming of the shrewd: novel eukaryotic genes from RNA viruses. BMC Biol 8 2

16. TaylorDJBruennJ 2009 The evolution of novel fungal genes from non-retroviral RNA viruses. BMC Biol 7 88

17. FrankACWolfeKH 2009 Evolutionary capture of viral and plasmid DNA by yeast nuclear chromosomes. Eukaryot Cell 8 1521 1531

18. ArakawaMNakamuraHUetakeYMatsumotoN 2002 Presence and distribution of double-stranded RNA elements in the white root rot fungus Rosellinia necatrix. Mycoscience 43 21 26

19. IkedaKNakamuraHArakawaMMatsumotoN 2004 Diversity and vertical transmission of double-stranded RNA elements in root rot pathogens of trees, Helicobasidium mompa and Rosellinia necatrix. Mycol Res 108 626 634

20. GhabrialSASuzukiN 2009 Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47 353 384

21. GhabrialSAOchoaWFBakerTNiberML 2008 Partitiviruses: general features. MahyBWJVRM Encyclopedia of Virology 3rd edn Oxford Elsevier 68 75

22. KooninEVWolfYINagasakiKDoljaVV 2008 The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol 6 925 939

23. MagidinMPittmanJKHirschiKDBartelB 2003 ILR2, a novel gene regulating IAA conjugate sensitivity and metal transport in Arabidopsis thaliana. Plant J 35 523 534

24. LiuHFuYJiangDLiGXieJ 2010 Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J Virol 84 11876 11887

25. InitiativeTAG 2000 Analysis of the genome of the flowering plant Arabidopsis thaliana. Nature 408 796 815

26. RennaLHantonSLStefanoGBortolottiLMisraV 2005 Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein. Plant Mol Biol 58 109 122

27. SchranzMELysakMAMitchell-OldsT 2006 The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11 535 542

28. TzanetakisIEPriceRMartinRR 2008 Nucleotide sequence of the tripartite Fragaria chiloensis cryptic virus and presence of the virus in the Americas. Virus Genes 36 267 272

29. ChenLChenJSZhangHChenSN 2006 Complete nucleotide sequences of three dsRNA segments from Raphanus sativus-root cv. Yidianhong [corrected] with leaf yellow edge symptoms. Arch Virol 151 2077 2083

30. WillenborgJMenzelWVettenHJMaissE 2009 Molecular characterization of two alphacryptovirus dsRNAs isolated from Daucus carota. Arch Virol 154 541 543

31. BlawidRSDMaissE 2008 Alphacryptovirus and Betacryptovirus. MahyBWJVRM Encyclopedia of Virology 3rd edn Oxford Elsevier 98 104

32. BoccardoGCandresseT 2005 Complete sequence of the RNA1 of an isolate of White clover cryptic virus 1, type species of the genus Alphacryptovirus. Arch Virol 150 399 402

33. SzegoAEnunluNDeshmukhSDVeliceasaDHunyadi-GulyasE 2010 The genome of Beet cryptic virus 1 shows high homology to certain cryptoviruses present in phylogenetically distant hosts. Virus Genes 40 267 276

34. BlawidRStephanDMaissE 2007 Molecular characterization and detection of Vicia cryptic virus in different Vicia faba cultivars. Arch Virol 152 1477 1488

35. SasayaTIshikawaKKoganezawaH 2002 The nucleotide sequence of RNA1 of Lettuce big-vein virus, genus Varicosavirus, reveals its relation to nonsegmented negative-strand RNA viruses. Virology 297 289 297

36. KondoHMaedaTShirakoYTamadaT 2006 Orchid fleck virus is a rhabdovirus with an unusual bipartite genome. J Gen Virol 87 2413 2421

37. HuangSLiRZhangZLiLGuX 2009 The genome of the cucumber, Cucumis sativus L. Nat Genet 41 1275 1281

38. VelascoRZharkikhAAffourtitJDhingraACestaroA 2010 The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 42 833 839

39. VivesMCGalipiensoLNavarroLMorenoPGuerriJ 2001 The nucleotide sequence and genomic organization of Citrus leaf blotch virus: candidate type species for a new virus genus. Virology 287 225 233

40. OssowskiSSchneebergerKLucas-LledoJIWarthmannNClarkRM 2010 The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327 92 94

41. ClaussMJKochMA 2006 Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci 11 449 459

42. BeilsteinMANagalingumNSClementsMDManchesterSRMathewsS 2010 Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci U S A 107 18724 18728

43. OyamaRKClaussMJFormanováNKroymannJSchmidKJ 2008 The shrunken genome Arabidopsis thaliana. Plant Syst Evol 273 257 271

44. ClarksonJJLimKYKovarikAChaseMWKnappS 2005 Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168 241 252

45. KochMHauboldBMitchell-OldsT 2001 Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am J Bot 88 534 544

46. KochMADobesCMatschingerMBleekerWVogelJ 2005 Evolution of the trnF(GAA) gene in Arabidopsis relatives and the Brassicaceae family: monophyletic origin and subsequent diversification of a plastidic pseudogene. Mol Biol Evol 22 1032 1043

47. BaileyCDKochMAMayerMMummenhoffKO'KaneSLJr 2006 Toward a global phylogeny of the Brassicaceae. Mol Biol Evol 23 2142 2160

48. CouvreurTLFranzkeAAl-ShehbazIABakkerFTKochMA 2010 Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol Biol Evol 27 55 71

49. LysakMAKochMABeaulieuJMMeisterALeitchIJ 2009 The dynamic ups and downs of genome size evolution in Brassicaceae. Mol Biol Evol 26 85 98

50. MinkGI 1993 Pollen and seed-transmitted viruses and viroids. Annu Rev Phytopathol 31 375 402

51. RoossinckMJ 2003 Plant RNA virus evolution. Curr Opin Microbiol 6 406 409

52. MaoriETanneESelaI 2007 Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes. Virology 362 342 349

53. ManiRSChinnaiyanAM 2010 Triggers for genomic rearrangements: insights into genomic, cellular and environmental influences. Nat Rev Genet 11 819 829

54. GuerriJPinaJAVivesMCNavarroLMorenoP 2004 Seed Transmission of Citrus leaf botch virus: Implications in Quarantine and Certification Programs. Plant Dis 88 906

55. ChibaSSalaipethLLinYHSasakiAKanematsuS 2009 A novel bipartite double-stranded RNA mycovirus from the white root rot fungus Rosellinia necatrix: molecular and biological characterization, taxonomic considerations, and potential for biological control. J Virol 83 12801 12812

56. MiuraEKatoYMatsushimaRAlbrechtVLaalamiS 2007 The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants. Plant Cell 19 1313 1328

57. FarukMIEusebio-CopeASuzukiN 2008 A host factor involved in hypovirus symptom expression in the chestnut blight fungus, Cryphonectria parasitica. J Virol 82 740 754

58. AltschulSFMaddenTLSchafferAAZhangJZhangZ 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402

59. KohanyOGentlesAJHankusLJurkaJ 2006 Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7 474

60. KatohKTohH 2008 Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9 286 298

61. TamuraKDudleyJNeiMKumarS 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

62. AbascalFZardoyaRPosadaD 2005 ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21 2104 2105

63. GuindonSDufayardJFLefortVAnisimovaMHordijkW 2010 New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59 307 321

64. HordijkWGascuelO 2005 Improving the efficiency of SPR moves in phylogenetic tree search methods based on maximum likelihood. Bioinformatics 21 4338 4347

65. AnisimovaMGascuelO 2006 Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55 539 552

66. KochMBJMitchell-OldsT 1999 Molecular systematics and evolution of Arabidopsis and Arabis. Plant Biol 1 529 537

67. SasayaTKusabaSIshikawaKKoganezawaH 2004 Nucleotide sequence of RNA2 of Lettuce big-vein virus and evidence for a possible transcription termination/initiation strategy similar to that of rhabdoviruses. J Gen Virol 85 2709 2717

68. DietzgenRGCallaghanBWetzelTDaleJL 2006 Completion of the genome sequence of Lettuce necrotic yellows virus, type species of the genus Cytorhabdovirus. Virus Res 118 16 22

69. GroupAP 2003 An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APGII. Bot J Linn Soc 141 399 436

70. UdvardiMKTabataSParniskeMStougaardJ 2005 Lotus japonicus: legume research in the fast lane. Trends Plant Sci 10 222 228