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Discovery of Replicating Circular RNAs by RNA-Seq and Computational Algorithms


Viroids are a unique class of subviral pathogens found in plants, and they are difficult to identify since they are free circular non-coding RNAs and often replicate to low levels in host cells. We previously described the computational algorithm PFOR that discovers viroids by analyzing total small RNAs of the infected plants obtained by next-generation sequencing platforms. However, the algorithm written in PERL language is very slow, and viroid identification depends on the in vivo accumulation of extensively overlapping sets of small RNAs to target viroids. Here we report the development of PFOR2 that adopted parallel programming in the C++ language and was significantly faster than PFOR. We also describe a simple computational program that after incorporation into PFOR2 is capable of identifying viroids from deep sequencing of long RNAs instead of small RNAs. Moreover, we report the identification of Grapevine latent viroid (GLVd) and Apple hammerhead viroid-like RNA by the computational approach. Since our new algorithms do not depend on the analysis of viroid-derived small RNAs produced in vivo, it is possible to discover viroids in a wide range of host species including plants, invertebrates and vertebrates.


Vyšlo v časopise: Discovery of Replicating Circular RNAs by RNA-Seq and Computational Algorithms. PLoS Pathog 10(12): e32767. doi:10.1371/journal.ppat.1004553
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004553

Souhrn

Viroids are a unique class of subviral pathogens found in plants, and they are difficult to identify since they are free circular non-coding RNAs and often replicate to low levels in host cells. We previously described the computational algorithm PFOR that discovers viroids by analyzing total small RNAs of the infected plants obtained by next-generation sequencing platforms. However, the algorithm written in PERL language is very slow, and viroid identification depends on the in vivo accumulation of extensively overlapping sets of small RNAs to target viroids. Here we report the development of PFOR2 that adopted parallel programming in the C++ language and was significantly faster than PFOR. We also describe a simple computational program that after incorporation into PFOR2 is capable of identifying viroids from deep sequencing of long RNAs instead of small RNAs. Moreover, we report the identification of Grapevine latent viroid (GLVd) and Apple hammerhead viroid-like RNA by the computational approach. Since our new algorithms do not depend on the analysis of viroid-derived small RNAs produced in vivo, it is possible to discover viroids in a wide range of host species including plants, invertebrates and vertebrates.


Zdroje

1. DienerTO (2003) Discovering viroids - a personal perspective. Nat Rev Microbiol 1: 75–80.

2. FloresR, HernandezC, de AlbaAEM, DarosJA, Di SerioF (2005) Viroids and viroid-host interactions. Annu Rev Phytopathol 43: 117–139.

3. DingB (2009) The biology of viroid-host interactions. Annu Rev Phytopathol 47: 105–131.

4. HuCC, HsuYH, LinNS (2009) Satellite RNAs and Satellite Viruses of Plants. Viruses-Basel 1: 1325–1350.

5. FloresR, GrubbD, ElleuchA, NohalesMA, DelgadoS, et al. (2011) Rolling-circle replication of viroids, viroid-like satellite RNAs and hepatitis delta virus variations on a theme. Rna Biol 8: 200–206.

6. SymonsRH (1997) Plant pathogenic RNAs and RNA catalysis. Nucleic Acids Res 25: 2683–2689.

7. WasseneggerM, HeimesS, RiedelL, SängerHL (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76: 567–576.

8. HutchinsCJ, RathjenPD, ForsterAC, SymonsRH (1986) Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res 14: 3627–3640.

9. ForsterAC, SymonsRH (1987) Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites. Cell 49: 211–220.

10. JeckWR, SorrentinoJA, WangK, SlevinMK, BurdCE, et al. (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19: 141–157.

11. DananM, SchwartzS, EdelheitS, SorekR (2012) Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res 40: 3131–3142.

12. HansenTB, JensenTI, ClausenBH, BramsenJB, FinsenB, et al. (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495: 384–388.

13. MemczakS, JensM, ElefsiniotiA, TortiF, KruegerJ, et al. (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495: 333–338.

14. RosenbergR, JohanssonMA, PowersAM, MillerBR (2013) Search strategy has influenced the discovery rate of human viruses. Proc Natl Acad Sci U S A 110: 13961–13964.

15. Owens RA, Flores R, Di Serio F, Li SF, Pallas V, et al. (2011)Viroids; King AM, Adams MJ, Lefkowitz EJ, Carstens EB, editors. London: Elsevier Academic Press.

16. OwensRA, SanoT, Duran-VilaN (2012) Plant viroids: isolation, characterization/detection, and analysis. Methods Mol Biol 894: 253–271.

17. WuQF, WangY, CaoMJ, PantaleoV, BurgyanJ, et al. (2012) Homology-independent discovery of replicating pathogenic circular RNAs by deep sequencing and a new computational algorithm. Proc Natl Acad Sci U S A 109: 3938–3943.

18. GomezG, MartinezG, PallasV (2009) Interplay between viroid-induced pathogenesis and RNA silencing pathways. Trends Plant Sci 14: 264–269.

19. HammannC, StegerG (2012) Viroid-specific small RNA in plant disease. Rna Biol 9: 809–819.

20. NavarroB, GiselA, RodioME, DelgadoS, FloresR, et al. (2012) Viroids: how to infect a host and cause disease without encoding proteins. Biochimie 94: 1474–1480.

21. OwensRA, HammondRW (2009) Viroid pathogenicity: one process, many faces. Viruses-Basel 1: 298–316.

22. OwensRA, DienerTO (1982) RNA intermediates in potato spindle tuber viroid replication. Proc Natl Acad Sci U S A 79: 113–117.

23. BranchAD, RobertsonHD (1984) A replication cycle for viroids and other small infectious RNA's. Science 223: 450–455.

24. Alexandrescu A (2001) Modern C++ design: generic programming and design patterns applied. Boston, MA.: Addison-Wesley Professional.

25. SymonsRH (1992) Small catalytic RNAs. Annu Rev Biochem 61: 641–671.

26. FaddaZ, DarosJA, FagoagaC, FloresR, Duran-VilaN (2003) Eggplant latent viroid, the candidate type species for a new genus within the family Avsunviroidae (hammerhead viroids). J Virol 77: 6528–6532.

27. HernandezC, FloresR (1992) Plus and minus RNAs of peach latent mosaic viroid self-cleave in vitro via hammerhead structures. Proc Natl Acad Sci U S A 89: 3711–3715.

28. BrueningG (1989) Compilation of self-cleaving sequences from plant virus satellite RNAs and other sources. Methods Enzymol 180: 546–558.

29. Di SerioF, DarosJA, RagozzinoA, FloresR (1997) A 451-nucleotide circular RNA from cherry with hammerhead ribozymes in its strands of both polarities. J Virol 71: 6603–6610.

30. HertelKJ, PardiA, UhlenbeckOC, KoizumiM, OhtsukaE, et al. (1992) Numbering system for the hammerhead. Nucleic Acids Res 20: 3252.

31. RubinoL, TousignantME, StegerG, KaperJM (1990) Nucleotide sequence and structural analysis of two satellite RNAs associated with chicory yellow mottle virus. J Gen Virol 71 (Pt 9): 1897–1903.

32. ZerbinoDR, BirneyE (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.

33. Di SerioF, GiselA, NavarroB, DelgadoS, de AlbaAEM, et al. (2009) Deep sequencing of the small RNAs derived from two symptomatic variants of a chloroplastic viroid:implications for their genesis and for pathogenesis. PLoS One 4: e7539.

34. NavarroB, PantaleoV, GiselA, MoxonS, DalmayT, et al. (2009) Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plant-viroid interaction. PLoS One 4: e7686.

35. BolducF, HoareauC, St-PierreP, PerreaultJP (2010) In-depth sequencing of the siRNAs associated with peach latent mosaic viroid infection. BMC Mol Biol 11: 16.

36. Di SerioF, de AlbaAEM, NavarroB, GiselA, FloresR (2010) RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus. J Virol 84: 2477–2489.

37. MartinezG, DonaireL, LlaveC, PallasV, GomezG (2010) High-throughput sequencing of Hop stunt viroid-derived small RNAs from cucumber leaves and phloem. Mol Plant Pathol 11: 347–359.

38. WangY, ShibuyaM, TanedaA, KurauchiT, SendaM, et al. (2011) Accumulation of Potato spindle tuber viroid-specific small RNAs is accompanied by specific changes in gene expression in two tomato cultivars. Virology 413: 72–83.

39. JiangDM, SanoT, TsujiM, ArakiH, SagawaK, et al. (2012) Comprehensive diversity analysis of viroids infecting grapevine in China and Japan. Virus Res 169: 237–245.

40. Bar-Joseph M (2003) Natural history of viroids—horticulture aspects. In: Hadidi A, Flores R, Randles JW, Semancik JS, editors. Viroids: Collingwood, Australia, CSIRO. pp. 246–251.

41. KeeseP, SymonsRH (1985) Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc Natl Acad Sci U S A 82: 4582–4586.

42. HashimotoJ, KoganezawaH (1987) Nucleotide sequence and secondary structure of apple scar skin viroid. Nucleic Acids Res 15: 7045–7052.

43. HencoK, SängerHL, RiesnerD (1979) Fine structure melting of viroids as studied by kinetic methods. Nucleic Acids Res 6: 3041–3059.

44. RiesnerD, HencoK, RokohlU, KlotzG, KleinschmidtAK, et al. (1979) Structure and structure formation of viroids. J Mol Biol 133: 85–115.

45. ItoT, SuzakiK, NakanoM, SatoA (2013) Characterization of a new apscaviroid from American persimmon. Arch Virol 158: 2629–2631.

46. QinL, ZhangZ, ZhaoX, WuX, ChenY, et al. (2014) Survey and analysis of simple sequence repeats (SSRs) present in the genomes of plant viroids. FEBS open bio 4: 185–189.

47. LevinJZ, YassourM, AdiconisXA, NusbaumC, ThompsonDA, et al. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 7: 709–715.

48. TariqMA, KimHJ, JejelowoO, PourmandN (2011) Whole-transcriptome RNAseq analysis from minute amount of total RNA. Nucleic Acids Res 39: e120.

49. WuQF, KimYC, LuJ, XuanZY, ChenJ, et al. (2008) Poly A- Transcripts Expressed in HeLa Cells. PLoS One 3: e2803.

50. SuzukiH, ZuoYH, WangJH, ZhangMQ, MalhotraA, et al. (2006) Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing. Nucleic Acids Res 34: e63.

51. FloresR, Gago-ZachertS, SerraP, SanjuanR, ElenaSF (2014) Viroids: Survivors from the RNA World? Annu Rev Microbiol 69: 395–414.

52. DienerTO (1995) Origin and evolution of viroids and viroid-like satellite RNAs. Virus Genes 11: 119–131.

53. Kawaguchi-ItoY, LiSF, TagawaM, ArakiH, GoshonoM, et al. (2009) Cultivated grapevines represent a symptomless reservoir for the transmission of Hop stunt viroid to hop crops: 15 years of evolutionary analysis. PLoS One 4: e8386.

54. ItoT, IekiH, OzakiK, ItoT (2001) Characterization of a new citrus viroid species tentatively termed Citrus viroid OS. Arch Virol 146: 975–982.

55. ChenW, TienP, JinLP, WangGP, LiuFC (1986) Study of viroid RNA isolated from apple scar skin disease tissues. Chin J Virol 2: 366–371.

56. KoganezawaH (1986) Further evidence for viroid etiology of apple scar skin and dapple apple diseases. Acta Hort 193: 29–34.

57. KoganezawaH, YanaseH, SakumaT (1983) Viroid-like RNA associated with apple scar skin (or dapple apple) disease. Acta Hort 130: 193–198.

58. BussiereF, OuelletJ, CoteF, LevesqueD, PerreaultJP (2000) Mapping in solution shows the peach latent mosaic viroid to possess a new pseudoknot in a complex, branched secondary structure. J Virol 74: 2647–2654.

59. GagoS, de la PenaM, FloresR (2005) A kissing-loop interaction in a hammerhead viroid RNA critical for its in vitro folding and in vivo viability. RNA 11: 1073–1083.

60. ZhangXM, SegersGC, SunQH, DengFY, NussDL (2008) Characterization of hypovirus-derived small RNAs generated in the chestnut blight fungus by an inducible DCL-2-dependent pathway. J Virol 82: 2613–2619.

61. DingSW, LuR (2011) Virus-derived siRNAs and piRNAs in immunity and pathogenesis. Curr Opin Virol 1: 533–544.

62. LiSF, OnoderaS, SanoT, YoshidaK, WangGP, et al. (1995) Gene diagnosis of viroids: comparisons of return-PAGE and hybridization using DIG-labeled DNA and RNA probes for practical diagnosis of hop stunt, citrus exocortis an apple scar skin viroids in their natural host plants. Ann Phytopathol Soc Jpn 61: 381–390.

63. HouWY, SanoT, LiF, WuZJ, LiL, et al. (2009) Identification and characterization of a new coleviroid (CbVd-5). Arch Virol 154: 315–320.

64. AliyariR, WuQF, LiHW, WangXH, LiF, et al. (2008) Mechanism of Induction and Suppression of Antiviral Immunity Directed by Virus-Derived Small RNAs in Drosophila. Cell Host Microbe 4: 387–397.

65. WuQF, LuoYJ, LuR, LauN, LaiEC, et al. (2010) Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc Natl Acad Sci U S A 107: 1606–1611.

66. LangmeadB, SalzbergSL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.

67. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.

68. NavarroB, FloresR (1997) Chrysanthemum chlorotic mottle viroid: Unusual structural properties of a subgroup of self-cleaving viroids with hammerhead ribozymes. Proc Natl Acad Sci U S A 94: 11262–11267.

69. VerhoevenJTJ, MeekesETM, RoenhorstJW, FloresR, SerraP (2013) Dahlia latent viroid: a recombinant new species of the family Pospiviroidae posing intriguing questions about its origin and classification. J Gen Virol 94: 711–719.

70. ZukerM (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415.

71. De RijkP, WuytsJ, De WachterR (2003) RnaViz 2: an improved representation of RNA secondary structure. Bioinformatics 19: 299–300.

72. XayaphoummineA, BucherT, IsambertH (2005) Kinefold web server for RNA/DNA folding path and structure prediction including pseudoknots and knots. Nucleic Acids Res 33: W605–W610.

73. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.

74. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and clustal X version 2.0. Bioinformatics 23: 2947–2948.

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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