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

PLoS Pathogens

Volumn 10, Issue 12, 2014, Pages

  Zhang, Zhixiang ^a,b   Qi, Shuishui ^a   Tang, Nan ^a   Zhang, Xinxin ^a   Chen, Shanshan ^b   Zhu, Pengfei ^a   Ma, Lin ^a   Cheng, Jinping ^a   Xu, Yun ^a   Lu, Meiguang ^b   Wang, Hongqing ^c   Ding, Shou Wei ^d   Li, Shifang ^b   Wu, Qingfa ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c CHINA AGRICULTURAL UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; HAMMERHEAD RIBOZYME; HELIX LOOP HELIX PROTEIN; SMALL INTERFERING RNA; RNA; RNA, CIRCULAR; VIRUS RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ALGORITHM; AMINO ACID SEQUENCE; ANIMAL VIRUS; APPLE HAMMERHEAD VIROID; ARTICLE; BIOINFORMATICS; COMPUTER ANALYSIS; COMPUTER LANGUAGE; CONTROLLED STUDY; GENE MAPPING; GENOME SIZE; GRAPEVINE LATENT VIROID; MOLECULAR CLONING; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PLANT VIRUS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROGRESSIVE FILTERING OF OVERLAPPING SMALL RNA ANALYSIS; RECOMBINANT PLASMID; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA CLEAVAGE; RNA HYBRIDIZATION; RNA REPLICATION; RNA SEQUENCE; RNA TRANSCRIPTION; STRUCTURE ANALYSIS; VIROID; VIRUS IDENTIFICATION; VIRUS INFECTION; BIOLOGY; CONFORMATION; GENETICS; MALUS; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; PROCEDURES; SEQUENCE ANALYSIS; VIRUS REPLICATION; VITIS;

ANIMALIA; APSCAVIROID; INVERTEBRATA; MALUS X DOMESTICA; VERTEBRATA; VIROIDS; VITIS;

ALGORITHMS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; MALUS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PHYLOGENY; RNA; RNA, VIRAL; SEQUENCE ANALYSIS, RNA; VIROIDS; VIRUS REPLICATION; VITIS;

EID: 84919623002     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004553     Document Type: Article

References (74)

1. Diener TO, (2003) Discovering viroids - a personal perspective. Nat Rev Microbiol 1: 75–80.
2. Flores R, Hernandez C, de Alba AEM, Daros JA, Di Serio F, (2005) Viroids and viroid-host interactions. Annu Rev Phytopathol 43: 117–139.
3. Ding B, (2009) The biology of viroid-host interactions. Annu Rev Phytopathol 47: 105–131.
4. Hu CC, Hsu YH, Lin NS, (2009) Satellite RNAs and Satellite Viruses of Plants. Viruses-Basel 1: 1325–1350.
5. Flores R, Grubb D, Elleuch A, Nohales MA, Delgado S, 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. Symons RH, (1997) Plant pathogenic RNAs and RNA catalysis. Nucleic Acids Res 25: 2683–2689.
7. Wassenegger M, Heimes S, Riedel L, Sänger HL, (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76: 567–576.
8. Hutchins CJ, Rathjen PD, Forster AC, Symons RH, (1986) Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res 14: 3627–3640.
9. Forster AC, Symons RH, (1987) Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites. Cell 49: 211–220.
10. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, et al. (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19: 141–157.
11. Danan M, Schwartz S, Edelheit S, Sorek R, (2012) Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res 40: 3131–3142.
12. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, et al. (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495: 384–388.
13. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, et al. (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495: 333–338.
14. Rosenberg R, Johansson MA, Powers AM, Miller BR, (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. Owens RA, Sano T, Duran-Vila N, (2012) Plant viroids: isolation, characterization/detection, and analysis. Methods Mol Biol 894: 253–271.
17. Wu QF, Wang Y, Cao MJ, Pantaleo V, Burgyan J, 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. Gomez G, Martinez G, Pallas V, (2009) Interplay between viroid-induced pathogenesis and RNA silencing pathways. Trends Plant Sci 14: 264–269.
19. Hammann C, Steger G, (2012) Viroid-specific small RNA in plant disease. Rna Biol 9: 809–819.
20. Navarro B, Gisel A, Rodio ME, Delgado S, Flores R, et al. (2012) Viroids: how to infect a host and cause disease without encoding proteins. Biochimie 94: 1474–1480.
21. Owens RA, Hammond RW, (2009) Viroid pathogenicity: one process, many faces. Viruses-Basel 1: 298–316.
22. Owens RA, Diener TO, (1982) RNA intermediates in potato spindle tuber viroid replication. Proc Natl Acad Sci U S A 79: 113–117.
23. Branch AD, Robertson HD, (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. Symons RH, (1992) Small catalytic RNAs. Annu Rev Biochem 61: 641–671.
26. Fadda Z, Daros JA, Fagoaga C, Flores R, Duran-Vila N, (2003) Eggplant latent viroid, the candidate type species for a new genus within the family Avsunviroidae (hammerhead viroids). J Virol 77: 6528–6532.
27. Hernandez C, Flores R, (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. Bruening G, (1989) Compilation of self-cleaving sequences from plant virus satellite RNAs and other sources. Methods Enzymol 180: 546–558.
29. Di Serio F, Daros JA, Ragozzino A, Flores R, (1997) A 451-nucleotide circular RNA from cherry with hammerhead ribozymes in its strands of both polarities. J Virol 71: 6603–6610.
30. Hertel KJ, Pardi A, Uhlenbeck OC, Koizumi M, Ohtsuka E, et al. (1992) Numbering system for the hammerhead. Nucleic Acids Res 20: 3252.
31. Rubino L, Tousignant ME, Steger G, Kaper JM, (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. Zerbino DR, Birney E, (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.
33. Di Serio F, Gisel A, Navarro B, Delgado S, de Alba AEM, 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. Navarro B, Pantaleo V, Gisel A, Moxon S, Dalmay T, 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. Bolduc F, Hoareau C, St-Pierre P, Perreault JP, (2010) In-depth sequencing of the siRNAs associated with peach latent mosaic viroid infection. BMC Mol Biol 11: 16.
36. Di Serio F, de Alba AEM, Navarro B, Gisel A, Flores R, (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. Martinez G, Donaire L, Llave C, Pallas V, Gomez G, (2010) High-throughput sequencing of Hop stunt viroid-derived small RNAs from cucumber leaves and phloem. Mol Plant Pathol 11: 347–359.
38. Wang Y, Shibuya M, Taneda A, Kurauchi T, Senda M, 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. Jiang DM, Sano T, Tsuji M, Araki H, Sagawa K, 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. 246–251.
41. Keese P, Symons RH, (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. Hashimoto J, Koganezawa H, (1987) Nucleotide sequence and secondary structure of apple scar skin viroid. Nucleic Acids Res 15: 7045–7052.
43. Henco K, Sänger HL, Riesner D, (1979) Fine structure melting of viroids as studied by kinetic methods. Nucleic Acids Res 6: 3041–3059.
44. Riesner D, Henco K, Rokohl U, Klotz G, Kleinschmidt AK, et al. (1979) Structure and structure formation of viroids. J Mol Biol 133: 85–115.
45. Ito T, Suzaki K, Nakano M, Sato A, (2013) Characterization of a new apscaviroid from American persimmon. Arch Virol 158: 2629–2631.
46. Qin L, Zhang Z, Zhao X, Wu X, Chen Y, 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. Levin JZ, Yassour M, Adiconis XA, Nusbaum C, Thompson DA, et al. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 7: 709–715.
48. Tariq MA, Kim HJ, Jejelowo O, Pourmand N, (2011) Whole-transcriptome RNAseq analysis from minute amount of total RNA. Nucleic Acids Res 39: e120.
49. Wu QF, Kim YC, Lu J, Xuan ZY, Chen J, et al. (2008) Poly A- Transcripts Expressed in HeLa Cells. PLoS One 3: e2803.
50. Suzuki H, Zuo YH, Wang JH, Zhang MQ, Malhotra A, 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. Flores R, Gago-Zachert S, Serra P, Sanjuan R, Elena SF, (2014) Viroids: Survivors from the RNA World? Annu Rev Microbiol 69: 395–414.
52. Diener TO, (1995) Origin and evolution of viroids and viroid-like satellite RNAs. Virus Genes 11: 119–131.
53. Kawaguchi-Ito Y, Li SF, Tagawa M, Araki H, Goshono M, 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. Ito T, Ieki H, Ozaki K, Ito T, (2001) Characterization of a new citrus viroid species tentatively termed Citrus viroid OS. Arch Virol 146: 975–982.
55. Chen W, Tien P, Jin LP, Wang GP, Liu FC, (1986) Study of viroid RNA isolated from apple scar skin disease tissues. Chin J Virol 2: 366–371.
56. Koganezawa H, (1986) Further evidence for viroid etiology of apple scar skin and dapple apple diseases. Acta Hort 193: 29–34.
57. Koganezawa H, Yanase H, Sakuma T, (1983) Viroid-like RNA associated with apple scar skin (or dapple apple) disease. Acta Hort 130: 193–198.
58. Bussiere F, Ouellet J, Cote F, Levesque D, Perreault JP, (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. Gago S, de la Pena M, Flores R, (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. Zhang XM, Segers GC, Sun QH, Deng FY, Nuss DL, (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. Ding SW, Lu R, (2011) Virus-derived siRNAs and piRNAs in immunity and pathogenesis. Curr Opin Virol 1: 533–544.
62. Li SF, Onodera S, Sano T, Yoshida K, Wang GP, 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. Hou WY, Sano T, Li F, Wu ZJ, Li L, et al. (2009) Identification and characterization of a new coleviroid (CbVd-5). Arch Virol 154: 315–320.
64. Aliyari R, Wu QF, Li HW, Wang XH, Li F, 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. Wu QF, Luo YJ, Lu R, Lau N, Lai EC, 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. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.
67. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.
68. Navarro B, Flores R, (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. Verhoeven JTJ, Meekes ETM, Roenhorst JW, Flores R, Serra P, (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. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415.
71. De Rijk P, Wuyts J, De Wachter R, (2003) RnaViz 2: an improved representation of RNA secondary structure. Bioinformatics 19: 299–300.
72. Xayaphoummine A, Bucher T, Isambert H, (2005) Kinefold web server for RNA/DNA folding path and structure prediction including pseudoknots and knots. Nucleic Acids Res 33: W605–W610.
73. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
74. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and clustal X version 2.0. Bioinformatics 23: 2947–2948.