In silico prediction and validation of potential gene targets for pospiviroid-derived small RNAs during tomato infection

Gene

Volumn 564, Issue 2, 2015, Pages 197-205

  Avina Padilla, Katia ^a,b   Martinez de la Vega, Octavio ^a   Rivera Bustamante, Rafael ^a   Martinez Soriano, Juan Pablo ^a   Owens, Robert A ^b   Hammond, Rosemarie W ^b   Vielle Calzada, Jean Philippe ^a  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Comparative genomics; Non coding RNA; RNA mediated gene regulation; Tomato planta macho viroid; Viroid pathogenesis

Indexed keywords

POSPIVIROID DERIVED SMALL RNA; SOLWD40 REPEAT PROTEIN; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; COMPUTER MODEL; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE TARGETING; NATURAL HOST; NONHUMAN; PATHOGENICITY; PLANT GENE; POSPIVIROID; POSPIVIROIDAE; POTATO SPINDLE TUBER; PRIORITY JOURNAL; RNA CLEAVAGE; RNA SEQUENCE; SEQUENCE HOMOLOGY; SOLWD40 REPEAT GENE; VIROIDAL PLANT DISEASE; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT DISEASE; TOMATO; VIROID; VIROLOGY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; LYCOPERSICON ESCULENTUM; MAGNOLIOPHYTA; POSPIVIROID; POSPIVIROIDAE; TOMATO PLANTA MACHO VIROID; VIROIDS;

ARABIDOPSIS; BASE SEQUENCE; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PLANT DISEASES; VIROIDS;

EID: 84928213621     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2015.03.076     Document Type: Article

References (74)

1. Akbergenov R., Si-Ammour A., Blevins T., Amin I., Kutter C., Vanderschuren H., Zhang P., Gruissem W., Meins F., Hohn T., Pooggin M.M. Molecular characterization of geminivirus-derived small RNAs in different plant species. Nucleic Acids Res. 2006, 34:462-471.
2. Baulcombe D. RNA silencing in plants. Nature 2004, 431:356-363.
3. Baumstark T., Schröder A.R., Riesner D. Viroid processing: switch from cleavage to ligation is driven by a change from a tetraloop to a loop E conformation. EMBO J. 1997, 16:599-610.
4. Branch A.D., Robertson H.D. A replication cycle for viroids and other small infectious RNA's. Science 1984, 223:450-455.
5. Daròs J.A., Flores R. Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6792-6797.
6. Daròs J.A., Elena S.F., Flores R. Viroids: an Ariadne's thread into the RNA labyrinth. EMBO Rep. 2006, 7:593-598.
7. Delgado S., Martínez de Alba A.E., Hernández C., Flores R. A short double-stranded RNA motif of Peach latent mosaic viroid contains the initiation and self-cleavage sites of both polarity strands. J. Virol. 2005, 79:12934-12943.
8. Di Serio F., Gisel A., Navarro B., Delgado S., Martínez de Alba A.-E., Donvito G., Flores R. Deep sequencing of the small RNAs derived from two symptomatic variants of a chloroplastic viroid: implications for their genesis and for pathogenesis. PLoS ONE 2009, 4(10):e7539.
9. Di Serio F., Flores R., Verhoeven J.Th.J., Li S.-F., Pallas V., Randles J.W., Sano T., Vidalakis G., Owens R.A. Current status of viroid taxonomy. Arch. Virol. 2014, 159:3467-3478.
10. Diener T.O. Ed: The Viroids 1987, Plenum Press, New York.
11. Diermann N., Matousek J., Junge M., Riesner D., Steger G. Characterization of plant miRNAs and small RNAs derived from potato spindle tuber viroid (PSTVd) in infected tomato. Biol. Chem. 2010, 391:1379-1390.
12. Ding B. The biology of viroid-host interactions. Annu. Rev. Phytopathol. 2009, 47:105-131.
13. Ding B. Viroids: self-replicating, mobile and fast-evolving noncoding regulatory RNAs. Wiley Interdiscip. Rev. RNA 2010, 2010(1):361-375.
14. Ding B., Itaya A. Viroid: a useful model for studying the basic principles of infection and RNA biology. Mol. Plant Microbe Interact. 2007, 20:7-20.
15. Eiras M., Kitajima E.W., Flores R., Daròs J.A. Existence in vivo of the loop E motif in potato spindle tuber viroid RNA. Arch. Virol. 2007, 152:1389-1393.
16. Flores R., De La Peña M., Navarro B. Chrysanthemum Chlorotic Mottle Viroid. Viroids 2003, 224-227. CSIRO Publishing, Collingwood, Victoria, Australia. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
17. Flores R., Hernández C., Martínez de Alba A.E., Daròs J.A., Di Serio F. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 2005, 43:117-139.
18. Flores R., Serra P., Minoia S., Di Serio F., Navarro B. Viroids: from genotype to phenotype just relying on RNA sequence and structural motifs. Front. Microbiol. 2012, 3:217.
19. Fusaro A.F., Matthew L., Smith N.A., Curtin S.J., Dedic-Hagan J., Ellacott G.A., Watson J.M., Wang M.B., Brosnan C., Carroll B.J., Waterhouse P.M. RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep. 2006, 7:1168-1175.
20. Galindo A.J., Smith D.R., Diener T.O. Etiology of Plant Macho, a viroid disease of tomato. Phytopathology 1982, 72:49-54.
21. Garcia-Ruiz H., Takeda A., Chapman E.J., Sullivan C.M., Fahlgren N., Brempelis K.J., Carrington J.C. Arabidopsis RNA-dependent RNA polymerase and Dicer-like proteins an antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 2010, 22:481-496.
22. Gómez G., Martinez G., Pallás V. Interplay between viroid-induced pathogenesis and RNA silencing pathways. Trends Plant Sci. 2009, 14:264-269.
23. Gozmanova M., Denti M.A., Minkov I.N., Tsagris M., Tabler M. Characterization of the RNA motif responsible for the specific interaction of potato spindle tuber viroid RNA (PSTVd) and the tomato protein Virp1. Nucleic Acids Res. 2003, 31:5534-5543.
24. Viroids 2003, CSIRO Publishing, Collingwood, Victoria, Australia, (370 pp.). A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
25. Hammann C., Steger G. Viroid-specific small RNA in plant disease. RNA Biol. 2012, 6:809-819.
26. Hammond R.W., Owens R.A. Mutational analysis of potato spindle tuber viroid reveals complex relationships between structure and infectivity. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:3967-3971.
27. Hammond R.W., Zhao Y. Modification of tobacco plant development by sense and antisense expression of the tomato viroid-induced AGC VIIIa protein kinase PKV suggests involvement in gibberellin signaling. BMC Plant Biol. 2000, 9:108.
28. Henco K., Sänger H.L., Riesner D. Fine structure melting of viroids as studied by kinetic methods. Nucleic Acids Res. 1979, 6:3041-3050.
29. Itaya A., Zhong X., Bundschuh R., Qi Y., Wang Y., Takeda R., Harris A.R., Molina C., Nelson R.S., Ding B. A structured viroid RNA is substrate for dicer-like cleavage to produce biologically active small RNAs but is resistant to RISC-mediated degradation. J. Virol. 2007, 81:2980-2994.
30. Ivanova D., Milev I., Vachev T., Baev V., Yahubyan G., Minkov G., Gozmanova M. Small RNA analysis of Potato spindle tuber viroid infected Phelipance ramose. Plant Physiol. Biochem. 2014, 74:276-292.
31. Kasschau K.D., Xie Z., Allen E., Llave C., Chapman E.J., Krizan K.A., Carrington J.C. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 2003, 4:205-217.
32. Keese P., Symons R.H. Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:4582-4586.
33. Kiefer M.C., Owens R.A., Diener T.O. Structural similarities between viroids and transposable genetic elements. Proc. Natl. Acad. Sci. U. S. A. 1983, 80:6234-6238.
34. Kong D., Li M., Dong Z., Ji H., Li X. Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses. Plant Cell Rep. 2014, 10.1007/s00299-014-1717-1.
35. Kumar S., Jordan M.C., Datla R., Cloutier S. The LuWD40-1 gene encoding WD repeat protein regulates growth and pollen viability in flax (Linum usitatissimum L.). PLoS One 2013, 8:e69124.
36. Lamesch P., Beradini T.Z., Li D., Swarbreck D., Wilks C., Sasidharan R., Muller R., Dreher K., Alexander D.L., Garcia-Hernandez M., Karthikeyan A.S., Lee C.H., Nelson W.D., Ploetz L., Singh S., Wensel A., Huala E. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 2012, 40(D1):D1202-D1210. 10.1093/nar/gkr1090.
37. Leuschner P.J.F., Ameres S.L., Kueng S., Martinez J. Cleavage of the siRNA passenger strand during RISC assembly in human cells. EMBO Rep. 2006, 7:314-320.
38. Llave C., Xie Z., Kasschau K.D., Carrington J.C. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 2002, 297:2053-2056.
39. Machida S., Yamahata N., Watanuki H., Owens R.A., Sano T. Successive accumulation of two size classes of viroid-specific small RNA in potato spindle tuber viroid-infected tomato plants. J. Gen. Virol. 2007, 88:3452-3457.
40. Maechler M., Rousseeuw P., Struyf A., Hubert M., Hornik K. Cluster: Cluster Analysis Basics and Extensions. R Package, Version 1.14.4 2013.
41. Mallory A.C., Reinhart B.J., Jones-Rhoades M.W., Tang G., Zamore P.D., Barton M.K., Bartel D.P. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5' region. EMBO J. 2004, 23:3356-3364.
42. Maniataki E., Martínez de Alba A.E., Sägesser R., Tabler M., Tsagris M. Viroid RNA systemic spread may depend on the interaction of a 71-nucleotide bulged hairpin with the host protein VirP1. RNA 2003, 9:346-354.
43. Markarian N., Li H.E., Ding S.W., Semancik J.S. RNA silencing as related to viroid-induced symptom expression. Arch. Virol. 2010, 149:397-406.
44. Martin R., Arenas C., Daròs J.A., Covarrubias A., Reyes J.L., Chua N.H. Characterization of small RNAs derived from citrus exocortis viroid (CEVd) in infected tomato plants. Virology 2007, 367:135-146.
45. Martínez de Alba A.E., Flores R., Hernández C. Two chloroplastic viroids induce the accumulation of the small RNAs associated with the post-transcriptional gene silencing. J. Virol. 2002, 76:13094-13096.
46. Mascheretti I., Battaglia R., Mainieri D., Altana A., Lauria M., Rossi V. The WD-40 repeat proteins NFC101 and NFC102 regulate different aspects of maize development through chromatin modification. Plant Cell 2013, 25:404-420.
47. Matousek J., Kozlova P., Orctova L., Schmitz A., Pesina K., Banach O., Diermann N., Steger G., Riesner D. Accumulation of viroid-specific small RNAs and increase in nucleolytic activities linked to viroid caused pathogenesis. Biol. Chem. 2007, 388:1-13.
48. Minola S., Carbonell A., Di Serio F., Gisel A., Carrington J.C., Navarro B., Flores R. Specific argonautes selectively bind small RNAs derived from Potato spindle tuber viroid and attenuate viroid accumulation in vivo. J. Virol. 2014, 88:11933-11945.
49. Navarro J.A., Vera A., Flores R. A chloroplastic RNA polymerase resistant to tagetitoxin is involved in replication of avocado sunblotch viroid. Virology 2000, 268:218-225.
50. Navarro B., Pantaleo V., Gisel A., Moxon S., Dalmay T. Deep sequencing of viroid-derived small RNAs from grapevine provides new insights on the role of RNA silencing in plant-viroid interaction. PLoS ONE 2009, 4(11):e7686.
51. Navarro B., Gisel A., Rodio M.E., Delgado S., Flores R., Di Serio F. Viroids: how to infect a host and cause disease without encoding proteins. Biochimie 2012, 94:1474-1480.
52. Navarro B., Gisel A., Rodio M.E., Delgado S., Flores R., Di Serio F. Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host mRNA as predicted by RNA silencing. Plant J. 2012, 70:991-1003.
53. Owens R.A., Steger G., Hu Y., Fels A., Hammond R.W., Riesner D. RNA structural features responsible for potato spindle tuber viroid pathogenicity. Virology 1996, 222:144-158.
54. Owens R.A., Tech K.B., Shao J.Y., Sano T., Baker C.J. Global analysis of tomato gene expression during Potato spindle tuber viroid infection reveals a complex array of changes affecting hormone signaling. Mol. Plant Microbe Interact. 2012, 25:582-598.
55. Papaefthimiou I., Hamilton A.J., Denti M.A., Baulcombe D.C., Tsagris M., Tabler M. Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of posttranscriptional gene silencing. Nucleic Acids Res. 2001, 29:2395-2400.
56. Rana T.M. Illuminating the silence: understanding the structure and function of small RNAs. Nat. Rev. Mol. Cell Biol. 2007, 8:23-36.
57. Rehmsmeier M., Steffen P., Hochsmann M., Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA 2004, 10:1507-1517.
58. Sano T., Barba M., Li S.F., Hadidi A. Viroids and RNA silencing: mechanism role in viroid pathogenicity and development of viroid-resistant plants. GM Crops 2010, 1:80-86.
59. Semancik J.S. Avocado Sunblotch Viroid. Viroids 2003, 171-177. CSIRO Publishing, Collingwood, Victoria, Australia. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
60. Smith T.F., Gaitatzes C., Saxena K., Neer E.J. The WD40 repeat: a common architecture for diverse functions. Trends Biochem. Sci. 1999, 24:181-185.
61. Stirnimann C.U., Petsalaki E., Russell R.B., Müller C.W. WD40 proteins propel cellular networks. Trends Biochem. Sci. 2010, 35:565-574.
62. St-Pierre P.I., Hassen F., Thompson D., Perreault J.P. Characterization of siRNAs associated with peach latent mosaic viroid infection. Virology 2009, 383:178-182.
63. Tabler M., Tsagris M. Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci. 2004, 9:339-348.
64. Vance V., Vaucheret H. RNA silencing in plants - defense and counterdefense. Science 2001, 292:2277-2280.
65. Vanitharani R., Chellappan P., Fauquet C.M. Short interfering RNA-mediated interference of gene expression and viral DNA accumulation in cultured plant cells. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9632-9636.
66. Verhoeven J., Jansen C., Willemen T.M., Kox L.F.F., Owens R.A., Roenhorst J. Natural infections of tomato by Citrus exocortis viroid, Columnea latent viroid. Potato spindle tuber viroid and Tomato chlorotic dwarf viroid. Eur. J. Plant Pathol. 2004, 110:823-831.
67. Visvader J.E., Symons R.H. Eleven new sequence variants of citrus exocortis viroid and the correlation of sequence with pathogenicity. Nucleic Acids Res. 1985, 113:2907-2920.
68. Voinnet O. Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility. Curr. Opin. Plant Biol. 2008, 11:464-470.
69. Wang M.B., Bian X.Y., Wu M., Liu L.X., Smith N.A., Isenegger D., Wu R.M., Masuta C., Vance V.B., Watson J.M., Rezaian A., Dennis E.S., Waterhouse P.M. On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3275-3280.
70. Wang Y., Shibuya M., Taneda A., Kurauchi T., Senda M., Owens R.A., Sano T. Accumulation of Potato spindle tuber viroid-specific small RNAs is accompanied by specific changes in gene expression in two tomato cultivars. Virology 2011, 413:72-83.
71. Wang Y., Hu X.J., Zou X.D., Wu X.H., Ye Z.Q., Wu Y.D. WDSPdb: a database for WD40-repeat proteins. Nucleic Acids Res. 2014, (Epub ahead of print). 10.1093/nar/gku1023.
72. Zamore P.D. Thirty-three years later, a glimpse at the ribonuclease III active site. Mol. Cell 2001, 8:1158-1160.
73. Zamore P.D. RNA interference: listening to the sound of silence. Nat. Struct. Biol. 2001, 8:746-750.
74. Zhang Y., Zhu X., Chen X., Song C., Zou Z., Wang Y., Wang M., Fang W., Li X. Identification and characterization of cold-responsive microRNAs in tea plant (Camellia sinensis) and their targets using high-throughput sequencing and degradome analysis. BMC Plant Biol. 2014, 14:271.