A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants

Nucleic Acids Research

Volumn 42, Issue 3, 2014, Pages 1553-1562

  Martinez, German ^a,b   Castellano, Mayte ^a   Tortosa, Maria ^a   Pallas, Vicente ^a   Gomez, Gustavo ^a  

^a CSIC   (Spain)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT DNA; RIBOSOME RNA; TRANSFER RNA; UNTRANSLATED RNA;

AGROBACTERIUM TUMEFACIENS; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CUCUMBER; DEMETHYLATION; DNA METHYLATION; DNA MODIFICATION; HOST PATHOGEN INTERACTION; NONHUMAN; NORTHERN BLOTTING; PLANT DISEASE; PLANT LEAF; PRIORITY JOURNAL; PROMOTER REGION; RNA EXTRACTION; RNA GENE; RNA TRANSCRIPTION; TRANSCRIPTION INITIATION; VIROID;

CUCUMIS SATIVUS; DNA METHYLATION; DNA, RIBOSOMAL; GENES, RRNA; PLANT DISEASES; RNA PRECURSORS; RNA, RIBOSOMAL; RNA, SMALL UNTRANSLATED; VIROIDS;

EID: 84896710969     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt968     Document Type: Article

References (56)

1. Ding, B. (2009) The biology of viroid-host interactions. Annu. Rev. Phytopathol., 47, 105-131.
2. Ding, B. (2010) Viroids: self-replicating, mobile, and fast-evolving noncoding regulatory RNAs. Wiley Interdiscip. Rev. RNA, 1, 362-375.
3. Navarro, B., Gisel, A., Rodio, M.E., Delgado, S., Flores, R. and Di Serio, F. (2012) Viroids: how to infect a host and cause disease without encoding proteins. Biochimie, 94, 1474-1480.
4. Zhao, Y., Owens, R.A. and Hammond, R.W. (2001) Use of a vector based on potato virus X in a whole plant assay to demonstrate nuclear targeting of potato spindle tuber viroid. J. Gen. Virol., 82, 1491-1497.
5. Gomez, G. and Pallas, V. (2012) Studies on subcellular compartmentalization of plant pathogenic noncoding RNAs give new insights into the intracellular RNA-traffic mechanisms. Plant Physiol., 159, 558-564.
6. Navarro, J.A., Vera, A. and Flores, R. (2000) A chloroplastic RNA polymerase resistant to tagetitoxin is involved in replication of avocado sunblotch viroid. Virology, 268, 218-225.
7. Nohales, M.A., Flores, R. and Daros, J.A. (2012) Viroid RNA redirects host DNA ligase 1 to act as an RNA ligase. Proc. Natl Acad. Sci. USA, 109, 13805-13810.
8. Nohales, M.A., Molina-Serrano, D., Flores, R. and Daros, J.A. (2012) Involvement of the chloroplastic isoform of tRNA ligase in the replication of viroids belonging to the family Avsunviroidae. J. Virol., 86, 8269-8276.
9. Zhong, X. and Ding, B. (2008) Distinct RNA motifs mediate systemic RNA trafficking. Plant Signal. Behav., 3, 58-59.
10. Gomez, G. and Pallas, V. (2004) A long-distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with Hop stunt viroid RNA. J. Virol., 78, 10104-10110.
11. Gomez, G. and Pallas, V. (2001) Identification of an in vitro ribonucleoprotein complex between a viroid RNA and a phloem protein from cucumber plants. Mol. Plant Microbe Interact., 14, 910-913.
12. Owens, R.A., Blackburn, M. and Ding, B. (2001) Possible involvement of the phloem lectin in long-distance viroid movement. Mol. Plant Microbe Interact., 14, 905-909.
13. Gomez, G. and Pallas, V. (2013) Viroids: a light in the darkness of the lncRNA-directed regulatory networks in plants. New Phytol., 198, 10-15.
14. Diener, T.O. (1981) Are viroids escaped introns? Proc. Natl Acad. Sci. USA, 78, 5014-5015.
15. Haas, B., Klanner, A., Ramm, K. and Sanger, H.L. (1988) The 7S RNA from tomato leaf tissue resembles a signal recognition particle RNA and exhibits a remarkable sequence complementarity to viroids. EMBO J., 7, 4063-4074.
16. Visvader, J.E. and Symons, R.H. (1985) Eleven new sequence variants of citrus exocortis viroid and the correlation of sequence with pathogenicity. Nucleic Acids Res., 13, 2907-2920.
17. Schnolzer, M., Haas, B., Raam, K., Hofmann, H. and Sanger, H.L. (1985) Correlation between structure and pathogenicity of potato spindle tuber viroid (PSTV). EMBO J., 4, 2181-2190.
18. Papaefthimiou, I., Hamilton, A., Denti, M., Baulcombe, D., Tsagris, M. and Tabler, M. (2001) Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res., 29, 2395-2400.
19. Wang, M.B., Bian, X.Y., Wu, L.M., Liu, L.X., Smith, N.A., Isenegger, D., Wu, R.M., Masuta, C., Vance, V.B., Watson, J.M. et al. (2004) On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc. Natl Acad. Sci. USA, 101, 3275-3280.
20. Gomez, G., Martinez, G. and Pallas, V. (2009) Interplay between viroid-induced pathogenesis and RNA silencing pathways. Trends Plant Sci., 14, 264-269.
21. Gomez, G., Martinez, G. and Pallas, V. (2008) Viroid-induced symptoms in Nicotiana benthamiana plants are dependent on RDR6 activity. Plant Physiol., 148, 414-423.
22. Navarro, B., Gisel, A., Rodio, M.E., Delgado, S., Flores, R. and Di Serio, F. (2012) 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., 70, 991-1003.
23. Dowen, R.H., Pelizzola, M., Schmitz, R.J., Lister, R., Dowen, J.M., Nery, J.R., Dixon, J.E. and Ecker, J.R. (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl Acad. Sci. USA, 109, E2183-E2191.
24. Law, J.A. and Jacobsen, S.E. (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet., 11, 204-220.
25. Matzke, M., Kanno, T., Daxinger, L., Huettel, B. and Matzke, A.J. (2009) RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol., 21, 367-376.
26. Zhang, X., Henderson, I.R., Lu, C., Green, P.J. and Jacobsen, S.E. (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc. Natl Acad. Sci. USA, 104, 4536-4541.
27. Haag, J.R. and Pikaard, C.S. (2011) Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol., 12, 483-492.
28. Gong, Z., Morales-Ruiz, T., Ariza, R.R., Roldan-Arjona, T., David, L. and Zhu, J.K. (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell, 111, 803-814.
29. Nuthikattu, S., McCue, A.D., Panda, K., Fultz, D., Defraia, C., Thomas, E.N. and Slotkin, R.K. (2013) The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiol., 162, 116-131.
30. Wassenegger, M., Heimes, S., Riedel, L. and Sanger, H.L. (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell, 76, 567-576.
31. Itaya, A., Matsuda, Y., Gonzales, R.A., Nelson, R.S. and Ding, B. (2002) Potato spindle tuber viroid strains of different pathogenicity induces and suppresses expression of common and unique genes in infected tomato. Mol. Plant Microbe Interact., 15, 990-999.
32. Owens, R.A., Tech, K.B., Shao, J.Y., Sano, T. and Baker, C.J. (2012) 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., 25, 582-598.
33. Tessitori, M., Maria, G., Capasso, C., Catara, G., Rizza, S., De Luca, V., Catara, A., Capasso, A. and Carginale, V. (2007) Differential display analysis of gene expression in Etrog citron leaves infected by Citrus viroid III. Biochim. Biophys. Acta, 1769, 228-235.
34. Herranz, M.C., Niehl, A., Rosales, M., Fiore, N., Zamorano, A., Granell, A. and Pallas, V. (2013) A remarkable synergistic effect at the transcriptomic level in peach fruits doubly infected by prunus necrotic ringspot virus and peach latent mosaic viroid. Virol. J., 10, 164.
35. Lison, P., Tarraga, S., Lopez-Gresa, P., Sauri, A., Torres, C., Campos, L., Belles, J.M., Conejero, V. and Rodrigo, I. (2013) A noncoding plant pathogen provokes both transcriptional and posttranscriptional alterations in tomato. Proteomics, 13, 833-844.
36. Gomez, G. and Pallas, V. (2006) Hop stunt viroid is processed and translocated in transgenic Nicotiana benthamiana plants. Mol. Plant Pathol., 7, 511-517.
37. Martinez, G., Donaire, L., Llave, C., Pallas, V. and 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. Pallas, V., Navarro, A. and Flores, R. (1987) Isolation of a viroidlike RNA from hop different from hop stunt viroid. J. Gen. Virol., 68, 3201-3205.
39. Gomez, G. and Pallas, V. (2007) Mature monomeric forms of Hop stunt viroid resist RNA silencing in transgenic plants. Plant J., 51, 1041-1049.
40. Dellaporta, S.L., Wood, J. and Hicks, J.B. (1983) A plant DNA minipreparation: version II. Plant Mol. Biol. Rep., 1, 19-21.
41. Martinez, G., Forment, J., Llave, C., Pallas, V. and Gomez, G. (2011) High-throughput sequencing, characterization and detection of new and conserved cucumber miRNAs. PLoS One, 6, e19523.
42. Long, E.O. and Dawid, I.B. (1980) Repeated genes in eukaryotes. Annu. Rev. Biochem., 49, 727-764.
43. Henras, A.K., Soudet, J., Gerus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A. and Henry, Y. (2008) The posttranscriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci., 65, 2334-2359.
44. Pontvianne, F., Blevins, T., Chandrasekhara, C., Feng, W., Stroud, H., Jacobsen, S.E., Michaels, S.D. and Pikaard, C.S. (2012) Histone methyltransferases regulating rRNA gene dose and dosage control in Arabidopsis. Genes Dev., 26, 945-957.
45. Preuss, S. and Pikaard, C.S. (2007) rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochim. Biophys. Acta, 1769, 383-392.
46. Earley, K.W., Pontvianne, F., Wierzbicki, A.T., Blevins, T., Tucker, S., Costa-Nunes, P., Pontes, O. and Pikaard, C.S. (2010) Mechanisms of HDA6-mediated rRNA gene silencing: suppression of intergenic Pol II transcription and differential effects on maintenance versus siRNA-directed cytosine methylation. Genes Dev., 24, 1119-1132.
47. Tucker, S., Vitins, A. and Pikaard, C.S. (2010) Nucleolar dominance and ribosomal RNA gene silencing. Curr. Opin. Cell Biol., 22, 351-356.
48. Layat, E., Cotterell, S., Vaillant, I., Yukawa, Y., Tutois, S. and Tourmente, S. (2012) Transcript levels, alternative splicing and proteolytic cleavage of TFIIIA control 5S rRNA accumulation during Arabidopsis thaliana development. Plant J., 71, 35-44.
49. Rodio, M.E., Delgado, S., De Stradis, A., Gomez, M.D., Flores, R. and Di Serio, F. (2007) A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell, 19, 3610-3626.
50. Yu, A., Lepere, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., Abraham, A.L., Penterman, J., Fischer, R.L., Voinnet, O. et al. (2013) Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc. Natl Acad. Sci. USA, 110, 2389-2394.
51. Sha, A.H., Lin, X.H., Huang, J.B. and Zhang, D.P. (2005) Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation-sensitive AFLP (MSAP) analysis. Mol. Genet. Genomics, 273, 484-490.
52. Boyko, A., Kathiria, P., Zemp, F.J., Yao, Y., Pogribny, I. and Kovalchuk, I. (2007) Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virusinduced plant genome instability). Nucleic Acids Res., 35, 1714-1725.
53. Rodriguez-Negrete, E., Lozano-Duran, R., Piedra-Aguilera, A., Cruzado, L., Bejarano, E.R. and Castillo, A.G. (2013) Geminivirus Rep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing. New Phytol., 199, 464-475.
54. Vaillant, I., Tutois, S., Cuvillier, C., Schubert, I. and Tourmente, S. (2007) Regulation of Arabidopsis thaliana 5S rRNA genes. Plant Cell Physiol., 48, 745-752.
55. Muhlbach, H.P. and Sanger, H.L. (1979) Viroid replication is inhibited by alpha-Amanitin. Nature, 278, 185-188.
56. Li, L.C. and Dahiya, R. (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics, 18, 1427-1431.