1887

Abstract

Like many plant RNA viruses, infection by potato spindle tuber viroid (PSTVd) is known to lead to RNA silencing and a marked reduction in visible disease. To examine the relationship between RNA silencing and this recovery phenomenon in greater detail, we have carried out time-course analyses of viroid-specific small RNA accumulation using several viroid–host combinations. These analyses revealed the presence of two size classes of viroid-specific small RNAs in infected plants, and sequence analysis subsequently demonstrated the presence of a previously undescribed cluster of small RNAs derived primarily from negative-strand PSTVd RNA. Although the clustering patterns were similar, the size distribution of PSTVd small RNAs isolated from symptomatic leaf tissue became more heterogeneous with time. The process by which viroid-specific small RNAs are generated appears to be more complicated than previously believed, possibly involving multiple DICER-LIKE activities, viroid RNA substrates and subcellular compartments.

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2007-12-01
2024-12-05
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References

  1. Denti M. A., Boutla A., Tsagris M., Tabler M. 2004; Short interfering RNAs specific for potato spindle tuber viroid are found in the cytoplasm but not in the nucleus. Plant J 37:762–769 [CrossRef]
    [Google Scholar]
  2. Ding B., Itaya A. 2007; Viroid: a useful model for studying the basic principles of infection and RNA biology. Mol Plant Microbe Interact 20:7–20 [CrossRef]
    [Google Scholar]
  3. Ebhardt H. A., Thi E. P., Wang M.-B., Unrau P. J. 2005; Extensive 3′ modification of small RNAs is modulated by helper component-proteinase expression. Proc Natl Acad Sci U S A 102:13398–13403 [CrossRef]
    [Google Scholar]
  4. Flores R., Hernández C., Martínez de Alba A. E., Daròs J. A., Di Serio F. 2005; Viroids and viroid-host interactions. Annu Rev Phytopathol 43:117–139 [CrossRef]
    [Google Scholar]
  5. Hadidi A., Flores R., Randles J. W., Semancik J. S. (editors) 2003 Viroids Collingwood, Australia: CSIRO Pub;
    [Google Scholar]
  6. Hamilton A., Voinnet O., Chappell L., Baulcombe D. 2002; Two classes of short interfering RNA in RNA silencing. EMBO J 21:4671–4679 [CrossRef]
    [Google Scholar]
  7. Herr A. J. 2005; Pathways through the small RNA world of plants. FEBS Lett 579:5879–5888 [CrossRef]
    [Google Scholar]
  8. Ho T., Pallett D., Rusholme R., Dalmay T., Wang H. 2006; A simplified method for cloning of short interfering RNAs from Brassica juncea infected with Turnip mosaic potyvirus and Turnip crinkle carmovirus . J Virol Methods 136:217–223 [CrossRef]
    [Google Scholar]
  9. Itaya A., Folimonov A., Matsuda Y., Nelson R. S., Ding B. 2001; Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol Plant Microbe Interact 14:1332–1334 [CrossRef]
    [Google Scholar]
  10. Itaya A., Zhong X., Bundschuh R., Qi Y., Wang Y., Takeda R., Harris A. R., Molina C., Nelson R. S., Ding B. 2007; 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 81:2980–2994 [CrossRef]
    [Google Scholar]
  11. Loss P., Schmitz M., Steger G., Riesner D. 1991; Formation of a thermodynamically metastable structure containing hairpin II is critical for infectivity of potato spindle tuber RNA. EMBO J 10:719–727
    [Google Scholar]
  12. Markarian N., Li H. W., Ding S. W., Semancik J. S. 2004; RNA silencing as related to viroid induced symptom expression. Arch Virol 149:397–406 [CrossRef]
    [Google Scholar]
  13. Martínez de Alba A. E., Flores R., Hernández C. 2002; Two chloroplastic viroids induce the accumulation of the small RNAs associated with post-transcriptional gene silencing. J Virol 76:13094–13096 [CrossRef]
    [Google Scholar]
  14. Molnár A., Csorba T., Lakatos L., Várallyay É., Lacomme C., Burgyán J. 2005; Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J Virol 79:7812–7818 [CrossRef]
    [Google Scholar]
  15. Pak J., Fire A. 2007; Distinct populations of primary and secondary effectors during RNAi in C. elegans . Science 315:241–244 [CrossRef]
    [Google Scholar]
  16. Papaefthimiou I., Hamilton A. J., Denti M. A., Baulcombe D. C., Tsagris M., Tabler M. 2001; Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of posttranscriptional gene silencing. Nucleic Acids Res 29:2395–2400 [CrossRef]
    [Google Scholar]
  17. Papp I., Mette M. F., Aufsatz W., Daxinger L., Schauer S. E., Ray A., van der Winden J., Matzke M., Matzke A. J. M. 2003; Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol 132:1382–1390 [CrossRef]
    [Google Scholar]
  18. Park M. Y., Wu G., Gonzalez-Sulser A., Vaucheret H., Poethig R. S. 2005; Nuclear processing and export of microRNAs in Arabidopsis . Proc Natl Acad Sci U S A 102:3691–3696 [CrossRef]
    [Google Scholar]
  19. Qi Y., Hannon G. J. 2005; Uncovering RNAi mechanisms in plants: biochemistry enters the foray. FEBS Lett 579:5899–5903 [CrossRef]
    [Google Scholar]
  20. Sano T., Matsuura Y. 2004; Accumulation of short interfering RNAs characteristic of RNA silencing precedes recovery of tomato plants from severe symptoms of Potato spindle tuber viroid infection. J Gen Plant Pathol 70:50–53 [CrossRef]
    [Google Scholar]
  21. Sijen T., Steiner F. A., Thijssen K. L., Plasterk R. H. A. 2007; Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315:244–247 [CrossRef]
    [Google Scholar]
  22. Steger G., Riesner D. 2003; Molecular characteristics. In Viroids pp 15–29 Edited by Hadidi A., Flores R., Randles J. W., Semancik J. S. Collingwood, Australia: CSIRO Pub;
    [Google Scholar]
  23. Tang G., Reinhart B. J., Bartel D. P., Zamore P. D. 2003; A biochemical framework for RNA silencing in plants. Genes Dev 17:49–63 [CrossRef]
    [Google Scholar]
  24. Tschudi C., Djikeng A., Shi H.-F., Ullu E. 2003; In vivo analysis of the RNA interference mechanism in Trypanosoma brucei . Methods 30:304–312 [CrossRef]
    [Google Scholar]
  25. Vaucheret H. 2006; Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771 [CrossRef]
    [Google Scholar]
  26. Wang M.-B., Bian X.-Y., Wu L.-M., Liu L.-X., Smith N., Isenegger D., Wu R.-M., Masuta C., Vance V. B. other authors 2004; On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc Natl Acad Sci U S A 101:3275–3280 [CrossRef]
    [Google Scholar]
  27. Xie Z., Johansen L. K., Gustafson A. M., Kasschau K. D., Lellis A. D., Zilberman D. 2004; Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:e104 [CrossRef]
    [Google Scholar]
  28. Yang Z., Ebright Y. W., Yu B., Chen X. 2006; HEN1 recognizes 21–24 nt small RNA duplexes and deposits a methyl group onto the 2′-OH of the 3′ terminal nucleotide. Nucleic Acids Res 34:667–675 [CrossRef]
    [Google Scholar]
  29. Yu B., Yang Z., Li J., Minakhina S., Yang M., Padgett R. W., Steward R., Chen X. 2005; Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935 [CrossRef]
    [Google Scholar]
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