On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites

doi:10.1073/pnas.0400104101

On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites

^*Commonwealth Scientific and Industrial Research Organisation Plant Industry, P.O. Box 1600, Canberra ACT 2601, Australia; ^‡Commonwealth Scientific and Industrial Research Organisation Plant Industry, P.O. Box 350, Glen Osmond SA 5064, Australia; ^¶Institute for Horticultural Development, Agriculture Victoria, Knoxfield VIC 3176, Australia; ^**Plant Virology Laboratory, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan; and ^††Department of Biological Sciences, University of South Carolina, Columbia, SC 29208

Communicated by William James Peacock, Commonwealth Scientific and Industrial Research Organization, Canberra, Australia, January 12, 2004 (received for review September 1, 2003)

Abstract

Viroids and most viral satellites have small, noncoding, and highly structured RNA genomes. How they cause disease symptoms without encoding proteins and why they have characteristic secondary structures are two longstanding questions. Recent studies have shown that both viroids and satellites are capable of inducing RNA silencing, suggesting a possible role of this mechanism in the pathology and evolution of these subviral RNAs. Here we show that preventing RNA silencing in tobacco, using a silencing suppressor, greatly reduces the symptoms caused by the Y satellite of cucumber mosaic virus. Furthermore, tomato plants expressing hairpin RNA, derived from potato spindle tuber viroid, developed symptoms similar to those of potato spindle tuber viroid infection. These results provide evidence suggesting that viroids and satellites cause disease symptoms by directing RNA silencing against physiologically important host genes. We also show that viroid and satellite RNAs are significantly resistant to RNA silencing-mediated degradation, suggesting that RNA silencing is an important selection pressure shaping the evolution of the secondary structures of these pathogens.

Footnotes

↵ † To whom correspondence should be addressed. E-mail: ming-bo.wang{at}csiro.au.
↵ § Present address: School of Science, Northeast Normal University, Changchun 130024, China.
↵ ∥ Present address: HortResearch, 120 Mount Albert Road, Private Bag 92169, Auckland, New Zealand.
Abbreviations: CMV, cucumber mosaic virus; hpRNA, hairpin RNA; PSTVd, potato spindle tuber viroid; Y-Sat, Y satellite; dsRNA, double-stranded RNA; siRNA, small interfering RNA; RISC, RNA-induced silencing complex; RPVSat, cereal yellow dwarf virus RPV satellite; GUS, β-glucuronidase; dpi, days postinoculation.