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Journal of Virology, March 2007, p. 2980-2994, Vol. 81, No. 6
0022-538X/07/$08.00+0     doi:10.1128/JVI.02339-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

A Structured Viroid RNA Serves as a Substrate for Dicer-Like Cleavage To Produce Biologically Active Small RNAs but Is Resistant to RNA-Induced Silencing Complex-Mediated Degradation{triangledown}

Asuka Itaya,1 Xuehua Zhong,1 Ralf Bundschuh,3,4,5 Yijun Qi,1,{dagger} Ying Wang,1 Ryuta Takeda,2 Ann R. Harris,6 Carlos Molina,1 Richard S. Nelson,6 and Biao Ding1,2,4*

Department of Plant Cellular and Molecular Biology and Plant Biotechnology Center, Ohio State University, Columbus, Ohio 43210,1 Molecular, Cellular, and Developmental Biology Program, Ohio State University, Columbus, Ohio 43210,2 Department of Physics, Ohio State University, Columbus, Ohio 43210,3 The RNA Group, Ohio State University, Columbus, Ohio 43210,4 Interdisciplinary Biophysics Graduate Program, Ohio State University, Columbus, Ohio 43210,5 Plant Biology Division, The Samuel R. Noble Foundation, Ardmore, Oklahoma 734016

Received 25 October 2006/ Accepted 21 December 2006

RNA silencing is a potent means of antiviral defense in plants and animals. A hallmark of this defense response is the production of 21- to 24-nucleotide viral small RNAs via mechanisms that remain to be fully understood. Many viruses encode suppressors of RNA silencing, and some viral RNAs function directly as silencing suppressors as counterdefense. The occurrence of viroid-specific small RNAs in infected plants suggests that viroids can trigger RNA silencing in a host, raising the question of how these noncoding and unencapsidated RNAs survive cellular RNA-silencing systems. We address this question by characterizing the production of small RNAs of Potato spindle tuber viroid (srPSTVds) and investigating how PSTVd responds to RNA silencing. Our molecular and biochemical studies provide evidence that srPSTVds were derived mostly from the secondary structure of viroid RNAs. Replication of PSTVd was resistant to RNA silencing, although the srPSTVds were biologically active in guiding RNA-induced silencing complex (RISC)-mediated cleavage, as shown with a sensor system. Further analyses showed that without possessing or triggering silencing suppressor activities, the PSTVd secondary structure played a critical role in resistance to RISC-mediated cleavage. These findings support the hypothesis that some infectious RNAs may have evolved specific secondary structures as an effective means to evade RNA silencing in addition to encoding silencing suppressor activities. Our results should have important implications in further studies on RNA-based mechanisms of host-pathogen interactions and the biological constraints that shape the evolution of infectious RNA structures.

* Corresponding author. Mailing address: Department of Plant Cellular and Molecular Biology and Plant Biotechnology Center, Ohio State University, 207 Rightmire Hall, 1060 Carmack Road, Columbus, OH 43210. Phone: (614) 247-6077. Fax: (614) 292-5379. E-mail: ding.35{at}osu.edu.

{triangledown} Published ahead of print on 3 January 2007.

{dagger} Present address: National Institute of Biological Sciences, Beijing, China.

Journal of Virology, March 2007, p. 2980-2994, Vol. 81, No. 6
0022-538X/07/$08.00+0     doi:10.1128/JVI.02339-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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