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Journal of Virology, September 2008, p. 8997-9007, Vol. 82, No. 18
0022-538X/08/$08.00+0     doi:10.1128/JVI.00719-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Viral Genome Methylation as an Epigenetic Defense against Geminiviruses{triangledown} ,{dagger}

Priya Raja, Bradley C. Sanville, R. Cody Buchmann, and David M. Bisaro*

Department of Molecular Genetics, Plant Biotechnology Center, and Program in Molecular, Cellular and Developmental Biology, The Ohio State University, Columbus, Ohio 43210

Received 1 April 2008/ Accepted 25 June 2008

Geminiviruses encapsidate single-stranded DNA genomes that replicate in plant cell nuclei through double-stranded DNA intermediates that associate with cellular histone proteins to form minichromosomes. Like most plant viruses, geminiviruses are targeted by RNA silencing and encode suppressor proteins such as AL2 and L2 to counter this defense. These related proteins can suppress silencing by multiple mechanisms, one of which involves interacting with and inhibiting adenosine kinase (ADK), a cellular enzyme associated with the methyl cycle that generates S-adenosyl-methionine, an essential methyltransferase cofactor. Thus, we hypothesized that the viral genome is targeted by small-RNA-directed methylation. Here, we show that Arabidopsis plants with mutations in genes encoding cytosine or histone H3 lysine 9 (H3K9) methyltransferases, RNA-directed methylation pathway components, or ADK are hypersensitive to geminivirus infection. We also demonstrate that viral DNA and associated histone H3 are methylated in infected plants and that cytosine methylation levels are significantly reduced in viral DNA isolated from methylation-deficient mutants. Finally, we demonstrate that Beet curly top virus L2– mutant DNA present in tissues that have recovered from infection is hypermethylated and that host recovery requires AGO4, a component of the RNA-directed methylation pathway. We propose that plants use chromatin methylation as a defense against DNA viruses, which geminiviruses counter by inhibiting global methylation. In addition, our results establish that geminiviruses can be useful models for genome methylation in plants and suggest that there are redundant pathways leading to cytosine methylation.

* Corresponding author. Mailing address: Biotechnology Center, The Ohio State University, 201 Rightmire Hall, 1060 Carmack Road, Columbus, OH 43210. Phone: (614) 292-3281. Fax: (614) 292-5379. E-mail: bisaro.1{at}osu.edu

{triangledown} Published ahead of print on 2 July 2008.

{dagger} Supplemental material for this article may be found at http://jvi.asm.org/.

Journal of Virology, September 2008, p. 8997-9007, Vol. 82, No. 18
0022-538X/08/$08.00+0     doi:10.1128/JVI.00719-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Buchmann, R. C., Asad, S., Wolf, J. N., Mohannath, G., Bisaro, D. M. (2009). Geminivirus AL2 and L2 Proteins Suppress Transcriptional Gene Silencing and Cause Genome-Wide Reductions in Cytosine Methylation. J. Virol. 83: 5005-5013 [Abstract] [Full Text]  
  • Rodriguez-Negrete, E. A., Carrillo-Tripp, J., Rivera-Bustamante, R. F. (2009). RNA Silencing against Geminivirus: Complementary Action of Posttranscriptional Gene Silencing and Transcriptional Gene Silencing in Host Recovery. J. Virol. 83: 1332-1340 [Abstract] [Full Text]  


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