Abstract
Gene silencing is a natural antiviral defense mechanism in plants. For effective infection, plant viruses encode viral silencing suppressors to counter this plant antiviral response. The geminivirus-encoded C4 protein has been identified as a gene silencing suppressor, but the underlying mechanism of action has not been characterized. Here, we report that Cotton Leaf Curl Multan virus (CLCuMuV) C4 protein interacts with S-adenosyl methionine synthetase (SAMS), a core enzyme in the methyl cycle, and inhibits SAMS enzymatic activity. By contrast, an R13A mutation in C4 abolished its capacity to interact with SAMS and to suppress SAMS enzymatic activity. Overexpression of wild-type C4, but not mutant C4R13A, suppresses both transcriptional gene silencing (TGS) and post-transcriptional gene silencing (PTGS). Plants infected with CLCuMuV carrying C4R13A show decreased levels of symptoms and viral DNA accumulation associated with enhanced viral DNA methylation. Furthermore, silencing of NbSAMS2 reduces both TGS and PTGS, but enhanced plant susceptibility to two geminiviruses CLCuMuV and Tomato yellow leaf curl China virus. These data suggest that CLCuMuV C4 suppresses both TGS and PTGS by inhibiting SAMS activity to enhance CLCuMuV infection in plants.
Highlights
In the course of plant-virus interactions, plants have evolved ingenious counter-attack mechanisms to diminish or eliminate invading viral pathogens
We report that a single geminiviral protein Cotton Leaf Curl Multan virus (CLCuMuV) C4 inhibits both plant transcriptional gene silencing (TGS) and post-transcriptional gene silencing (PTGS) to promote an effective viral infection
We show that CLCuMuV C4 protein interacts with S-adenosyl methionine synthetase (SAMS), a core enzyme in methyl cycle, and inhibits SAMS activity
Summary
In the course of plant-virus interactions, plants have evolved ingenious counter-attack mechanisms to diminish or eliminate invading viral pathogens. Of various plant antiviral defenses, gene silencing can target either viral RNAs for degradation through post-transcriptional gene silencing (PTGS) or DNA sequences of DNA viruses for epigenetic modification through transcriptional gene silencing (TGS) [1,2]. DNA cytosine methylation is an important epigenetic marker for gene silencing and controls plant development and gene expression. It plays an important role in plant defense against invading DNA viruses [3,4,5]. In PTGS, the methyltransferase HEN1 adds a 2’-O-methyl group to the 3’-terminal nucleotide of small RNAs to protect them from a 3’-end uridylation activity [7]. Several publications have proposed that some DNA viruses can interfere with the proper function of the methyl cycle to reduce plant DNA methylation for effective infection [9,10,11,12]
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