Journal Article

Virus infection triggers widespread silencing of host genes by a distinct class of endogenous siRNAs in Arabidopsis

Qiu, Yan-Hong, Du, Peng, Gal-On, Amit, Wang, Xianbing, Cao, Mengji, Ding, Shou-Wei, Li, Wanxiang, Li, Yi, Yu, Yun-Qi, Zhou, Changyong

2014

Overview

Significance RNAi-mediated antiviral immunity directs specific virus resistance by virus-derived siRNAs in contrast to broad-spectrum resistance triggered in innate immunity by host pattern recognition receptors. Here we show that induction of antiviral RNAi in Arabidopsis is associated with production of a genetically distinct class of virus-activated siRNAs (vasiRNAs) by RNA-dependent RNA polymerase-1 to target hundreds of host genes for RNA silencing by Argonaute-2. Production of vasiRNAs is induced by viruses from two different supergroups of RNA virus families, targeted for inhibition by Cucumber mosaic virus, and correlated with virus resistance independently of viral siRNAs. We propose that antiviral RNAi activates broad-spectrum antiviral activity via widespread silencing of host genes directed by vasiRNAs in addition to specific antiviral defense by viral siRNAs. Antiviral immunity controlled by RNA interference (RNAi) in plants and animals is thought to specifically target only viral RNAs by the virus-derived small interfering RNAs (siRNAs). Here we show that activation of antiviral RNAi in Arabidopsis plants is accompanied by the production of an abundant class of endogenous siRNAs mapped to the exon regions of more than 1,000 host genes and rRNA. These virus-activated siRNAs (vasiRNAs) are predominantly 21 nucleotides long with an approximately equal ratio of sense and antisense strands. Genetically, vasiRNAs are distinct from the known plant endogenous siRNAs characterized to date and instead resemble viral siRNAs by requiring Dicer-like 4 and RNA-dependent RNA polymerase 1 (RDR1) for biogenesis. However, loss of EXORIBONUCLEASE4/THYLENE-INSENSITIVE5 enhances vasiRNA biogenesis and virus resistance without altering the biogenesis of viral siRNAs. We show that vasiRNAs are active in directing widespread silencing of the target host genes and that Argonaute-2 binds to and is essential for the silencing activity of vasiRNAs. Production of vasiRNAs is readily detectable in Arabidopsis after infection by viruses from two distinct supergroups of plant RNA virus families and is targeted for inhibition by the silencing suppressor protein 2b of Cucumber mosaic virus. These findings reveal RDR1 production of Arabidopsis endogenous siRNAs and identify production of vasiRNAs to direct widespread silencing of host genes as a conserved response of plants to infection by diverse viruses. A possible function for vasiRNAs to confer broad-spectrum antiviral activity distinct to the virus-specific antiviral RNAi by viral siRNAs is discussed.

• Publisher: National Academy of Sciences,National Acad Sciences
• Subject: antiviral properties / Antivirals / Arabidopsis / Arabidopsis - genetics / Arabidopsis - immunology / Arabidopsis - virology / Arabidopsis Proteins - genetics / Biological Sciences / Biosynthesis / Blotting, Northern / Cucumber mosaic virus / Cucumovirus - genetics / Cucumovirus - immunology / Cucumovirus - physiology / Disease Resistance - genetics / Disease Resistance - immunology / Flowers & plants / Gene Expression Regulation, Plant / Genes / Host-Pathogen Interactions - genetics / Host-Pathogen Interactions - immunology / Immunity / Infections / innate immunity / Messenger RNA / Mutation / Plant Diseases - genetics / Plant Diseases - immunology / Plant Diseases - virology / Plant Viruses - genetics / Plant Viruses - immunology / Plant Viruses - physiology / Plants / Proteins / receptors / RNA / RNA Interference / RNA polymerase / RNA, Plant - genetics / RNA, Plant - immunology / RNA, Small Interfering - genetics / RNA, Small Interfering - immunology / Small interfering RNA / Viruses