Viral Infection Induces Expression of Novel Phased MicroRNAs from Conserved Cellular MicroRNA Precursors

Du, Peng; Wu, Jiang; Zhang, Jiayao; Zhao, Shuqi; Zheng, Hong; Gao, Ge; Wei, Liping; Li, Yang

doi:10.1371/journal.ppat.1002176

Cited by 164 publications

(166 citation statements)

References 81 publications

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“…3A). It has been reported that RSV infection induced the expression of OsRDR1 in rice (Satoh et al, 2010;Du et al, 2011). As we have shown that RSV infection induced the accumulation of miR444 (Fig.…”

Section: Overexpression Of Mir444 Increases Rice Resistance Against Vsupporting

confidence: 72%

“…RDR1 orthologs have been reported to be virus or salicylic acid inducible in different plants, including Arabidopsis, Nicotiana spp., Medicago truncatula, maize (Zea mays), and rice (Oryza sativa; Yang et al, 2004;Alamillo et al, 2006;He et al, 2010;Satoh et al, 2010;Du et al, 2011), and to provide basal resistance to several viruses by participating in the biogenesis of virusderived secondary siRNAs (Diaz-Pendon et al, 2007;Qi et al, 2009;Garcia-Ruiz et al, 2010;Wang et al, 2010). Recently, it was reported that RDR1 also is responsible for the production of a distinct class of virus-activated siRNAs, which direct widespread silencing of host genes to confer broad-spectrum antiviral activity in Arabidopsis (Cao et al, 2014), indicating that RDR1 plays a key role in antiviral resistance by silencing both the viral RNAs and the host immunity-related genes.…”

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confidence: 99%

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A Signaling Cascade from miR444 to RDR1 in Rice Antiviral RNA Silencing Pathway

et al. 2016

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Plant RNA-DEPENDENT RNA POLYMERASE1 (RDR1) is a key component of the antiviral RNA-silencing pathway, contributing to the biogenesis of virus-derived small interfering RNAs. This enzyme also is responsible for producing virusactivated endogenous small interfering RNAs to stimulate the broad-spectrum antiviral activity through silencing host genes. The expression of RDR1 orthologs in various plants is usually induced by virus infection. However, the molecular mechanisms of activation of RDR1 expression in response to virus infection remain unknown. Here, we show that a monocot-specific microRNA, miR444, is a key factor in relaying the antiviral signaling from virus infection to OsRDR1 expression. The expression of miR444 is enhanced by infection with Rice stripe virus (RSV), and overexpression of miR444 improves rice (Oryza sativa) resistance against RSV infection accompanied by the up-regulation of OsRDR1 expression. We further show that three miR444 targets, the MIKC C -type MADS box proteins OsMADS23, OsMADS27a, and OsMADS57, form homodimers and heterodimers between them to repress the expression of OsRDR1 by directly binding to the CArG motifs of its promoter. Consequently, an increased level of miR444 diminishes the repressive roles of OsMADS23, OsMADS27a, and OsMADS57 on OsRDR1 transcription, thus activating the OsRDR1-dependent antiviral RNA-silencing pathway. We also show that overexpression of miR444-resistant OsMADS57 reduced OsRDR1 expression and rice resistance against RSV infection, and knockout of OsRDR1 reduced rice resistance against RSV infection. In conclusion, our results reveal a molecular cascade in the rice antiviral pathway in which miR444 and its MADS box targets directly control OsRDR1 transcription.RNA silencing mediated by regulatory small RNAs (microRNAs [miRNAs] and small interfering RNAs [siRNAs]) negatively regulates gene expression at the posttranscriptional level or at the transcriptional level in eukaryotic organisms. Besides small RNAs, plant RNA-silencing pathways incorporate several kinds of core protein components, such as DICER-LIKE (DCL) RNase III endonucleases, which process long doublestranded RNA (dsRNA) into small RNA duplexes; ARGONAUTEs (AGOs), the major effector of the RNA-induced silencing complexes, which bind to small RNAs for silencing target RNAs; and RNA-dependent RNA polymerases (RDRs), which are required for copying single-stranded RNAs into dsRNAs for downstream processing by DCLs. Multiple DCLs, AGOs, and RDRs have evolved in plants and thus form an array of RNA-silencing pathways (Axtell, 2013;Martínez de Alba et al., 2013;Bologna and Voinnet, 2014). Among them, the antiviral RNA-silencing pathway is the earliest described and most extensively studied. It is well known that the antiviral silencing pathway directly targets viral RNAs. Briefly, as in Arabidopsis (Arabidopsis thaliana), the stem-loop structures and dsRNA replication intermediates of viral RNAs are recognized and cleaved by DCLs (DCL4 and DCL2) to produce primary virus-derived small interferi...

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Section: Overexpression Of Mir444 Increases Rice Resistance Against Vsupporting

confidence: 72%

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confidence: 99%

A Signaling Cascade from miR444 to RDR1 in Rice Antiviral RNA Silencing Pathway

et al. 2016

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“…] differentially induced by pathogen infection is the first step to investigate their functions in host immunity against the pathogen. Previously, a set of miRNAs were identified to be involved in plant immunity against bacterial and viral pathogens (Navarro et al, 2006;Du et al, 2011;Radwan et al, 2011;Seo et al, 2013). Recently, host miRNAs were also found to be responsive to the infection of an increasing list of filamentous pathogens, such as Cronartium quercuum (Lu et al, 2007), Erysiphe graminis (Xin et al, 2010), Fusarium virguliforme (Radwan et al, 2011), Phytophthora sojae (Guo et al, 2011), and Verticillium dahliae (Yin et al, 2012;Yang et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Multiple Rice MicroRNAs Are Involved in Immunity against the Blast Fungus Magnaporthe oryzae

et al. 2013

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MicroRNAs (miRNAs) are indispensable regulators for development and defense in eukaryotes. However, the miRNA species have not been explored for rice (Oryza sativa) immunity against the blast fungus Magnaporthe oryzae, the most devastating fungal pathogen in rice production worldwide. Here, by deep sequencing small RNA libraries from susceptible and resistant lines in normal conditions and upon M. oryzae infection, we identified a group of known rice miRNAs that were differentially expressed upon M. oryzae infection. They were further classified into three classes based on their expression patterns in the susceptible japonica line Lijiangxin Tuan Hegu and in the resistant line International Rice Blast Line Pyricularia-Kanto51-m-Tsuyuake that contains a single resistance gene locus, Pyricularia-Kanto 51-m (Pikm), within the Lijiangxin Tuan Hegu background. RNA-blot assay of nine of them confirmed sequencing results. Real-time reverse transcription-polymerase chain reaction assay showed that the expression of some target genes was negatively correlated with the expression of miRNAs. Moreover, transgenic rice plants overexpressing miR160a and miR398b displayed enhanced resistance to M. oryzae, as demonstrated by decreased fungal growth, increased hydrogen peroxide accumulation at the infection site, and up-regulated expression of defense-related genes. Taken together, our data indicate that miRNAs are involved in rice immunity against M. oryzae and that overexpression of miR160a or miR398b can enhance rice resistance to the disease.

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“…Coimmunoprecipitation with FLAG-and HA-specific antibodies was used to obtain (ix) AGO1 and (x) AGO2 complexes, respectively, from the FLAG-AGO1/ago1-36 and HA-AGO2 plants 14 d after infection with Fny CMV-Δ2b for extracting total loaded small RNAs for the construction and sequencing of small RNA libraries as described (52). Bioinformatic analysis was carried out as described previously (13,15,53). Briefly, small RNAs in the size range of 18-26 nt were used for further analysis after removing the adaptor sequences.…”

Section: Methodsmentioning

confidence: 99%

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

Cao

Wang

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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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.RNA silencing | microbiology | plant biology | viral suppressor of RNAi

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Viral Infection Induces Expression of Novel Phased MicroRNAs from Conserved Cellular MicroRNA Precursors

Cited by 164 publications

References 81 publications

A Signaling Cascade from miR444 to RDR1 in Rice Antiviral RNA Silencing Pathway

A Signaling Cascade from miR444 to RDR1 in Rice Antiviral RNA Silencing Pathway

Multiple Rice MicroRNAs Are Involved in Immunity against the Blast Fungus Magnaporthe oryzae

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

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