Small RNAs — the secret agents in the plant–pathogen interactions

Weiberg, Arne; Jin, Hailing

doi:10.1016/j.pbi.2015.05.033

Cited by 126 publications

(97 citation statements)

References 87 publications

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“…During this process, differential expression of endogenous sRNAs accompanies defense responses to pathogen attack (Katiyar‐Agarwal & Jin, ). Studies of sRNA biogenesis and sRNA functioning genes have shown that impairing these genes reduces the defense against certain pathogens (Weiberg & Jin, ). We show here the A. tauschii AGO4a antibody specifically pulled down 24‐nt siRNAs that began with the base adenine, a typical characteristic of AGO4a proteins, as observed in Arabidopsis (Mi et al ., ) and rice (Wu et al ., ).…”

Section: Discussionmentioning

confidence: 99%

“…These observations suggest that reduced DNA methylation promotes host defense responses against pathogen infection (Yu et al ., ). Among the key components of the RdDM pathway, AGO4a is required for resistance to P. syringae in Arabidopsis (Agorio & Vera, ); small RNAs (sRNAs) also play a role in plant immunity in this system (Weiberg & Jin, ). However, little information is known about DNA methylation dynamics in crops such as wheat, one of the most important staple foods worldwide.…”

Section: Introductionmentioning

confidence: 99%

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DNA methylation dynamics during the interaction of wheat progenitor Aegilops tauschii with the obligate biotrophic fungus Blumeria graminis f. sp. tritici

et al. 2018

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DNA methylation is dynamically involved in plant immunity, but little information is known about its roles in plant interactions with biotrophic fungi, especially in temperate grasses such as wheat (Triticum aestivum). Using wheat diploid progenitor Aegilops tauschii accession AL8/78, the genome of which has been sequenced, we assessed the extent of DNA methylation in response to infection with Blumeria graminis f. sp. tritici (Bgt), which causes powdery mildew. Upon Bgt infection, ARGONAUTE4a (AGO4a) was significantly downregulated in A. tauschii, which was accompanied by a substantial reduction in AGO4a-sorted 24-nt siRNA levels, especially for genes near transposable elements (TAGs). Bisulfite sequencing revealed abundant differentially methylated regions (DMRs) with CHH hypomethylation. TAGs bearing CHH-hypomethylated DMRs were enriched for 'response to stress' functions, including receptor kinase, peroxidase, and pathogenesis-related genes. Virus-induced gene silencing (VIGS) of a DOMAINS REARRANGED METHYLASE 2 (DRM2) homolog enhanced plant resistance to Bgt. The effect of CHH hypomethylation was exemplified by the upregulation of a pathogenesis-related β-1,3-glucanse gene implicated in Bgt defense. These findings support the idea that dynamic DNA methylation represents a regulatory layer in the complex mechanism of plant immunity, which could be exploited to improve disease resistance in common wheat.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

DNA methylation dynamics during the interaction of wheat progenitor Aegilops tauschii with the obligate biotrophic fungus Blumeria graminis f. sp. tritici

et al. 2018

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“…One such essential antiviral response is RNA silencing (4-6), a cellular mechanism conserved from lower eukaryotes to mammals to regulate endogenous gene expression at the transcriptional and posttranscriptional levels (7,8). To activate antiviral RNA silencing, the viral double-stranded RNAs (dsRNAs), which may originate during viral replication, as a result of internal pairing of viral RNA molecules, or through de novo synthesis by the host RNA-dependent RNA polymerase 6 (RDR6)/ suppressor of gene silencing 3 (SGS3) complex using viral genomic fragments as the template, are processed by Dicer-like (DCL) proteins into small 20-to 24-nucleotide (nt) RNA duplexes termed virus-derived short interfering RNAs (vsiRNAs).…”

mentioning

confidence: 99%

The Potyvirus Silencing Suppressor Protein VPg Mediates Degradation of SGS3 via Ubiquitination and Autophagy Pathways

Cheng

Wang

2017

J Virol

134

115

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RNA silencing is an innate antiviral immunity response of plants and animals. To counteract this host immune response, viruses have evolved an effective strategy to protect themselves by the expression of viral suppressors of RNA silencing (VSRs). Most potyviruses encode two VSRs, helper component-proteinase (HCPro) and viral genome-linked protein (VPg). The molecular biology of the former has been well characterized, whereas how VPg exerts its function in the suppression of RNA silencing is yet to be understood. In this study, we show that infection by Turnip mosaic virus (TuMV) causes reduced levels of suppressor of gene silencing 3 (SGS3), a key component of the RNA silencing pathway that functions in doublestranded RNA synthesis for virus-derived small interfering RNA (vsiRNA) production. We also demonstrate that among 11 TuMV-encoded viral proteins, VPg is the only one that interacts with SGS3. We furthermore present evidence that the expression of VPg alone, independent of viral infection, is sufficient to induce the degradation of SGS3 and its intimate partner RNA-dependent RNA polymerase 6 (RDR6). Moreover, we discover that the VPg-mediated degradation of SGS3 occurs via both the 20S ubiquitin-proteasome and autophagy pathways. Taken together, our data suggest a role for VPg-mediated degradation of SGS3 in suppression of silencing by VPg.IMPORTANCE Potyviruses represent the largest group of known plant viruses and cause significant losses of many agriculturally important crops in the world. In order to establish infection, potyviruses must overcome the host antiviral silencing response. A viral protein called VPg has been shown to play a role in this process, but how it works is unclear. In this paper, we found that the VPg protein of Turnip mosaic virus (TuMV), which is a potyvirus, interacts with a host protein named SGS3, a key protein in the RNA silencing pathway. Moreover, this interaction leads to the degradation of SGS3 and its interacting and functional partner RDR6, which is another essential component of the RNA silencing pathway. We also identified the cellular pathways that are recruited for the VPg-mediated degradation of SGS3. Therefore, this work reveals a possible mechanism by which VPg sabotages host antiviral RNA silencing to promote virus infection. KEYWORDS RDR6, RNA silencing, SGS3, VPg, VSR, autophagy, potyvirus, ubiquitination T o establish systemic infection, an invading virus must remodel and recruit host elements and overcome resistance responses through complex molecular virushost interactions (1-3). One such essential antiviral response is RNA silencing (4-6), a cellular mechanism conserved from lower eukaryotes to mammals to regulate endogenous gene expression at the transcriptional and posttranscriptional levels (7, 8). To activate antiviral RNA silencing, the viral double-stranded RNAs (dsRNAs), which may

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“…The impact of sRNA on the ecological interactions between parasites and their hosts is already well appreciated (reviewed in 156 ). The possibility of cross-kingdom regulation of gene expression via ingested sRNAs could also be of particular ecological interest.…”

Section: Discussionmentioning

confidence: 99%

Uptake and impact of natural diet-derived small RNA in invertebrates: Implications for ecology and agriculture

Chan

Snow

2016

RNA Biology

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The putative transfer and gene regulatory activities of diet-derived small RNAs (sRNAs) in ingesting animals are still debated. The existence of natural uptake of diet-derived sRNA by invertebrate species could have significant implication for our understanding of ecological relationships and could synergize with efforts to use RNA interference (RNAi) technology in agriculture. Here, we synthesize information gathered from studies in invertebrates using natural or artificial dietary delivery of sRNA and from studies of sRNA in vertebrate animals and plants to review our current understanding of uptake and impact of natural dietderived sRNA on invertebrates. Our understanding has been influenced and sometimes confounded by the diversity of invertebrates and ingested plants studied, our limited insights into how gene expression may be modulated by dietary sRNAs at the mechanistic level, and the paucity of studies focusing directly on natural uptake of sRNA. As such, we suggest 2 strategies to investigate this phenomenon more comprehensively and thus facilitate the realization of its potentially broad impact on ecology and agriculture in the future.

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Small RNAs — the secret agents in the plant–pathogen interactions

Cited by 126 publications

References 87 publications

DNA methylation dynamics during the interaction of wheat progenitor Aegilops tauschii with the obligate biotrophic fungus Blumeria graminis f. sp. tritici

DNA methylation dynamics during the interaction of wheat progenitor Aegilops tauschii with the obligate biotrophic fungus Blumeria graminis f. sp. tritici

The Potyvirus Silencing Suppressor Protein VPg Mediates Degradation of SGS3 via Ubiquitination and Autophagy Pathways

Uptake and impact of natural diet-derived small RNA in invertebrates: Implications for ecology and agriculture

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