Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection

Wang, Ming; Weiberg, Arne; Lin, Feng; Thomma, B.P.H.J.; Huang, Hsien Da; Jin, Hailing

doi:10.1038/nplants.2016.151

Cited by 617 publications

(818 citation statements)

References 52 publications

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“…Research of HIGS showed that host sRNAs generated by artificial transgenic expression can translocate into colonised pathogen cells to turn down virulence gene expression (Wang et al 2015). In the last few years, HIGS had proven to efficiently control pests, nematodes, filamentous pathogens and parasitic plants (Wang et al 2016). Our latest study described that transgenic cotton plants expressing artificial siRNAs specifically targeting VdH1i gain significant resistance against vascular wilt disease (Zhang et al 2016a).…”

Section: Discussionmentioning

confidence: 99%

“…Previous study identified that some Botrytis cinerea sRNAs can hijack host RNAi by binding to host Argonaute 1 (AGO1) to silence Arabidopsis and tomato genes involved in immunity (Weiberg et al 2013). In Arabidopsis and tomato, expressing sRNAs that target B. cinerea DCL gene attenuated fungal pathogenicity and growth (Wang et al 2016). RNAi-deficient Arabidopsis mutants showed affected defence against Verticillium and Fusarium , but not other fungal pathogens including Alternaria brassicicola, B. cinerea and Plectosphaerella cucumerina (Ellendorff et al 2009).…”

Section: Introductionmentioning

confidence: 99%

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Genome-wide profiling of sRNAs in the Verticillium dahliae-infected Arabidopsis roots

et al. 2018

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Small RNAs (sRNAs, including small interfering RNAs [siRNAs] and micro RNAs [miRNAs]) are key mediators of RNA silencing (or RNA interference), which play important roles in plant development and response to biotic and abiotic stimulation. Verticillium wilt is a plant vascular disease caused by the soil-borne fungal pathogens, such as Verticillium dahliae. We previously reported that V. dahliae infection increased two plant endogenous miRNAs that were exported to fungal cell to silence virulence genes. To investigate plant sRNAs in genome-wide response to V. dahliae infection, in this study, we constructed two sRNA libraries from Arabidopsis roots with and without V. dahliae infection, respectively. In total, 31 conserved miRNAs were found to be differentially expressed during the early stage of infection with V. dahliae using sRNA sequencing. Among these, the expression levels of miR160, miR164, miR166, miR167, miR390 and miR156h were confirmed by northern blot. Reverse transcription quantitative real time polymerase chain reaction results showed that the induction of miRNAs (miR160, miR164, miR166 and miR167) upon V. dahliae infection downregulated the expression of their targeted genes (ARF10, NAC1, PHV and ARF6), respectively. In addition, we identified specific phased siRNAs generated from distinct regions of two libraries. Profiling of these miRNAs and sRNAs lay the foundation for further understanding and utilising the host-induced gene silencing strategy to control plant vascular pathogens.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genome-wide profiling of sRNAs in the Verticillium dahliae-infected Arabidopsis roots

et al. 2018

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“…Our recent study suggested that the fungal plant pathogen Verticillium dahliae, the causal agent of Verticillium wilt, also uses pathogen sRNAs (Vd-sRNAs) as effectors, as Vd-sRNAs were found to be loaded into Arabidopsis Argonaute1 (AGO1) during infection. 34 The majority of the predicted host targets of these VdsRNA effectors are putative factors of plant immunity. In addition, animal parasites, such as the gastrointestinal nematode Heligmosomoides polygyrus, also secrete sRNAs via extracellular vesicles.…”

Section: Introductionmentioning

confidence: 99%

Botrytis small RNA Bc-siR37 suppresses plant defense genes by cross-kingdom RNAi

et al. 2017

Self Cite

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Pathogens secrete effector proteins to suppress host immune responses. Recently, we showed that an aggressive plant fungal pathogen Botrytis cinerea can also deliver small RNA effectors into host cells to suppress host immunity. B. cinerea sRNAs (Bc-sRNAs) translocate into host plants and hijack the plant RNAi machinery to induce cross-kingdom RNAi of host immune responsive genes. Here, we functionally characterized another Bc-sRNA effector Bc-siR37 that is predicted to target at least 15 Arabidopsis genes, including WRKY transcription factors, receptor-like kinases, and cell wall-modifying enzymes. Upon B. cinerea infection, the expression level of Bc-siR37 was induced, and at least eight predicted Arabidopsis target genes were downregulated. These target genes were also suppressed in the transgenic Arabidopsis plants overexpressing Bc-siR37, which exhibited enhanced disease susceptibility to B. cinerea. Furthermore, the knockout mutants of the Bc-siR37 targets, At-WRKY7, At-PMR6, and At-FEI2, also exhibited enhanced disease susceptibility to B. cinerea, giving further support that these genes indeed play a positive role in plant defense against B. cinerea. Our study demonstrates that analysis of pathogen sRNA effectors can be a useful tool to help identify host immunity genes against the corresponding pathogen.

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“…Recent studies from two different research groups demonstrate fungal control by exogenous application of sRNAs to F. graminearum [53] and B. cinerea [54]. The so-called spray-induced gene silencing (SIGS) might provide novel biotechnological opportunities to control fungal diseases.…”

Section: Rna Silencing and Plant Defence: An Outlookmentioning

confidence: 99%

Signs of Silence: Small RNAs and Antifungal Responses in Arabidopsis thaliana and Zea mays

Balmer¹,

Paoli²,

Si‐Ammour³

et al. 2017

Plant Engineering

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Plant small RNAs (sRNAs) are pivotal regulators of gene expression, which are crucial in maintaining genome integrity and flexibility during development, abiotic and biotic stress responses. Current evidence suggests that sRNAs might be inherent to the sophisticated plant innate immune system battling bacteria. However, the role of sRNAs during antifungal plant defences is less clear. Therefore, this chapter investigates the sRNA-mediated plant antifungal responses against the hemibiotrophic fungi Colletotrichum higginsianum and Colletotrichum graminicola in their respective compatible hosts Arabidopsis thaliana and Zea mays. A phenotypic and metabolomic analysis of A. thaliana sRNA mutants in response to C. higginsianum infection was performed, showing a hormonal and metabolic imbalance during fungal infection in these plants. To find whether fungal-induced sRNA could directly regulate defence genes in an agricultural important plant model, the expression of maize miRNAs in response to C. graminicola leaf and root infections was investigated. The results revealed the tissue-specific local and systemic adaptation of the miRNA transcriptome, where only a few miRNAs were targeting defence pathways. The general picture presented here points towards a role of sRNAs as fine-tuners of genetic and metabolomic defence response layers. This chapter also further discusses the potential of utilizing sRNA-based fungal control strategies.

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Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection

Cited by 617 publications

References 52 publications

Genome-wide profiling of sRNAs in the Verticillium dahliae-infected Arabidopsis roots

Genome-wide profiling of sRNAs in the Verticillium dahliae-infected Arabidopsis roots

Botrytis small RNA Bc-siR37 suppresses plant defense genes by cross-kingdom RNAi

Signs of Silence: Small RNAs and Antifungal Responses in Arabidopsis thaliana and Zea mays

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