Dicer-Like Proteins Regulate Sexual Development via the Biogenesis of Perithecium-Specific MicroRNAs in a Plant Pathogenic Fungus Fusarium graminearum

Zeng, Wenping; Wang, Jie; Wang, Ying; Lin, Jing; Fù, Yànpíng; Xiè, Jiǎtāo; Chen, Tao; Liu, Huiquan; Chéng, Jiāsēn

doi:10.3389/fmicb.2018.00818

Cited by 38 publications

(51 citation statements)

References 73 publications

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“…However, even if the Z. tritici sRNAs do not play a direct role in the interaction with wheat, they may play a role at specific developmental stages of the fungus, as has been shown for other plant pathogenic fungi (Kim et al, 2015;Raman et al, 2017;Zeng et al, 2018). Also, we cannot discard the possibility that Z. tritici sRNAs may be acting at the transcriptional or translational level.…”

Section: Rnai Does Not Play Important Roles In Z Tritici During Wheamentioning

confidence: 89%

Small RNA Bidirectional Crosstalk During the Interaction Between Wheat and Zymoseptoria tritici

Wiedmer

Palma‐Guerrero

2020

Front. Plant Sci.

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Cross-kingdom RNA interference (RNAi) has been shown to play important roles during plant-pathogen interactions, and both plants and pathogens can use small RNAs (sRNAs) to silence genes in each other. This bidirectional cross-kingdom RNAi was still unexplored in the wheat-Zymoseptoria tritici pathosystem. Here, we performed a detailed analysis of the sRNA bidirectional crosstalk between wheat and Z. tritici. Using a combination of small RNA sequencing (sRNA-seq) and microRNA sequencing (mRNA-seq), we were able to identify known and novel sRNAs and study their expression and their action on putative targets in both wheat and Z. tritici. We predicted the target genes of all the sRNAs in either wheat or Z. tritici transcriptome and used degradome analysis to validate the cleavage of these gene transcripts. We could not find any clear evidence of a cross-kingdom RNAi acting by mRNA cleavage in this pathosystem. We also found that the fungal sRNA enrichment was lower in planta than during in vitro growth, probably due to the lower expression of the only Dicer gene of the fungus during plant infection. Our results support the recent finding that Z. tritici sRNAs cannot play important roles during wheat infection. However, we also found that the fungal infection induced wheat sRNAs regulating the expression of specific wheat genes, including auxin-related genes, as an immune response. These results indicate a role of sRNAs in the regulation of wheat defenses during Z. tritici infection. Our findings contribute to improve our understanding of the interactions between wheat and Z. tritici.

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Section: Rnai Does Not Play Important Roles In Z Tritici During Wheamentioning

confidence: 89%

Small RNA Bidirectional Crosstalk During the Interaction Between Wheat and Zymoseptoria tritici

Wiedmer

Palma‐Guerrero

2020

Front. Plant Sci.

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“…However, the mechanistic roles of Fg RNAi components in these processes are inadequately understood. Nevertheless, existing data suggest that there is a functional diversification of Fg AGO1/ Fg DCL2- and Fg AGO2/ Fg DCL1-regulated pathways (Chen et al 2015; Son et al 2017; Zeng et al 2018; Gaffar et al 2019).…”

Section: Discussionmentioning

confidence: 99%

“…In addition, we recently demonstrated that Fg AGO2 and Fg DCL1 are required for sex-specific RNAi (Gaffar et al 2019). Moreover, Fg AGO2 and Fg DCL1 participate in the biogenesis of perithecium-specific microRNAs (Zeng et al 2018).…”

Section: Introductionmentioning

confidence: 99%

RNA-spray-mediated silencing ofFusarium graminearum AGOandDCLgenes improve barley disease resistance

Werner

Gaffar

Schuemann

et al. 2019

Preprint

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AbstractOver the last decade, several studies have revealed the enormous potential of RNA-silencing strategies as a potential alternative to conventional pesticides for plant protection. We have previously shown that targeted gene silencing mediated by an in planta expression of non-coding inhibitory double-stranded RNAs (dsRNAs) can protect host plants against various diseases with unprecedented efficiency. In addition to the generation of RNA-silencing (RNAi) signals in planta, plants can be protected from pathogens and pests by spray-applied RNA-based biopesticides. Despite the striking efficiency of RNA-silencing-based technologies holds for agriculture, the molecular mechanisms underlying spray-induced gene silencing (SIGS) strategies are virtually unresolved, a requirement for successful future application in the field. Based on our previous work, we predict that the molecular mechanism of SIGS is controlled by the fungal-silencing machinery. In this study, we used SIGS to compare the silencing efficiencies of computationally-designed versus manually-designed dsRNA constructs targeting ARGONAUTE and DICER genes of Fusarium graminearum (Fg). We found that targeting key components of the fungal RNAi machinery via SIGS could protect barley leaves from Fg infection and that the manual design of dsRNAs resulted in higher gene-silencing efficiencies than the tool-based design. Moreover, our results indicate the possibility of cross-kingdom RNA silencing in the Fg-barley interaction, a phenomenon in which sRNAs operate as effector molecules to induce gene silencing between species from different kingdoms, such as a plant host and their interacting pathogens.

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“…This wouldn't be unprecedented as some fungal species, including Ustilago maydis, which is a serious pathogen of maize, have lost RNAi (Billmyre et al, 2013). Furthermore, knockout of either DCL, AGO, or RdRp encoding genes in another fungal pathogen of wheat, F. graminearum, did not compromise pathogenicity towards wheat (Kim et al, 2015;and own unpublished data) and it has been recently demonstrated that the RNAi machinery in F. graminearum is mainly involved in the regulation of sexual development (Kim et al, 2015;Zeng et al, 2018). It would be interesting to investigate in future studies whether the same may be true for Z. tritici.…”

Section: Discussionmentioning

confidence: 99%

Analysis of small RNA silencing in Zymoseptoria tritici – wheat interactions

Kettles

Hofinger

et al. 2018

Preprint

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Cross-kingdom small RNA (sRNA) silencing has recently emerged as a mechanism facilitating fungal colonization and disease development. Here we characterized RNAi pathways in Zymoseptoria tritici, a major fungal pathogen of wheat, and assessed their contribution to pathogenesis. Computational analysis of fungal sRNA and host mRNA sequencing datasets was used to define the global sRNA populations in Z. tritici and predict their mRNA targets in wheat. 389 in planta-induced sRNA loci were identified. sRNAs generated from some of these loci were predicted to target wheat mRNAs including those potentially involved in pathogen defense. However, molecular approaches failed to validate targeting of selected wheat mRNAs by fungal sRNAs. Mutant strains of Z. tritici carrying deletions of genes encoding key components of RNAi such as Dicer-like (DCL) and Argounate (AGO) proteins were generated, and virulence bioassays suggested that these are dispensable for full infection of wheat. Nonetheless, our results did suggest the existence of non-canonical DCL-independent pathway(s) for sRNA biogenesis in Z. tritici. dsRNA targeting essential fungal genes applied in vitro or generated from an RNA virus vector in planta in a procedure known as HIGS (Host-Induced Gene Silencing) was ineffective in preventing Z. tritici growth or disease. We also demonstrated that Z. tritici is incapable of dsRNA uptake. Collectively, our data suggest that RNAi approaches for gene function analyses in this fungal species and potentially also as a control measure may not be as effective as has been demonstrated for some other plant pathogenic fungi.

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Dicer-Like Proteins Regulate Sexual Development via the Biogenesis of Perithecium-Specific MicroRNAs in a Plant Pathogenic Fungus Fusarium graminearum

Cited by 38 publications

References 73 publications

Small RNA Bidirectional Crosstalk During the Interaction Between Wheat and Zymoseptoria tritici

Small RNA Bidirectional Crosstalk During the Interaction Between Wheat and Zymoseptoria tritici

RNA-spray-mediated silencing ofFusarium graminearum AGOandDCLgenes improve barley disease resistance

Analysis of small RNA silencing in Zymoseptoria tritici – wheat interactions

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