Inside-out: from endosomes to extracellular vesicles in fungal RNA transport

Kwon, Seomun; Tisserant, Constance; Tulinski, Markus; Weiberg, Arne; Feldbrügge, Michael

doi:10.1016/j.fbr.2020.01.001

Cited by 21 publications

(18 citation statements)

References 116 publications

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“…vasinfectum were described to induce a phytotoxic response in plants (Bleackley et al, 2019b), which reinforce this hypothesis. This subject has been discussed in detail in recent reviews (Huang et al, 2019;Kwon et al, 2020).…”

Section: Cell-to-cell Communication Mediated By Evsmentioning

confidence: 99%

Extracellular Vesicles in Fungi: Past, Present, and Future Perspectives

Rizzo

Rodrigues

Janbon

2020

Front. Cell. Infect. Microbiol.

105

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Extracellular vesicles (EVs) have garnered much interest in the cell biology and biomedical research fields. Many studies have reported the existence of EVs in all types of living cells, including in fifteen different fungal genera. EVs play diverse biological roles, from the regulation of physiological events and response to specific environmental conditions to the mediation of highly complex interkingdom communications. This review will provide a historical perspective on EVs produced by fungi and an overview of the recent discoveries in the field. We will also review the current knowledge about EV biogenesis and cargo, their role in cell-to-cell interactions, and methods of EV analysis. Finally, we will discuss the perspectives of EVs as vehicles for the delivery of biologically active molecules.

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Section: Cell-to-cell Communication Mediated By Evsmentioning

confidence: 99%

Extracellular Vesicles in Fungi: Past, Present, and Future Perspectives

Rizzo

Rodrigues

Janbon

2020

Front. Cell. Infect. Microbiol.

105

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“…This sRNA-based crosstalk, also known as cross-species RNAi, was first described by Weiberg et al [57], demonstrating that the fungal pathogen Botrytis cinerea produces sRNAs that mimic plant sRNAs and bind to A. thaliana AGO1 to antagonistically silence important plant immunity genes [57]. Similarly to the suggested plant EV-mediated sRNA transport, it is proposed that fungal sRNA delivery is also facilitated by EVs [31]. To prove this hypothesis, EVs isolated from different fungal pathogens, such as Ustilago maydis [30], Zymoseptoria tritici [20], Fusarium oxysporum [4,16] and F. graminearum [17,48], were established, which lay the foundation for further study of cross-species RNA transport in plant-fungus interactions in the near future.…”

Section: Open Accessmentioning

confidence: 90%

Extracellular vesicles isolated from dsRNA-sprayed barley plants exhibit no growth inhibition or gene silencing in Fusarium graminearum

Schlemmer

Lischka

Wegner

et al. 2022

Fungal Biol Biotechnol

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Numerous reports have shown that incorporating a double-stranded RNA (dsRNA)-expressing transgene into plants or applying dsRNA by spraying it onto their leaves successfully protects them against invading pathogens exploiting the mechanism of RNA interference (RNAi). How dsRNAs or siRNAs are transferred between donor host cells and recipient fungal cells is largely unknown. It is speculated that plant extracellular vesicles (EVs) function as RNA shuttles between plants and their pathogens. Recently, we found that EVs isolated from host-induced gene silencing (HIGS) or spray-induced gene silencing (SIGS) plants contained dsRNA-derived siRNAs. In this study, we evaluated whether isolated EVs from dsRNA-sprayed barley (Hordeum vulgare) plants affected the growth of the phytopathogenic ascomycete Fusarium graminearum. Encouraged by our previous finding that dropping barley-derived EVs on F. graminearum cultures caused fungal stress phenotypes, we conducted an in vitro growth experiment in microtiter plates where we co-cultivated F. graminearum with plant EVs isolated from dsRNA-sprayed barley leaves. We observed that co-cultivation of F. graminearum macroconidia with barley EVs did not affect fungal growth. Furthermore, plant EVs containing SIGS-derived siRNA appeared not to affect F. graminearum growth and showed no gene silencing activity on F. graminearum CYP51 genes. Based on our findings, we concluded that either the amount of SIGS-derived siRNA was insufficient to induce target gene silencing in F. graminearum, indicating that the role of EVs in SIGS is minor, or that F. graminearum uptake of plant EVs from liquid cultures was inefficient or impossible.

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“…A diverse collection of plant sRNAs, including miRNAs and siRNAs, are selectively loaded into the EVs of plant cells [ 85 , 163 ]. It was suggested that fungal sRNAs delivery is facilitated by EVs, similar to the suggested plant-extracellular vesicle-mediated sRNA transport [ 166 ]. To test this hypothesis, EVs isolated from various fungal pathogens including F. oxysporum [ 167 , 168 ], F. graminearum [ 168 , 169 ], Z. tritici [ 170 ], and Ustilago maydis [ 171 ], were established and this laid a foundation for future study of cross-kingdom RNA transport in plant-fungal pathogen interactions [ 172 ].…”

Section: Translocation Of Non-proteinaceous Effectors Across Kingdoms...mentioning

confidence: 99%

Fungal Secondary Metabolites and Small RNAs Enhance Pathogenicity during Plant-Fungal Pathogen Interactions

Mapuranga

Chang

Zhang

et al. 2022

JoF

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Fungal plant pathogens use proteinaceous effectors as well as newly identified secondary metabolites (SMs) and small non-coding RNA (sRNA) effectors to manipulate the host plant’s defense system via diverse plant cell compartments, distinct organelles, and many host genes. However, most molecular studies of plant–fungal interactions have focused on secreted effector proteins without exploring the possibly equivalent functions performed by fungal (SMs) and sRNAs, which are collectively known as “non-proteinaceous effectors”. Fungal SMs have been shown to be generated throughout the plant colonization process, particularly in the early biotrophic stages of infection. The fungal repertoire of non-proteinaceous effectors has been broadened by the discovery of fungal sRNAs that specifically target plant genes involved in resistance and defense responses. Many RNAs, particularly sRNAs involved in gene silencing, have been shown to transmit bidirectionally between fungal pathogens and their hosts. However, there are no clear functional approaches to study the role of these SM and sRNA effectors. Undoubtedly, fungal SM and sRNA effectors are now a treasured land to seek. Therefore, understanding the role of fungal SM and sRNA effectors may provide insights into the infection process and identification of the interacting host genes that are targeted by these effectors. This review discusses the role of fungal SMs and sRNAs during plant-fungal interactions. It will also focus on the translocation of sRNA effectors across kingdoms, the application of cross-kingdom RNA interference in managing plant diseases and the tools that can be used to predict and study these non-proteinaceous effectors.

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Inside-out: from endosomes to extracellular vesicles in fungal RNA transport

Cited by 21 publications

References 116 publications

Extracellular Vesicles in Fungi: Past, Present, and Future Perspectives

Extracellular Vesicles in Fungi: Past, Present, and Future Perspectives

Extracellular vesicles isolated from dsRNA-sprayed barley plants exhibit no growth inhibition or gene silencing in Fusarium graminearum

Fungal Secondary Metabolites and Small RNAs Enhance Pathogenicity during Plant-Fungal Pathogen Interactions

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