Transmission of potato spindle tuber viroid between &lt;i&gt;Phytophthora infestans&lt;/i&gt; and host plants

Afanasenko, Olga; Хютти, А. В.; Мироненко, Н. В.; Lashina, Nina M.

doi:10.18699/vjgb-22-34

Cited by 10 publications

(14 citation statements)

References 46 publications

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“…We further demonstrated that HSVd could be bi-directionally transmitted between plant and fungus during the fungal colonization of the plant. Similarly, the transmission of PSTVd between P. infestans and the host plants under laboratory conditions was also recently demonstrated [ 16 ]. However, the occurrence of the cross-kingdom infection of viroids between plants and fungi in natural settings is still unexplored.…”

Section: Introductionmentioning

confidence: 82%

“…Viroids have been reported to infect and replicate in susceptible plant species [ 2 , 11 , 12 ], the unicellular yeast fungus Saccharomyces cerevisiae [ 13 ], cyanobacteria [ 14 ], filamentous plant-pathogenic fungi [ 15 ], and to some extent, an oomycete Phytoptora infestant [ 16 ]. Previously, our research group artificially introduced viroids into three filamentous plant pathogenic ascomycete fungi, Cryphonectria parasitica , Valsa mali , and Fusarium graminearum via the transfection of fungal spheroplasts with viroid RNA.…”

Section: Introductionmentioning

confidence: 99%

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Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi

Tian

Wei

Bian

et al. 2022

Cells

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Viroids are the smallest known infectious agents that are thought to only infect plants. Here, we reveal that several species of plant pathogenic fungi that were isolated from apple trees infected with apple scar skin viroid (ASSVd) carried ASSVd naturally. This finding indicates the spread of viroids to fungi under natural conditions and further suggests the possible existence of mycoviroids in nature. A total of 117 fungal isolates were isolated from ASSVd-infected apple trees, with the majority (85.5%) being an ascomycete Alternaria alternata and the remaining isolates being other plant-pathogenic or -endophytic fungi. Out of the examined samples, viroids were detected in 81 isolates (69.2%) including A. alternata as well as other fungal species. The phenotypic comparison of ASSVd-free specimens developed by single-spore isolation and ASSVd-infected fungal isogenic lines showed that ASSVd affected the growth and pathogenicity of certain fungal species. ASSVd confers hypovirulence on ascomycete Epicoccum nigrum. The mycobiome analysis of apple tree-associated fungi showed that ASSVd infection did not generally affect the diversity and structure of fungal communities but specifically increased the abundance of Alternaria species. Taken together, these data reveal the occurrence of the natural spread of viroids to plants; additionally, as an integral component of the ecosystem, viroids may affect the abundance of certain fungal species in plants. Moreover, this study provides further evidence that viroid infection could induce symptoms in certain filamentous fungi.

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Section: Introductionmentioning

confidence: 82%

Section: Introductionmentioning

confidence: 99%

Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi

Tian

Wei

Bian

et al. 2022

Cells

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“…Indeed, artificial inoculations showed that fungi are suitable hosts of plant viruses of the phylum Kitrinoviricota , such as in the case of the replication of brome mosaic virus (genus Bromovirus , family Bromoviridae ) and tomato bushy stunt virus (genus Tombusvirus , family Tombusviridae ) in Saccharomyces cerevisiae (yeast), a unicellular fungus [ 15 , 16 ], and the replication of tobacco mosaic virus (TMV, genus Tobamovirus , family Virgaviridae ) and other plant RNA viruses in plant pathogenic filamentous ascomycetes fungi, Colletotrichum acutatum, and Fusarium graminearum as well as in the plant pathogenic oomycete Phytophthora infestans [ 17 , 18 , 19 ]. Moreover, by artificial inoculation, some viroids, subviral agents of plants, were shown to infect plant pathogenic ascomycetes, Cryphonectria parasitica , Valsa mali, and F. graminearum, as well as P. infestans [ 20 , 21 ]. Importantly, our research group discovered the natural infection of a plant virus in a plant pathogenic basidiomycetous fungus.…”

Section: Introductionmentioning

confidence: 99%

“…Under laboratory conditions, CMV, TMV, viroid, and the fungal virus Cryphonectria hypovirus 1 (genus Hypovirus , family Hypoviridae ) can be bidirectionally transferred between the plant and fungus or oomycete during the fungal colonialization of plants [ 19 , 20 , 21 , 22 ]. This observation is in line with the current knowledge that during fungal infection, plants and fungi interact by exchanging cellular contents, including various macromolecules such as protein effectors and small RNAs [ 23 , 24 ].…”

Section: Introductionmentioning

confidence: 99%

Common but Nonpersistent Acquisitions of Plant Viruses by Plant-Associated Fungi

Cao

Liu

Pang

et al. 2022

Viruses

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Investigating a virus’s host range and cross-infection is important for better understanding the epidemiology and emergence of viruses. Previously, our research group discovered a natural infection of a plant RNA virus, cumber mosaic virus (genus Cucumovirus, family Bromoviridae), in a plant pathogenic basidiomycetous fungus, Rhizoctonia solani, isolated from a potato plant grown in the field. Here, we further extended the study to investigate whether similar cross-infection of plant viruses occurs widely in plant-associated fungi in natural conditions. Various vegetable plants such as spinach, leaf mustard, radish, celery, and other vegetables that showed typical virus-like diseases were collected from the fields in Shandong Province, China. High-throughput sequencing revealed that at least 11 known RNA viruses belonging to different genera, including Potyvirus, Fabavirus, Polerovirus, Waikavirus, and Cucumovirus, along with novel virus candidates belonging to other virus genera, infected or associated with the collected vegetable plants, and most of the leaf samples contained multiple plant viruses. A large number of filamentous fungal strains were isolated from the vegetable leaf samples and subjected to screening for the presence of plant viruses. RT-PCR and Sanger sequencing of the PCR products revealed that among the 169 fungal strains tested, around 50% were carrying plant viruses, and many of the strains harbored multiple plant viruses. The plant viruses detected in the fungal isolates were diverse (10 virus species) and not limited to particular virus genera. However, after prolonged maintenance of the fungal culture in the laboratory, many of the fungal strains have lost the virus. Sequencing of the fungal DNA indicated that most of the fungal strains harboring plant viruses were related to plant pathogenic and/or endophytic fungi belonging to the genera Alternaria, Lecanicillium, and Sarocladium. These observations suggest that the nonpersistent acquisition of plant viruses by fungi may commonly occur in nature. Our findings highlight a possible role for fungi in the life cycle, spread, and evolution of plant viruses.

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“…TMV was also shown to replicate in F. graminearum by inoculation through the transfection of fungal protoplasts [ 63 ]. Moreover, C. parasitica , Valsa mali , F. graminearum , and the oomycete Phytoptora infestans can also host plant viroids, the subviral agents [ 64 , 65 ]. Importantly, our study previously discovered a natural infection of cucumber mosaic virus (CMV, genus Cucumovirus ) in Rhizoctonia solani strains isolated from a potato plant [ 66 ].…”

Section: Introductionmentioning

confidence: 99%

Similar Characteristics of siRNAs of Plant Viruses Which Replicate in Plant and Fungal Hosts

Pang

Peng

Bian

et al. 2022

Biology

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RNA silencing is a host innate antiviral mechanism which acts via the synthesis of viral-derived small interfering RNAs (vsiRNAs). We have previously reported the infection of phytopathogenic fungi by plant viruses such as cucumber mosaic virus (CMV) and tobacco mosaic virus (TMV). Furthermore, fungal RNA silencing was shown to suppress plant virus accumulation, but the characteristics of plant vsiRNAs associated with the antiviral response in this nonconventional host remain unknown. Using high-throughput sequencing, we characterized vsiRNA profiles in two plant RNA virus–fungal host pathosystems: CMV infection in phytopathogenic fungus Rhizoctonia solani and TMV infection in phytopathogenic fungus Fusarium graminearum. The relative abundances of CMV and TMV siRNAs in the respective fungal hosts were much lower than those in the respective experimental plant hosts, Nicotiana benthamiana and Nicotiana tabacum. However, CMV and TMV siRNAs in fungi had similar characteristics to those in plants, particularly in their size distributions, proportion of plus and minus senses, and nucleotide preference for the 5′ termini of vsiRNAs. The abundance of TMV siRNAs largely decreased in F. graminearum mutants with a deletion in either dicer-like 1 (dcl1) or dcl2 genes which encode key proteins for the production of siRNAs and antiviral responses. However, deletion of both dcl1 and dcl2 restored TMV siRNA accumulation in F. graminearum, indicating the production of dcl-independent siRNAs with no antiviral function in the absence of the dcl1 and dcl2 genes. Our results suggest that fungal RNA silencing recognizes and processes the invading plant RNA virus genome in a similar way as in plants.

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Transmission of potato spindle tuber viroid between <i>Phytophthora infestans</i> and host plants

Cited by 10 publications

References 46 publications

Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi

Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi

Common but Nonpersistent Acquisitions of Plant Viruses by Plant-Associated Fungi

Similar Characteristics of siRNAs of Plant Viruses Which Replicate in Plant and Fungal Hosts

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