Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection

Andika, Ida Bagus; Wei, Shuang; ChunMei, Cao; Salaipeth, Lakha; Kondō, Hideki; Sun, Liying

doi:10.1073/pnas.1714916114

Cited by 129 publications

(110 citation statements)

References 64 publications

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“…Indeed, there are a number of examples of the successful or promising use of mycoviruses to control fungal diseases (37)(38)(39). Interestingly, a number of studies have recently demonstrated that phytopathogenic fungi could be a suitable host of some plant viruses (40)(41)(42), which extends the previously known compatibility of plant viruses and yeast (S. cerevisiae) as hosts (43,44). Conversely, mycoviruses originating from marine fungi (Penicillium aurantiogriseum var.…”

Section: Significancementioning

confidence: 96%

“…The finding that plant viroids can infect phytopathogenic fungi raises the question of whether viroids could be horizontally transferred from the plant to fungus during colonization of plant tissue by the fungal pathogens. In fact, under laboratory conditions, we have previously demonstrated the transfer of a plant RNA virus from the plant to fungus, an event that possibly occurs in natural settings (42). To explore this possibility, we inoculated viroid-free wild-type and Δdcl2 mutant strains of F. graminearum to HSVd-infected N. benthamiana plants.…”

Section: Viroids Could Be Bidirectionally Transferred Between Plants Andmentioning

confidence: 99%

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Symptomatic plant viroid infections in phytopathogenic fungi

Wei

Bian

Andika

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Viroids are pathogenic agents that have a small, circular noncoding RNA genome. They have been found only in plant species; therefore, their infectivity and pathogenicity in other organisms remain largely unexplored. In this study, we investigate whether plant viroids can replicate and induce symptoms in filamentous fungi. Seven plant viroids representing viroid groups that replicate in either the nucleus or chloroplast of plant cells were inoculated to three plant pathogenic fungi, Cryphonectria parasitica, Valsa mali, and Fusarium graminearum. By transfection of fungal spheroplasts with viroid RNA transcripts, each of the three, hop stunt viroid (HSVd), iresine 1 viroid, and avocado sunblotch viroid, can stably replicate in at least one of those fungi. The viroids are horizontally transmitted through hyphal anastomosis and vertically through conidia. HSVd infection severely debilitates the growth of V. mali but not that of the other two fungi, while in F. graminearum and C. parasitica, with deletion of dicer-like genes, the primary components of the RNA-silencing pathway, HSVd accumulation increases. We further demonstrate that HSVd can be bidirectionally transferred between F. graminearum and plants during infection. The viroids also efficiently infect fungi and induce disease symptoms when the viroid RNAs are exogenously applied to the fungal mycelia. These findings enhance our understanding of viroid replication, host range, and pathogenicity, and of their potential spread to other organisms in nature.plant viroid | fungus | transmission | pathogenicity V iroids are infectious pathogenic agents possessing small, nonencapsidated, circular single-stranded RNAs that, to date, have been found to naturally infect only plants (1, 2). Viroids infect a wide variety of higher plant species, causing devastating diseases in many crops, particularly vegetables, fruits, and ornamental plants (3). In crop plants, viroids are known to spread by vegetative propagation; by mechanical agricultural practices; and, in certain cases, through seeds, pollen, and insect transmission (3, 4). As viroids do not encode any proteins and do not require a helper agent for their multiplication and survival, the biological activities of viroids are entirely dependent on direct interactions of their RNA genome or its derivatives with cellular host components (5-9). Viroid replication or processing of its RNAs in the yeast, Saccharomyces cerevisiae, and cyanobacterium, Nostoc (Nostocales), have been demonstrated (10-12).Currently, at least 34 viroid species have been identified and are classified into two families, Avsunviroidae and Pospiviroidae (13-15). The members of Avsunviroidae (type species: Avocado sunblotch viroid) replicate in the chloroplasts or plastids through symmetric rolling-circle replication using the host nuclear-encoded polymerase. Their RNAs form highly branched secondary structures and have ribozyme activities. Members of Pospiviroidae (type species: Potato spindle tuber viroid) replicate and accumulate in the nucleus th...

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Section: Significancementioning

confidence: 96%

Section: Viroids Could Be Bidirectionally Transferred Between Plants Andmentioning

confidence: 99%

Symptomatic plant viroid infections in phytopathogenic fungi

Wei

Bian

Andika

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…Valsa mali but not C. parasitica , and F. graminearum [59] . Due to the close contact between phytopathogenic fungi and plants a change in host range of a tobamo-like virus is plausible.…”

Section: Acidomyces Richmondensis Tobamo-like Virus 1 (Artlv1)mentioning

confidence: 84%

Discovery of new mycoviral genomes within publicly available fungal transcriptomic datasets

Gilbert

Holcomb

Allscheid

et al. 2019

Preprint

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The distribution and diversity of RNA viruses in fungi is incompletely understood due to the often cryptic nature of mycoviral infections and the focused study of primarily pathogenic and/or economically important fungi. As most viruses that are known to infect fungi possess either single-stranded or double-stranded RNA genomes, transcriptomic data provides the opportunity to query for viruses in diverse fungal samples without any a priori knowledge of virus infection.Here we describe a systematic survey of all transcriptomic datasets from fungi belonging to the subphylum Pezizomycotina. Using a simple but effective computational pipeline that uses reads discarded during normal RNA-seq analyses, followed by identification of a viral RNA-dependent RNA polymerase (RdRP) motif in de novo assembled contigs, 59 viruses from 44 different fungi were identified. Among the viruses identified, 89% were determined to be new species and 68% are, to our knowledge, the first virus described from the fungal species. Comprehensive analyses of both nucleotide and inferred protein sequences characterize the phylogenetic relationships between these viruses and the known set of mycoviral sequences and support the classification of up to four new families and two new genera. Thus the results provide a deeper understanding of the scope of mycoviral diversity while also increasing the distribution of fungal hosts. Further, this study demonstrates the suitability of analyzing RNA-seq data to facilitate rapid discovery of new viruses.

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“…Uromyces potyvirus A and Zymoseptoria comovirus A showed strong similarity to other viruses from plants, indicating that both fungi transmit plant viruses that infect both fungi and plants. Fungal transmission of a plant virus has been reported (41). Moreover, plants are known hosts for viruses in the family Virgaviridae , which were also identified in fungi, suggesting that fungi could be alternative hosts.…”

Section: Discussionmentioning

confidence: 99%

Identification of viruses from fungal transcriptomes

Choi

Chu

et al. 2020

Preprint

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Viruses infecting fungi are referred to as mycoviruses. Here, we carried out in silico mycovirome studies using public fungal transcriptomes. We identified 468 virus-associated contigs assigned to five orders, 21 families, 26 genera, and 88 species. We assembled 120 viral genomes with diverse RNA and DNA genomes. The phylogenetic tree and genome organization unveiled the possible host origin of mycovirus species and diversity of their genome structures. Most identified mycoviruses were originated from fungi; however, some mycoviruses had strong phylogenetic relationships with those from insects and plants. The viral abundance and mutation frequency of mycoviruses were very low; however, the compositions and populations of mycoviruses were very complex. Although coinfection of diverse mycoviruses in the fungi was common in our study, most mycoviromes had a dominant virus species. The compositions and populations of mycoviruses were more complex than we expected. Monilinia viromes revealed that there were strong deviations in the composition of viruses and viral abundance among samples. Gigaspora viromes showed that the chemical strigolactone might promote virus replication and mutations, while symbiosis with endobacteria might suppress virus replication and mutations. This study revealed the diversity and host distribution of mycoviruses.

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Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection

Cited by 129 publications

References 64 publications

Symptomatic plant viroid infections in phytopathogenic fungi

Symptomatic plant viroid infections in phytopathogenic fungi

Discovery of new mycoviral genomes within publicly available fungal transcriptomic datasets

Identification of viruses from fungal transcriptomes

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