Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus
We have previously discovered a virus neo-lifestyle exhibited by a capsidless positive-sense (+), single-stranded (ss) RNA virus YkV1 (family Yadokariviridae) and an unrelated double-stranded (ds) RNA virus YnV1 (proposed family "Yadonushiviridae") in a phytopathogenic ascomycete, Rosellin...
| Autores: | , , , , |
|---|---|
| Tipo de recurso: | artículo |
| Estado: | Versión publicada |
| Fecha de publicación: | 2022 |
| País: | España |
| Institución: | Consejo Superior de Investigaciones Científicas (CSIC) |
| Repositorio: | DIGITAL.CSIC. Repositorio Institucional del CSIC |
| OAI Identifier: | oai:digital.csic.es:10261/305771 |
| Acceso en línea: | http://hdl.handle.net/10261/305771 https://api.elsevier.com/content/abstract/scopus_id/85140856953 |
| Access Level: | acceso abierto |
| Palabra clave: | Virus-virus interaction RNA viruses Capsidless Fungal viruses Multilayered interaction Mutualism and parasitism Plant-pathogenic fungi Virus macroevolution |
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Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus |
| title |
Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus |
| spellingShingle |
Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus Sato, Yukiyo Virus-virus interaction RNA viruses Capsidless Fungal viruses Multilayered interaction Mutualism and parasitism Plant-pathogenic fungi Virus macroevolution |
| title_short |
Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus |
| title_full |
Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus |
| title_fullStr |
Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus |
| title_full_unstemmed |
Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus |
| title_sort |
Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a Fungus |
| dc.creator.none.fl_str_mv |
Sato, Yukiyo Hisano, Sakae López Herrera, Carlos Kondo, Hideki Suzuki, Nobuhiro |
| author |
Sato, Yukiyo |
| author_facet |
Sato, Yukiyo Hisano, Sakae López Herrera, Carlos Kondo, Hideki Suzuki, Nobuhiro |
| author_role |
author |
| author2 |
Hisano, Sakae López Herrera, Carlos Kondo, Hideki Suzuki, Nobuhiro |
| author2_role |
author author author author |
| dc.contributor.none.fl_str_mv |
Yomogi Japan Society for the Promotion of Science Ministry of Education, Culture, Sports, Science and Technology (Japan) Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72] |
| dc.subject.none.fl_str_mv |
Virus-virus interaction RNA viruses Capsidless Fungal viruses Multilayered interaction Mutualism and parasitism Plant-pathogenic fungi Virus macroevolution |
| topic |
Virus-virus interaction RNA viruses Capsidless Fungal viruses Multilayered interaction Mutualism and parasitism Plant-pathogenic fungi Virus macroevolution |
| description |
We have previously discovered a virus neo-lifestyle exhibited by a capsidless positive-sense (+), single-stranded (ss) RNA virus YkV1 (family Yadokariviridae) and an unrelated double-stranded (ds) RNA virus YnV1 (proposed family "Yadonushiviridae") in a phytopathogenic ascomycete, Rosellinia necatrix. YkV1 has been proposed to replicate in the capsid provided by YnV1 as if it were a dsRNA virus and enhance YnV1 replication in return. Recently, viruses related to YkV1 (yadokariviruses) have been isolated from diverse ascomycetous fungi. However, it remains obscure whether such viruses generally show the YkV1-like lifestyle. Here, we identified partner viruses for three distinct yadokariviruses, YkV3, YkV4a, and YkV4b, isolated from R. necatrix that were coinfected with multiple dsRNA viruses phylogenetically distantly related to YnV1. We first established transformants of R. necatrix carrying single yadokarivirus cDNAs and fused them with infectants by single partner candidate dsRNA viruses. Consequently, YkV3 and YkV4s replicated only in the presence of RnMBV3 (family Megabirnaviridae) and RnMTV1 (proposed family "Megatotiviridae"), respectively. The partners were mutually interchangeable between the two YkV4 strains and three RnMTV1 strains but not between other combinations involving YkV1 or YkV3. In contrast to YkV1 enhancing YnV1 accumulation, YkV4s reduced RnMTV1 accumulation to different degrees according to strains. Interestingly, YkV4 rescued the host R. necatrix from impaired growth induced by RnMTV1. YkV3 exerted no apparent effect on its partner (RnMBV3) or host fungus. Overall, we revealed that while yadokariviruses generally require partner dsRNA viruses for replication, each yadokarivirus partners with a different dsRNA virus species in the three diverse families and shows a distinct symbiotic relation in a fungus. IMPORTANCE A capsidless (+)ssRNA virus YkV1 (family Yadokariviridae) highjacks the capsid of an unrelated dsRNA virus YnV1 (proposed family "Yadonushiviridae") in a phytopathogenic ascomycete, while YkV1 trans-enhances YnV1 replication. Herein, we identified the dsRNA virus partners of three yadokariviruses (YkV3, YkV4a, and YkV4b) with genome organization different from YkV1 as being different from YnV1 at the suborder level. Their partners were mutually interchangeable between the two YkV4 strains and three strains of the partner virus RnMTV1 (proposed family "Megatotiviridae") but not between other combinations involving YkV1 or YkV3. Unlike YkV1, YkV4s reduced RnMTV1 accumulation and rescued the host fungus from impaired growth induced by RnMTV1. YkV3 exerted no apparent effect on its partner (RnMBV3, family Megabirnaviridae) or host fungus. These revealed that while each yadokarivirus has a species-specific partnership with a dsRNA virus, yadokariviruses collectively partner extremely diverse dsRNA viruses and show three-layered complex mutualistic/antagonistic interactions in a fungus. |
| publishDate |
2022 |
| dc.date.none.fl_str_mv |
2022 2023 2023 |
| dc.type.none.fl_str_mv |
info:eu-repo/semantics/article http://purl.org/coar/resource_type/c_6501 Publisher's version info:eu-repo/semantics/publishedVersion |
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article |
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publishedVersion |
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http://hdl.handle.net/10261/305771 https://api.elsevier.com/content/abstract/scopus_id/85140856953 |
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http://hdl.handle.net/10261/305771 https://api.elsevier.com/content/abstract/scopus_id/85140856953 |
| dc.language.none.fl_str_mv |
Inglés |
| language_invalid_str_mv |
Inglés |
| dc.relation.none.fl_str_mv |
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1128/mbio.01685-22 https://doi.org/10.1128/mbio.01685-22 Sí |
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info:eu-repo/semantics/openAccess |
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openAccess |
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application/pdf |
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American Society for Microbiology |
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American Society for Microbiology |
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reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC instname:Consejo Superior de Investigaciones Científicas (CSIC) |
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Consejo Superior de Investigaciones Científicas (CSIC) |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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1869425105998708736 |
| spelling |
Three-Layered Complex Interactions among Capsidless (+)ssRNA Yadokariviruses, dsRNA Viruses, and a FungusSato, YukiyoHisano, SakaeLópez Herrera, CarlosKondo, HidekiSuzuki, NobuhiroVirus-virus interactionRNA virusesCapsidlessFungal virusesMultilayered interactionMutualism and parasitismPlant-pathogenic fungiVirus macroevolutionWe have previously discovered a virus neo-lifestyle exhibited by a capsidless positive-sense (+), single-stranded (ss) RNA virus YkV1 (family Yadokariviridae) and an unrelated double-stranded (ds) RNA virus YnV1 (proposed family "Yadonushiviridae") in a phytopathogenic ascomycete, Rosellinia necatrix. YkV1 has been proposed to replicate in the capsid provided by YnV1 as if it were a dsRNA virus and enhance YnV1 replication in return. Recently, viruses related to YkV1 (yadokariviruses) have been isolated from diverse ascomycetous fungi. However, it remains obscure whether such viruses generally show the YkV1-like lifestyle. Here, we identified partner viruses for three distinct yadokariviruses, YkV3, YkV4a, and YkV4b, isolated from R. necatrix that were coinfected with multiple dsRNA viruses phylogenetically distantly related to YnV1. We first established transformants of R. necatrix carrying single yadokarivirus cDNAs and fused them with infectants by single partner candidate dsRNA viruses. Consequently, YkV3 and YkV4s replicated only in the presence of RnMBV3 (family Megabirnaviridae) and RnMTV1 (proposed family "Megatotiviridae"), respectively. The partners were mutually interchangeable between the two YkV4 strains and three RnMTV1 strains but not between other combinations involving YkV1 or YkV3. In contrast to YkV1 enhancing YnV1 accumulation, YkV4s reduced RnMTV1 accumulation to different degrees according to strains. Interestingly, YkV4 rescued the host R. necatrix from impaired growth induced by RnMTV1. YkV3 exerted no apparent effect on its partner (RnMBV3) or host fungus. Overall, we revealed that while yadokariviruses generally require partner dsRNA viruses for replication, each yadokarivirus partners with a different dsRNA virus species in the three diverse families and shows a distinct symbiotic relation in a fungus. IMPORTANCE A capsidless (+)ssRNA virus YkV1 (family Yadokariviridae) highjacks the capsid of an unrelated dsRNA virus YnV1 (proposed family "Yadonushiviridae") in a phytopathogenic ascomycete, while YkV1 trans-enhances YnV1 replication. Herein, we identified the dsRNA virus partners of three yadokariviruses (YkV3, YkV4a, and YkV4b) with genome organization different from YkV1 as being different from YnV1 at the suborder level. Their partners were mutually interchangeable between the two YkV4 strains and three strains of the partner virus RnMTV1 (proposed family "Megatotiviridae") but not between other combinations involving YkV1 or YkV3. Unlike YkV1, YkV4s reduced RnMTV1 accumulation and rescued the host fungus from impaired growth induced by RnMTV1. YkV3 exerted no apparent effect on its partner (RnMBV3, family Megabirnaviridae) or host fungus. These revealed that while each yadokarivirus has a species-specific partnership with a dsRNA virus, yadokariviruses collectively partner extremely diverse dsRNA viruses and show three-layered complex mutualistic/antagonistic interactions in a fungus.This study was supported in part by Yomogi Inc. (to N.S.) and Grants-in-Aid for Scientific Research (S), Research on Innovative Areas, and Grants-in-Aid for JSPS fellows from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (MEXT) (KAKENHI 21H05035, 21K18222, 16H06436, 16H06429, and 16K21723 to N.S. and H.K.; and 19J00261 to Y.S.).Peer reviewedAmerican Society for MicrobiologyYomogiJapan Society for the Promotion of ScienceMinistry of Education, Culture, Sports, Science and Technology (Japan)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202320232022info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/305771https://api.elsevier.com/content/abstract/scopus_id/85140856953reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésThe underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1128/mbio.01685-22https://doi.org/10.1128/mbio.01685-22Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3057712026-05-22T06:33:51Z |
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15.812429 |