Replication of single viruses across the kingdoms, Fungi, Plantae, and Animalia

It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously been hypothesized that single members of the family Partitiviridae could cross multiple kingdoms. Partitiviridae accommodates members charac...

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Published inProceedings of the National Academy of Sciences Vol. 121; no. 25; p. e2318150121
Main Authors Telengech, Paul, Hyodo, Kiwamu, Ichikawa, Hiroaki, Kuwata, Ryusei, Kondo, Hideki, Suzuki, Nobuhiro
Format Journal Article
LanguageEnglish
Published United States Proceedings of the National Academy of Sciences 18.06.2024
National Academy of Sciences
Subjects
Animalia
Animals
Biological Sciences
Cell lines
Daucus carota
Daucus carota - microbiology
Daucus carota - virology
Double-stranded RNA
Drosophila melanogaster
Electrophoresis
Flowers & plants
Fungal Viruses - classification
Fungal Viruses - genetics
Fungal Viruses - physiology
Fungi
Host plants
Host preferences
Host range
Insects
Nicotiana - microbiology
Nicotiana - virology
Nicotiana benthamiana
Nicotiana tabacum
Partitiviridae
Phylogeny
Plant Diseases - microbiology
Plant Diseases - virology
Plant viruses
Plantae
Protoplasts
Protoplasts - virology
Replication
RNA Viruses - genetics
RNA Viruses - physiology
Rosellinia necatrix
Spodoptera - microbiology
Spodoptera - virology
Spodoptera frugiperda
Virions
Virus Replication
Animalia
partitivirus
fungal virus
cross-kingdom infection
Plantae
Online AccessGet full text

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Abstract It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously been hypothesized that single members of the family Partitiviridae could cross multiple kingdoms. Partitiviridae accommodates members characterized by their simple bisegmented double-stranded RNA genome; asymptomatic infections of host organisms; the absence of an extracellular route for entry in nature; and collectively broad host range. Herein, we show the replicability of single fungal partitiviruses in three kingdoms of host organisms: Fungi, Plantae, and Animalia. Betapartitiviruses of the phytopathogenic fungus Rosellinia necatrix could replicate in protoplasts of the carrot ( Daucus carota ), Nicotiana benthamiana and Nicotiana tabacum , in some cases reaching a level detectable by agarose gel electrophoresis. Moreover, betapartitiviruses showed more robust replication than the tested alphapartitiviruses. One of the fungal betapartitiviruses, RnPV18, could persistently and stably infect carrot plants regenerated from virion-transfected protoplasts. Both alpha- and betapartitiviruses, although with different host preference, could replicate in two insect cell lines derived from the fall armyworm Spodoptera frugiperda and the fruit fly Drosophila melanogaster . Our results indicate the replicability of single partitiviruses in members of three kingdoms and provide insights into virus adaptation, host jumping, and evolution.
AbstractList Viruses generally have narrow host ranges due to constraints imposed at various steps of infection, and they rarely cross kingdom barriers. We have found that single fungal partitiviruses with a bipartite double-stranded RNA (dsRNA) genome can replicate in tobacco cells transfected with purified particles and systemically infect whole carrot plants regenerated from transfected protoplasts. There are five partitivirus genera based on phylogeny and hosts. Members of Betapartitivirus showed greater replication in plant cells than members of Alphapartitivirus . Both alpha- and beta-partitiviruses were capable of entering spontaneously without any transfection reagent and replicating in two insect cell lines from Spodoptera frugiperda and Drosophila melanogaster . Our results indicate the replicability of single dsRNA viruses in members of three terrestrial kingdoms: Fungi, Plantae, and Animalia. It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously been hypothesized that single members of the family Partitiviridae could cross multiple kingdoms. Partitiviridae accommodates members characterized by their simple bisegmented double-stranded RNA genome; asymptomatic infections of host organisms; the absence of an extracellular route for entry in nature; and collectively broad host range. Herein, we show the replicability of single fungal partitiviruses in three kingdoms of host organisms: Fungi, Plantae, and Animalia. Betapartitiviruses of the phytopathogenic fungus Rosellinia necatrix could replicate in protoplasts of the carrot ( Daucus carota ), Nicotiana benthamiana and Nicotiana tabacum , in some cases reaching a level detectable by agarose gel electrophoresis. Moreover, betapartitiviruses showed more robust replication than the tested alphapartitiviruses. One of the fungal betapartitiviruses, RnPV18, could persistently and stably infect carrot plants regenerated from virion-transfected protoplasts. Both alpha- and betapartitiviruses, although with different host preference, could replicate in two insect cell lines derived from the fall armyworm Spodoptera frugiperda and the fruit fly Drosophila melanogaster . Our results indicate the replicability of single partitiviruses in members of three kingdoms and provide insights into virus adaptation, host jumping, and evolution.
It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously been hypothesized that single members of the family Partitiviridae could cross multiple kingdoms. Partitiviridae accommodates members characterized by their simple bisegmented double-stranded RNA genome; asymptomatic infections of host organisms; the absence of an extracellular route for entry in nature; and collectively broad host range. Herein, we show the replicability of single fungal partitiviruses in three kingdoms of host organisms: Fungi, Plantae, and Animalia. Betapartitiviruses of the phytopathogenic fungusRosellinia necatrix could replicate in protoplasts of the carrot (Daucus carota), Nicotiana benthamiana and Nicotiana tabacum, in some cases reaching a level detectable by agarose gel electrophoresis. Moreover, betapartitiviruses showed more robust replication than the tested alphapartitiviruses. One of the fungal betapartitiviruses, RnPV18, could persistently and stably infect carrot plants regenerated from virion-transfected protoplasts. Both alpha- and betapartitiviruses, although with different host preference, could replicate in two insect cell lines derived from the fall armyworm Spodoptera frugiperda and the fruit fly Drosophila melanogaster. Our results indicate the replicability of single partitiviruses in members of three kingdoms and provide insights into virus adaptation, host jumping, and evolution.It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously been hypothesized that single members of the family Partitiviridae could cross multiple kingdoms. Partitiviridae accommodates members characterized by their simple bisegmented double-stranded RNA genome; asymptomatic infections of host organisms; the absence of an extracellular route for entry in nature; and collectively broad host range. Herein, we show the replicability of single fungal partitiviruses in three kingdoms of host organisms: Fungi, Plantae, and Animalia. Betapartitiviruses of the phytopathogenic fungusRosellinia necatrix could replicate in protoplasts of the carrot (Daucus carota), Nicotiana benthamiana and Nicotiana tabacum, in some cases reaching a level detectable by agarose gel electrophoresis. Moreover, betapartitiviruses showed more robust replication than the tested alphapartitiviruses. One of the fungal betapartitiviruses, RnPV18, could persistently and stably infect carrot plants regenerated from virion-transfected protoplasts. Both alpha- and betapartitiviruses, although with different host preference, could replicate in two insect cell lines derived from the fall armyworm Spodoptera frugiperda and the fruit fly Drosophila melanogaster. Our results indicate the replicability of single partitiviruses in members of three kingdoms and provide insights into virus adaptation, host jumping, and evolution.
It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously been hypothesized that single members of the family Partitiviridae could cross multiple kingdoms. Partitiviridae accommodates members characterized by their simple bisegmented double-stranded RNA genome; asymptomatic infections of host organisms; the absence of an extracellular route for entry in nature; and collectively broad host range. Herein, we show the replicability of single fungal partitiviruses in three kingdoms of host organisms: Fungi, Plantae, and Animalia. Betapartitiviruses of the phytopathogenic fungusRosellinia necatrix could replicate in protoplasts of the carrot (Daucus carota), Nicotiana benthamiana and Nicotiana tabacum, in some cases reaching a level detectable by agarose gel electrophoresis. Moreover, betapartitiviruses showed more robust replication than the tested alphapartitiviruses. One of the fungal betapartitiviruses, RnPV18, could persistently and stably infect carrot plants regenerated from virion-transfected protoplasts. Both alpha- and betapartitiviruses, although with different host preference, could replicate in two insect cell lines derived from the fall armyworm Spodoptera frugiperda and the fruit fly Drosophila melanogaster. Our results indicate the replicability of single partitiviruses in members of three kingdoms and provide insights into virus adaptation, host jumping, and evolution.
It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously been hypothesized that single members of the family Partitiviridae could cross multiple kingdoms. Partitiviridae accommodates members characterized by their simple bisegmented double-stranded RNA genome; asymptomatic infections of host organisms; the absence of an extracellular route for entry in nature; and collectively broad host range. Herein, we show the replicability of single fungal partitiviruses in three kingdoms of host organisms: Fungi, Plantae, and Animalia. Betapartitiviruses of the phytopathogenic fungus Rosellinia necatrix could replicate in protoplasts of the carrot ( Daucus carota ), Nicotiana benthamiana and Nicotiana tabacum , in some cases reaching a level detectable by agarose gel electrophoresis. Moreover, betapartitiviruses showed more robust replication than the tested alphapartitiviruses. One of the fungal betapartitiviruses, RnPV18, could persistently and stably infect carrot plants regenerated from virion-transfected protoplasts. Both alpha- and betapartitiviruses, although with different host preference, could replicate in two insect cell lines derived from the fall armyworm Spodoptera frugiperda and the fruit fly Drosophila melanogaster . Our results indicate the replicability of single partitiviruses in members of three kingdoms and provide insights into virus adaptation, host jumping, and evolution.
It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously been hypothesized that single members of the family could cross multiple kingdoms. accommodates members characterized by their simple bisegmented double-stranded RNA genome; asymptomatic infections of host organisms; the absence of an extracellular route for entry in nature; and collectively broad host range. Herein, we show the replicability of single fungal partitiviruses in three kingdoms of host organisms: Fungi, Plantae, and Animalia. Betapartitiviruses of the phytopathogenic fungus could replicate in protoplasts of the carrot ( ), and , in some cases reaching a level detectable by agarose gel electrophoresis. Moreover, betapartitiviruses showed more robust replication than the tested alphapartitiviruses. One of the fungal betapartitiviruses, RnPV18, could persistently and stably infect carrot plants regenerated from virion-transfected protoplasts. Both alpha- and betapartitiviruses, although with different host preference, could replicate in two insect cell lines derived from the fall armyworm and the fruit fly . Our results indicate the replicability of single partitiviruses in members of three kingdoms and provide insights into virus adaptation, host jumping, and evolution.
Author Ryusei Kuwata
Hideki Kondo
Kiwamu Hyodo
Nobuhiro Suzuki
Paul Telengech
Hiroaki Ichikawa
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Copyright Copyright National Academy of Sciences Jun 18, 2024
Copyright © 2024 the Author(s). Published by PNAS. 2024
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Keywords Animalia
partitivirus
fungal virus
cross-kingdom infection
Plantae
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Snippet It is extremely rare that a single virus crosses host barriers across multiple kingdoms. Based on phylogenetic and paleovirological analyses, it has previously...
Viruses generally have narrow host ranges due to constraints imposed at various steps of infection, and they rarely cross kingdom barriers. We have found that...
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SubjectTerms Animalia
Animals
Biological Sciences
Cell lines
Daucus carota
Daucus carota - microbiology
Daucus carota - virology
Double-stranded RNA
Drosophila melanogaster
Electrophoresis
Flowers & plants
Fungal Viruses - classification
Fungal Viruses - genetics
Fungal Viruses - physiology
Fungi
Host plants
Host preferences
Host range
Insects
Nicotiana - microbiology
Nicotiana - virology
Nicotiana benthamiana
Nicotiana tabacum
Partitiviridae
Phylogeny
Plant Diseases - microbiology
Plant Diseases - virology
Plant viruses
Plantae
Protoplasts
Protoplasts - virology
Replication
RNA Viruses - genetics
RNA Viruses - physiology
Rosellinia necatrix
Spodoptera - microbiology
Spodoptera - virology
Spodoptera frugiperda
Virions
Virus Replication
Title Replication of single viruses across the kingdoms, Fungi, Plantae, and Animalia
URI https://cir.nii.ac.jp/crid/1873962441311655680
https://www.ncbi.nlm.nih.gov/pubmed/38865269
https://www.proquest.com/docview/3072012686
https://www.proquest.com/docview/3067915070
https://pubmed.ncbi.nlm.nih.gov/PMC11194502
Volume 121
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