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

The transmission of viral infections between plant and fungal hosts has been suspected to occur, based on phylogenetic and other findings, but has not been directly observed in nature. Here, we report the discovery of a natural infection of the phytopathogenic fungus Rhizoctonia solani by a plant vi...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 114; no. 46; pp. 12267 - 12272
Main Authors Andika, Ida Bagus, Wei, Shuang, Cao, Chunmei, Salaipeth, Lakha, Kondo, Hideki, Sun, Liying
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 14.11.2017
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Abstract The transmission of viral infections between plant and fungal hosts has been suspected to occur, based on phylogenetic and other findings, but has not been directly observed in nature. Here, we report the discovery of a natural infection of the phytopathogenic fungus Rhizoctonia solani by a plant virus, cucumber mosaic virus (CMV). The CMV-infected R. solani strain was obtained from a potato plant growing in Inner Mongolia Province of China, and CMV infection was stable when this fungal strain was cultured in the laboratory. CMV was horizontally transmitted through hyphal anastomosis but not vertically through basidiospores. By inoculation via protoplast transfection with virions, a reference isolate of CMV replicated in R. solani and another phytopathogenic fungus, suggesting that some fungi can serve as alternative hosts to CMV. Importantly, in fungal inoculation experiments under laboratory conditions, R. solani could acquire CMV from an infected plant, as well as transmit the virus to an uninfected plant. This study presents evidence of the transfer of a virus between plant and fungus, and it further expands our understanding of plant–fungus interactions and the spread of plant viruses.
AbstractList Virus cross-infection is an important topic in understanding the course of virus dissemination and evolution. Viruses may spread between the same host species or into taxonomically distinct organisms. The occurrences of cross-kingdom viral infection for certain virus groups are suggested by the current virus taxonomic data. In particular, several plants and fungal viruses show close phylogenetic relationships, but productive transmission of virus between plant and fungal hosts in nature has not been directly demonstrated. Here, we describe the natural infection of Rhizoctonia solani fungus by a plant virus, cucumber mosaic virus (CMV). We further demonstrate that R. solani can acquire and transmit CMV during plant infection. Our findings are evidence of cross-kingdom virus transmission from the plant to fungus. The transmission of viral infections between plant and fungal hosts has been suspected to occur, based on phylogenetic and other findings, but has not been directly observed in nature. Here, we report the discovery of a natural infection of the phytopathogenic fungus Rhizoctonia solani by a plant virus, cucumber mosaic virus (CMV). The CMV-infected R. solani strain was obtained from a potato plant growing in Inner Mongolia Province of China, and CMV infection was stable when this fungal strain was cultured in the laboratory. CMV was horizontally transmitted through hyphal anastomosis but not vertically through basidiospores. By inoculation via protoplast transfection with virions, a reference isolate of CMV replicated in R. solani and another phytopathogenic fungus, suggesting that some fungi can serve as alternative hosts to CMV. Importantly, in fungal inoculation experiments under laboratory conditions, R. solani could acquire CMV from an infected plant, as well as transmit the virus to an uninfected plant. This study presents evidence of the transfer of a virus between plant and fungus, and it further expands our understanding of plant–fungus interactions and the spread of plant viruses.
The transmission of viral infections between plant and fungal hosts has been suspected to occur, based on phylogenetic and other findings, but has not been directly observed in nature. Here, we report the discovery of a natural infection of the phytopathogenic fungus Rhizoctonia solani by a plant virus, cucumber mosaic virus (CMV). The CMV-infected R. solani strain was obtained from a potato plant growing in Inner Mongolia Province of China, and CMV infection was stable when this fungal strain was cultured in the laboratory. CMV was horizontally transmitted through hyphal anastomosis but not vertically through basidiospores. By inoculation via protoplast transfection with virions, a reference isolate of CMV replicated in R. solani and another phytopathogenic fungus, suggesting that some fungi can serve as alternative hosts to CMV. Importantly, in fungal inoculation experiments under laboratory conditions, R. solani could acquire CMV from an infected plant, as well as transmit the virus to an uninfected plant. This study presents evidence of the transfer of a virus between plant and fungus, and it further expands our understanding of plant-fungus interactions and the spread of plant viruses.
The transmission of viral infections between plant and fungal hosts has been suspected to occur, based on phylogenetic and other findings, but has not been directly observed in nature. Here, we report the discovery of a natural infection of the phytopathogenic fungus by a plant virus, cucumber mosaic virus (CMV). The CMV-infected strain was obtained from a potato plant growing in Inner Mongolia Province of China, and CMV infection was stable when this fungal strain was cultured in the laboratory. CMV was horizontally transmitted through hyphal anastomosis but not vertically through basidiospores. By inoculation via protoplast transfection with virions, a reference isolate of CMV replicated in and another phytopathogenic fungus, suggesting that some fungi can serve as alternative hosts to CMV. Importantly, in fungal inoculation experiments under laboratory conditions, could acquire CMV from an infected plant, as well as transmit the virus to an uninfected plant. This study presents evidence of the transfer of a virus between plant and fungus, and it further expands our understanding of plant-fungus interactions and the spread of plant viruses.
Significance Virus cross-infection is an important topic in understanding the course of virus dissemination and evolution. Viruses may spread between the same host species or into taxonomically distinct organisms. The occurrences of cross-kingdom viral infection for certain virus groups are suggested by the current virus taxonomic data. In particular, several plants and fungal viruses show close phylogenetic relationships, but productive transmission of virus between plant and fungal hosts in nature has not been directly demonstrated. Here, we describe the natural infection of Rhizoctonia solani fungus by a plant virus, cucumber mosaic virus (CMV). We further demonstrate that R. solani can acquire and transmit CMV during plant infection. Our findings are evidence of cross-kingdom virus transmission from the plant to fungus. The transmission of viral infections between plant and fungal hosts has been suspected to occur, based on phylogenetic and other findings, but has not been directly observed in nature. Here, we report the discovery of a natural infection of the phytopathogenic fungus Rhizoctonia solani by a plant virus, cucumber mosaic virus (CMV). The CMV-infected R. solani strain was obtained from a potato plant growing in Inner Mongolia Province of China, and CMV infection was stable when this fungal strain was cultured in the laboratory. CMV was horizontally transmitted through hyphal anastomosis but not vertically through basidiospores. By inoculation via protoplast transfection with virions, a reference isolate of CMV replicated in R. solani and another phytopathogenic fungus, suggesting that some fungi can serve as alternative hosts to CMV. Importantly, in fungal inoculation experiments under laboratory conditions, R. solani could acquire CMV from an infected plant, as well as transmit the virus to an uninfected plant. This study presents evidence of the transfer of a virus between plant and fungus, and it further expands our understanding of plant–fungus interactions and the spread of plant viruses.
Author Kondo, Hideki
Wei, Shuang
Cao, Chunmei
Salaipeth, Lakha
Andika, Ida Bagus
Sun, Liying
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  organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China
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  givenname: Shuang
  surname: Wei
  fullname: Wei, Shuang
  organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China
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  givenname: Chunmei
  surname: Cao
  fullname: Cao, Chunmei
  organization: Potato Research Center, Inner Mongolia Academy of Agricultural & Animal Husbandry Sciences, Hohhot, China
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  givenname: Lakha
  surname: Salaipeth
  fullname: Salaipeth, Lakha
  organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China
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  organization: Institute of Plant Science and Resources, Okayama University, Kurashiki, 710-0046, Japan
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  givenname: Liying
  surname: Sun
  fullname: Sun, Liying
  organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China
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Edited by James L. Van Etten, University of Nebraska–Lincoln, Lincoln, NE, and approved October 6, 2017 (received for review August 23, 2017)
Author contributions: I.B.A. and L. Sun designed research; I.B.A., S.W., C.C., L. Salaipeth, and L. Sun performed research; I.B.A., H.K., and L. Sun analyzed data; and I.B.A., H.K., and L. Sun wrote the paper.
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Snippet The transmission of viral infections between plant and fungal hosts has been suspected to occur, based on phylogenetic and other findings, but has not been...
Significance Virus cross-infection is an important topic in understanding the course of virus dissemination and evolution. Viruses may spread between the same...
Virus cross-infection is an important topic in understanding the course of virus dissemination and evolution. Viruses may spread between the same host species...
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SubjectTerms Anastomosis
Basidiospores
Biological Sciences
Fungi
Infections
Inoculation
Pathogens
Phylogeny
Phytopathogenic fungi
Plant diseases
Plant viruses
Potatoes
Transfection
Viral infections
Virions
Viruses
Subtitle A naturally occurring cross-kingdom viral infection
Title Phytopathogenic fungus hosts a plant virus
URI https://www.jstor.org/stable/26486561
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Volume 114
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