Facilitative and synergistic interactions between fungal and plant viruses
Plants and fungi are closely associated through parasitic or symbiotic relationships in which bidirectional exchanges of cellular contents occur. Recently, a plant virus was shown to be transmitted from a plant to a fungus, but it is unknown whether fungal viruses can also cross host barriers and sp...
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| Vydané v: | Proceedings of the National Academy of Sciences - PNAS Ročník 117; číslo 7; s. 3779 |
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| Hlavní autori: | , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
18.02.2020
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| ISSN: | 1091-6490, 1091-6490 |
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| Abstract | Plants and fungi are closely associated through parasitic or symbiotic relationships in which bidirectional exchanges of cellular contents occur. Recently, a plant virus was shown to be transmitted from a plant to a fungus, but it is unknown whether fungal viruses can also cross host barriers and spread to plants. In this study, we investigated the infectivity of Cryphonectria hypovirus 1 (CHV1, family
), a capsidless, positive-sense (+), single-stranded RNA (ssRNA) fungal virus in a model plant,
CHV1 replicated in mechanically inoculated leaves but did not spread systemically, but coinoculation with an unrelated plant (+)ssRNA virus, tobacco mosaic virus (TMV, family
), or other plant RNA viruses, enabled CHV1 to systemically infect the plant. Likewise, CHV1 systemically infected transgenic plants expressing the TMV movement protein, and coinfection with TMV further enhanced CHV1 accumulation in these plants. Conversely, CHV1 infection increased TMV accumulation when TMV was introduced into a plant pathogenic fungus,
In the in planta
inoculation experiment, we demonstrated that TMV infection of either the plant or the fungus enabled the horizontal transfer of CHV1 from the fungus to the plant, whereas CHV1 infection enhanced fungal acquisition of TMV. Our results demonstrate two-way facilitative interactions between the plant and fungal viruses that promote cross-kingdom virus infections and suggest the presence of plant-fungal-mediated routes for dissemination of fungal and plant viruses in nature. |
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| AbstractList | Plants and fungi are closely associated through parasitic or symbiotic relationships in which bidirectional exchanges of cellular contents occur. Recently, a plant virus was shown to be transmitted from a plant to a fungus, but it is unknown whether fungal viruses can also cross host barriers and spread to plants. In this study, we investigated the infectivity of Cryphonectria hypovirus 1 (CHV1, family
), a capsidless, positive-sense (+), single-stranded RNA (ssRNA) fungal virus in a model plant,
CHV1 replicated in mechanically inoculated leaves but did not spread systemically, but coinoculation with an unrelated plant (+)ssRNA virus, tobacco mosaic virus (TMV, family
), or other plant RNA viruses, enabled CHV1 to systemically infect the plant. Likewise, CHV1 systemically infected transgenic plants expressing the TMV movement protein, and coinfection with TMV further enhanced CHV1 accumulation in these plants. Conversely, CHV1 infection increased TMV accumulation when TMV was introduced into a plant pathogenic fungus,
In the in planta
inoculation experiment, we demonstrated that TMV infection of either the plant or the fungus enabled the horizontal transfer of CHV1 from the fungus to the plant, whereas CHV1 infection enhanced fungal acquisition of TMV. Our results demonstrate two-way facilitative interactions between the plant and fungal viruses that promote cross-kingdom virus infections and suggest the presence of plant-fungal-mediated routes for dissemination of fungal and plant viruses in nature. Plants and fungi are closely associated through parasitic or symbiotic relationships in which bidirectional exchanges of cellular contents occur. Recently, a plant virus was shown to be transmitted from a plant to a fungus, but it is unknown whether fungal viruses can also cross host barriers and spread to plants. In this study, we investigated the infectivity of Cryphonectria hypovirus 1 (CHV1, family Hypoviridae), a capsidless, positive-sense (+), single-stranded RNA (ssRNA) fungal virus in a model plant, Nicotiana tabacum CHV1 replicated in mechanically inoculated leaves but did not spread systemically, but coinoculation with an unrelated plant (+)ssRNA virus, tobacco mosaic virus (TMV, family Virgaviridae), or other plant RNA viruses, enabled CHV1 to systemically infect the plant. Likewise, CHV1 systemically infected transgenic plants expressing the TMV movement protein, and coinfection with TMV further enhanced CHV1 accumulation in these plants. Conversely, CHV1 infection increased TMV accumulation when TMV was introduced into a plant pathogenic fungus, Fusarium graminearum In the in planta F. graminearum inoculation experiment, we demonstrated that TMV infection of either the plant or the fungus enabled the horizontal transfer of CHV1 from the fungus to the plant, whereas CHV1 infection enhanced fungal acquisition of TMV. Our results demonstrate two-way facilitative interactions between the plant and fungal viruses that promote cross-kingdom virus infections and suggest the presence of plant-fungal-mediated routes for dissemination of fungal and plant viruses in nature.Plants and fungi are closely associated through parasitic or symbiotic relationships in which bidirectional exchanges of cellular contents occur. Recently, a plant virus was shown to be transmitted from a plant to a fungus, but it is unknown whether fungal viruses can also cross host barriers and spread to plants. In this study, we investigated the infectivity of Cryphonectria hypovirus 1 (CHV1, family Hypoviridae), a capsidless, positive-sense (+), single-stranded RNA (ssRNA) fungal virus in a model plant, Nicotiana tabacum CHV1 replicated in mechanically inoculated leaves but did not spread systemically, but coinoculation with an unrelated plant (+)ssRNA virus, tobacco mosaic virus (TMV, family Virgaviridae), or other plant RNA viruses, enabled CHV1 to systemically infect the plant. Likewise, CHV1 systemically infected transgenic plants expressing the TMV movement protein, and coinfection with TMV further enhanced CHV1 accumulation in these plants. Conversely, CHV1 infection increased TMV accumulation when TMV was introduced into a plant pathogenic fungus, Fusarium graminearum In the in planta F. graminearum inoculation experiment, we demonstrated that TMV infection of either the plant or the fungus enabled the horizontal transfer of CHV1 from the fungus to the plant, whereas CHV1 infection enhanced fungal acquisition of TMV. Our results demonstrate two-way facilitative interactions between the plant and fungal viruses that promote cross-kingdom virus infections and suggest the presence of plant-fungal-mediated routes for dissemination of fungal and plant viruses in nature. |
| Author | Kondo, Hideki Pang, Tianxing Lian, Ziqian Bian, Ruiling Wei, Shuang Wu, Yunfeng Andika, Ida Bagus Sun, Liying Liu, Xili Niu, Erbo |
| Author_xml | – sequence: 1 givenname: Ruiling surname: Bian fullname: Bian, Ruiling organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, 712100 Yangling, China – sequence: 2 givenname: Ida Bagus surname: Andika fullname: Andika, Ida Bagus organization: College of Plant Health and Medicine, Qingdao Agricultural University, 266109 Qingdao, China – sequence: 3 givenname: Tianxing surname: Pang fullname: Pang, Tianxing organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, 712100 Yangling, China – sequence: 4 givenname: Ziqian surname: Lian fullname: Lian, Ziqian organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, 712100 Yangling, China – sequence: 5 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, 712100 Yangling, China – sequence: 6 givenname: Erbo surname: Niu fullname: Niu, Erbo organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, 712100 Yangling, China – sequence: 7 givenname: Yunfeng surname: Wu fullname: Wu, Yunfeng organization: Key Laboratory of Integrated Pest Management on Crops In Northwestern Loess Plateau, Ministry of Agriculture, Northwest A&F University, 712100 Yangling, China – sequence: 8 givenname: Hideki surname: Kondo fullname: Kondo, Hideki organization: Institute of Plant Science and Resources, Okayama University, 710-0046 Kurashiki, Japan – sequence: 9 givenname: Xili surname: Liu fullname: Liu, Xili organization: State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, 712100 Yangling, China – sequence: 10 givenname: Liying surname: Sun fullname: Sun, Liying email: sunliying@nwafu.edu.cn organization: Key Laboratory of Integrated Pest Management on Crops In Northwestern Loess Plateau, Ministry of Agriculture, Northwest A&F University, 712100 Yangling, China |
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| SubjectTerms | Fungal Viruses - physiology Fusarium - physiology Fusarium - virology Nicotiana - virology Plant Diseases - virology Plant Viruses - physiology Tobacco Mosaic Virus - physiology |
| Title | Facilitative and synergistic interactions between fungal and plant viruses |
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