A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus Colletotrichum

ABSTRACTColletotrichum spp. are economically important phytopathogenic fungi that cause anthracnose in a variety of plant species worldwide. Hypovirulence-associated mycoviruses provide new options for the biological control of plant fungal diseases. Here, we found a novel partitivirus from Colletot...

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Main Authors: Jun Zi Zhu, Ze Lan Qiu, Bi Da Gao, Xiao Gang Li, Jie Zhong
Format: Article
Language:English
Published: American Society for Microbiology 2024-02-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mbio.02530-23
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author Jun Zi Zhu
Ze Lan Qiu
Bi Da Gao
Xiao Gang Li
Jie Zhong
author_facet Jun Zi Zhu
Ze Lan Qiu
Bi Da Gao
Xiao Gang Li
Jie Zhong
author_sort Jun Zi Zhu
collection DOAJ
description ABSTRACTColletotrichum spp. are economically important phytopathogenic fungi that cause anthracnose in a variety of plant species worldwide. Hypovirulence-associated mycoviruses provide new options for the biological control of plant fungal diseases. Here, we found a novel partitivirus from Colletotrichum alienum and named it Colletotrichum alienum partitivirus 1 (CaPV1). CaPV1 contained two dsRNA segments encoding an RNA-dependent RNA polymerase and a capsid protein and was classified under the genus Gammapartitivirus of the family Partitiviridae. CaPV1 significantly decreased host virulence, mycelial growth, appressorial development, and appressorium turgor but increased conidial production with abnormal morphology. In addition, CaPV1 could be successfully transfected into other Colletotrichum species, including C. fructicola, C. spaethianum, and C. gloeosporioides, and caused hypovirulence, indicating the broad application potential of this virus. CaPV1 caused significant transcriptional rewiring of the host fungus C. alienum. Notably, some genes related to vesicle transport in the CaPV1-infected strain were downregulated, consistent with the impaired endocytosis pathway in this fungus. When the Rab gene CaRab7, which is associated with endocytosis in vesicle transport, was knocked out, the virulence of the mutants was reduced. Overall, our findings demonstrated that CaPV1 has the potential to control anthracnose caused by Colletotrichum, and the mechanism by which Colletotrichum induces hypovirulence is caused by affecting vesicle transport.IMPORTANCEColletotrichum is a kind of economically important phytopathogenic fungi that cause anthracnose disease in a variety of plant species worldwide. We found a novel mycovirus of the Gammapartitivirus genus and Partitiviridae family from the phytopathogenic fungus Colletotrichum alienum and named it CaPV1. This study revealed that CaPV1 infection significantly decreased host virulence and fitness by affecting mycelial growth, appressorial development, and appressorium turgor. In addition, CaPV1 could also infect other Colletotrichum species, including C. fructicola, C. spaethianum, and C. gloeosporioides, by viral particle transfection and resulting in hypovirulence of these Colletotrichum species. Transcriptomic analysis showed that CaPV1 caused significant transcriptional rewiring of the host fungus C. alienum, especially the genes involved in vesicle transport. Moreover, endocytosis and gene knockout assays demonstrated that the mechanism underlying CaPV1-induced hypovirulence is, at least in part, caused by affecting the vesicle transport of the host fungus. This study provided insights into the mechanisms underlying the pathogenesis of Colletotrichum species and mycovirus-fungus interactions, linking the role of mycovirus and fungus vesicle transport systems in shaping fungal pathogenicity.
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spelling doaj.art-b1c56d28f74a416aa19fe1531e9082c72024-02-14T14:00:56ZengAmerican Society for MicrobiologymBio2150-75112024-02-0115210.1128/mbio.02530-23A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus ColletotrichumJun Zi Zhu0Ze Lan Qiu1Bi Da Gao2Xiao Gang Li3Jie Zhong4Hunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, Hunan Agricultural University, Changsha, Hunan, ChinaHunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, Hunan Agricultural University, Changsha, Hunan, ChinaHunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, Hunan Agricultural University, Changsha, Hunan, ChinaHunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, Hunan Agricultural University, Changsha, Hunan, ChinaHunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, Hunan Agricultural University, Changsha, Hunan, ChinaABSTRACTColletotrichum spp. are economically important phytopathogenic fungi that cause anthracnose in a variety of plant species worldwide. Hypovirulence-associated mycoviruses provide new options for the biological control of plant fungal diseases. Here, we found a novel partitivirus from Colletotrichum alienum and named it Colletotrichum alienum partitivirus 1 (CaPV1). CaPV1 contained two dsRNA segments encoding an RNA-dependent RNA polymerase and a capsid protein and was classified under the genus Gammapartitivirus of the family Partitiviridae. CaPV1 significantly decreased host virulence, mycelial growth, appressorial development, and appressorium turgor but increased conidial production with abnormal morphology. In addition, CaPV1 could be successfully transfected into other Colletotrichum species, including C. fructicola, C. spaethianum, and C. gloeosporioides, and caused hypovirulence, indicating the broad application potential of this virus. CaPV1 caused significant transcriptional rewiring of the host fungus C. alienum. Notably, some genes related to vesicle transport in the CaPV1-infected strain were downregulated, consistent with the impaired endocytosis pathway in this fungus. When the Rab gene CaRab7, which is associated with endocytosis in vesicle transport, was knocked out, the virulence of the mutants was reduced. Overall, our findings demonstrated that CaPV1 has the potential to control anthracnose caused by Colletotrichum, and the mechanism by which Colletotrichum induces hypovirulence is caused by affecting vesicle transport.IMPORTANCEColletotrichum is a kind of economically important phytopathogenic fungi that cause anthracnose disease in a variety of plant species worldwide. We found a novel mycovirus of the Gammapartitivirus genus and Partitiviridae family from the phytopathogenic fungus Colletotrichum alienum and named it CaPV1. This study revealed that CaPV1 infection significantly decreased host virulence and fitness by affecting mycelial growth, appressorial development, and appressorium turgor. In addition, CaPV1 could also infect other Colletotrichum species, including C. fructicola, C. spaethianum, and C. gloeosporioides, by viral particle transfection and resulting in hypovirulence of these Colletotrichum species. Transcriptomic analysis showed that CaPV1 caused significant transcriptional rewiring of the host fungus C. alienum, especially the genes involved in vesicle transport. Moreover, endocytosis and gene knockout assays demonstrated that the mechanism underlying CaPV1-induced hypovirulence is, at least in part, caused by affecting the vesicle transport of the host fungus. This study provided insights into the mechanisms underlying the pathogenesis of Colletotrichum species and mycovirus-fungus interactions, linking the role of mycovirus and fungus vesicle transport systems in shaping fungal pathogenicity.https://journals.asm.org/doi/10.1128/mbio.02530-23mycovirushypovirulenceColletotrichum speciesPartitivirusendocytosis
spellingShingle Jun Zi Zhu
Ze Lan Qiu
Bi Da Gao
Xiao Gang Li
Jie Zhong
A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus Colletotrichum
mBio
mycovirus
hypovirulence
Colletotrichum species
Partitivirus
endocytosis
title A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus Colletotrichum
title_full A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus Colletotrichum
title_fullStr A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus Colletotrichum
title_full_unstemmed A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus Colletotrichum
title_short A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus Colletotrichum
title_sort novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus colletotrichum
topic mycovirus
hypovirulence
Colletotrichum species
Partitivirus
endocytosis
url https://journals.asm.org/doi/10.1128/mbio.02530-23
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