Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission
Abstract Non-self recognition is a fundamental aspect of life, serving as a crucial mechanism for mitigating proliferation of molecular parasites within fungal populations. However, studies investigating the potential interference of plants with fungal non-self recognition mechanisms are limited. He...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-06-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-49110-6 |
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| author | Du Hai Jincang Li Daohong Jiang Jiasen Cheng Yanping Fu Xueqiong Xiao Huanran Yin Yang Lin Tao Chen Bo Li Xiao Yu Qing Cai Wei Chen Ioly Kotta-Loizou Jiatao Xie |
| author_facet | Du Hai Jincang Li Daohong Jiang Jiasen Cheng Yanping Fu Xueqiong Xiao Huanran Yin Yang Lin Tao Chen Bo Li Xiao Yu Qing Cai Wei Chen Ioly Kotta-Loizou Jiatao Xie |
| author_sort | Du Hai |
| collection | DOAJ |
| description | Abstract Non-self recognition is a fundamental aspect of life, serving as a crucial mechanism for mitigating proliferation of molecular parasites within fungal populations. However, studies investigating the potential interference of plants with fungal non-self recognition mechanisms are limited. Here, we demonstrate a pronounced increase in the efficiency of horizontal mycovirus transmission between vegetatively incompatible Sclerotinia sclerotiorum strains in planta as compared to in vitro. This increased efficiency is associated with elevated proline concentration in plants following S. sclerotiorum infection. This surge in proline levels attenuates the non-self recognition reaction among fungi by inhibition of cell death, thereby facilitating mycovirus transmission. Furthermore, our field experiments reveal that the combined deployment of hypovirulent S. sclerotiorum strains harboring hypovirulence-associated mycoviruses (HAVs) together with exogenous proline confers substantial protection to oilseed rape plants against virulent S. sclerotiorum. This unprecedented discovery illuminates a novel pathway by which plants can counteract S. sclerotiorum infection, leveraging the weakening of fungal non-self recognition and promotion of HAVs spread. These promising insights provide an avenue to explore for developing innovative biological control strategies aimed at mitigating fungal diseases in plants by enhancing the efficacy of horizontal HAV transmission. |
| format | Article |
| id | doaj-art-3d45ee3a5ba04666b03c535ebec7e5fc |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-06-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-3d45ee3a5ba04666b03c535ebec7e5fc2025-08-20T03:43:11ZengNature PortfolioNature Communications2041-17232024-06-0115111310.1038/s41467-024-49110-6Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmissionDu Hai0Jincang Li1Daohong Jiang2Jiasen Cheng3Yanping Fu4Xueqiong Xiao5Huanran Yin6Yang Lin7Tao Chen8Bo Li9Xiao Yu10Qing Cai11Wei Chen12Ioly Kotta-Loizou13Jiatao Xie14National Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural UniversitySchool of Life and Medical Sciences, University of HertfordshireNational Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityAbstract Non-self recognition is a fundamental aspect of life, serving as a crucial mechanism for mitigating proliferation of molecular parasites within fungal populations. However, studies investigating the potential interference of plants with fungal non-self recognition mechanisms are limited. Here, we demonstrate a pronounced increase in the efficiency of horizontal mycovirus transmission between vegetatively incompatible Sclerotinia sclerotiorum strains in planta as compared to in vitro. This increased efficiency is associated with elevated proline concentration in plants following S. sclerotiorum infection. This surge in proline levels attenuates the non-self recognition reaction among fungi by inhibition of cell death, thereby facilitating mycovirus transmission. Furthermore, our field experiments reveal that the combined deployment of hypovirulent S. sclerotiorum strains harboring hypovirulence-associated mycoviruses (HAVs) together with exogenous proline confers substantial protection to oilseed rape plants against virulent S. sclerotiorum. This unprecedented discovery illuminates a novel pathway by which plants can counteract S. sclerotiorum infection, leveraging the weakening of fungal non-self recognition and promotion of HAVs spread. These promising insights provide an avenue to explore for developing innovative biological control strategies aimed at mitigating fungal diseases in plants by enhancing the efficacy of horizontal HAV transmission.https://doi.org/10.1038/s41467-024-49110-6 |
| spellingShingle | Du Hai Jincang Li Daohong Jiang Jiasen Cheng Yanping Fu Xueqiong Xiao Huanran Yin Yang Lin Tao Chen Bo Li Xiao Yu Qing Cai Wei Chen Ioly Kotta-Loizou Jiatao Xie Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission Nature Communications |
| title | Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission |
| title_full | Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission |
| title_fullStr | Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission |
| title_full_unstemmed | Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission |
| title_short | Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission |
| title_sort | plants interfere with non self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission |
| url | https://doi.org/10.1038/s41467-024-49110-6 |
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