Plants interfere with non-self recognition of a phytopathogenic fungus via proline accumulation to facilitate mycovirus transmission

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 and Jiatao Xie ()
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Du Hai: Huazhong Agricultural University
Jincang Li: Huazhong Agricultural University
Daohong Jiang: Huazhong Agricultural University
Jiasen Cheng: Huazhong Agricultural University
Yanping Fu: Huazhong Agricultural University
Xueqiong Xiao: Huazhong Agricultural University
Huanran Yin: Huazhong Agricultural University
Yang Lin: Huazhong Agricultural University
Tao Chen: Huazhong Agricultural University
Bo Li: Huazhong Agricultural University
Xiao Yu: Huazhong Agricultural University
Qing Cai: Huazhong Agricultural University
Wei Chen: Huazhong Agricultural University
Ioly Kotta-Loizou: University of Hertfordshire
Jiatao Xie: Huazhong Agricultural University

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-49110-6

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