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

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 de...

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Bibliographic Details
Published in:Nature communications Vol. 15; no. 1; pp. 4748 - 13
Main Authors: Hai, Du, Li, Jincang, Jiang, Daohong, Cheng, Jiasen, Fu, Yanping, Xiao, Xueqiong, Yin, Huanran, Lin, Yang, Chen, Tao, Li, Bo, Yu, Xiao, Cai, Qing, Chen, Wei, Kotta-Loizou, Ioly, Xie, Jiatao
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 04.06.2024
Nature Publishing Group
Nature Portfolio
Subjects:
631/158/855
631/326/193/2539
631/326/596/2563
Apoptosis
Ascomycota - physiology
Ascomycota - virology
Biological control
Brassica napus - microbiology
Brassica napus - virology
Cell death
Field tests
Fungal diseases
Fungal Viruses - genetics
Fungal Viruses - physiology
Fungi
Host-Pathogen Interactions
Humanities and Social Sciences
Infections
multidisciplinary
Parasites
Phytopathogenic fungi
Plant diseases
Plant Diseases - microbiology
Plant Diseases - virology
Population studies
Proline
Proline - metabolism
Proteins
Rapeseed
Recognition
Science
Science (multidisciplinary)
Self-recognition
Virulence
ISSN:2041-1723, 2041-1723
Online Access:Get full text
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Summary: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. Mycoviruses are obligate parasites of fungi. Here, Hai et al. show that mycoviruses can induce hypovirulence in the fungus Sclerotinia, and plants infected by Sclerotinia facilitate the transmission of these mycoviruses, thereby helping the plants defend against Sclerotinia.
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ISSN:2041-1723
2041-1723
DOI:10.1038/s41467-024-49110-6