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.

非自我识别是生命的一个基本方面，是减轻真菌种群内分子寄生虫增殖的关键机制。然而，调查植物对真菌非自我识别机制的潜在干扰的研究是有限的。在这里，我们证明与体外相比，植物中营养不相容的核盘菌菌株之间的水平真菌病毒传播效率显着增加。这种效率的提高与核盘菌感染后植物中脯氨酸浓度的升高有关。脯氨酸水平的激增通过抑制细胞死亡来减弱真菌之间的非自我识别反应，从而促进真菌病毒的传播。此外，我们的田间实验表明，将含有低毒力相关真菌病毒（HAV）的低毒力核盘菌菌株与外源脯氨酸结合使用，可以为油菜植物提供实质性保护，使其免受剧毒核盘菌的侵害。这一史无前例的发现揭示了一种新的途径，植物可以利用该途径利用真菌非自我识别的减弱和促进 HAV 的传播来抵抗核盘菌感染。这些有希望的见解为探索开发创新生物控制策略提供了一条途径，旨在通过增强 HAV 水平传播的功效来减轻植物中的真菌病害。