Verticillium wilt is a severe plant disease that causes massive losses in multiple crops. Increasing the plant resistance to Verticillium wilt is a critical challenge worldwide. Here, we report that the hemibiotrophic Verticillium dahliae-secreted Asp f2-like protein VDAL causes leaf wilting when applied to cotton leaves in vitro but enhances the resistance to V. dahliae when overexpressed in Arabidopsis or cotton without affecting the plant growth and development. VDAL protein interacts with Arabidopsis E3 ligases plant U-box 25 (PUB25) and PUB26 and is ubiquitinated by PUBs in vitro. However, VDAL is not degraded by PUB25 or PUB26 in planta. Besides, the pub25 pub26 double mutant shows higher resistance to V. dahliae than the wild-type. PUBs interact with the transcription factor MYB6 in a yeast two-hybrid screen. MYB6 promotes plant resistance to Verticillium wilt while PUBs ubiquitinate MYB6 and mediate its degradation. VDAL competes with MYB6 for binding to PUBs, and the role of VDAL in increasing Verticillium wilt resistance depends on MYB6. Taken together, these results suggest that plants evolute a strategy to utilize the invaded effector protein VDAL to resist the V. dahliae infection without causing a hypersensitive response (HR); alternatively, hemibiotrophic pathogens may use some effectors to keep plant cells alive during its infection in order to take nutrients from host cells. This study provides the molecular mechanism for plants increasing disease resistance when overexpressing some effector proteins without inducing HR, and may promote searching for more genes from pathogenic fungi or bacteria to engineer plant disease resistance.

中文翻译：

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黄萎病菌效应子 VDAL 通过与 PUB25 和 PUB26 E3 连接酶相互作用以增强黄萎病抗性来保护 MYB6 免受降解

黄萎病是一种严重的植物病害，会导致多种作物的大量损失。提高植物对黄萎病的抗性是世界范围内的一项重大挑战。在这里，我们报告了半营养型大丽轮枝菌分泌的 Asp f2 样蛋白 VDAL 在体外应用于棉花叶片时会导致叶片萎蔫，但在拟南芥或棉花中过度表达时会增强对大丽花的抗性，而不影响植物的生长和发育。VDAL 蛋白与拟南芥 E3 连接酶植物 U-box 25 (PUB25) 和 PUB26 相互作用，并在体外被 PUB 泛素化。然而，VDAL 在足底不会被 PUB25 或 PUB26 降解。此外，pub25 pub26 双突变体对大丽花的抗性高于野生型。PUB 在酵母双杂交筛选中与转录因子 MYB6 相互作用。MYB6 促进植物对黄萎病的抗性，而 PUBs 泛素化 MYB6 并介导其降解。VDAL 与 MYB6 竞争与 PUB 的结合，而 VDAL 在增加黄萎病抗性中的作用取决于 MYB6。总之，这些结果表明植物进化出一种利用入侵的效应蛋白 VDAL 抵抗大丽花感染而不引起过敏反应 (HR) 的策略。或者，半营养型病原体可能使用一些效应器在感染期间使植物细胞保持活力，以便从宿主细胞中获取营养。该研究为植物在过度表达某些效应蛋白而不诱导HR的情况下增加抗病性提供了分子机制，并可能促进从病原真菌或细菌中寻找更多基因来改造植物抗病性。