Abstract Understanding the evolutionary history of a virus and the mechanisms influencing the direction of its evolution is essential for the development of more durable strategies to control the virus in crop fields. While the deployment of host resistance in crops is the most efficient means to control various viruses, host resistance itself can act as strong selective pressure and thus play a critical role in the evolution of virus virulence. Cucumber mosaic virus (CMV), a plant RNA virus with high evolutionary capacity, has caused endemic disease in various crops worldwide, including pepper (Capsicum annuum L.), because of frequent emergence of resistance-breaking variants. In this study, we examined the molecular and evolutionary characteristics of recently emerged, resistance-breaking CMV variants infecting pepper. Our population genetics analysis revealed that the high divergence capacity of CMV RNA1 might have played an essential role in the host-interactive evolution of CMV and in shaping the CMV population structure in pepper. We also demonstrated that nonsynonymous mutations in RNA1 encoding the 1a protein enabled CMV to overcome the deployed resistance in pepper. Our findings suggest that resistance-driven selective pressures on RNA1 might have contributed in shaping the unique evolutionary pattern of CMV in pepper. Therefore, deployment of a single resistance gene may reduce resistance durability against CMV and more integrated approaches are warranted for successful control of CMV in pepper.

中文翻译：

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新出现的黄瓜花叶病毒抗性破坏变体代表了 RNA 病毒正在进行的宿主相互作用进化

摘要 了解病毒的进化历史以及影响其进化方向的机制对于制定更持久的策略来控制农田中的病毒至关重要。虽然在作物中部署宿主抗性是控制各种病毒的最有效手段，但宿主抗性本身可以作为强大的选择压力，从而在病毒毒力的进化中发挥关键作用。黄瓜花叶病毒 (CMV) 是一种具有高进化能力的植物 RNA 病毒，由于频繁出现抗性破坏变体，已在包括辣椒 (Capsicum annuum L.) 在内的全球多种作物中引起地方病。在这项研究中，我们检查了最近出现的感染辣椒的抗性破坏 CMV 变体的分子和进化特征。我们的群体遗传学分析表明，CMV RNA1 的高分化能力可能在 CMV 的宿主相互作用进化和塑造辣椒中的 CMV 群体结构中发挥了重要作用。我们还证明了编码 1a 蛋白的 RNA1 中的非同义突变使 CMV 能够克服辣椒中部署的抗性。我们的研究结果表明，对 RNA1 的抗性驱动的选择压力可能有助于塑造辣椒中 CMV 的独特进化模式。因此，单个抗性基因的部署可能会降低对 CMV 的抗性持久性，并且需要更综合的方法来成功控制辣椒中的 CMV。