Qin Li, Wang Xiaoqing, Dai Zhaoji, Shen Wentao, Li Fangfang, Wang Aiming, Valli Adrián A, Cui Hongguang
Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests (Ministry of Education), School of Tropical Agriculture and Forestry, Hainan University, Haikou, China.
National Key Laboratory for Tropical Crops Breeding, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou & Sanya, China.
PLoS Pathog. 2025 Jun 26;21(6):e1013012. doi: 10.1371/journal.ppat.1013012. eCollection 2025 Jun.
Potyviridae is the largest family of plant-infecting RNA viruses. All members of the family (potyvirids) have single-stranded positive-sense RNA genomes, with polyprotein processing as the expression strategy. The 5'-proximal regions of all potyvirids, except bymoviruses, encode two types of leader proteases: the serine protease P1 and the cysteine protease HCPro. However, their arrangement and sequence composition vary greatly among genera or even species. The leader proteases play multiple important roles in different potyvirid-host combinations, including RNA silencing suppression and virus transmission. Here, we report that viruses in the genus Arepavirus, which encode two HCPro leader proteases in tandem (HCPro1-HCPro2), can naturally lose the coding sequences for these two proteins during infection. Notably, this loss is associated with a shift in foliage symptoms from severe necrosis to mild chlorosis or even asymptomatic infections. Further analysis revealed that the deleted region is flanked by two short repeated sequences in the parental isolates, suggesting that recombination during virus replication likely drives this genomic deletion. Reverse genetic approaches confirmed that the loss of leader proteases weakens RNA silencing suppression and other critical functions. A field survey of areca palm trees displaying varied symptom severity identified a transitional stage in which full-length viruses and deletion mutants coexist in the same tree. Based on these findings, we propose a scenario in which full-length isolates drive robust infections and facilitate plant-to-plant transmission, eventually giving rise to leader protease-less variants that mitigate excessive damage to host trees, allowing long-term coexistence with the perennial host. To our knowledge, this is the first report of potyvirid self-attenuation via coding sequence loss.
马铃薯Y病毒科是感染植物的RNA病毒中最大的一个科。该科所有成员（马铃薯Y病毒属病毒）都具有单链正义RNA基因组，以多聚蛋白加工作为表达策略。除大麦黄花叶病毒属病毒外，所有马铃薯Y病毒属病毒的5'近端区域都编码两种类型的前导蛋白酶：丝氨酸蛋白酶P1和半胱氨酸蛋白酶HCPro。然而，它们的排列和序列组成在不同属甚至不同种之间差异很大。前导蛋白酶在不同的马铃薯Y病毒属病毒-宿主组合中发挥多种重要作用，包括RNA沉默抑制和病毒传播。在此，我们报告称，阿雷帕病毒属中的病毒串联编码两种HCPro前导蛋白酶（HCPro1-HCPro2），在感染过程中可自然丢失这两种蛋白的编码序列。值得注意的是，这种丢失与叶片症状从严重坏死转变为轻度黄化甚至无症状感染有关。进一步分析表明，缺失区域两侧在亲本分离株中有两个短重复序列，这表明病毒复制过程中的重组可能驱动了这种基因组缺失。反向遗传学方法证实，前导蛋白酶的缺失削弱了RNA沉默抑制和其他关键功能。对表现出不同症状严重程度的槟榔树进行的田间调查确定了一个过渡阶段，在此阶段全长病毒和缺失突变体共存于同一棵树中。基于这些发现，我们提出了一种设想，即全长分离株引发强烈感染并促进植物间传播，最终产生无前导蛋白酶的变体，减轻对宿主树的过度损害，从而与多年生宿主长期共存。据我们所知，这是关于马铃薯Y病毒属病毒通过编码序列丢失实现自我衰减的首次报道。
