Wang Xin-Ru, Wang Chao, Ban Fei-Xue, Ghanim Murad, Pan Li-Long, Qian Li-Xin, Liu Yin-Quan, Wang Xiao-Wei, Liu Shu-Sheng
Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou, China.
Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel.
mSystems. 2020 Sep 22;5(5):e00433-20. doi: 10.1128/mSystems.00433-20.
Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus within the family , which are transmitted by whiteflies of the species complex in a persistent manner, we revealed that virus-induced apoptosis in insect vectors can facilitate viral accumulation and transmission. We found that infection with tomato yellow leaf curl virus activated the apoptosis pathway in Suppressing apoptosis by inhibitors or silencing significantly reduced viral accumulation, while the activation of apoptosis increased viral accumulation Moreover, the positive effect of whitefly apoptosis on virus accumulation and transmission was not due to its cross talk with the autophagy pathway that suppresses begomovirus infection in whiteflies. We further showed that viral replication, rather than the viral coat protein, is likely the critical factor in the activation of apoptosis by the virus. These novel findings indicate that similarly to many animal and a few plant RNA viruses, plant DNA viruses may activate apoptosis in their insect vectors leading to enhanced viral accumulation and transmission. Of the approximately 1,100 known plant viruses, about one-third are DNA viruses that are vectored by insects. Plant virus infections often induce cellular and molecular responses in their insect vectors, which can, in many cases, affect the spread of viruses. However, the mechanisms underlying vector responses that affect virus accumulation and transmission are poorly understood. Here, we examined the role of virus-induced apoptosis in the transmission of begomoviruses, a group of single-stranded plant DNA viruses that are transmitted by whiteflies and cause extensive damage to many crops worldwide. We demonstrated that virus infection can induce apoptosis in the insect vector conferring protection to the virions from degradation, leading to enhanced viral accumulation and transmission to host plants. Our findings provide valuable clues for designing new strategies to block the transmission of insect-vectored plant viruses, particularly plant DNA viruses.
细胞凋亡通常被认为是抵御病毒感染的第一道防线。然而,细胞凋亡在植物病毒与其昆虫介体相互作用中的作用鲜有研究。通过研究 科内 属的植物DNA病毒,这些病毒由 种复合体的粉虱以持久性方式传播,我们发现病毒诱导昆虫介体中的细胞凋亡可促进病毒积累和传播。我们发现感染番茄黄化曲叶病毒会激活 中的细胞凋亡途径。用抑制剂抑制细胞凋亡或沉默 会显著降低病毒积累,而细胞凋亡的激活则增加病毒积累。此外,粉虱细胞凋亡对病毒积累和传播的积极作用并非由于其与抑制粉虱中双生病毒感染的自噬途径相互作用。我们进一步表明,病毒复制而非病毒外壳蛋白可能是病毒激活细胞凋亡的关键因素。这些新发现表明,与许多动物和少数植物RNA病毒类似,植物DNA病毒可能在其昆虫介体中激活细胞凋亡,从而导致病毒积累和传播增强。在大约1100种已知植物病毒中,约三分之一是由昆虫传播的DNA病毒。植物病毒感染通常会在其昆虫介体中引发细胞和分子反应,在许多情况下,这些反应会影响病毒的传播。然而,影响病毒积累和传播的介体反应背后的机制尚不清楚。在这里,我们研究了病毒诱导的细胞凋亡在双生病毒传播中的作用,双生病毒是一类单链植物DNA病毒,由粉虱传播,对全球许多作物造成广泛损害。我们证明病毒感染可诱导昆虫介体中的细胞凋亡,为病毒粒子提供保护使其免受降解,从而导致病毒积累增加并传播至寄主植物。我们的研究结果为设计新策略以阻断昆虫传播的植物病毒尤其是植物DNA病毒的传播提供了有价值的线索。