Ghosh Saptarshi, Mondal Banani, Jassar Ola, Ghanim Murad, Gautam Saurabh, Reddy Netla Vamsidhar, Srinivasan Rajagopalbabu
Department of Entomology, University of Georgia, Griffin, Georgia, USA.
Department of Entomology, The Volcani Center, Agriculture Research Organization, Rishon Lezion, Israel.
J Virol. 2025 Mar 18;99(3):e0217224. doi: 10.1128/jvi.02172-24. Epub 2025 Feb 11.
Begomoviruses are whitefly-transmitted ss-DNA viruses that infect dicotyledonous plants and contribute to major economic losses to global crop production. Invasion and establishment of an aggressive cryptic species of , known as the B cryptic species, has severely constrained vegetable production in the southeastern and southwestern United States. Disruption of genes/pathways critical for whitefly-mediated transmission can be effective for the management of begomoviruses. In this study, yeast two-hybrid (Y2H)-based screening of cDNA library identified a cyclic adenosine monophosphate (cAMP)-specific phosphodiesterase-4 (PDE4) of the whitefly as an interacting partner with capsid proteins (CPs) of old- and new-world begomoviruses. Interactions of PDE4 with begomovirus CPs were validated by glutathione-S-transferase (GST) pull-down assay and co-immunolocalization in whitefly midgut. The PDE4 family of enzymes hydrolyzes cAMP and regulates intracellular cAMP levels. This study conclusively proves that acquisition of begomoviruses downregulates the expression of PDE4 (mRNA and protein) resulting in elevated cAMP levels within the whitefly. The role of cAMP post virus acquisition is further elucidated wherein elevation of cAMP by chemical inhibition or gene (PDE4) silencing resulted in increased retention and transmission of begomoviruses. Similarly, decreased cAMP levels resulted in reduced begomovirus retention. The results of this study demonstrate that whitefly-mediated transmission of begomoviruses is regulated by intracellular cAMP by unknown mechanisms.
Begomoviruses, transmitted by the sweetpotato whitefly ( Gennadius), are the causal agents of many economically important plant virus diseases. Lack of host plant resistance against begomoviruses, high whitefly abundance, and whitefly's ability to develop insecticide resistance rapidly often render the commonly used management practice ineffective. This study demonstrates how begomovirus retention within whitefly and its transmission can be modulated by altering cyclic adenosine monophosphate (cAMP) expression of its insect vector. Naturally occurring bio-pesticides that target insect cAMPs are known. Our findings can lead to alternative strategies for the management of begomoviruses by targeting whitefly cAMP using chemicals, botanicals, or RNAi-based insecticides.
双生病毒是由粉虱传播的单链DNA病毒，可感染双子叶植物，并给全球作物生产造成重大经济损失。一种具有侵袭性的隐性烟粉虱物种（称为B隐性物种）的入侵和定殖，已严重制约了美国东南部和西南部的蔬菜生产。破坏对粉虱介导的传播至关重要的基因/途径，可能对双生病毒的治理有效。在本研究中，基于酵母双杂交（Y2H）对烟粉虱cDNA文库进行筛选，鉴定出一种烟粉虱的环磷酸腺苷（cAMP）特异性磷酸二酯酶4（PDE4），它是新旧世界双生病毒衣壳蛋白（CP）的相互作用伴侣。通过谷胱甘肽-S-转移酶（GST）下拉试验和在烟粉虱中肠的共免疫定位，验证了PDE4与双生病毒CP的相互作用。PDE4酶家族水解cAMP并调节细胞内cAMP水平。本研究确凿地证明，获取双生病毒会下调PDE4（mRNA和蛋白质）的表达，导致烟粉虱体内cAMP水平升高。进一步阐明了病毒获取后cAMP的作用，其中通过化学抑制或基因（PDE4）沉默使cAMP升高，导致双生病毒的留存和传播增加。同样，cAMP水平降低导致双生病毒留存减少。本研究结果表明，粉虱介导的双生病毒传播受细胞内cAMP调控，但其机制尚不清楚。
由甘薯粉虱（烟粉虱）传播的双生病毒，是许多具有重要经济意义的植物病毒病的病原体。缺乏对双生病毒的寄主植物抗性、粉虱数量众多以及粉虱迅速产生抗药性的能力，常常使常用的治理措施无效。本研究证明了如何通过改变其昆虫载体的环磷酸腺苷（cAMP）表达来调节双生病毒在粉虱体内的留存及其传播。已知有针对昆虫cAMP的天然生物农药。我们的研究结果可通过使用化学物质、植物提取物或基于RNA干扰的杀虫剂靶向粉虱cAMP，从而为双生病毒的治理带来替代策略。
