Begomovirus capsid proteins interact with cyclic adenosine monophosphate (cAMP)-specific phosphodiesterase of its whitefly vector and modulate virus retention within its vector.

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 Bemisia tabaci, 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 B. tabaci 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. IMPORTANCE: Begomoviruses, transmitted by the sweetpotato whitefly (Bemisia tabaci 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.