Proteomic Analyses of Whitefly-Begomovirus Interactions Reveal the Inhibitory Role of Tumorous Imaginal Discs in Viral Retention

Abstract

In nature, plant viruses are mostly transmitted by hemipteran insects, such as aphids, leafhoppers, and whiteflies. However, the molecular mechanisms underlying the interactions between virus and insect vector are poorly known. Here, we investigate the proteomic interactions between tomato yellow leaf curl virus (TYLCV, genus Begomovirus, family Geminiviridae), a plant virus, and its vector whitefly (Bemisia tabaci) species complex. First, using a yeast two-hybrid system, we identified 15 candidate whitefly proteins interacting with the coat protein of TYLCV. GO and KEGG pathway analysis implicated that these 15 whitefly proteins are of different biological functions/processes mainly including metabolic process, cell motility, signal transduction, and response to stimulus. We then found that the whitefly protein tumorous imaginal discs (Tid), one of the 15 whitefly proteins identified, had a stable interaction with TYLCV CP in vitro, and the DnaJ_C domain of Tid 301−499aa may be the viral binding site. During viral retention, the expression of whitefly protein Tid was observed to increase at the protein level, and feeding whiteflies with dsRNA or antibody against Tid resulted in a higher quantity of TYLCV in the whitefly body, suggesting the role of Tid in antiviral infection. Our data indicate that the induction of Tid following viral acquisition is likely a whitefly immune response to TYLCV infection.

Plant-virus-insect tritrophic interactions: insights into the functions of geminivirus virion-sense strand genes

“…CP, must interact with whitefly-derived proteins. In agreement with this, several such candidates have been identified [5,7,[44][45][46] (figure 2). Moreover, whiteflies are also known to possess several bacterial endosymbionts (such as Arsenophonus, Cardinium, Fritschea, Hamiltonella, Portiera, Rickettsia and Wolbachia) in the whitefly midgut that are implicated to influence virus transmission [5,49].…”

“…For example, viral acquisition led to up-and downregulation of insect's defence genes [41][42][43]. Upon feeding, a saliva effector [45,46]. Any variations in the expression of genes/pathways involved in different whitefly species/pathotypes during feeding might provide clues about the host factors (either beneficial or harmful) involved in virus acquisition/retention.…”

Implication of the Whitefly Protein Vps Twenty Associated 1 (Vta1) in the Transmission of Cotton Leaf Curl Multan Virus

“…The split-ubiquitin yeast two-hybrid system (Dualsystems Biotech, Zurich, Switzerland) was used to identify Asia II 1 whitefly proteins that interact with the CLCuMuV CP [ 11 ]. A cDNA library of Asia II 1 whitefly was constructed in the prey plasmid, SfiI-digested pPR3-N, with the EasyClone cDNA library construction kit (Dualsystems Biotech, Zurich, Switzerland).…”

“…During this process, TYLCV hijacks clathrin-mediated endocytosis and the endosomal network to cross the midgut barrier of the whitefly vector [ 8 , 9 ]. Moreover, the coat protein (CP) of TYLCV may interact with many whitefly proteins, thereby facilitating virus transmission [ 3 , 10 , 11 , 12 ]. Two recent reviews on whitefly transmission of begomoviruses indicate that the transmission efficiency of a given virus may vary with different whitefly species, and different viruses may be transmitted with disparate efficiencies by a given whitefly species [ 3 , 10 ].…”

PEBP regulates balance between apoptosis and autophagy, enabling coexistence of arbovirus and insect vector

“…Different pre-domain sequences of PEBP4 from whitefly MEAM1 and from MED reasonably explained the results of Y2H and CoIP, as well as failure to screen any PEBPs in MEAM1 species that could interact with TYLCV CP (Zhao et al, 2020b;Zhao et al, 2020c). Although TYLCV could also induce PCD in MEAM1 species, the most striking difference is the initiation timepoint of PCD after acquiring TYLCV.…”