An Investigation Of The Effect Of Tomato Vellow Leaf Curl China Virus On The Feeding Behavior Of The Whitefly Bemisia Tabaci Using Electrical Penetration Graph

The Middle East-Asia Minor1(MEAM1) cryptic species of the whitefly Bemisia tabaci complex is one of the most important invasive pests in China and has caused serious damages in this country in recent years. MEAM1damages plants mainly through vectoring plant viruses, of which the Tomato yellow leaf curl China virus (TYLCCNV) is transmitted by B. tabaci and stands as a threat to crops such as tomato and tobacco. Virus-vector interactions play very important roles in determining the population dynamics of both insect vectors and plant pathogens. Earlier studies from our laboratory revealed the complex interplay between TYLCCNV and MEAM1whitefly. The TYLCCNV presence in its vector may be harmful to the population growth of MEAM1. But on TYLCCNV-infected tobacco, whiteflies performed better in terms of longevity, fecundity and assimilation of nutrients.In this study, we made an attempt to investigate TYLCCNV-MEAM1interactions from the perspective of the feeding behavior of the insect vector through the use of Electrical Penetration Graph (EPG). We investigated virus-whitefly interactions in the following three aspects:(1) The direct effect of TYLCCNV on the feeding behavior of the insect vector;(2) the comprehensive effect of TYLCCNV on the vector when the insect feed on virus-infected plants; and (3) The effect of vectors’feeding behavior on the transmission of TYLCCNV.1. The direct effect of TYLCCNV on the feeding behavior of whiteflyWe did the experiments using cotton, a non-host plant of TYLCCNV. The viruliferous MEAM1whiteflies attempted more probes, spent shorter time on average pathway duration and more time from the first probe to reach the phloem. The time of phloem ingestion was longer for non-viruliferous than viruliferous whiteflies. The results showed that the virus negatively affected the feeding behavior of MEAM1in many ways.2. The comprehensive effect of TYLCCNV on the feeding behavior of whiteflyWhiteflies spent more time crawling and searching for appropriate probing sites and delayed the first probe on infected tobacco, and this delay may be caused by the physical and/or physiological change of leaves. Viruliferous whiteflies attempted more probes than non-viruliferous whiteflies on healthy tobacco. We speculate that virus infection may perturb its stylet penetration. The average number of probes was fewer for whiteflies on virus-infected than on uninfected plants, indicating that the virus had positive effects on the probing of the whitefly via the plant. Moreover, this positive effect of the virus through host plant seemed to have surpassed the direct negative effect of virus on whiteflies. The whiteflies could more easily reach the phloem when the host plant and vector were both infected by the virus, and they also spent more time ingesting. The combined evidence indicated that TYLCCNV benefited the feeding behavior of whitefly indirectly. In addition, the whitefly vectors can take up more viruses when they had more phloem ingestion, which in turn facilitates the transmission and spreading of the virus.3. The effect of vectors’feeding behavior on transmission of TYLCCNVWe compared the feeding behavior of non-viruliferous and viruliferous whiteflies on young plants of tobacco. Virus infection increased the ingestion of whitefly but not its salivation. We speculate that TYLCCNV may benefit its own spreading via enhanced performance of its vector but not increase in salivation of the vector.Overall, TYLCCNV can affect the feeding behavior of whiteflies on their pathway to phloem and also ingestion. The virus negatively affects the feeding behavior directly, i.e. the presence of the virus in its vector perturbs whitefly feeding. However, the virus has both negative and positive effects on the vector when the whitefly feeds on virus-infected plants, and the indirect positive effect surpasses the direct negative effect. TYLCCNV may facilitate its spread by promoting sap ingestion by its vectors. The physiological mechanisms underlying the direct and indirect effects of TYLCCNV on the feeding behavior of MEAM1warrants investigation in the future.