It is known that plant viruses can change the performance of their vectors. However, there have been no reports on whether or how a semipersistent plant virus manipulates the feeding behaviors of its whitefly vectors. Cucurbit chlorotic yellows virus (CCYV) (genus Crinivirus, family Closteroviridae) is an emergent plant virus in many Asian countries and is transmitted specifically by B and Q biotypes of tobacco whitefly, Bemisia tabaci (Gennadius), in a semipersistent manner. In the present study, we used electrical penetration graph (EPG) technique to investigate the effect of CCYV on the feeding behaviors of B. tabaci. The results showed that CCYV altered feeding behaviors of both biotypes and sexes of B. tabaci with different degrees. CCYV had stronger effects on feeding behaviors of Q biotype than those of B biotype, by increasing duration of phloem salivation and sap ingestion, and could differentially manipulate feeding behaviors of males and females in both biotype whiteflies, with more phloem ingestion in Q biotype males and more non-phloem probing in B biotype males than their respective females. With regard to feeding behaviors related to virus transmission, these results indicated that, when carrying CCYV, B. tabaci Q biotype plays more roles than B biotype, and males make greater contribution than females.

Cucurbit chlorotic yellows virus (CCYV) (genus Crinivirus, family Closteroviridae) is an emerging plant virus, and is now spreading and causing severe economic losses to cucurbit crops in many Asian countries. CCYV is believed to be transmitted specifically by the sweetpotato whitefly, Bemisia tabaci, in a semipersistent manner. In the present study, we provide direct evidence for the semipersistent transmission of CCYV by Mediterranean (MED) cryptic species of B. tabaci complex. We investigated CCYV transmission characteristics, and immunofluorescently labeled and localized the virus retention site within the vector by laser confocal microscopy. Whiteflies required ≥1 h of acquisition access period (AAP) to successfully acquire CCYV, and the proportion of RT-PCR positive whitefly individuals reached to 100% at 48 h of AAP. CCYV virons could be retained within vectors as long as 12 d, but the proportion of RT-PCR positive whiteflies dropped to 55% by 3 d. Groups of thirty whiteflies given a 24 h of inoculation access period (IAP) to inoculate CCYV on cucumber plants showed a transmission efficiency rate of 72.73%. The retention site of CCYV virons was located in the foregut of virion-fed vectors. These results definitely indicated the semipersistent transmission mode of CCYV by B. tabaci MED.

Plant viruses can affect vector’s behaviors in order to enhance viral transmission. Cucurbit chlorotic yellows virus (CCYV) (genus Crinivirus) is an emergent RNA plant virus and is transmitted specifically by biotypes B and Q of tobacco whitefly, Bemisia tabaci (Gennadius), in a semipersistent manner. We used the electrical penetration graph (EPG) to investigate the effect of CCYV on the feeding behaviors of B. tabaci biotypes B and Q. CCYV could affect, both directly and indirectly, the feeding behaviors of B. tabaci to various degrees, depending on biotypes and sexes of the insect. CCYV showed stronger direct effects on biotype Q than on biotype B in terms of increased non-phloem probing and phloem salivation. CCYV increased non-phloem probing and phloem salivation more on females than on males of biotype Q, and increased phloem salivation more on females than on males of biotype B. CCYV had stronger indirect effects, via virus-infested plants, on biotype B than on biotype Q by enhancing phloem sap ingestion and feeding bouts. CCYV increased non-phloem probing and feeding bouts more on males than on females of biotype B, and decreased phloem sap ingestion more on males than on females on biotype Q indirectly. The results clearly indicated that CCYV affects the feeding behaviors of B. tabaci, which may lead to increased ability of the B. tabaci for CCYV transmission.

Background: Plant metabolites play vital roles in regulating the behavior of herbivore insects. Virus infection can universally alter plant metabolites to manipulate the orientation and feeding behaviors of insect vector, to favor the transmission of virus. Thus, determining the differentially accumulated metabolites of plant upon virus infection could provide insights into understanding how the triple interactions among plant, virus and insect vector happens. Our previous studies have found that vector whitefly Bemisia tabaci (Gennadius, Hemiptera: Aleyrodidae) showed different orientation behavior and performance on CCYV-infected and healthy cucumber plants. Cucurbit chlorotic yellows virus (CCYV) is exclusively transmitted by B. tabaci in a semi-persistent mode. In this study, we take the CCYV, B. tabaci and cucumber as a research system to explore the functions of phyto-metabolites in the triple interactions. Results: A total of 612 metabolites changed upon CCYV infection were monitored. Metabolites mainly enriched in flavonoids, lipids, nucleotides and their derivatives. At 7 days post CCYV inoculation (dpi), the contents of lipids, terpenoids and flavonoids remarkably decreased, while amino acids, nucleotides and their derivatives notably up-accumulated. At 15 dpi, the accumulation of flavonoids were still significantly reduced upon CCYV infection, while lipids, amino acids, nucleotides and derivatives were remarkably enhanced. Most of significantly increased metabolites were lipids (lysophosphatidylethanolamine, LPE; lysophosphatidylcholine, LPC and their isomers). Also, the number of significantly changed metabolites increased with the infection period. However, only a few organic acids and phenolic acids showed difference between CCYV-infected and healthy cucumber plants. Conclusions: CCYV infection repressed the defensive flavonoids, terpeneoids metabolism but triggered the lipids, amino acids and nucleotides metabolism with the inoculation period. This result suggests that CCYV-infection makes cucumber plants more susceptible for whiteflies attack and CCYV infection. The reduction of defensive comounds and the increase of amino acids may be partially responsible for enhancing feeding preference of whiteflies to CCYV-infected hosts. CCYV may hijacked lipid metabolism for virus replication and assembly.