The Interactions Between The Whitefly, Bemisia Tabaci, Two Begomoviruses (TYLCCNV And TbCSV) And Their Host Plants

(1) The B biotype of the whitefly, Bemisia tabaci (Gennadius), has invaded many countries and regions of the world in the last 20 years, and has been one of the most important crop pests worldwide. This insect has caused extensive crop damage through direct feeding and transmission of geminiviruses. The interactions between the whitefly, geminiviruses and host plants may have played important roles in the invasion and outbreaks of the whitefly and the plant virus diseases. In this study, we conducted a series of experiments to examine the interactions between the three types of organisms. We used the B biotype and a non-B biotype ZHJ-1 of Bemisia tabaci collected from Zhejiang, China, two geminiviruses, Tomato yellow leaf curl China virus (TYLCCNV) and Tobacco curly shoot virus (TbCSV), that are recently recorded in China, and two plants, tobacco and tomato, as the model systems for the study.(2) Using PCR for detection, we found that 40% of the B biotype adults carried virus DNA for both TYLCCNV and TbCSV following a period of 30 min access to virus-infected plants, and in all adults after a 12 h period of access. All ZHJ-1 adults acquired TYLCCNV or TbCSV after a 48 h period of access to the virus-infected plants. Viruliferous B and ZHJ-1 adults retained TYLCCNV DNA for their entire life when placed on healthy cotton plants. Viruliferous ZHJ-1 adults retained TbCSV DNA for their entire life when placed on healthy cotton plants but the B biotype adults did not. Transmission of TYLCCNV was achieved with one B or ZHJ-1 adult per plant, and the probability of transmission reached 100% when the number of adults was increased to ten per plant. The efficiency for TYLCCNV transmission to healthy plants by adults of both B and ZHJ-1 was much higher than that for TbCSV.(3) We used PCR to investigate the transmission of TYLCCNV and TbCSV by B biotype of B. tabaci via mating and ovum. Both TYLCCNV and TbCSV were not transmitted via mating from viruliferous females to non-viruliferous males or from viruliferous males to non-viruliferous females, neither through transovarial transmission to their offspring. The F1 adults produced by viruliferous females were found non-viruliferous.(4) B biotype whiteflies feeding continuously on TYLCCNV-infected or TbCSV-infected tobacco plants deposited 2.2 and 2.2 times more eggs, and lived 3.2 and 1.8 times longer respectively, compared to those feeding on healthy tobacco plants. In contrast, ZHJ-1 whiteflies feeding on virus-infected plants showed similar fecundity and longevity to those feeding on healthy plants.(5) In the B biotype, female adults that developed from TYLCCNV-infected tobacco plants produced 18 times more eggs and lived 25 days longer, compared to those developed from healthy plants. Similarly, female adults that developed from TbCSV-infected tobacco plants produced 12 times more eggs and lived 21 days longer, compared to those developed from healthy plants.(6) Infection of B biotype or ZHJ-1 whitefly adults with TYLCCNV led to a 23.2% or a 33.1% reduction in the mean number of eggs laid on healthy cotton plants, and a11.2 d and a 10.5 d reduction in longevity respectively, compared to adults that had not acquired either of the viruses. In contrast, infection of the B biotype adults with TbCSV led to a 29.5% increase in the mean number of eggs laid. However, the mean number of eggs deposited by TbCSV-infected ZHJ-1 adults was similar to that by non-viruliferous insects. The adult longevity of TbCSV-infected B biotype or ZHJ-1 female adults on healthy cotton plants was similar to that of non-viruliferous adults.(7) In both the B biotype and ZHJ-1 whiteflies, their carboxylesterase activity decreased with the increase of time feeding on healthy tobacco plants, and in contrast their carboxylesterase activity increased as their time feeding on TYLCCNV-infected or TbCSV-infected tobacco plants increased.We summarize the important novel findings as follows:(1) For the first time, the B biotype and ZHJ-1 of Bemisia tabaci were shown to be effective vectors for both TYLCCNV and TbCSV, and the two biotypes of whitefly differed in their capacity to acquire, retain and transmit the two begomoviruses.(2) For the first time, the infection of tobacco plants with TYLCCNV or TbCSV significantly was shown to increase the fecundity and longevity of female adults of the B biotype B. tabaci feeding on these plants, and with the increase of time feeding on virus-infected plants, the fecundity and longevity of the whiteflies further increased. In contrast, female adults of ZHJ-1 feeding on virus-infected plants did not increase their fecundity or longevity. Thus infection of host plants with geminiviruses may promote the population increase of the B biotype but not the non-B ZHJ-1. This positive interaction between the B biotype whitefly, begomoviruses and host plants may have played a major role in the widespread invasion of B biotype, in the frequent displacement of the non-B biotype whiteflies by the B biotype, as well as in the widespread outbreaks of plant diseases caused by begomoviruses.(3) Carboxylesterase activity of whiteflies of both biotypes was shown to increase with the increase of time feeding on TYLCCNV-infected or TbCSV-infected tobacco plants. Such an increase may be an important physiological response of the whiteflies to increase their performance when feeding on virus-infected host plants.