Enhanced Vitellogenesis in a Whitefly via Feeding on a Begomovirus-Infected Plant

Abstract

BackgroundThe MEAM1 (B biotype) Bemisia tabaci (Gennadius) is one of the most widespread and damaging whitefly cryptic species. Our previous studies discovered that the MEAM1 whitefly indirectly benefits from interactions with the tomato yellow leaf curl China virus (TYLCCNV) via accelerated ovarian development and increased fecundity. However, the physiological mechanism of begomoviruse-infected plants acting on the reproduction of the insect vector was unknown.Methodology/Principal FindingsBiochemical and molecular properties of vitellogenin (Vg) and vitellin (Vt) were characterized in the MEAM1 whitefly. In addition, kinetics of Vt levels in ovary and Vg levels in hemolymph in different stages were detected using a sandwich ELISA. The level of hemolymph Vg increased rapidly after eclosion. A significantly higher level of hemolymph Vg and ovary Vt were observed in whiteflies feeding on virus-infected tobacco plants than those feeding on uninfected plants. In order to detect the levels of Vg mRNA transcription, complete vitellogenin (Vg) mRNA transcripts of 6474 bp were sequenced. Vg mRNA level in whiteflies feeding on virus-infected plants was higher than those feeding on uninfected plants. However, virus-infection of the whiteflies per se, as demonstrated using an artificial diet system, did not produce significant changes in Vg mRNA level.Conclusions/SignificanceIn MEAM1 whitefly, increased levels of both vitellin and vitellogenin as well as increased transcription of Vg mRNA are associated with feeding on begomovirus-infected plants, thus providing a mechanism for accelerated vitellogenesis. We conclude that MEAM1 whitefly profits from feeding on begomovirus-infected plants for yolk protein synthesis and uptake, and thereby increases its fecundity. These results not only provide insights into the molecular and physiological mechanisms underlying the elevated reproduction of a whitefly species through its association with a begomovirus-infected plant, but also provide a better understanding of the molecular mechanisms related to whitefly reproduction.

Triazophos‐induced vertical transmission of rice stripe virus is associated with host vitellogenin in the small brown planthopper Laodelphax striatellus

“…It is noteworthy that LsVg had significantly increased expression after RSV infection revealed by transcriptomic analyses of whole‐body SBPH . In Bemisia tabaci , Vg mRNA expression was also significantly increased after feeding on virus‐infected plants . These results suggest that Vg expression modulated by virus would facilitate the spread of virus.…”

“…55,56 In Bemisia tabaci, Vg mRNA expression was also significantly increased after feeding on virus-infected plants. 57 These results suggest that Vg expression modulated by virus would facilitate the spread of virus.…”

Levels of the endosymbiont Rickettsia in the whitefly Bemisia tabaci are influenced by the expression of vitellogenin

“…Although the number of vitellogenin genes varies in different insect species (Tufail et al, 2005), it was reported that in Be. tabaci the vitellogenin is encoded by only a single gene and the full transcript sequence is about 6.5 kb (Guo et al, 2012). A high abundance of vitellogenin transcript was also observed in the transcriptomes of different insects, such as the potato psyllid Bactericera cockerelli (Hail et al, 2010) and small brown planthopper, Laodelphax striatellus .…”

Feeding on a Begomovirus‐infected Plant Enhances Fecundity via Increased Expression of an Insulin‐like Peptide in the Whitefly, Meam1

“…So far, it is thought that viral infection may repress plant defenses against whiteflies, and the suppressed plant defenses in turn might allow the whiteflies to elevate its primary metabolism. Higher metabolism may increase nutritional assimilation and enhance vitellogenesis (Guo et al., ; Wang et al., ; Zhang et al., ). The whitefly nutritional status is probably modulated to regulate physiological processes, such as development and reproductive maturation in whitefly.…”