Vitellogenin Facilitates Associations between the Whitefly and a Bacteriocyte Symbiont.

Integration between animal reproduction and symbiont inheritance is fundamental in symbiosis biology, but the underlying molecular mechanisms are largely unknown. Vitellogenin (Vg) is critical for oogenesis, and it is also a pathogen pattern recognition molecule in some animals. Previous studies have shown that Vg is involved in the regulation of symbiont abundance and transmission. However, the mechanisms by which an insect and its symbiont contribute to the function of Vg and how Vg impacts the persistence of insect-microbe symbiosis remain largely unclear. Symbionts are transovarially transmitted via maternal inheritance of the bacteriocytes in the whitefly Bemisia tabaci. Surprisingly, Vg is localized in bacteriocytes of whiteflies. Vg could be synthesized in whitefly bacteriocytes by the gene expressed in these cells or exported into bacteriocytes from hemolymph via the Vg receptor. We further found that the juvenile hormone and " Portiera aleyrodidarum" (here termed ) control the level and localization of Vg in whiteflies. Immunocapture PCR revealed interactions between Vg and . Suppressing Vg expression reduced abundance as well as whitefly oogenesis and fecundity. Thus, we reveal that Vg facilitated the persistence of whitefly-bacteriocyte symbiont associations. This study will provide insight into the key role of Vg in the coevolution of insect reproduction and symbiont inheritance. Intracellular heritable symbionts have been incorporated into insect reproductive and developmental biology by various mechanisms. All Bemisia tabaci species harbor the obligate symbiont in specialized insect cells called bacteriocytes. We report that the whitefly juvenile hormone and determined vitellogenin (Vg) localization in bacteriocytes of whiteflies. In turn, Vg affected whitefly fecundity as well as fitness and transmission of the symbiont. Our findings show that Vg, a multifunctional protein, is indispensable for symbiont integration into the reproduction and development of insects. This reflects the outcome of long-term coevolution of the insect-microbe symbiosis.