Liaoning Key Laboratory of Economic and Applied Entomology, College of Plant Protection, Shenyang Agricultural University, Shenyang, China.
mBio. 2023 Feb 28;14(1):e0299022. doi: 10.1128/mbio.02990-22. Epub 2023 Jan 24.
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.
共生生物学中，动物繁殖和共生体遗传之间的整合是基础，但其中的分子机制在很大程度上尚不清楚。卵黄蛋白原 (Vg) 对卵母细胞的发生至关重要，在某些动物中也是病原体模式识别分子。先前的研究表明，Vg 参与调节共生体的丰度和传递。然而，昆虫及其共生体如何共同作用于 Vg 的功能以及 Vg 如何影响昆虫-微生物共生体的持久性等问题在很大程度上仍不清楚。共生体通过白蝇烟粉虱的母系遗传，经由细菌细胞传递给后代。令人惊讶的是，Vg 存在于烟粉虱的细菌细胞中。Vg 可以由这些细胞中表达的基因在白蝇细菌细胞中合成，或者通过 Vg 受体从血淋巴中输出到细菌细胞中。我们还发现，保幼激素和“Portiera aleyrodidarum”（此处称为）控制着白蝇中 Vg 的水平和定位。免疫捕获 PCR 揭示了 Vg 与的相互作用。抑制 Vg 的表达会降低的丰度以及白蝇的卵母细胞发生和繁殖力。因此，我们揭示了 Vg 促进了白蝇-细菌共生体的共生关系的维持。本研究将为深入了解 Vg 在昆虫生殖与共生体遗传协同进化中的关键作用提供新的见解。 内共生体已通过各种机制纳入昆虫生殖和发育生物学中。所有烟粉虱物种都在称为细菌细胞的专门昆虫细胞中携带必需共生体。我们报告说，白蝇的保幼激素和决定了白蝇细菌细胞中卵黄蛋白原 (Vg) 的定位。反过来，Vg 影响白蝇的繁殖力以及共生体的适应性和传播。我们的研究结果表明，多功能蛋白 Vg 对于共生体整合到昆虫的生殖和发育中是不可或缺的。这反映了昆虫-微生物共生体长期协同进化的结果。
