New insights into the transovarial transmission of the symbiontRickettsiain whiteflies

Endosymbiont transmission via eggs to future host generations has been recognized as the main strategy for its persistence in insect hosts; however, the mechanisms for transmission have yet to be elucidated. Here, we describe the dynamic locations ofRickettsiain the ovarioles and eggs during oogenesis and embryogenesis in a globally significant pest whiteflyBemisia tabaci. Field populations of the whitefly have a high prevalence ofRickettsia, and in all Rickettsia-infected individuals, the bacterium distributes in the body cavity of the host, especially in the midgut, fat body, hemocytes, hemolymph, and near bacteriocytes. The distribution ofRickettsiawas subjected to dynamic changes in the ovary during oogenesis, and our ultrastructural observations indicated that the bacteria infect host ovarioles during early developmental stages via two routes: (i) invasion of the tropharium by endocytosis and then transmission into vitellarium via nutritive cord and (ii) entry into vitellarium by hijacking bacteriocyte translocation. Most of theRickettsiaare degraded in the oocyte cytoplasm in late-stage oogenesis. However, a few reside beneath the vitelline envelope of mature eggs, spread into the embryo, and proliferate during embryogenesis to sustain high-fidelity transmission to the next generation. Our findings provide novel insights into the maternal transmission underpinning the persistence and spread of insect symbionts.

Automated summary

Endosymbiont Rickettsia is transmitted to the next generation of insect hosts through eggs, with a dynamic distribution pattern in the ovaries and eggs of the whitefly Bemisia tabaci. The bacteria infect host ovarioles during early developmental stages via two routes and survive in mature eggs to proliferate during embryogenesis for high-fidelity transmission to the next generation. This study provides novel insights into the maternal transmission mechanisms of insect symbionts.