New insights into the transovarial transmission of the symbiont Rickettsia in whiteflies

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w insights into the transovarial transmission of the symbiont Rickettsia in whiteflies 1

1

2*

Hongwei Shan , Yinquan Liu , Junbo Luan & Shusheng Liu 1

1*

Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, 2

Hangzhou 310058, China; College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, China

Received August 2, 2020; accepted August 17, 2020; published online September 30, 2020

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 of Rickettsia in the ovarioles and eggs during oogenesis and embryogenesis in a globally significant pest whitefly Bemisia tabaci. Field populations of the whitefly have a high prevalence of Rickettsia, 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 of Rickettsia was 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 the Rickettsia are 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. Bemisia tabaci, Rickettsia, symbiosis, vertical transmission Citation:

Shan, H., Liu, Y., Luan, J., and Liu, S. (2020). New insights into the transovarial transmission of the symbiont Rickettsia in whiteflies. Sci China Life Sci 63, https://doi.org/10.1007/s11427-020-1801-7

INTRODUCTION Microbial symbioses are widespread in arthropods. The intimate association of microorganisms with their hosts can be mutualistic or commensal, and many obligate symbionts, such as the well-studied Buchnera that provides aphids with essential nutrients, are required for host survival and reproduction (Baumann, 2005; Douglas, 1998). Facultative symbionts may also confer ecologically important traits to hosts (Oliver et al., 2010). Usually, such beneficial symbionts cannot exist in a free-living state, and vertical trans*Corresponding authors (Shusheng Liu, email: [email protected]; Junbo Luan, email: [email protected])

mission is critical to their persistence across host generations (Bright and Bulgheresi, 2010). In some intracellular bacteria, symbionts are strictly located in specialized host cells known as bacterio