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Insect Bacterial Symbiont-Mediated Vitellogenin Uptake into Oocytes To Support Egg Development

Many insect species, such as aphids, leafhoppers, planthoppers, and whiteflies harbor obligate bacterial symbionts that can be transovarially transmitted to offspring through the oocytes of female insects. Whether obligate bacterial symbionts can carry important molecules/resources to the embryos to...

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Autores principales: Mao, Qianzhuo, Wu, Wei, Huang, Lingzhi, Yi, Ge, Jia, Dongsheng, Chen, Qian, Chen, Hongyan, Wei, Taiyun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7667026/
https://www.ncbi.nlm.nih.gov/pubmed/33172995
http://dx.doi.org/10.1128/mBio.01142-20
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author Mao, Qianzhuo
Wu, Wei
Huang, Lingzhi
Yi, Ge
Jia, Dongsheng
Chen, Qian
Chen, Hongyan
Wei, Taiyun
author_facet Mao, Qianzhuo
Wu, Wei
Huang, Lingzhi
Yi, Ge
Jia, Dongsheng
Chen, Qian
Chen, Hongyan
Wei, Taiyun
author_sort Mao, Qianzhuo
collection PubMed
description Many insect species, such as aphids, leafhoppers, planthoppers, and whiteflies harbor obligate bacterial symbionts that can be transovarially transmitted to offspring through the oocytes of female insects. Whether obligate bacterial symbionts can carry important molecules/resources to the embryos to support egg development is still unknown. Here, we show that the vitellogenin (Vg) precursor of rice leafhopper Nephotettix cincticeps is biosynthesized by the fat body, secreted into the hemolymph and subsequently cleaved into the 35- and 178-kDa subunits, whereas only the 178-kDa subunit is taken up by the leading end of oocytes in a receptor-dependent manner or moves into the posterior pole of the terminal oocyte in association with obligate bacterial symbiont “Candidatus Nasuia deltocephalinicola” (hereafter Nasuia) in a receptor-independent manner. Furthermore, the 178-kDa Vg subunit can directly interact with a surface channel molecule (porin) on the envelope of Nasuia, allowing Vg to enter bacterial cytoplasm. Thus, Vg can hitchhike the ancient oocyte entry path of Nasuia, the common obligate symbiont of leafhoppers. Knocking down a Nasuia growth-related protein expression or treatment with porin antibody strongly prevents the ability of Nasuia to carry Vgs into oocytes and impair insect egg development. Nasuia-carried Vgs provide at least 20% of the total Vgs in the developing eggs. We anticipate that the bacterial symbiont-mediated Vg uptake into oocytes to support efficient egg development may be a common pattern shared by many insects.
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spelling pubmed-76670262020-11-17 Insect Bacterial Symbiont-Mediated Vitellogenin Uptake into Oocytes To Support Egg Development Mao, Qianzhuo Wu, Wei Huang, Lingzhi Yi, Ge Jia, Dongsheng Chen, Qian Chen, Hongyan Wei, Taiyun mBio Research Article Many insect species, such as aphids, leafhoppers, planthoppers, and whiteflies harbor obligate bacterial symbionts that can be transovarially transmitted to offspring through the oocytes of female insects. Whether obligate bacterial symbionts can carry important molecules/resources to the embryos to support egg development is still unknown. Here, we show that the vitellogenin (Vg) precursor of rice leafhopper Nephotettix cincticeps is biosynthesized by the fat body, secreted into the hemolymph and subsequently cleaved into the 35- and 178-kDa subunits, whereas only the 178-kDa subunit is taken up by the leading end of oocytes in a receptor-dependent manner or moves into the posterior pole of the terminal oocyte in association with obligate bacterial symbiont “Candidatus Nasuia deltocephalinicola” (hereafter Nasuia) in a receptor-independent manner. Furthermore, the 178-kDa Vg subunit can directly interact with a surface channel molecule (porin) on the envelope of Nasuia, allowing Vg to enter bacterial cytoplasm. Thus, Vg can hitchhike the ancient oocyte entry path of Nasuia, the common obligate symbiont of leafhoppers. Knocking down a Nasuia growth-related protein expression or treatment with porin antibody strongly prevents the ability of Nasuia to carry Vgs into oocytes and impair insect egg development. Nasuia-carried Vgs provide at least 20% of the total Vgs in the developing eggs. We anticipate that the bacterial symbiont-mediated Vg uptake into oocytes to support efficient egg development may be a common pattern shared by many insects. American Society for Microbiology 2020-11-10 /pmc/articles/PMC7667026/ /pubmed/33172995 http://dx.doi.org/10.1128/mBio.01142-20 Text en Copyright © 2020 Mao et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Mao, Qianzhuo
Wu, Wei
Huang, Lingzhi
Yi, Ge
Jia, Dongsheng
Chen, Qian
Chen, Hongyan
Wei, Taiyun
Insect Bacterial Symbiont-Mediated Vitellogenin Uptake into Oocytes To Support Egg Development
title Insect Bacterial Symbiont-Mediated Vitellogenin Uptake into Oocytes To Support Egg Development
title_full Insect Bacterial Symbiont-Mediated Vitellogenin Uptake into Oocytes To Support Egg Development
title_fullStr Insect Bacterial Symbiont-Mediated Vitellogenin Uptake into Oocytes To Support Egg Development
title_full_unstemmed Insect Bacterial Symbiont-Mediated Vitellogenin Uptake into Oocytes To Support Egg Development
title_short Insect Bacterial Symbiont-Mediated Vitellogenin Uptake into Oocytes To Support Egg Development
title_sort insect bacterial symbiont-mediated vitellogenin uptake into oocytes to support egg development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7667026/
https://www.ncbi.nlm.nih.gov/pubmed/33172995
http://dx.doi.org/10.1128/mBio.01142-20
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