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Posterior concentration of Wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of Wolbachia in host Trichogramma wasps

INTRODUCTION: The bacterial endosymbiont, Wolbachia spp. induce thelytokous parthenogenesis in certain parasitoid wasps, such as the egg parasitoid wasps Trichogramma spp. To complete the cycle of vertical transmission, Wolbachia displays efficient transovarial transmission by targeting the reproduc...

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Autores principales: Zhou, Jin-Cheng, Dong, Qian-Jin, Shang, Dan, Ning, Su-Fang, Zhang, Huan-Huan, Wang, Ying, Che, Wu-Nan, Dong, Hui, Zhang, Li-Sheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10324615/
https://www.ncbi.nlm.nih.gov/pubmed/37424778
http://dx.doi.org/10.3389/fcimb.2023.1198428
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author Zhou, Jin-Cheng
Dong, Qian-Jin
Shang, Dan
Ning, Su-Fang
Zhang, Huan-Huan
Wang, Ying
Che, Wu-Nan
Dong, Hui
Zhang, Li-Sheng
author_facet Zhou, Jin-Cheng
Dong, Qian-Jin
Shang, Dan
Ning, Su-Fang
Zhang, Huan-Huan
Wang, Ying
Che, Wu-Nan
Dong, Hui
Zhang, Li-Sheng
author_sort Zhou, Jin-Cheng
collection PubMed
description INTRODUCTION: The bacterial endosymbiont, Wolbachia spp. induce thelytokous parthenogenesis in certain parasitoid wasps, such as the egg parasitoid wasps Trichogramma spp. To complete the cycle of vertical transmission, Wolbachia displays efficient transovarial transmission by targeting the reproductive tissues and often exhibits strong tissue-specific tropism in their host. METHOD: The present study aimed to describe the basic Wolbachia distribution patterns that occur during the development of Wolbachia-infected, thelytokous Trichogramma dendrolimi, and T. pretiosum. We used fluorescence in situ hybridization (FISH) to investigate Wolbachia signal dynamics during early embryogenesis (from 30 to 120 min). Wolbachia titers and distributions from the embryo to adult stages of Trichogramma after early embryogenesis were detected by absolute quantitative polymerase chain reaction (AQ-PCR) and FISH. The symmetry ratios (SR) of the Wolbachia signals were calculated using the SR odds ratios in the anterior and posterior parts of the host. The SR was determined to describe Wolbachia tropism during early embryogenesis and various developmental stages of Trichogramma. RESULTS: Wolbachia was concentrated in the posterior part of the embryo during early embryogenesis and the various developmental stages of both T. dendrolimi and T. pretiosum. Wolbachia density increased with the number of nuclei and the initial mitotic division frequency during early embryogenesis. The total Wolbachia titer increased with postembryogenesis development in both T. dendrolimi and T. pretiosum. However, the Wolbachia densities relative to body size were significantly lower at the adult and pupal stages than they were at the embryonic stage. DISCUSSION: The present work revealed that posterior Wolbachia concentration during early host embryogenesis determined Wolbachia localization in adult wasps. By this mechanism, Wolbachia exhibits efficient vertical transmission across generations by depositing only female Wolbachia-infected offspring. The results of this study describe the dynamics of Wolbachia during the development of their Trichogramma host. The findings of this investigation helped clarify Wolbachia tropism in Trichogramma wasps.
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spelling pubmed-103246152023-07-07 Posterior concentration of Wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of Wolbachia in host Trichogramma wasps Zhou, Jin-Cheng Dong, Qian-Jin Shang, Dan Ning, Su-Fang Zhang, Huan-Huan Wang, Ying Che, Wu-Nan Dong, Hui Zhang, Li-Sheng Front Cell Infect Microbiol Cellular and Infection Microbiology INTRODUCTION: The bacterial endosymbiont, Wolbachia spp. induce thelytokous parthenogenesis in certain parasitoid wasps, such as the egg parasitoid wasps Trichogramma spp. To complete the cycle of vertical transmission, Wolbachia displays efficient transovarial transmission by targeting the reproductive tissues and often exhibits strong tissue-specific tropism in their host. METHOD: The present study aimed to describe the basic Wolbachia distribution patterns that occur during the development of Wolbachia-infected, thelytokous Trichogramma dendrolimi, and T. pretiosum. We used fluorescence in situ hybridization (FISH) to investigate Wolbachia signal dynamics during early embryogenesis (from 30 to 120 min). Wolbachia titers and distributions from the embryo to adult stages of Trichogramma after early embryogenesis were detected by absolute quantitative polymerase chain reaction (AQ-PCR) and FISH. The symmetry ratios (SR) of the Wolbachia signals were calculated using the SR odds ratios in the anterior and posterior parts of the host. The SR was determined to describe Wolbachia tropism during early embryogenesis and various developmental stages of Trichogramma. RESULTS: Wolbachia was concentrated in the posterior part of the embryo during early embryogenesis and the various developmental stages of both T. dendrolimi and T. pretiosum. Wolbachia density increased with the number of nuclei and the initial mitotic division frequency during early embryogenesis. The total Wolbachia titer increased with postembryogenesis development in both T. dendrolimi and T. pretiosum. However, the Wolbachia densities relative to body size were significantly lower at the adult and pupal stages than they were at the embryonic stage. DISCUSSION: The present work revealed that posterior Wolbachia concentration during early host embryogenesis determined Wolbachia localization in adult wasps. By this mechanism, Wolbachia exhibits efficient vertical transmission across generations by depositing only female Wolbachia-infected offspring. The results of this study describe the dynamics of Wolbachia during the development of their Trichogramma host. The findings of this investigation helped clarify Wolbachia tropism in Trichogramma wasps. Frontiers Media S.A. 2023-06-22 /pmc/articles/PMC10324615/ /pubmed/37424778 http://dx.doi.org/10.3389/fcimb.2023.1198428 Text en Copyright © 2023 Zhou, Dong, Shang, Ning, Zhang, Wang, Che, Dong and Zhang https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Zhou, Jin-Cheng
Dong, Qian-Jin
Shang, Dan
Ning, Su-Fang
Zhang, Huan-Huan
Wang, Ying
Che, Wu-Nan
Dong, Hui
Zhang, Li-Sheng
Posterior concentration of Wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of Wolbachia in host Trichogramma wasps
title Posterior concentration of Wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of Wolbachia in host Trichogramma wasps
title_full Posterior concentration of Wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of Wolbachia in host Trichogramma wasps
title_fullStr Posterior concentration of Wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of Wolbachia in host Trichogramma wasps
title_full_unstemmed Posterior concentration of Wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of Wolbachia in host Trichogramma wasps
title_short Posterior concentration of Wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of Wolbachia in host Trichogramma wasps
title_sort posterior concentration of wolbachia during the early embryogenesis of the host dynamically shapes the tissue tropism of wolbachia in host trichogramma wasps
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10324615/
https://www.ncbi.nlm.nih.gov/pubmed/37424778
http://dx.doi.org/10.3389/fcimb.2023.1198428
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