Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in <i>Bombus terrestris</i> Queens

Reproductive diapause is an overwintering strategy for <i>Bombus terrestris</i>, which is an important pollinator for agricultural production. However, the precise mechanisms underlying reproductive diapause in bumblebees remain largely unclear. Here, a combination analysis of proteomics...

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Main Authors: Yan Liu, Ruijuan Wang, Long Su, Shan Zhao, Xiaoyan Dai, Hao Chen, Guang’an Wu, Hao Zhou, Li Zheng, Yifan Zhai
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/13/10/862
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author Yan Liu
Ruijuan Wang
Long Su
Shan Zhao
Xiaoyan Dai
Hao Chen
Guang’an Wu
Hao Zhou
Li Zheng
Yifan Zhai
author_facet Yan Liu
Ruijuan Wang
Long Su
Shan Zhao
Xiaoyan Dai
Hao Chen
Guang’an Wu
Hao Zhou
Li Zheng
Yifan Zhai
author_sort Yan Liu
collection DOAJ
description Reproductive diapause is an overwintering strategy for <i>Bombus terrestris</i>, which is an important pollinator for agricultural production. However, the precise mechanisms underlying reproductive diapause in bumblebees remain largely unclear. Here, a combination analysis of proteomics and phosphoproteomics was used to reveal the mechanisms that occur during and after diapause in three different phases: diapause (D), postdiapause (PD), and founder postdiapause (FPD). In total, 4655 proteins and 10,600 phosphorylation sites of 3339 proteins were identified. Diapause termination and reactivation from D to the PD stage were characterized by the upregulation of proteins associated with ribosome assembly and biogenesis, transcription, and translation regulation in combination with the upregulation of phosphoproteins related to neural signal transmission, hormone biosynthesis and secretion, and energy-related metabolism. Moreover, the reproductive program was fully activated from PD to the FPD stage, as indicated by the upregulation of proteins related to fat digestion and absorption, the biosynthesis of unsaturated fatty acids, fatty acid elongation, protein processing in the endoplasmic reticulum, and the upregulation of energy-related metabolism at the phosphoproteome level. We also predicted a kinase–substrate interaction network and constructed protein–protein networks of proteomic and phosphoproteomic data. These results will help to elucidate the mechanisms underlying the regulation of diapause in <i>B. terrestris</i> for year-round mass breeding.
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spelling doaj.art-3c1b74a0febe4cdeabaac971891bd2062023-11-24T00:37:20ZengMDPI AGInsects2075-44502022-09-01131086210.3390/insects13100862Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in <i>Bombus terrestris</i> QueensYan Liu0Ruijuan Wang1Long Su2Shan Zhao3Xiaoyan Dai4Hao Chen5Guang’an Wu6Hao Zhou7Li Zheng8Yifan Zhai9Institute of Plant Protection, Shandong Academy of Agricultural Sciences, 23788 Gongye North Road, Jinan 250100, ChinaInstitute of Plant Protection, Shandong Academy of Agricultural Sciences, 23788 Gongye North Road, Jinan 250100, ChinaInstitute of Plant Protection, Shandong Academy of Agricultural Sciences, 23788 Gongye North Road, Jinan 250100, ChinaInstitute of Plant Protection, Shandong Academy of Agricultural Sciences, 23788 Gongye North Road, Jinan 250100, ChinaInstitute of Plant Protection, Shandong Academy of Agricultural Sciences, 23788 Gongye North Road, Jinan 250100, ChinaInstitute of Plant Protection, Shandong Academy of Agricultural Sciences, 23788 Gongye North Road, Jinan 250100, ChinaKey Laboratory of Natural Enemies Insects, Ministry of Agriculture and Rural Affairs, Jinan 250100, ChinaKey Laboratory of Natural Enemies Insects, Ministry of Agriculture and Rural Affairs, Jinan 250100, ChinaInstitute of Plant Protection, Shandong Academy of Agricultural Sciences, 23788 Gongye North Road, Jinan 250100, ChinaInstitute of Plant Protection, Shandong Academy of Agricultural Sciences, 23788 Gongye North Road, Jinan 250100, ChinaReproductive diapause is an overwintering strategy for <i>Bombus terrestris</i>, which is an important pollinator for agricultural production. However, the precise mechanisms underlying reproductive diapause in bumblebees remain largely unclear. Here, a combination analysis of proteomics and phosphoproteomics was used to reveal the mechanisms that occur during and after diapause in three different phases: diapause (D), postdiapause (PD), and founder postdiapause (FPD). In total, 4655 proteins and 10,600 phosphorylation sites of 3339 proteins were identified. Diapause termination and reactivation from D to the PD stage were characterized by the upregulation of proteins associated with ribosome assembly and biogenesis, transcription, and translation regulation in combination with the upregulation of phosphoproteins related to neural signal transmission, hormone biosynthesis and secretion, and energy-related metabolism. Moreover, the reproductive program was fully activated from PD to the FPD stage, as indicated by the upregulation of proteins related to fat digestion and absorption, the biosynthesis of unsaturated fatty acids, fatty acid elongation, protein processing in the endoplasmic reticulum, and the upregulation of energy-related metabolism at the phosphoproteome level. We also predicted a kinase–substrate interaction network and constructed protein–protein networks of proteomic and phosphoproteomic data. These results will help to elucidate the mechanisms underlying the regulation of diapause in <i>B. terrestris</i> for year-round mass breeding.https://www.mdpi.com/2075-4450/13/10/862<i>Bombus terrestris</i>diapauseTMT quantitative proteomicsTMT quantitative phosphoproteomics
spellingShingle Yan Liu
Ruijuan Wang
Long Su
Shan Zhao
Xiaoyan Dai
Hao Chen
Guang’an Wu
Hao Zhou
Li Zheng
Yifan Zhai
Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in <i>Bombus terrestris</i> Queens
Insects
<i>Bombus terrestris</i>
diapause
TMT quantitative proteomics
TMT quantitative phosphoproteomics
title Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in <i>Bombus terrestris</i> Queens
title_full Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in <i>Bombus terrestris</i> Queens
title_fullStr Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in <i>Bombus terrestris</i> Queens
title_full_unstemmed Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in <i>Bombus terrestris</i> Queens
title_short Integrative Proteomic and Phosphoproteomic Analyses Revealed Complex Mechanisms Underlying Reproductive Diapause in <i>Bombus terrestris</i> Queens
title_sort integrative proteomic and phosphoproteomic analyses revealed complex mechanisms underlying reproductive diapause in i bombus terrestris i queens
topic <i>Bombus terrestris</i>
diapause
TMT quantitative proteomics
TMT quantitative phosphoproteomics
url https://www.mdpi.com/2075-4450/13/10/862
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