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Molecular & Cellular Proteomics

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In-depth Proteome of the Hypopharyngeal Glands of Honeybee Workers Reveals Highly Activated Protein and Energy Metabolism in Priming the Secretion of Royal Jelly

Han Hu, Gebreamlak Bezabih, Mao Feng, Qiaohong Wei, Xufeng Zhang, Fan Wu, Lifeng Meng, Yu Fang, Bin Han, Chuan Ma and View ORCID ProfileJianke Li  Correspondence email
Molecular & Cellular Proteomics April 1, 2019, First published on January 7, 2019, 18 (4) 606-621; https://doi.org/10.1074/mcp.RA118.001257
Han Hu
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Gebreamlak Bezabih
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Mao Feng
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Qiaohong Wei
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Xufeng Zhang
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Fan Wu
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Lifeng Meng
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Yu Fang
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Bin Han
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Chuan Ma
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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Jianke Li
From the ‡ Institute of Apicultural Research/Key Laboratory of Pollinating Insect Biology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, No. 1 Beigou Xiangshan, Beijing, 100093, China
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  • ORCID record for Jianke Li
  • For correspondence: apislijk@163.com
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Graphical Abstract

Figure1
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Highlights

  • In-depth proteome underpins the gland ontogeny and age-specific activity of the HGs.

  • The well-developed acini in the HGs of NBs promote the RJ secretary activities.

  • The enhanced protein and energy metabolism in the HGs boost the stronger RJ secretion of RJBs.

Abstract

Royal jelly (RJ) is a secretion of the hypopharyngeal glands (HGs) of honeybee workers. High royal jelly producing bees (RJBs), a stock of honeybees selected from Italian bees (ITBs), have developed a stronger ability to produce RJ than ITBs. However, the mechanism underpinning the high RJ-producing performance in RJBs is still poorly understood. We have comprehensively characterized and compared the proteome across the life span of worker bees between the ITBs and RJBs. Our data uncover distinct molecular landscapes that regulate the gland ontogeny and activity corresponding with age-specific tasks. Nurse bees (NBs) have a well-developed acini morphology and cytoskeleton of secretory cells in HGs to prime the gland activities of RJ secretion. In RJB NBs, pathways involved in protein synthesis and energy metabolism are functionally induced to cement the enhanced RJ secretion compared with ITBs. In behavior-manipulated RJB NBs, the strongly expressed proteins implicated in protein synthesis and energy metabolism further demonstrate their critical roles in the regulation of RJ secretion. Our findings provide a novel understanding of the mechanism consolidating the high RJ-output in RJBs.

  • Protein Identification*
  • Protein Synthesis*
  • Ribosomes*
  • Molecular biology*
  • Energy metabolism

Footnotes

  • Author contributions: H.H. and J.L. designed research; H.H., M.F., Q.W., Y.F., and C.M. performed research; H.H., G.B., and L.M. analyzed data; H.H., G.B., and B.H. wrote the paper; X.Z., F.W., and L.M. contributed new reagents/analytic tools.

  • ↵* This work is supported by the Agricultural Science and Technology Innovation Program (CAAS-ASTIP-2015-IAR), and the earmarked fund for Modern Agro-Industry Technology Research System (CARS-44) in China.

  • ↵Embedded Image This article contains supplemental material.

  • Received December 12, 2018.
  • © 2019 Hu et al.

Published by The American Society for Biochemistry and Molecular Biology, Inc.

Author's Choice—Final version open access under the terms of the Creative Commons CC-BY license.

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In-depth Proteome of the Hypopharyngeal Glands of Honeybee Workers Reveals Highly Activated Protein and Energy Metabolism in Priming the Secretion of Royal Jelly
Han Hu, Gebreamlak Bezabih, Mao Feng, Qiaohong Wei, Xufeng Zhang, Fan Wu, Lifeng Meng, Yu Fang, Bin Han, Chuan Ma, Jianke Li
Molecular & Cellular Proteomics April 1, 2019, First published on January 7, 2019, 18 (4) 606-621; DOI: 10.1074/mcp.RA118.001257

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In-depth Proteome of the Hypopharyngeal Glands of Honeybee Workers Reveals Highly Activated Protein and Energy Metabolism in Priming the Secretion of Royal Jelly
Han Hu, Gebreamlak Bezabih, Mao Feng, Qiaohong Wei, Xufeng Zhang, Fan Wu, Lifeng Meng, Yu Fang, Bin Han, Chuan Ma, Jianke Li
Molecular & Cellular Proteomics April 1, 2019, First published on January 7, 2019, 18 (4) 606-621; DOI: 10.1074/mcp.RA118.001257
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Molecular & Cellular Proteomics: 18 (4)
Molecular & Cellular Proteomics
Vol. 18, Issue 4
1 Apr 2019
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