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Transcriptional and physiological responses of hypopharyngeal glands in honeybees (Apis mellifera L.) infected by Nosema ceranae

  • Zhiguo Li
  • Jingfang He
  • Tiantian Yu
  • Yanping Chen
  • Wei-Fone Huang
  • Jingnan Huang
  • Yazhou Zhao
  • Hongyi Nie
  • Songkun SuEmail author
Original article


Nosema ceranae infection induces energetic stress, malnutrition, and precocious foraging in Apis mellifera. This study investigated effects of N. ceranae infection on the gene expression, protein content, and enzyme activity in the hypopharyngeal gland of nurse bees. The 285 differentially expressed genes were found between N. ceranae-infected and control bees using RNA-Seq, and 279 were upregulated and 6 were downregulated in infected bees. The protein level was significantly lower in infected bees than in controls, implying protein dysmetabolism and energetic stress in infected bees. The ELISA test showed that the specific activity of amylase was significantly higher in infected bees than in controls. The elevated enzymic activities were accompanied by an increased expressed level of hemolymph juvenile hormone-binding protein-encoding gene in infected bees, suggesting the possibility of Nosema-infected nurse bees to engage in behaviors that are normally performed by foragers.


honeybees Nosema ceranae hypopharyngeal gland differentially expressed genes physiological responses 


Authors’ contribution

ZGL, JFH, and SKS conceived this research and designed experiments; ZGL, WFH, and HYN participated in the design and interpretation of the data; JFH, TTY, and JNH performed experiments and analysis; ZGL, YPC, SKS, and YZZ wrote the paper and participated in the revisions of it. All authors read and approved the final manuscript.

Funding information

This research was supported by the earmarked fund for Modern Agro-Industry Technology Research System (No. CARS-45-KXJ3) and Fujian Agriculture and Forestry University Foundation for Outstanding Youth (XJQ201606).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Bee SciencesFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Bee Research LaboratoryUSDA-ARSBeltsvilleUSA
  3. 3.Institute of Apiculture ResearchChinese Academy of Agricultural SciencesBeijingChina

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