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Title: Transcriptional and physiological responses of hypopharyngeal glands in honey bees (Apis mellifera L.) infected by Nosema ceranae

Author
item LI, ZHIGUO - Fujian Agriculture And Forest University
item HE, JINGFANG - Fujian Agriculture And Forest University
item YU, TIANTIAN - Fujian Agriculture And Forest University
item Chen, Yanping - Judy
item HUANG, WEI-FONG - Fujian Agriculture And Forest University
item HUANG, JINGNAN - Fujian Agriculture And Forest University
item ZHAO, YAZHOU - Chinese Academy Of Agricultural Sciences
item NIE, HONGYI - Fujian Agriculture And Forest University
item SU, SONGKUN - Fujian Agriculture And Forest University

Submitted to: Apidologie
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/12/2018
Publication Date: 1/15/2019
Citation: Li, Z., He, J., Yu, T., Chen, Y., Huang, W., Huang, J., Zhao, Y., Nie, H., Su, S. 2019. Transcriptional and physiological responses of hypopharyngeal glands in honey bees (Apis mellifera L.) infected by Nosema ceranae. Apidologie. 50(1):51-62. https://doi.org/10.1007/s13592-018-0617-8.
DOI: https://doi.org/10.1007/s13592-018-0617-8

Interpretive Summary: Honey bee Nosema disease caused by Nosema ceranae, a fungal parasite of adult honey bees, has been associated with bee colony declines worldwide. N. ceranae infection adversely affects honey bee health in multiple ways, including weakening the immune system, imposing energetic stress, and decreasing the performance and lifespan of adult bees. We conducted a study to investigate the effects of N. ceranae infection on the structure and function of hypopharyngeal glands (HPGs) which are located in the head of the nurse bees and produce royal jelly to feed larvae and queen. Our results showed that N. ceranae infection resulted in a significant decrease in total protein level and enzyme activity in HPGs, implying nutritional dysfunction and energetic stress in infected bees. These results from this study provide novel insights into the mechanisms underlying Nosema disease progression and in turn will have the potential to contribute to the improvement of bee disease management programs. The results should be of interest to the researchers, graduate students, apiary inspectors, beekeepers and policymakers in the bee society worldwide.

Technical Abstract: Nosema ceranae is an intestinal intracellular pathogen of honey bees. Since its emergence as a virulent pathogen of the European honey bee A. mellifera, N. ceranae infection has often implicated in colony declines worldwide and poses a severe threat to the health and well-being of its new host. Growing evidence has shown that N. ceranae infection affects the structure and function of hypopharyngeal gland (HPGs) which is well developed in the nurse bee and synthesizes major components of royal jelly supplied to all larvae and queen. Thus, physiological changes of HPGs can have a strong negative effect on brood rearing and colony growth. Although extensive studies have been conducted on nutritional, physiological and behavioral changes in Nosema-infected honey bee, little is known about the transcriptional changes in the HPGs of honey bees infected with N. ceranae. The present study investigated the effects of N. ceranae infection on the gene expression, protein contents, and enzyme activities in the HPGs of nurse workers. The results showed that there were 285 differential expressed genes consisting of 279 upregulated genes and 6 down-regulated genes in response to the N. ceranae infection. The results also showed that N. ceranae infection resulted in a decreased total protein level in HPGs, implying protein dysmetabolism and energetic stress in infected bees. In contrast to a decreased level of total protein expression, the activities of hydrolysis enzymes including amylase, glucose oxidase and a-glucosidase that are expressed specifically in the HPGs of forager bees for processing nectar into honey were found to be increased in N. ceranae infected bee. Further, the elevated enzymic activities were found to accompany by an increased expressed level of hemolymph juvenile hormone-binding protein-encoding gene and neuropeptide-encoding genes in N. ceranae infected bees, suggesting a high probability of Nosema-infected nurse workers to engage in behaviors that are normally performed by foragers. These results from this study provide novel insights into the mechanisms underlying Nosema pathogenesis and in turn will have the potential to make the contribution to the improvement of honey bee disease management programs.