Circadian clock genes are differentially modulated during the daily cycles and chronological age in the social honeybee (Apis mellifera)
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The circadian clock is an advantageous adaptive system that enables organisms to predict and anticipate the daily environmental changes. The circadian rhythms are generated molecularly through the expression of clock genes, based on autoregulatory feedback loops. Honeybees are an excellent model to investigate how the circadian rhythms are modulated accordingly to the social context, behavioral plasticity, and task-related activities. Here, we show how the clock genes behave during the daily cycles in adult worker heads of Apis mellifera. Our results point to the clock genes period and cryptochrome as essential regulators of the circadian rhythms associated to the behavioral maturation in this social insect. We also identified putative miRNA-target and protein-protein interactions involving honeybee clock genes, indicating regulatory networks behind the adjustment of the molecular clock.
Keywordscircadian clock clock genes circadian rhythms honeybees miRNAs
FAPESP, Process Nº 2014/14194-4.
All authors have contributed equally to the work: Fabiano C.P. Abreu and Zilá L.P. Simões elaborated the idea of this work, experimental procedures were performed by Fabiano C. P. Abreu, and Flavia C.P. Freitas performed the computational analyses.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Dunlap, J., Loros, J., DeCoursey, P. (2004) Chronobiology: biological timekeeping. Sunderland: Sinauer AssociatesGoogle Scholar
- Elsik, C. G., Worley, K. C., Bennett, A. K., Beye, M., Camara, F., Childers, C. P., … & Elhaik, E. (2014). Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC genomics, 15(1), 86Google Scholar
- Fuchikawa, T., Beer, K., Linke-Winnebeck, C., Ben-David, R., Kotowoy, A., Tsang, V. W. K., Warman, G. R., Winnebeck, E. C., Helfrich-Foster, C., Bloch, G. (2017) Neuronal circadian clock protein oscillations are similar in behaviourally rhythmic forager honeybees and in arrhythmic nurses. Open Biol. 7: 170047Google Scholar
- Gu, H., Xiao, J., Niu, L., Wang, B., Ma, G., Dunn, D. W., Huang, D. (2014) Adaptive evolution of the circadian gene timeout in insects. Sci. Rep. 4: 4212Google Scholar
- Macedo, L. M., Nunes, F. M., Freitas, F. C., Pires, C. V., Tanaka, E. D., Martins, J. R., Piulachs, M. D., Cristino, A. S., Pinheiro, D. G., Simões, Z. L. (2016) MicroRNA signatures characterizing caste-independent ovarian activity in queen and worker honeybees (Apis mellifera L.). Insect Mol Biol. 25: 216–226.CrossRefPubMedGoogle Scholar
- Reddy, K. L., Wohlwill, A., Katzen, A., Dzitoeva, S., Lin, M., Holbrook, S., Storti, R.V. (2000) The Drosophila PAR Domain Protein 1 (Pdp1) gene encodes multiple differentially expressed mRNAs and proteins through the use of multiple enhancers and promoters. Dev. Biol. 224, 401–414.Google Scholar
- Rubin, E. B., Shemesh, Y., Cohen, M., Elgavish, S., Robertson, H. M., Bloch, G. (2006) Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Gen. Res. 16:1352–1365CrossRefGoogle Scholar
- Saunders, D. S. (2002). Insect clocks. Amsterdam: Elsevier.Google Scholar
- Woźnicka, O., Görlich, A., Sigrist, S., Pyza, E. (2015) BRP-170 and BRP190 isoforms of Bruchpilot protein differentially contribute to the frequency of synapses and synaptic circadian plasticity in the visual system of Drosophila. Front. Cell. Neurosc. 9: 238Google Scholar
- Xing, W., Busino, L., Hinds, T. R., Marionni, S. T., Saifee, N. H., Bush, M. F., … & Zheng, N. (2013). SCFFBXL3 ubiquitin ligase targets cryptochromes at their cofactor pocket. Nature, 496 (7443), 64–68Google Scholar
- Yoo, S. H., Mohawk, J. A., Siepka, S. M., Shan, Y., Huh, S. K., Hong, H. K., … & Nussbaum, J. (2013). Competing E3 ubiquitin ligases govern circadian periodicity by degradation of CRY in nucleus and cytoplasm. Cell, 152 (5), 1091–1105.Google Scholar