Microarray analysis of natural socially regulated plasticity in circadian rhythms of honey bees

Sandra L. Rodriguez-Zas*, Bruce R. Southey, Yair Shemesh, Elad B. Rubin, Mira Cohen, Gene E. Robinson, Guy Bloch

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

45 Scopus citations

Abstract

Honey bee workers care for ("nurse") the brood around the clock without circadian rhythmicity, but then they forage outside with strong circadian rhythms and a consolidated nightly rest. This chronobiological plasticity is associated with variation in the expression of the canonical "clock genes" that regulate the circadian clock: nurse bees show no brain rhythms of expression, while foragers do. These results suggest that the circadian system is organized differently in nurses and foragers. Nurses switch to activity with circadian rhythms shortly after being removed from the hive, suggesting that at least some clock cells in their brain continue to measure time while in the hive. We performed a microarray genome-wide survey to determine general patterns of brain gene expression in nurses and foragers sampled around the clock. We found 160 and 541 transcripts that exhibited significant sinusoidal oscillations in nurses and foragers, respectively, with peaks of expression distributed throughout the day in both task groups. Consistent with earlier studies, transcripts of genes involved in circadian rhythms, including Clockwork Orange that has not been studied before in bees, oscillated in foragers but not in nurses. The oscillating transcripts also were enriched for genes involved in the visual system, "development" and "response to stimuli" (foragers), "muscle contraction" and "microfilament motor gene expression" (nurses), and "generation of precursor metabolites" and "energy" (both). Transcripts of genes encoding P450 enzymes oscillated in both nurses and foragers but with a different phase. This study identified new putative clock-controlled genes in the honey bee and suggests that some brain functions show circadian rhythmicity even in nurse bees that are active around the clock.

Original languageAmerican English
Pages (from-to)12-24
Number of pages13
JournalJournal of Biological Rhythms
Volume27
Issue number1
DOIs
StatePublished - Feb 2012

Bibliographical note

Funding Information:
The authors thank Raphael Nir and Niv Bachanof for assistance with the bees, T. Nguyen for performing microarray analysis, A. Eisenstein for preprocessing the microarray data (“spot finding”), and Zeeshan Fazal for formatting and making the microarray data available in ArrayExpress. This research was supported by the National Institutes of Health (NIH) National Institutes of General Medical Sciences (grant number 1R01GM068946) to S.R.Z. and G.E.R., NIH National Institutes of Drug Abuse (grant numbers R21DA027548 and P30DA018310) to S.R.Z. and B.R.S., respectively, NIH National Cancer Institute (grant number 5R03CA143975) to S.R.Z., National Science Foundation Frontiers in Biological Research grant “BeeSpace” (grant number EF 0425852), the US-Israel Binational Science Foundation (grant numbers 2001-022-2 [to G.B. and G.E.R.] and 2003-151-04 [to G.B.]), and the Israel Science Foundation (grant number 452/_07) to G.B.

Keywords

  • P450
  • clock genes
  • gene expression
  • honey bee
  • social behavior
  • transcriptome

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