Effects of age and nutritional state on the expression of gustatory receptors in the honeybee (Apis mellifera)

PLoS One. 2017 Apr 12;12(4):e0175158. doi: 10.1371/journal.pone.0175158. eCollection 2017.

Abstract

Gustatory receptors (Grs) expressed in insect taste neurons signal the presence of carbohydrates, sugar alcohols, CO2, bitter compounds and oviposition stimulants. The honeybee (Apis mellifera) has one of the smallest Gr gene sets (12 Gr genes) of any insect whose genome has been sequenced. Honeybees live in eusocial colonies with a division of labour and perform age-dependent behavioural tasks, primarily food collection. Here, we used RT-qPCR to quantify Gr mRNA in honeybees at two ages (newly-emerged and foraging-age adults) to examine the relationship between age-related physiology and expression of Gr genes. We measured the Gr mRNAs in the taste organs and also the brain and gut. The mRNA of all Gr genes was detected in all tissues analysed but showed plasticity in relative expression across tissues and in relation to age. Overall, Gr gene expression was higher in the taste organs than in the internal tissues but did not show an overall age-dependent difference. In contrast Gr gene expression in brain was generally higher in foragers, which may indicate greater reliance on internal nutrient sensing. Expression of the candidate sugar receptors AmGr1, AmGr2 and AmGr3 in forager brain was affected by the types of sugars bees fed on. The levels of expression in the brain were greater for AmGr1 but lower for AmGr2 and AmGr3 when bees were fed with glucose and fructose compared with sucrose. Additionally, AmGr3 mRNA was increased in starved bees compared to bees provided ad libitum sucrose. Thus, expression of these Grs in forager brain reflects both the satiety state of the bee (AmGr3) and the type of sugar on which the bee has fed.

MeSH terms

  • Age Factors
  • Aging
  • Animals
  • Bees / genetics
  • Bees / metabolism*
  • Brain / metabolism
  • Diet
  • Gene Expression
  • Insect Proteins / genetics
  • Insect Proteins / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism*

Substances

  • Insect Proteins
  • RNA, Messenger
  • Receptors, G-Protein-Coupled

Grants and funding

This work was supported jointly by the Newcastle University Faculty of Medical Sciences MRes/PhD, http://www.ncl.ac.uk/medicalsciences/ [C0169N3009 scholarship to NKS], the Biotechnology and Biological Sciences Research Council, http://www.bbsrc.ac.uk/ [BB/M00709X/1 to GAW and DF], a Leverhulme Trust research project grant, https://www.leverhulme.ac.uk/ [Grant number RPG-2012-708 to GAW] and a grant from the Biotechnology and Biological Sciences Research Council; Natural Environment Research Council; the Wellcome Trust; Department for Environment, Food and Rural Affairs, and the Scottish Government under the Insect Pollinators Initiative [Grant number BB/I000968/1 to GAW]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.