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

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.

Differential expression of a fructose receptor gene in honey bee workers according to age and behavioral role

“…AmGr1 is expressed in the antennae of foragers, and functions as a gustatory receptor for certain kinds of sugar other than fructose; AmGr2 acts as a coreceptor with AmGr1 (Jung et al., ). Recently, three candidate sugar receptors , AmGr1 , AmGr2 , and AmGr3 , were shown to be the most expressed of all 10 Gr genes in the gustatory organs, brains, and guts of both foragers and newly emerged bees (Simcock, Wakeling, Ford, & Wright, ). Given that antennae allow honey bees to recognize sugars suitable for food, and that AmGr1 is expressed in the antennae, it is likely that Gr accurately transmit external signals into the sensory neurons.…”

“…Fructose receptor genes have been identified in several insects to date, including Drosophila melanogaster , Bombyx mori , and Helicover armigera (Jiang et al., ; Miyamoto, Slone, Song, & Amrein, ; Sato, Tanaka, & Touhara, ). The fructose receptor identified in D. melanogaster , Gr43 ( DmGr43 ), comprises a clade with a single lineage that is phylogenetically distinct from those of other sugar receptors and from those of bitter and CO 2 receptors (Kikuta et al., ; Park et al., ; Simcock et al., ; Smadja, Shi, Butlin, & Robertson, ). In B. mori , Gr43 ‐like receptor genes such as BmGr9 respond to fructose (Sato et al., ), whereas a paralogous gene, BmGr10 , responds to myo ‐inositol and epi ‐inositol, rather than to fructose or other carbohydrates (Kikuta et al., ).…”

“…In B. mori , Gr43 ‐like receptor genes such as BmGr9 respond to fructose (Sato et al., ), whereas a paralogous gene, BmGr10 , responds to myo ‐inositol and epi ‐inositol, rather than to fructose or other carbohydrates (Kikuta et al., ). Phylogenetic analyses predict that AmGr3 in the honey bee may function as a Gr43 ‐like fructose receptor (Park et al., ; Robertson & Wanner, ; Simcock et al., ); however, it is impossible to identify the characteristics of AmGr3 based on the alignment of amino acid residues alone, and the prediction remains to be tested with biochemical evidence. Thus, although AmGr3 is considered a prime candidate as the gene governing fructose recognition in honey bees, it remains possible that AmGr3 responds to saccharides other than fructose.…”

“…Therefore, we hypothesized that antennae are involved in gustation in nurse bees, in which case Gr , perhaps including AmGr3 , should be strongly expressed in these tissues. Based on evidence that Gr gene expression varies during development (Simcock et al., ), we hypothesized that the expression of Gr genes related to sugar recognition changes depending on the tasks a worker performs. We examined Gr gene expression in age‐dependent divisions of workers using quantitative Reverse transcription‐PCR (qRT‐PCR).…”

CRISPR/Cas9 mediated mutations as a new tool for studying taste in honeybees

“…In contrast to many other insects such as the 35 fruit fly (Drosophila melanogaster) with 68 genes and mosquitoes (Anopheles gambiae) with 75 genes, 36 the genome of the honeybee comprises only ten genes coding for gustatory receptors (Grs) [4]. Among 37 these only three code for sugar receptors: AmGr1, AmGr2 and AmGr3 [4] [8]. The taste receptors are 38 expressed in the brain, the antennae, mouthparts, tarsi and the gut of the honeybee.…”