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Front Physiol
2022 Jan 01;13:1089669. doi: 10.3389/fphys.2022.1089669.
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Sugar perception in honeybees.
Değirmenci L
,
Rogé Ferreira FL
,
Vukosavljevic A
,
Heindl C
,
Keller A
,
Geiger D
,
Scheiner R
.
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Honeybees (Apis mellifera) need their fine sense of taste to evaluate nectar and pollen sources. Gustatory receptors (Grs) translate taste signals into electrical responses. In vivo experiments have demonstrated collective responses of the whole Gr-set. We here disentangle the contributions of all three honeybee sugar receptors (AmGr1-3), combining CRISPR/Cas9 mediated genetic knock-out, electrophysiology and behaviour. We show an expanded sugar spectrum of the AmGr1 receptor. Mutants lacking AmGr1 have a reduced response to sucrose and glucose but not to fructose. AmGr2 solely acts as co-receptor of AmGr1 but not of AmGr3, as we show by electrophysiology and using bimolecular fluorescence complementation. Our results show for the first time that AmGr2 is indeed a functional receptor on its own. Intriguingly, AmGr2 mutants still display a wildtype-like sugar taste. AmGr3 is a specific fructose receptor and is not modulated by a co-receptor. Eliminating AmGr3 while preserving AmGr1 and AmGr2 abolishes the perception of fructose but not of sucrose. Our comprehensive study on the functions of AmGr1, AmGr2 and AmGr3 in honeybees is the first to combine investigations on sugar perception at the receptor level and simultaneously in vivo. We show that honeybees rely on two gustatory receptors to sense all relevant sugars.
Figure S1: Representative TEVC recordings of sugar-induced currents derived from Xenopus oocytes expressing different Gr-ensembles. The gustatory receptors AmGr1-3 have been transiently expressed in Xenopus oocytes either alone or in different Gr combinations. Oocytes were clamped at a holding membrane potential of -80 mV and tested for sugar response to sucrose (Suc), glucose (Gluc), fructose (Fruc), maltose (Malt), arabinose (Arab), mannose (Mann), galactose (Galac), raffinose (Raffi) and melezitose (Mele) (160 mM each; perfusion indicated by bars). For quantification of sugar specificities, sugar-induced steady-state currents (ISS) were recorded at a membrane potential of -140 mV and normalized to the currents in either sucrose (A, C, D and F) or fructose (B and E) solution (bar diagrams). A AmGr1 (mean of n = 16 oocytes ± SD); B AmGr3 (mean of n = 8 oocytes ± SD); C AmGr1 and AmGr2 co-expression (mean of n = 13 oocytes ± SD); D AmGr1 and AmGr3 co-expression (mean of n = 13 oocytes ± SD); E AmGr2 and AmGr3 co-expression (mean of n = 9 oocytes ± SD); F AmGr1, AmGr2 and AmGr3 co-expression (mean of n = 10 oocytes ± SD); G AmGr2, Inset: magnification of the current trace of AmGr2-expressing oocyte for sucrose, glucose and fructose application.
Figure S3: Fluorescence-based studies of Xenopus oocytes expressing YFP-tagged AmGr1-3 constructs. Schematic models of YFP-tagged AmGrs and AmGrs tagged with YFP halves for BiFC experiments (A and B, upper panels); Pictures show a quarter of an optical slice of an oocyte, representing an overlay of brightfield and detection of fluorescence (depicted in yellow). Images were taken with a confocal laser scanning microscope (A and B, lower panels). (A) Representative images of AmGr1 3 tagged with YFP to the N-terminus (YFP::AmGr1; YFP::AmGr2; YFP::AmGr3) transiently expressed in Xenopus oocytes. (B) Interaction studies of AmGr1 and AmGr2 by bimolecular fluorescence complementation (BiFC). N- and C-terminal YFP halves fused to either AmGr1 or AmGr2 subunits complemented YFP fluorescence when co-expressed in oocytes, indicating physical interaction, i.e. via homomerization of AmGr1 subunits (YFPN::AmGr1 + YFPC::AmGr1) or AmGr2 subunits (YFPN::AmGr2 + YFPC::AmGr2). When corresponding YFP halves were fused to AmGr1 and AmGr2 (YFPN::AmGr1 + YFPC::AmGr2 / YFPN::AmGr2 + YFPC::AmGr1) co-expression in oocytes led to yellow fluorescence (YFP complementation), indicating physical interaction of AmGr1 and AmGr2 subunits that assemble to heterotetrameric receptors. N-terminal YFP half fused to AmGr1, co-expressed with C-terminal YFP half fused to AmGr3 (YFPN::AmGr1 + YFPC::AmGr3), yields no fluorescence, suggesting that heteromer formation does not occur. When corresponding YFP halves fused to AmGr2 and AmGr3 (YFPN::AmGr2 + YFPC::AmGr3) are co-expressed, fluorescence signals can be detected, indicative of heteromerization. (Scale bar = 200 µm)
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