Molecular basis of fatty acid taste in Drosophila.

Ji-Eun Ahn,Yan Chen,Hubert Amrein

doi:10.7554/elife.30115

Abstract

Behavioral studies have established that Drosophila appetitive taste responses towards fatty acids are mediated by sweet sensing Gustatory Receptor Neurons (GRNs). Here we show that sweet GRN activation requires the function of the Ionotropic Receptor genes IR25a, IR76b and IR56d. The former two IR genes are expressed in several neurons per sensillum, while IR56d expression is restricted to sweet GRNs. Importantly, loss of appetitive behavioral responses to fatty acids in IR25a and IR76b mutant flies can be completely rescued by expression of respective transgenes in sweet GRNs. Interestingly, appetitive behavioral responses of wild type flies to hexanoic acid reach a plateau at ~1%, but decrease with higher concentration, a property mediated through IR25a/IR76b independent activation of bitter GRNs. With our previous report on sour taste, our studies suggest that IR-based receptors mediate different taste qualities through cell-type specific IR subunits.

Highlights

Detection of food compounds plays a critical role in feeding behavior
Using Ca2+ imaging, we report that tarsal sweet Gustatory Receptor Neurons (GRNs) are activated by fatty acids, and we show that IR25a and IR76b are expressed in numerous GRNs, including sweet GRNs, where they are required for their activation by fatty acids, but not by sugars
The notion that sweet GRNs are exclusively tuned to sugar has recently been challenged, as it was shown that flies exhibit sweet GRN -dependent appetitive behavioral responses to fatty acids (Masek and Keene, 2013)

Summary

Introduction

Detection of food compounds plays a critical role in feeding behavior. Likewise, the ability to avoid harmful chemicals is essential to navigate the evaluation of suboptimal food sources that might contain toxins or are contaminated with microorganism producing harmful chemicals. Receptors for sugars, amino acids and fatty acids have been identified in mammals (Cartoni et al, 2010; Galindo et al, 2012; Max et al, 2001; Montmayeur et al, 2001; Nelson et al, 2001; Zhao et al, 2003), and other vertebrates (Ishimaru et al, 2005), albeit in some, receptor types for certain nutritious chemicals have been lost (Baldwin et al, 2014; Jiang et al, 2012; Jin et al, 2011; Lagerstrom et al, 2006; Zhao et al, 2012) In mice, these various types of receptors are expressed in distinct populations of taste cells located mainly in taste buds on the tongue. We found that hexanoic acid activates bitter GRNs, albeit in an IR25a/IR76b independent manner, suggesting that bitter and sweet GRN activation modulate feeding response to this ligand Consistent with this hypothesis, inhibition of neural transmission of sweet GRNs abolishes PER responses completely, while the same manipulation of bitter GRNs results in further increase in PER responses to hexanoic acid. These observations suggest a model in which activation of bitter GRNs counteract the activation of sweet GRNs to suppress feeding responses to hexanoic acid, possibly to moderate intake of this nutrient compound

Results

Discussion

Materials and methods

Funding Funder National Institutes of Health