Elsevier

Food Quality and Preference

Volume 30, Issue 2, December 2013, Pages 202-216
Food Quality and Preference

Do polymorphisms in chemosensory genes matter for human ingestive behavior?

https://doi.org/10.1016/j.foodqual.2013.05.013Get rights and content

Highlights

  • Genetic variation in chemosensation is more common than previously thought.

  • This variation is known to alter sensations from and preference for food.

  • Recent data suggests these differences extend beyond taste to include odor and touch.

  • We summarize current knowledge, emphasizing human behavioral data.

Abstract

In the last decade, basic research in chemoreceptor genetics and neurobiology has revolutionized our understanding of individual differences in chemosensation. From an evolutionary perspective, chemosensory variations appear to have arisen in response to different living environments, generally in the avoidance of toxins and to better detect vital food sources. Today, it is often assumed that these differences may drive variable food preferences and choices, with downstream effects on health and wellness. A growing body of evidence indicates chemosensory variation is far more complex than previously believed. However, just because a genetic polymorphism results in altered receptor function in cultured cells or even behavioral phenotypes in the laboratory, this variation may not be sufficient to influence food choice in free living humans. Still, there is ample evidence to indicate allelic variation in TAS2R38 predicts variation in bitterness of synthetic pharmaceuticals (e.g., propylthiouracil) and natural plant compounds (e.g., goitrin), and this variation associates with differential intake of alcohol and vegetables. Further, this is only one of 25 unique bitter taste genes (TAS2Rs) in humans, and emerging evidence suggests other TAS2Rs may also contain polymorphisms that are functional with respect to ingestive behavior. For example, TAS2R16 polymorphisms are linked to the bitterness of naturally occurring plant compounds and alcoholic beverage intake, a TAS2R19 polymorphism associates with differences in quinine bitterness and grapefruit bitterness and liking, and TAS2R31 polymorphisms associate with differential bitterness of plant compounds like aristolochic acid and the sulfonyl amide sweeteners saccharin and acesulfame-K. More critically with respect to food choices, these polymorphisms may vary independently from each other within and across individuals, meaning a monolithic one-size-fits-all approach to bitterness needs to be abandoned. Nor are genetic differences restricted to bitterness. Perceptual variation has also been associated with polymorphisms in genes involved in odors associated with meat defects (boar taint), green/grassy notes, and cilantro, as well as umami and sweet tastes (TAS1R1/2/3). Here, a short primer on receptor genetics is provided, followed by a summary of current knowledge, and implications for human ingestive behavior are discussed.

Introduction

The term ‘taste’ is often used by the public to describe flavor, the integrated sensation arising from the combination of input from the taste, olfactory and somatosensory systems (Delwiche, 2004, Mattes, 2009). ‘Taste’ in this colloquial sense is reported by consumers as the greatest factor in food purchase decisions (IFIC, 2012). While ‘price’ and ‘healthfulness’ have grown in their influence in recent year, as of 2012, ‘taste’ remains the top consideration in purchase decisions (IFIC, 2012). A substantial body of evidence indicates individuals differ greatly in flavor perception, due in part to genetic variations in chemoreceptor genes. These differences in biology have been implicated as drivers of food choice, highlighting the need for behavioral scientists, sensory practitioners and product developers to be aware of these differences. Collectively, these data also suggest variability across individuals is not a source of noise to be minimized in sensory testing; rather, this variation is what is interesting, both in its own right from a basic science standpoint, and in translation as a potential driver of differential food choices (i.e., market segmentation).

Recently it has become clear that variation in chemosensation is far more complex than previously believed. Of the 25 unique bitter taste genes in humans (TAS2Rs), the most studied is TAS2R38, which explains differential bitterness of synthetic thiourea compounds (e.g., propylthiouracil) and natural plant toxins (e.g., goitrin). Notably, TAS2R38 variation also associates with differential intake of both alcohol and vegetables. However, this is just one of many examples to emerge within the last few years. Nor are such differences limited to bitterness, as differences in chemosensory perception have also been documented for odor (OR7D4), as well as umami and sweet tastes (TAS1R1/TAS1R3 and TAS1R2/TAS1R3 respectively). Other evidence suggests variation in the gustin (CA6) and gustducin (GNAT3) genes may also associate with variation in the intensity of bitter and sweet sensations, respectively.

Functional variation in taste, smell and oral somatosensory systems may affect myriad sensory attributes elicited by food. Much of this variation has a genetic basis, and as personalized genomics becomes more feasible, it is likely that food manufacturers will target products to particular groups based on preferences predicted by genetics. The largest challenge will be to assemble a broad range of genetic variability into a small number of groups (segments) that manufacturers can target on the basis of differential preferences.

Additionally, growing evidence suggests ‘taste’ receptors are expressed in many other tissues in the body (we place taste in quotes to emphasize activation of these receptors may not elicit a conscious perception). The degree to which extra-oral chemoreceptors influence metabolic processes or ingestive behavior via postprandial learning are just beginning to be explored; nor do we have a good understanding how polymorphisms in the genes encoding these receptors may influence learning or metabolism. This is an extremely active area of research (e.g., (Behrens and Meyerhof, 2010, Breer et al., 2012, Clark et al., 2012, Dotson et al., 2010, Dotson et al., 2008, Sclafani et al., 2010)), so it is likely our understanding will increase greatly over the coming decade.

In this review, a brief overview on receptor genetics is provided, followed by a summary of current knowledge on functional variation to date with examples for taste, smell and oral somatosensation. Throughout, we highlight the implications for human ingestive behavior outside of the laboratory, as well as gaps in our current knowledge. The next two sections provide an overview of some foundational biological concepts relevant to chemoreceptor genetics; readers who are comfortable with these concepts may want to skip ahead to Section 4.

Section snippets

Approaches from quantitative and molecular genetics

Although learning and prior exposure may play a role, a substantial proportion of the observed variation in chemosensory perception may be attributed to genetic variation. Researchers have attempted to elucidate these mechanisms by using several distinct but complementary methods from quantitative and molecular genetics. These are detailed below in Sections 2.2 Quantitative genetics – twin designs, 2.3 Molecular genetics – candidate gene, candidate SNP, and genome wide association studies after

Brief refresher on receptor biology

The lock-and-key model was proposed in 1894 by Emile Fisher to describe enzyme specificity, and it is still a useful way to conceptualize how molecules (ligands) bind to and activate chemoreceptors. Chemoreceptors are found in the mouth, nose and throat, serving as binding sites for myriad volatile and non-volatile chemicals in our environment. Transduction events mediated by these receptors cause signaling cascades that culminate in sensations of taste, smell and irritation. These receptors

Bitter taste differences

Variable bitter taste perception is the best-known example of genetic variation in oral sensation. In this section, we review the prototypical example as it relates to ingestive behavior, and then discuss several other more recent findings.

Sweet taste differences

Sweetness, like bitterness, is transduced via G-protein coupled receptors (GPCRs). The sweet receptor is a heterodimer formed from the protein products of two genes, TAS1R2 and TAS1R3. Since the first sweetener-binding model was proposed in 1914, many different models of sweet receptor and ligand interactions have been proposed, which have evolved over time as the knowledge in this area has grown (see (DuBois, 2011, Hayes, 2008) for comprehensive reviews). The advancement of X-ray

Influence of polymorphisms on umami savory sensations

Umami, from the Japanese word for deliciousness, describes the savory, meaty taste elicited by l-glutamate, first isolated from seaweed in 1908. The taste receptor for umami is a heterodimer encoded by the TAS1R1 and TAS1R3 genes (the hT1R3 protein is shared by the sweet and umami heterodimer complexes). The hT1R1/hT1R3 dimer is also stimulated by 5′ ribonucleotides, and is therefore believed to have evolved as an indicator of dietary sources of amino acids. Evidence suggests that

Salty and sour taste – minimal evidence to date

Variation in the perception of sour and of salt taste have not received the same degree of attention as the three GPCR mediated prototypical tastes. Twin studies suggest salt perception appears to be more dependent on environmental influences than genetic factors (Wise, Hansen, Reed, & Breslin, 2007). Additionally, salt preferences are strongly influenced by physiological state (Wald and Lesham, 2003), and are more variable in women than men (Hayes, Sullivan, & Duffy, 2010), presumably due to

SNPs in the gustin (CA6) gene may have non-quality specific effects on taste

Gustin, a zinc metalloprotein, is thought to be a trophic factor involved in the development of taste buds (Henkin, Martin, & Agarwal, 1999). Variations in the gustin gene CA6 were recently reported to associate with some of the bitterness of PROP (Calo et al., 2011). As mentioned above in Section 4, most of the observed variation in PROP bitterness can be explained by variation in the TAS2R38 gene (Bufe et al., 2005, Kim et al., 2003, Prodi et al., 2004); the remainder of the unexplained

Creaminess perception

Creaminess is an important quality in many types of foods, and these sensations can arise from varying levels of fat or starch in a food. Chocolate and ice cream are two highly liked foods, and part of their appeal has been linked to their dynamic texture as they melt in the mouth (Hyde & Witherly, 1993). As they melt, they decrease in oral viscosity, and the degree of this ‘thinning’ in viscosity is linked to their perceived creaminess and to consumer sensory acceptance (Prindiville et al.,

Odor

Neurons that are present in the olfactory epithelium transmit electrical impulses when the receptors they express are stimulated (Hasin-Brumshtein, Lancet, & Olender, 2009). Each neuron expresses one odorant receptor (OR) gene, monoallelically (Chess, Simon, Cedar, & Axel, 1994). These are transmitted to synaptic complexes, and each stimulus (odorant) is a unique combination of activated units (Hasin-Brumshtein et al., 2009). Early work hypothesized that smells were interpreted through a

Summary and conclusions

Biological differences in chemosensory ability from SNPs and CNVs are both commonplace and highly variable from person to person. This appears to be partly a result of evolutionary processes that have driven us to detect a vast array of potential toxins as well as potential foodstuffs, through both gustation, olfaction, and oral somatosensation. This is exemplified by the fact that although many SNPs are associated with differences in perception across multiple taste qualities, by far the most

Acknowledgments

This review was based on an oral presentation at the 9th Pangborn Sensory Science Symposium in Toronto, Canada by the lead author. The scope has been expanded to the present form and refined with the assistance of the coauthors. This work was funded by a National Institutes of Health grant from the National Institute National of Deafness and Communication Disorders [DC010904] to JEH, United States Department of Agriculture Hatch Project PEN04332 funds, and funds from the Pennsylvania State

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