Major taste loss in carnivorous mammals

Jiang, Peihua; Josue, Jesusa; Li, Xia; Gläser, Dieter; Li, Weihua; Brand, Joseph G.; Margolskee, Robert F.; Reed, Danielle R.; Beauchamp, Gary K.

doi:10.1073/pnas.1118360109

Cited by 239 publications

(230 citation statements)

References 36 publications

Supporting

Mentioning

209

Contrasting

Unclassified

Order By: Relevance

“…For instance, carnivorous mammals, which eat no sweet food, have an inactivated form of the sweet receptor [60,61], and some herbivorous animals, which eat no meat, have lost their amino acid receptor [62]. Likewise, animals that swallow their food whole have major taste loss [63]. However, at least one mystery remains.…”

Section: Genetic Differences In Sweet Taste Detectionmentioning

confidence: 98%

Heritable differences in chemosensory ability among humans

Newcomb

Xia

Reed

2012

Flavour

View full text Add to dashboard Cite

The combined senses of taste, smell and the common chemical sense merge to form what we call 'flavor.' People show marked differences in their ability to detect many flavors, and in this paper, we review the role of genetics underlying these differences in perception. Most of the genes identified to date encode receptors responsible for detecting tastes or odorants. We list these genes and describe their characteristics, beginning with the best-studied case, that of differences in phenylthiocarbamide (PTC) detection, encoded by variants of the bitter taste receptor gene TAS2R38. We then outline examples of genes involved in differences in sweet and umami taste, and discuss what is known about other taste qualities, including sour and salty, fat (termed pinguis), calcium, and the 'burn' of peppers. Although the repertoire of receptors involved in taste perception is relatively small, with 25 bitter and only a few sweet and umami receptors, the number of odorant receptors is much larger, with about 400 functional receptors and another 600 potential odorant receptors predicted to be non-functional. Despite this, to date, there are only a few cases of odorant receptor variants that encode differences in the perception of odors: receptors for androstenone (musky), isovaleric acid (cheesy), cis-3-hexen-1-ol (grassy), and the urinary metabolites of asparagus. A genome-wide study also implicates genes other than olfactory receptors for some individual differences in perception. Although there are only a small number of examples reported to date, there may be many more genetic variants in odor and taste genes yet to be discovered.Keywords: Flavor, Genetics, Evolution, Taste, Odor, Receptor, Polymorphism Review Why we differ in taste perceptionHumans use several kinds of information to decide what to eat, and the combination of experience and sensory evaluation helps us to choose whether to consume a particular food. If the sight, smell, and taste of the food are acceptable, and we see others enjoying it, we finish chewing and swallow it. Several senses combine to create the idea of food flavor in the brain. For example, a raw chili pepper has a crisp texture, an odor, a bitter and sour taste, and a chemesthetic 'burn.' Each of these sensory modalities is associated with a particular group of receptors: at least three subtypes of somatosensory receptors (touch, pain, and temperature), human odor receptors, which respond either singly or in combination; [1,2], at least five types of taste receptors (bitter, sour, sweet, salty, and umami (the savory experience associated with monosodium glutamate [3])), and several families of other receptors tuned to the irritating chemicals in foods, especially of herbs and spices (for example, eugenol found in cloves [4] or allicin found in garlic [5]). The information from all these receptors are transmitted to the brain, where it is processed and integrated [6]. Experience is a potent modifier of chemosensory perception, and persistent exposure to an odorant is enough to change...

show abstract

Section: Genetic Differences In Sweet Taste Detectionmentioning

confidence: 98%

Heritable differences in chemosensory ability among humans

Newcomb

Xia

Reed

2012

Flavour

View full text Add to dashboard Cite

show abstract

“…In higher vertebrates frequent independent expansions and pseudogenization events resulted in differently sized Tas2r gene repertoires (12). Consequently, the number of putatively functional Tas2r genes varies considerably in vertebrates, ranging from 0 in baleen and tooth whales as well as penguins (13)(14)(15)(16) to more than 50 in Western clawed frogs and 80 in Coelacanth (17)(18)(19)(20). Thus, humans with ϳ25 and mice with ϳ35 putatively functional members possess average size Tas2r repertoires (21).…”

mentioning

confidence: 99%

Comprehensive Analysis of Mouse Bitter Taste Receptors Reveals Different Molecular Receptive Ranges for Orthologous Receptors in Mice and Humans

Lossow

Hübner

Roudnitzky

et al. 2016

Journal of Biological Chemistry

179

277

View full text Add to dashboard Cite

One key to animal survival is the detection and avoidance of potentially harmful compounds by their bitter taste. Variable numbers of taste 2 receptor genes expressed in the gustatory end organs enable bony vertebrates (Euteleostomi) to recognize numerous bitter chemicals. It is believed that the receptive ranges of bitter taste receptor repertoires match the profiles of bitter chemicals that the species encounter in their diets. Human and mouse genomes contain pairs of orthologous bitter receptor genes that have been conserved throughout evolution. Moreover, expansions in both lineages generated species-specific sets of bitter taste receptor genes. It is assumed that the orthologous bitter taste receptor genes mediate the recognition of bitter toxins relevant for both species, whereas the lineagespecific receptors enable the detection of substances differently encountered by mice and humans. By challenging 34 mouse bitter taste receptors with 128 prototypical bitter substances in a heterologous expression system, we identified cognate compounds for 21 receptors, 19 of which were previously orphan receptors. We have demonstrated that mouse taste 2 receptors, like their human counterparts, vary greatly in their breadth of tuning, ranging from very broadly to extremely narrowly tuned receptors. However, when compared with humans, mice possess fewer broadly tuned receptors and an elevated number of narrowly tuned receptors, supporting the idea that a large receptor repertoire is the basis for the evolution of specialized receptors. Moreover, we have demonstrated that sequence-orthologous bitter taste receptors have distinct agonist profiles. Species-specific gene expansions have enabled further diversification of bitter substance recognition spectra.The plethora of natural compounds that taste bitter for humans comprises numerous chemicals with pharmacological activities that can make them powerful toxins, such as the alkaloids strychnine and colchicine or the sesquiterpene lactone picrotoxinin (1). However, compounds believed to exert health-beneficial effects such as the antioxidative phytoestrogen genistein from soy (2), the analgesic drug acetaminophen (3), or various polyphenols also taste bitter (4). To avoid ingestion of bitter substances that would pose a threat to organisms, efficient recognition and rejection mechanisms have developed throughout the animal kingdom. In bony vertebrates (Euteleostomi), the avoidance of bitter compounds is centered on taste receptors that detect potentially harmful substances with high accuracy and adequate sensitivity (5). Vertebrate bitter taste receptors, called taste 2 receptors (TAS2R (human) or Tas2r (murine)), 2 are G protein-coupled receptors only remotely related to other classes of this large and enormously versatile receptor family (6 -10). During evolution the first Tas2r genes appeared in the genomes of bony fish (11). In higher vertebrates frequent independent expansions and pseudogenization events resulted in differently sized Tas2r gene repertoires (12). Cons...

show abstract

“…Specifically, if our understanding of the physiological function of a gene is complete and accurate, the gene should be inactivated or pseudogenized in and only in organisms in which the presumed function of the gene has become useless or harmful. On the basis of multiple independent pseudogenizations of the sweet taste receptor gene Tas1r2 in obligated carnivores and piscivores (fish eaters) and similar independent pseudogenizations of the umami taste receptor gene Tas1r1 in marine mammals, Jiang et al (1) concluded that "loss of taste receptor function" is "directly related to feeding specializations." We believe that this conclusion is unwarranted.…”

mentioning

confidence: 99%

“…Jiang et al (1) further contended that sea lions and dolphins need not sense the umami taste because they swallow food whole. Although it is true that Tas1r1 is pseudogenized in these two species, the authors ignore the previous finding that Tas1r1 is also pseudogenized or missing in all bats examined, regardless of their diet (fruits, insects, or blood) (3).…”

mentioning

confidence: 99%

Mismatches between feeding ecology and taste receptor evolution: An inconvenient truth

Zhao

Zhang

2012

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Comparative and evolutionary biology can not only verify laboratory findings of gene functions but also provide insights into their physiological roles in nature that are sometimes difficult to discern in the laboratory. Specifically, if our understanding of the physiological function of a gene is complete and accurate, the gene should be inactivated or pseudogenized in and only in organisms in which the presumed function of the gene has become useless or harmful. On the basis of multiple independent pseudogenizations of the sweet taste receptor gene Tas1r2 in obligated carnivores and piscivores (fish eaters) and similar independent pseudogenizations of the umami taste receptor gene Tas1r1 in marine mammals, Jiang et al. (1) concluded that "loss of taste receptor function" is "directly related to feeding specializations." We believe that this conclusion is unwarranted.Jiang et al. (1) contended that obligated carnivores and piscivores need not sense sweet because meat contains little carbohydrate. Although pseudogenized Tas1r2 was indeed found only in obligated carnivores and piscivores among 18 studied species of Carnivora, two obligated carnivores they examined (ferret and Canadian otter) still possess an intact Tas1r2 (1). There is no indication that the current feeding ecology of these two species appeared so recently in evolution that neutral null mutations have not had time to fix in their Tas1r2. The three pinnipeds studied share a common ancestry of obligated meateating, yet no single null mutation of Tas1r2 is shared between them, suggesting that the pseudogenizations are not closely related to their diet. Outside Carnivora, vampire bats lack an intact Tas1r2 despite the presence of carbohydrates in blood, their sole diet (2). It is probable that the pseudogenization of Tas1r2 in vampire bats is related to the narrowness of their diet rather than the specific diet they use. Tas1r2 is also missing in the genome sequences of the herbivorous horse and omnivorous pig, but no satisfactory explanation exists (2). Furthermore, Tas1r2 is absent in all bird genomes sequenced thus far (2), irrespective of their diet.Jiang et al.(1) further contended that sea lions and dolphins need not sense the umami taste because they swallow food whole. Although it is true that Tas1r1 is pseudogenized in these two species, the authors ignore the previous finding that Tas1r1 is also pseudogenized or missing in all bats examined, regardless of their diet (fruits, insects, or blood) (3). Although the pseudogenization of Tas1r1 in the giant panda (4) occurred at approximately the same time as it switched from being a meat-eater to a plant-eater (5), and thus may be related to the feeding ecology, herbivorous mammals, such as the horse and cow, still carry an intact Tas1r1 (5).Clearly, the presence/absence of intact Tas1r2 and Tas1r1 in mammals and other vertebrates is sometimes inconsistent with the known functions of these genes and the involved tastes. These mismatches indicate that our understanding of the physiological functio...

show abstract

Major taste loss in carnivorous mammals

Cited by 239 publications

References 36 publications

Heritable differences in chemosensory ability among humans

Heritable differences in chemosensory ability among humans

Comprehensive Analysis of Mouse Bitter Taste Receptors Reveals Different Molecular Receptive Ranges for Orthologous Receptors in Mice and Humans

Mismatches between feeding ecology and taste receptor evolution: An inconvenient truth

Contact Info

Product

Resources

About