Pseudogenization of a Sweet-Receptor Gene Accounts for Cats' Indifference toward Sugar

Li, Xia; Li, Weihua; Wang, Hong; Cao, Jie; Maehashi, Kenji; Huang, Liquan; Bachmanov, Alexander A.; Reed, Danielle R.; Legrand-Defretin, Véronique; Beauchamp, Gary K.; Brand, Joseph G.

doi:10.1371/journal.pgen.0010003

Cited by 205 publications

(167 citation statements)

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“…Taste targets nutrient-related non-volatile molecules in solution and is defined as the group of sensations mediated by the chemosensory system located in the oral cavity (Matsunami and Amrein 2003). With the exception of cats (Beauchamp et al 1977;Li et al 2005), all mammals studied seem to share significant similarities in their five primary taste activities (sweet, umami, salty, sour and bitter) (Mombaerts 2000). In general, taste reception mechanisms are associated to mouth papillae.…”

Section: Taste (Gustation)mentioning

confidence: 99%

“…Taste perception is intimately related to species nature and quality of food and diet selection (Forbes 1998;Margolskee 2002;Montmayeur and Matsunami 2002;Nelson et al 2002;Goff and Klee 2006;Li et al 2005;Shi and Zhang 2006). The biodiversity of taste across species is, therefore, a mirror image of the ecological niches that they have adapted to.…”

Section: Comparative Taste Biologymentioning

confidence: 99%

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Unfolding the codes of short-term feed appetence in farm and companion animals. A comparative oronasal nutrient sensing biology review

Roura¹,

Humphrey²,

Tedó³

et al. 2008

Can. J. Anim. Sci.

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Roura, E., Humphrey, B., Tedo´, G. and Ipharraguerre, I. 2008. Unfolding the codes of short-term feed appetence in farm and companion animals. A comparative oronasal nutrient sensing biology review. Can. J. Anim. Sci. 88: 535Á558. The evolution of the chemical senses has resulted in a sensory apparatus for high taste and smell acuity in mammals and birds to ensure self-nourishment. Such peripheral chemosensory systems function as a code to unfold the nutritional value of feedstuffs. Food ingestion simultaneously evokes odor, taste and thermo-mechanical (somatosensing) sensations. Olfaction represents the capacity to identify feed volatiles that are predominantly derived from essential nutrients in plants.Comparative biology of olfaction shows that primates and chickens have a smaller olfactory epithelium and fewer olfactory receptor (OR) genes than non-primate mammals studied to date including farm and companion animals, such as the pig, the cow, the dog, the cat and the horse. A significant proportion of the total OR genes in mammals and birds have lost their functionality (pseudogenes) in a process that seems to reflect a decrease in the animal's reliance on the sense of smell, particularly in humans and cows. The taste system allows animals to recognize a diverse repertoire of nutrient (sugars, amino acids, salts, acids and fats) or toxic related chemical entities that provide valuable information about the quality of food. Taste senses non-volatile molecules in the oral cavity through taste receptors (TR). The TR are expressed in the sensory cells forming the taste buds of the tongue's papillae. Taste cells are linked to a network of solitary chemosensory cells diffused through many non-taste tissues involved in metabolic homeostasis. The number of functional taste receptor genes (TASR) in humans is equivalent to that in other mammals and superior to that in chickens. The TASR family 1 (TAS1R coding for umami and sweet TR) is conserved, in number and type, across the species evaluated, with the exception of the sweet receptor in chicken and feline species. The TASR family 2 (TAS2R coding for bitter TR) shows a strong adaptive capacity to dietary sources and digestive physiology across vertebrates. Pseudogenization (loss of gene functionality) in the TAS2R family seems to be a frequent strategy. The implications of oronasal nutrient sensing related to comparative animal feeding strategies and behaviors such as neophobia, feed refusal and hedonic preferences are discussed. Feed palatability and appetence might be one of the main driving forces in short-term feed consumption. Finally, practical applications relevant to animal production are outlined.Key words: Nutrient sensing, taste, olfaction, somatosensing, feed intake, farm, companion animals Roura, E., Humphrey, B., Tedo´, G. et Ipharraguerre, I. 2008. Le code de l'appe´tence a`court terme chez les animaux domestiques et de compagnie. Biologie comparative de la de´tection bucco-nasale des e´le´ments nutritifs. Can. J. Anim. Sci. 88: 535Á558. En e´voluant, ...

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Section: Taste (Gustation)mentioning

confidence: 99%

Section: Comparative Taste Biologymentioning

confidence: 99%

Unfolding the codes of short-term feed appetence in farm and companion animals. A comparative oronasal nutrient sensing biology review

Roura¹,

Humphrey²,

Tedó³

et al. 2008

Can. J. Anim. Sci.

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“…Humans have changed over time and adapted to specific environments that contain some types of food but not others; this in turn has tailored our sense of taste and, by extension, our genome and individual genes. Nonhuman species provide evidence that the sense of taste has been shaped by evolution; for instance, cats and some other carnivorous species, in addition to chickens, 4 have lost the function of their sweet receptor 5 —they no longer need to taste “sweet” because the foods they eat, the flesh of other animals or starchy grains, contain little sugar. The availability of food may have shaped nearly the entire genome—in yeast, and probably other organisms as well, most genes are involved either directly or indirectly with nutrition and metabolism.…”

Section: Introductionmentioning

confidence: 99%

Genetics of Taste and Smell

Reed

Knaapila

2010

Progress in Molecular Biology and Translational Science

218

118

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Eating is dangerous. While food contains nutrients and calories that animals need to produce heat and energy, it may also contain harmful parasites, bacteria, or chemicals. To guide food selection, the senses of taste and smell have evolved to alert us to the bitter taste of poisons and the sour taste and off-putting smell of spoiled foods. These sensory systems help people and animals to eat defensively, and they provide the brake that helps them avoid ingesting foods that are harmful. But choices about which foods to eat are motivated by more than avoiding the bad; they are also motivated by seeking the good, such as fat and sugar. However, just as not everyone is equally capable of sensing toxins in food, not everyone is equally enthusiastic about consuming high-fat, high-sugar foods. Genetic studies in humans and experimental animals strongly suggest that the liking of sugar and fat is influenced by genotype; likewise, the abilities to detect bitterness and the malodors of rotting food are highly variable among individuals. Understanding the exact genes and genetic differences that affect food intake may provide important clues in obesity treatment by allowing caregivers to tailor dietary recommendations to the chemosensory landscape of each person.

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“…Cats, obligate carnivores, are behaviorally insensitive to sweet-tasting compounds (12,13). We proposed that this behavioral insensitivity was a consequence of the pseudogenization of Tas1r2 (14). Tas1r2 also is known to be pseudogenized in chicken, tongueless Western clawed frogs, and vampire bats (11,15).…”

mentioning

confidence: 99%

Major taste loss in carnivorous mammals

Jiang

Josue

et al. 2012

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

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Mammalian sweet taste is primarily mediated by the type 1 taste receptor Tas1r2/Tas1r3, whereas Tas1r1/Tas1r3 act as the principal umami taste receptor. Bitter taste is mediated by a different group of G protein-coupled receptors, the Tas2rs, numbering 3 to ∼66, depending on the species. We showed previously that the behavioral indifference of cats toward sweet-tasting compounds can be explained by the pseudogenization of the Tas1r2 gene, which encodes the Tas1r2 receptor. To examine the generality of this finding, we sequenced the entire coding region of Tas1r2 from 12 species in the order Carnivora. Seven of these nonfeline species, all of which are exclusive meat eaters, also have independently pseudogenized Tas1r2 caused by ORF-disrupting mutations. Fittingly, the purifying selection pressure is markedly relaxed in these species with a pseudogenized Tas1r2. In behavioral tests, the Asian otter (defective Tas1r2) showed no preference for sweet compounds, but the spectacled bear (intact Tas1r2) did. In addition to the inactivation of Tas1r2, we found that sea lion Tas1r1 and Tas1r3 are also pseudogenized, consistent with their unique feeding behavior, which entails swallowing food whole without chewing. The extensive loss of Tas1r receptor function is not restricted to the sea lion: the bottlenose dolphin, which evolved independently from the sea lion but displays similar feeding behavior, also has all three Tas1rs inactivated, and may also lack functional bitter receptors. These data provide strong support for the view that loss of taste receptor function in mammals is widespread and directly related to feeding specializations.diet | sweetener I t is widely believed that most mammals perceive five basic taste qualities: sweet, umami, bitter, salty, and sour. The receptors for sweet, umami and bitter tastes are G protein-coupled receptors (GPCRs) (1). Sweet taste is mediated largely by a heteromer of two closely related Tas1r (type 1 taste receptor) family GPCRs: Tas1r2 and Tas1r3 (2-5). Tas1r1, another member of the Tas1r family, in combination with Tas1r3, forms an umami taste receptor (6). Tas1r receptors are class C GPCRs. Unlike sweet and umami tastes, bitter taste is mediated by Tas2r family GPCRs, which belong to class A GPCRs and are structurally unrelated to Tas1r family receptors (7,8). The genes encoding Tas2r receptors, the Tas2r genes, differ substantially in gene number and primary sequences among species, most likely reflecting the likelihood that these genes are required for detecting toxic or harmful substances in a species' ecological niche (9-11).Direct evidence for a close correlation between taste function and feeding ecology comes from work on domestic and wild Felidae. Cats, obligate carnivores, are behaviorally insensitive to sweet-tasting compounds (12, 13). We proposed that this behavioral insensitivity was a consequence of the pseudogenization of Tas1r2 (14). Tas1r2 also is known to be pseudogenized in chicken, tongueless Western clawed frogs, and vampire bats (11,15). The loss of th...

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Pseudogenization of a Sweet-Receptor Gene Accounts for Cats' Indifference toward Sugar

Cited by 205 publications

References 41 publications

Unfolding the codes of short-term feed appetence in farm and companion animals. A comparative oronasal nutrient sensing biology review

Unfolding the codes of short-term feed appetence in farm and companion animals. A comparative oronasal nutrient sensing biology review

Genetics of Taste and Smell

Major taste loss in carnivorous mammals

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