It is generally
believed that most mammals perceive five basic taste qualities: sweet, umami
(tasty), bitter, salty, and sour. The receptors for sweet, umami and bitter
tastes are G protein-coupled receptors (GPCRs). Sweet taste is mediated largely
by a heteromer of two closely related Tas1r (type 1 taste receptor) family
GPCRs: Tas1r2 and Tas1r3. Tas1r1, another member of the Tas1r family, in
combination with Tas1r3, forms an umami taste receptor. 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. 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.
Sweet taste Tas1r2 genes are pseudogenized in domestic cats which show indifference
to sweet taste. Similarly, in other members (e.g., tiger and cheetah) of the
cat family Tas1r2 genes are
pseudogenized. In a recent study Jiang et al. (1) sequenced all exons of Tas1r2 genes from several carnivore species
including obligate carnivores (e.g., domestic and wild cats), relatively
omnivorous species (e.g., bears), and strict herbivores (e.g., giant panda). They
found that loss-of-function mutations occurred in different positions of exons
of Tas1r2 genes of obligate
carnivores (Fig. 1), which are scattered on the phylogenetic tree (Fig. 2).
This result indicates that pseudogenization of Tas1r2 genes resulting in loss of sweet taste occurred
independently in several carnivore lineages in relatively short periods of
time.
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Fig. 1. Widespread pseudogenization of
the sweet-taste receptor gene Tas1r2. The above diagram shows the
positions of ORF-disrupting mutations in Tas1r2 from selected species of
carnivores. The functional dog Tas1r2 gene structure is shown as a
reference. The positions where ORF-disrupting mutations occurred are marked
with a red asterisk (*).
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Fig.
2. Evolutionary
tree of Tas1r2 genes from 18 species of carnivores. Species with a
pseudogenized Tas1r2 are marked with a diamond (red and gray depict
species characterized in this study and the previous study, respectively).
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Furthermore, Jiang et al. showed
that in sea lion (Carnivora) and dolphin (Cetacea) which swallow whole food and
have a reduced number of taste buds on tongue Tas1r1 and Tas1r3 genes
are pseudogenized. They also failed to find intact Tas2r genes that encode bitter taste receptors in the dolphin
genome. This result indicates the loss of umami taste as well as the loss of
sweet taste in sea lion and dolphin and suggests the loss of bitter taste in
the latter. Jiang
et al. present the view that the loss of taste receptor genes is a consequence
of dietary specialization in mammals (1).
However, Zhao and Zhang (2) pointed
out that (i) although Tas1r2 genes
are pseudogenized only in obligate carnivores in Jiang et al. (1), ferret and
Canadian otter, which are also obligate carnivores, still possess intact Tas1r2 genes and (ii) although three
pinnipeds share the common ancestry of obligate meat-eating, none of the null
mutations in Tas1r2 genes are shared by
these species. Moreover, a previous study of Zhao and Zhang’s group (3) showed
that (iii) Tas1r2 genes are
pseudogenized in vampire bats which feed solely on blood containing
carbohydrate and (iv) Tas1r2 genes
are missing in herbivorous horse and omnivorous pig as well as in all available
birds’ genome sequences irrespective of their diet. Tas1r1 genes that encode umami taste receptors are pseudogenized in
all bats regardless of their diet (fruit, insect, blood) (4). In Zhao and
Zhang’s view the relationship between the diet of species and the loss of
function of taste receptor genes is quite complex and sometimes inconsistent.
Jiang et al. (5) responded to
Zhao and Zhang (2) stating that (i) prefect correspondence between the exclusive
meat-eating diet and the loss of taste receptor genes should not be expected
because the loss of sweet taste receptor genes occurs stochastically and
therefore is a time-dependent and ongoing process after diet switch, (ii) whether
the common ancestor depended solely on meat-eating diet is not known, (iii) vampire
bats unlikely require sweet taste because of the very small amount of carbohydrate
in blood, and (iv) some studies showed the presence of Tas1r2 genes in horse and pig and these species show preference of
sweet taste.
Although Jiang et al. (5)
responded to Zhao and Zhang’s (2) questions, some questions remain unanswered.
For example, why are no sweet taste receptor genes found in birds regardless of
their diets?
Although the two groups of authors
have different opinions on the relationship of the diet and loss of taste
receptor genes, both of them recognize a need for better understanding of
physiological mechanisms of taste and taste receptors to understand the
relationship between diet and gene loss (1, 2).
The abstract of Jiang et al.’s
paper (1) is as follows.
Abstract
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.
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References
1. Jiang P, Josue J, Li X, Galser D, Li W, Brand JG,
Margolskee RF, Reed DR, Beauchamp GK. 2012. Major taste loss in carnivorous mammals. Proc. Natl. Acad. Sci. USA. 109:4956-4961.
2. Zhao H, Zhang J. 2012. Mismatches between feeding ecology and taste
receptor evolution: An inconvenient truth. Proc. Natl. Acad. Sci.USA, doi: 10.1073/pnas.1205205109.
3. Zhao H, Zhou Y, Pinto CM, Charles-Dominique P,
Galindo-Gonzalez J, Zhang S, Zhang J. 2010. Evolution of the sweet taste receptor gene Tas1r2 in bats. Mol. Biol. Evol. 27; 2642-2650.
4. Zhao H, Xu D, Zhang S, Zhang J. 2012. Genomic and genetic evidence for the loss of umami taste in bats. Genome Biol. Evol. 4:73-79.
5. Jiang P, Josue J, Li X, Galser D, Li W, Brand JG,
Margolskee RF, Reed DR, Beauchamp GK. 2012. Reply to Zhao and Zhnag: Loss of
taste receptor function in mammals is directly related to feeding
specializations. Proc. Natl. Acad. Sci. USA, doi: 10.1073/pnas.1205581109.
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