Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

Taste is a vital chemical sense for feeding behaviour. In mammals, the umami and sweet taste receptors comprise three members of the taste receptor type 1 (T1R/TAS1R) family: T1R1, T1R2 and T1R3. Because their functional homologues exist in teleosts, only three TAS1R genes generated by gene duplication are believed to have been inherited from the common ancestor of bony vertebrates. Here, we report five previously uncharacterized TAS1R members in vertebrates, TAS1R4, TAS1R5, TAS1R6, TAS1R7 and TAS1R8, based on genome-wide survey of diverse taxa. We show that mammalian and teleost fish TAS1R2 and TAS1R3 genes are paralogues. Our phylogenetic analysis suggests that the bony vertebrate ancestor had nine TAS1Rs resulting from multiple gene duplications. Some TAS1Rs were lost independently in descendent lineages resulting in retention of only three TAS1Rs in mammals and teleosts. Combining functional assays and expression analysis of non-teleost fishes we show that the novel T1Rs form heterodimers in taste-receptor cells and recognize a broad range of ligands such as essential amino acids, including branched-chain amino acids, which have not been previously considered as T1R ligands. This study reveals diversity of taste sensations in both modern vertebrates and their ancestors, which might have enabled vertebrates to adapt to diverse habitats on Earth.

DOI： 10.1038/s41559-023-02258-8

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Language：English   Publishing type：Research paper (scientific journal)  

Sugars are an important class of nutrients found in the flowers and fruits of angiosperms (flowering plants). Although T1R2-T1R3 has been identified as the mammalian sweet receptor, some birds rely on a repurposed T1R1-T1R3 savory receptor to sense sugars. Moreover, as the radiation of flowering plants occurred later than the last common ancestor of amniotes, sugar may not have been an important diet item for amniotes early in evolution, raising the question of whether T1R2-T1R3 is a universal sugar sensor or only a mammalian innovation. Here, using brief-access behavioral tests and functional characterization of taste receptors, we demonstrate that the nectar-taking Madagascar giant day gecko (Phelsuma grandis) can sense sugars through the T1R2-T1R3 receptor. These results reveal the existence of T1R2-based sweet taste in a non-avian reptile, which has important implications for our understanding of the evolutionary history of sugar detection in amniotes.

DOI： 10.1016/j.cub.2022.10.061

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Language：English   Publishing type：Research paper (scientific journal)  

Sensory receptors evolve, and changes to their response profiles can directly impact sensory perception and affect diverse behaviors, from mate choice to foraging decisions.1-3 Although receptor sensitivities can be highly contingent on changes occurring early in a lineage's evolutionary history,4 subsequent shifts in a species' behavior and ecology may exert selective pressure to modify and even reverse sensory receptor capabilities.5-7 Neither the extent to which sensory reversion occurs nor the mechanisms underlying such shifts is well understood. Using receptor profiling and behavioral tests, we uncover both an early gain and an unexpected subsequent loss of sugar sensing in woodpeckers, a primarily insectivorous family of landbirds.8,9 Our analyses show that, similar to hummingbirds10 and songbirds,4 the ancestors of woodpeckers repurposed their T1R1-T1R3 savory receptor to detect sugars. Importantly, whereas woodpeckers seem to have broadly retained this ability, our experiments demonstrate that wrynecks (an enigmatic ant-eating group sister to all other woodpeckers) selectively lost sugar sensing through a novel mechanism involving a single amino acid change in the T1R3 transmembrane domain. The identification of this molecular microswitch responsible for a sensory shift in taste receptors provides an example of the molecular basis of a sensory reversion in vertebrates and offers novel insights into structure-function relationships during sensory receptor evolution.

DOI： 10.1016/j.cub.2022.07.059

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Language：English   Publishing type：Research paper (scientific journal)  

Sensory receptor evolution can imply trade-offs between ligands, but the extent to which such trade-offs occur and the underlying processes shaping their evolution is not well understood. For example, hummingbirds have repurposed their ancestral savory receptor (T1R1-T1R3) to detect sugars, but the impact of this sensory shift on amino acid perception is unclear. Here, we use functional and behavioral approaches to show that the hummingbird T1R1-T1R3 acts as a bifunctional receptor responsive to both sugars and amino acids. Our comparative analyses reveal substantial functional diversity across the hummingbird radiation and suggest an evolutionary timeline for T1R1-T1R3 retuning. Finally, we identify a novel form of synergism between sugars and amino acids in vertebrate taste receptors. This work uncovers an unexplored axis of sensory diversity, suggesting new ways in which nectar chemistry and pollinator preferences can coevolve.

DOI： 10.1093/molbev/msab367

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：Elsevier {BV}  

DOI： 10.1016/j.bbrep.2021.101123

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)   Publisher：Elsevier {BV}  

Taste perception plays an essential role in food selection. Umami (savory) tastes are sensed by a taste receptor complex, T1R1/T1R3, that detects proteinogenic amino acids.1 High sensitivity to l-glutamate (l-Glu) is a characteristic of human T1R1/T1R3, but the T1R1/T1R3 of other vertebrates does not consistently show this l-Glu response.1,2 Here, we demonstrate that the l-Glu sensitivity of T1R1/T1R3 is a derived state that has evolved repeatedly in large primates that rely on leaves as protein sources, after their divergence from insectivorous ancestors. Receptor expression experiments show that common amino acid substitutions at ligand binding sites that render T1R1/T1R3 sensitive to l-Glu occur independently at least three times in primate evolution. Meanwhile T1R1/T1R3 senses 5'-ribonucleotides as opposed to l-Glu in several mammalian species, including insectivorous primates. Our chemical analysis reveal that l-Glu is one of the major free amino acids in primate diets and that insects, but not leaves, contain large amounts of free 5'-ribonucleotides. Altering the ligand-binding preference of T1R1/T1R3 from 5'-ribonucleotides to l-Glu might promote leaf consumption, overcoming bitter and aversive tastes. Altogether, our results provide insight into the foraging ecology of a diverse mammalian radiation and help reveal how evolution of sensory genes facilitates invasion of new ecological niches.

DOI： 10.1016/j.cub.2021.08.002

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)   Publisher：American Association for the Advancement of Science ({AAAS})  

<jats:p>Early events in the evolutionary history of a clade can shape the sensory systems of descendant lineages. Although the avian ancestor may not have had a sweet receptor, the widespread incidence of nectar-feeding birds suggests multiple acquisitions of sugar detection. In this study, we identify a single early sensory shift of the umami receptor (the T1R1-T1R3 heterodimer) that conferred sweet-sensing abilities in songbirds, a large evolutionary radiation containing nearly half of all living birds. We demonstrate sugar responses across species with diverse diets, uncover critical sites underlying carbohydrate detection, and identify the molecular basis of sensory convergence between songbirds and nectar-specialist hummingbirds. This early shift shaped the sensory biology of an entire radiation, emphasizing the role of contingency and providing an example of the genetic basis of convergence in avian evolution.</jats:p>

DOI： 10.1126/science.abf6505

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

Taste is a vital sensation for vertebrates, enabling the detection of nutritionally important substances or potential toxins. A heteromeric complex of two class C GPCRs, T1R1 and T1R3, was identified as the umami (savory) taste receptor. Amino acids and 5'-ribonucleotides are well known to be natural ligands for human T1R1/T1R3. In this study, we reveal that methional, which is a familiar flavor component in foods, is an allosteric modulator of T1R1/T1R3. Receptor expression experiments showed that methional served as a positive allosteric modulator (PAM) of human T1R1/T1R3 and functioned as a negative allosteric modulator (NAM) of mouse T1R1/T1R3. Although amino acids and 5'-ribonucleotides bound to the extracellular domain of T1R1, the use of interspecies chimeric receptors demonstrated that methional interacted with the transmembrane domain of T1R1. Site-directed mutagenesis and molecular modeling showed that methional could potentially bind at two distinct sites in the transmembrane domain of T1R1 and that the amino acid residues in the bottom of the allosteric pocket engendered the switch between the PAM and NAM modes, which could contribute to switching the binding position of methional. These results may be applicable for elucidating the molecular mechanisms underlying ligand recognition by other class C GPCRs.

DOI： 10.1038/s41598-018-30315-x

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

DOI： 10.1126/science.1255097

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

DOI： 10.1007/s00726-014-1713-3

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

DOI： 10.1074/jbc.M113.494443

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

DOI： 10.1021/jf2029835

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

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Language：Japanese  

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