Evolution of the primate glutamate taste sensor from a nucleotide sensor

• Published in: Current biology 2021-10, Vol.31 (20), p.4641-4649.e5
• Main Authors: Toda, Yasuka, Hayakawa, Takashi, Itoigawa, Akihiro, Kurihara, Yosuke, Nakagita, Tomoya, Hayashi, Masahiro, Ashino, Ryuichi, Melin, Amanda D., Ishimaru, Yoshiro, Kawamura, Shoji, Imai, Hiroo, Misaka, Takumi
• Format: Article
• Language: English
• Subjects: Amino Acids; Animals; dietary transition; feeding behavior; folivorous; Glutamic Acid; GPCR; insectivorous; Ligands; Mammals; Nucleotides; parallel evolution; primate evolution; Primates; Receptors, G-Protein-Coupled - metabolism; Ribonucleotides; T1R1/T1R3; Taste - physiology; taste receptor; umami
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.08.002

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. [Display omitted] •The ancestral type of primate T1R1/T1R3 was sensitive to nucleotides of insects•T1R1/T1R3 of large primates evolved to detect l-Glu found in folivorous diets•l-Glu preference might overcome aversive tastes of leaves and promote consumption Toda et al. investigate the evolutionary plasticity of T1R1/T1R3 for detecting amino acids by using functional, behavioral, phylogenetic, and ecological approaches in diverse primate lineages. T1R1/T1R3 of large primates underwent adaptive evolution that improved their ability to detect l-glutamate, which is a major free amino acid in leafy diets.