Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo 113-8657, Japan; Department of Agricultural Chemistry, School of Agriculture, Meiji University, Kawasaki, Kanagawa 214-8571, Japan; Japan Society for the Promotion of Science, Tokyo 102-0083, Japan.
Faculty of Environmental Earth Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan; Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan; Japan Monkey Centre, Inuyama, Aichi 484-0081, Japan.
Curr Biol. 2021 Oct 25;31(20):4641-4649.e5. doi: 10.1016/j.cub.2021.08.002. Epub 2021 Aug 26.
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. 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. 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.
味觉感知在食物选择中起着至关重要的作用。鲜味（美味）的味道是由味觉受体复合物 T1R1/T1R3 感知的，该复合物检测蛋白氨基酸。对 l-谷氨酸（l-Glu）的高灵敏度是人类 T1R1/T1R3 的特征，但其他脊椎动物的 T1R1/T1R3 并不总是表现出这种 l-Glu 反应。在这里，我们证明 T1R1/T1R3 的 l-Glu 敏感性是一种衍生状态，在依赖叶子作为蛋白质来源的大型灵长类动物从食虫祖先分化后，已经在它们身上反复进化。受体表达实验表明，在灵长类动物进化过程中，至少有三次在配体结合位点发生常见氨基酸取代，使 T1R1/T1R3 对 l-Glu 敏感。同时，T1R1/T1R3 在包括食虫灵长类动物在内的几种哺乳动物中感知 5'-核苷酸而不是 l-Glu。我们的化学分析表明，l-Glu 是灵长类动物饮食中的主要游离氨基酸之一，而昆虫而不是叶子含有大量游离 5'-核苷酸。改变 T1R1/T1R3 的配体结合偏好从 5'-核苷酸到 l-Glu 可能会促进叶子的消耗，克服苦味和厌恶的味道。总的来说，我们的研究结果为哺乳动物多样化辐射的觅食生态学提供了深入了解，并有助于揭示感觉基因的进化如何促进对新生态位的入侵。
