Functional Diversity and Evolution of Bitter Taste Receptors in Egg-Laying Mammals

Author:

Itoigawa Akihiro12ORCID,Hayakawa Takashi34ORCID,Zhou Yang5ORCID,Manning Adrian D.6ORCID,Zhang Guojie7ORCID,Grutzner Frank8ORCID,Imai Hiroo9ORCID

Affiliation:

1. Department of Cellular and Molecular Biology, Primate Research Institute, Kyoto University , Inuyama, Aichi, Japan

2. Department of Agricultural Chemistry, School of Agriculture, Meiji University , Kawasaki, Kanagawa, Japan

3. Faculty of Environmental Earth Science, Hokkaido University , Sapporo, Hokkaido, Japan

4. Japan Monkey Centre , Inuyama, Aichi, Japan

5. BGI-Shenzhen , Shenzhen, China

6. Fenner School of Environment and Society, The Australian National University , Canberra, ACT, Australia

7. Department of Biology, University of Copenhagen , Kobenhavn, Denmark

8. School of Biological Sciences, The University of Adelaide , Adelaide, SA, Australia

9. Molecular Biology Section, Center for the Evolutionary Origins of Human Behavior, Kyoto University , Inuyama, Aichi, Japan

Abstract

Abstract Egg-laying mammals (monotremes) are a sister clade of therians (placental mammals and marsupials) and a key clade to understand mammalian evolution. They are classified into platypus and echidna, which exhibit distinct ecological features such as habitats and diet. Chemosensory genes, which encode sensory receptors for taste and smell, are believed to adapt to the individual habitats and diet of each mammal. In this study, we focused on the molecular evolution of bitter taste receptors (TAS2Rs) in monotremes. The sense of bitter taste is important to detect potentially harmful substances. We comprehensively surveyed agonists of all TAS2Rs in platypus (Ornithorhynchus anatinus) and short-beaked echidna (Tachyglossus aculeatus) and compared their functions with orthologous TAS2Rs of marsupial and placental mammals (i.e., therians). As results, the agonist screening revealed that the deorphanized monotreme receptors were functionally diversified. Platypus TAS2Rs had broader receptive ranges of agonists than those of echidna TAS2Rs. While platypus consumes a variety of aquatic invertebrates, echidna mainly consumes subterranean social insects (ants and termites) as well as other invertebrates. This result indicates that receptive ranges of TAS2Rs could be associated with feeding habits in monotremes. Furthermore, some orthologous receptors in monotremes and therians responded to β-glucosides, which are feeding deterrents in plants and insects. These results suggest that the ability to detect β-glucosides and other substances might be shared and ancestral among mammals.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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