Vasopressin-oxytocin–type signaling is ancient and has a conserved water homeostasis role in euryhaline marine planarians

Author:

Kobayashi Aoshi1ORCID,Hamada Mayuko1ORCID,Yoshida Masa-aki2ORCID,Kobayashi Yasuhisa13ORCID,Tsutsui Naoaki14ORCID,Sekiguchi Toshio56,Matsukawa Yuta1ORCID,Maejima Sho1ORCID,Gingell Joseph J.7ORCID,Sekiguchi Shoko1,Hamamoto Ayumu18,Hay Debbie L.69ORCID,Morris John F.10,Sakamoto Tatsuya1,Sakamoto Hirotaka110ORCID

Affiliation:

1. Ushimado Marine Institute (UMI), Graduate School of Natural Science and Technology, Okayama University, Ushimado, Setouchi, Okayama 701-4303, Japan.

2. Oki Marine Biological Station, Shimane University, 194 Kamo, Okinoshima, Oki, Shimane 685-0024, Japan.

3. Laboratory for Aquatic Biology, Department of Fisheries, Faculty of Agriculture, Kindai University, Nakamachi, Nara, Japan.

4. Department of Marine Bioresources, Faculty of Bioresources, Mie University, Tsu, Mie 514-8507, Japan.

5. Noto Marine Laboratory, Institute of Nature and Environmental Technology, Division of Marine Environmental Studies, Kanazawa University, Ogi, Noto-cho, Ishikawa 927-0553, Japan.

6. School of Biological Sciences and Maurice Wilkins Centre for Molecular Biodiscovery, University of Auckland, Auckland, New Zealand.

7. Vertex Pharmaceuticals (Europe) Ltd., Milton Park, Abingdon OX11 4RW, UK.

8. Department of Biology, Faculty of Science, Okayama University, 3-1-1 Kita-ku, Tsushimanaka, Okayama 700-8530, Japan.

9. Department of Pharmacology and Toxicology, University of Otago, Otago, New Zealand.

10. Department of Physiology, Anatomy, and Genetic, Le Gros Clark Building, University of Oxford, South Parks Road, Oxford OX1 3QX, UK.

Abstract

Vasopressin/oxytocin (VP/OT)–related peptides are essential for mammalian antidiuresis, sociosexual behavior, and reproduction. However, the evolutionary origin of this peptide system is still uncertain. Here, we identify orthologous genes to those for VP/OT in Platyhelminthes, intertidal planarians that have a simple bilaterian body structure but lack a coelom and body-fluid circulatory system. We report a comprehensive characterization of the neuropeptide derived from this VP/OT-type gene, identifying its functional receptor, and name it the “platytocin” system. Our experiments with these euryhaline planarians, living where environmental salinities fluctuate due to evaporation and rainfall, suggest that platytocin functions as an “antidiuretic hormone” and also organizes diverse actions including reproduction and chemosensory-associated behavior. We propose that bilaterians acquired physiological adaptations to amphibious lives by such regulation of the body fluids. This neuropeptide-secreting system clearly became indispensable for life even without the development of a vascular circulatory system or relevant synapses.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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