The multi-level regulation of clownfish metamorphosis by thyroid hormones

Summary: Most marine organisms have a biphasic life cycle during which pelagic larvae transform into radically different juveniles. In vertebrates, the role of thyroid hormones (THs) in triggering this transition is well known, but how the morphological and physiological changes are integrated in a...

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Main Authors: Natacha Roux, Saori Miura, Mélanie Dussenne, Yuki Tara, Shu-hua Lee, Simon de Bernard, Mathieu Reynaud, Pauline Salis, Agneesh Barua, Abdelhay Boulahtouf, Patrick Balaguer, Karine Gauthier, David Lecchini, Yann Gibert, Laurence Besseau, Vincent Laudet
Format: Article
Language:English
Published: Elsevier 2023-07-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723006721
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author Natacha Roux
Saori Miura
Mélanie Dussenne
Yuki Tara
Shu-hua Lee
Simon de Bernard
Mathieu Reynaud
Pauline Salis
Agneesh Barua
Abdelhay Boulahtouf
Patrick Balaguer
Karine Gauthier
David Lecchini
Yann Gibert
Laurence Besseau
Vincent Laudet
author_facet Natacha Roux
Saori Miura
Mélanie Dussenne
Yuki Tara
Shu-hua Lee
Simon de Bernard
Mathieu Reynaud
Pauline Salis
Agneesh Barua
Abdelhay Boulahtouf
Patrick Balaguer
Karine Gauthier
David Lecchini
Yann Gibert
Laurence Besseau
Vincent Laudet
author_sort Natacha Roux
collection DOAJ
description Summary: Most marine organisms have a biphasic life cycle during which pelagic larvae transform into radically different juveniles. In vertebrates, the role of thyroid hormones (THs) in triggering this transition is well known, but how the morphological and physiological changes are integrated in a coherent way with the ecological transition remains poorly explored. To gain insight into this question, we performed an integrated analysis of metamorphosis of a marine teleost, the false clownfish (Amphiprion ocellaris). We show how THs coordinate a change in color vision as well as a major metabolic shift in energy production, highlighting how it orchestrates this transformation. By manipulating the activity of liver X regulator (LXR), a major regulator of metabolism, we also identify a tight link between metabolic changes and metamorphosis progression. Strikingly, we observed that these regulations are at play in the wild, explaining how hormones coordinate energy needs with available resources during the life cycle.
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spelling doaj.art-eaaaa56e65d6463498b1511cc2a8f5b72023-06-23T04:42:54ZengElsevierCell Reports2211-12472023-07-01427112661The multi-level regulation of clownfish metamorphosis by thyroid hormonesNatacha Roux0Saori Miura1Mélanie Dussenne2Yuki Tara3Shu-hua Lee4Simon de Bernard5Mathieu Reynaud6Pauline Salis7Agneesh Barua8Abdelhay Boulahtouf9Patrick Balaguer10Karine Gauthier11David Lecchini12Yann Gibert13Laurence Besseau14Vincent Laudet15Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, Observatoire Océanologique, 66650 Banyuls-sur-Mer, France; Okinawa Institute of Science and Technology, 1919-1 Tancha, Onna son, Okinawa 904-0495, JapanOkinawa Institute of Science and Technology, 1919-1 Tancha, Onna son, Okinawa 904-0495, JapanSorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, Observatoire Océanologique, 66650 Banyuls-sur-Mer, FranceOkinawa Institute of Science and Technology, 1919-1 Tancha, Onna son, Okinawa 904-0495, JapanMarine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, 23-10, Dah-Uen Rd., Jiau Shi, I-Lan 262, TaiwanAltrabio SAS, 30 Rue Pré-Gaudry, 69007 Lyon, FranceOkinawa Institute of Science and Technology, 1919-1 Tancha, Onna son, Okinawa 904-0495, JapanSorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, Observatoire Océanologique, 66650 Banyuls-sur-Mer, FranceOkinawa Institute of Science and Technology, 1919-1 Tancha, Onna son, Okinawa 904-0495, JapanInstitut de Recherche en Cancérologie de Montpellier (IRCM), INSERM, University of Montpellier, 34090 Montpellier, FranceInstitut de Recherche en Cancérologie de Montpellier (IRCM), INSERM, University of Montpellier, 34090 Montpellier, FranceInstitut de Génomique Fonctionnelle de Lyon, CNRS UMR 5242, INRAE USC 1370 École Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, 46 allée d’Italie, 69007 Lyon, FrancePSL Research University, EPHE-UPVD-CNRS-UAR 3278 CRIOBE BP 1013, 98729 Papetoai, Moorea, French Polynesia; Laboratoire d’Excellence “CORAIL,” 66100 Perpignan, FranceDepartment of Cell and Molecular Biology, University of Mississippi Medical Center, 2500 North State Street, Jackson, MS 39216, USASorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, Observatoire Océanologique, 66650 Banyuls-sur-Mer, France; Corresponding authorOkinawa Institute of Science and Technology, 1919-1 Tancha, Onna son, Okinawa 904-0495, Japan; Marine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, 23-10, Dah-Uen Rd., Jiau Shi, I-Lan 262, Taiwan; Corresponding authorSummary: Most marine organisms have a biphasic life cycle during which pelagic larvae transform into radically different juveniles. In vertebrates, the role of thyroid hormones (THs) in triggering this transition is well known, but how the morphological and physiological changes are integrated in a coherent way with the ecological transition remains poorly explored. To gain insight into this question, we performed an integrated analysis of metamorphosis of a marine teleost, the false clownfish (Amphiprion ocellaris). We show how THs coordinate a change in color vision as well as a major metabolic shift in energy production, highlighting how it orchestrates this transformation. By manipulating the activity of liver X regulator (LXR), a major regulator of metabolism, we also identify a tight link between metabolic changes and metamorphosis progression. Strikingly, we observed that these regulations are at play in the wild, explaining how hormones coordinate energy needs with available resources during the life cycle.http://www.sciencedirect.com/science/article/pii/S2211124723006721CP: Developmental biologyCP: Metabolism
spellingShingle Natacha Roux
Saori Miura
Mélanie Dussenne
Yuki Tara
Shu-hua Lee
Simon de Bernard
Mathieu Reynaud
Pauline Salis
Agneesh Barua
Abdelhay Boulahtouf
Patrick Balaguer
Karine Gauthier
David Lecchini
Yann Gibert
Laurence Besseau
Vincent Laudet
The multi-level regulation of clownfish metamorphosis by thyroid hormones
Cell Reports
CP: Developmental biology
CP: Metabolism
title The multi-level regulation of clownfish metamorphosis by thyroid hormones
title_full The multi-level regulation of clownfish metamorphosis by thyroid hormones
title_fullStr The multi-level regulation of clownfish metamorphosis by thyroid hormones
title_full_unstemmed The multi-level regulation of clownfish metamorphosis by thyroid hormones
title_short The multi-level regulation of clownfish metamorphosis by thyroid hormones
title_sort multi level regulation of clownfish metamorphosis by thyroid hormones
topic CP: Developmental biology
CP: Metabolism
url http://www.sciencedirect.com/science/article/pii/S2211124723006721
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