Expression of estrogen-receptor related receptors in amphioxus and zebrafish: implications for the evolution of posterior brain segmentation at the invertebrate-to-vertebrate transition

Authors

  • Pierre-Luc Bardet,

    1. Laboratoire de Biologie Moléculaire de la Cellule, CNRS UMR 5161, IFR128 BioSciences Lyon-Gerland, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, 69007 Lyon, France
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    • 1 Present address: NIMR, Mammalian development, The Ridgeway-Mill Hill, London NW7 1AA, UK.

  • Michael Schubert,

    1. Laboratoire de Biologie Moléculaire de la Cellule, CNRS UMR 5161, IFR128 BioSciences Lyon-Gerland, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, 69007 Lyon, France
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  • Béatrice Horard,

    1. Laboratoire de Biologie Moléculaire de la Cellule, CNRS UMR 5161, IFR128 BioSciences Lyon-Gerland, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, 69007 Lyon, France
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  • Linda Z. Holland,

    1. Marine Biology Research Division, Scripps Institution of Oceanography, La Jolla, CA 92093-0202, USA
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  • Vincent Laudet,

    Corresponding author
    1. Laboratoire de Biologie Moléculaire de la Cellule, CNRS UMR 5161, IFR128 BioSciences Lyon-Gerland, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, 69007 Lyon, France
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  • Nicholas D. Holland,

    1. Marine Biology Research Division, Scripps Institution of Oceanography, La Jolla, CA 92093-0202, USA
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  • Jean-Marc Vanacker

    Corresponding author
    1. Laboratoire de Biologie Moléculaire de la Cellule, CNRS UMR 5161, IFR128 BioSciences Lyon-Gerland, Ecole Normale Supérieure de Lyon, 46 Allée d'Italie, 69007 Lyon, France
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    • 2Present address: Laboratoire Génotypes et Phénotypes Tumoraux, INSERM EMI229, CRLC Val d'Aurelle-Paul Lamarque, 34298 Montpellier cedex 5, France.


*Authors for correspondence (emails: vincent.laudet@ens-lyon.fr and jvanacker@valdorel.fnclcc.fr)

Abstract

Summary The evolutionary origin of vertebrate hindbrain segmentation is unclear since the amphioxus, the closest living invertebrate relative to the vertebrates, possesses a hindbrain homolog that displays no gross morphological segmentation. Three of the estrogen-receptor related (ERR) receptors are segmentally expressed in the zebrafish hindbrain, suggesting that their common ancestor was expressed in a similar, reiterated manner. We have also cloned and determined the developmental expression of the single homolog of the vertebrate ERR genes in the amphioxus (AmphiERR). This gene is also expressed in a segmented manner in a region considered homologous to the vertebrate hindbrain. In contrast to the expression of amphioxus islet (a LIM-homeobox gene that also labels motoneurons), AmphiERR expression persists longer in the hindbrain homolog and does not later extend to additional posterior cells. In addition, AmphiERR and one of its vertebrate homologs (ERRα) are expressed in the developing somitic musculature of amphioxus and zebrafish, respectively. Altogether, our results are consistent with fine structural evidence suggesting that the amphioxus hindbrain is segmented, and indicate that chordate ERR gene expression is a marker for both hindbrain and muscle segmentation. Furthermore, our data support an evolution model of chordate brain segmentation: originally, the program for anterior segmentation in the protochordate ancestors of the vertebrates resided in the developing axial mesoderm which imposed reiterated patterning on the adjacent neural tube; during early vertebrate evolution, this segmentation program was transferred to and controlled by the neural tube.

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