Altering the temporal regulation of one transcription factor drives evolutionary trade-offs between head sensory organs

Ramaekers, Ariane; Claeys, Annelies; Kapun, Martin; Mouchel-Vielh, Emmanuèle; Potier, Delphine; Weinberger, Simon; Grillenzoni, Nicola; Dardalhon-Cuménal, Delphine; Yan, Jiekun; Wolf, Reinhard; Flatt, Thomas; Buchner, Erich; Hassan, Bassem A.

doi:10.1016/j.devcel.2019.07.027

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Altering the temporal regulation of one transcription factor drives evolutionary trade-offs between head sensory organs

Ramaekers, Ariane Institut du Cerveau et de la Moelle Epinière (ICM) - Hôpital Pitié-Salpêtrière, Sorbonne Université, Inserm, CNRS, Paris, France -
Claeys, Annelies VIB Center for Brain and Disease, VIB, Leuven, Belgium - Center for Human Genetics, University of Leuven School of Medicine, Leuven, Belgium
Kapun, Martin Department of Biology, University of Fribourg, Switzerland -
Mouchel-Vielh, Emmanuèle Sorbonne Université, CNRS, Laboratoire de Biologie du Développement, Institut de Biologie Paris Seine, LBD-IBPS), Paris, France
Potier, Delphine Aix-Marseille Université, CNRS, INSERM, CIML, Marseille, France
Weinberger, Simon VIB Center for Brain and Disease, VIB, Leuven, Belgium - Center for Human Genetics, University of Leuven School of Medicine, Leuven, Belgium
Grillenzoni, Nicola Institut du Cerveau et de la Moelle Epinière (ICM) - Hôpital Pitié-Salpêtrière, Sorbonne Université, Inserm, CNRS, Paris, France
Dardalhon-Cuménal, Delphine Sorbonne Université, CNRS, Laboratoire de Biologie du Développement, Institut de Biologie Paris Seine, LBD-IBPS), Paris, France
Yan, Jiekun VIB Center for Brain and Disease, VIB, Leuven, Belgium - Center for Human Genetics, University of Leuven School of Medicine, Leuven, Belgium
Wolf, Reinhard Rudolf Virchow Center for Experimental Biomedicine, University of Würzburg, Germany
Flatt, Thomas Department of Biology, University of Fribourg, Switzerland
Buchner, Erich Institute for Clinical Neurobiology, University Hospital Würzburg, Germany
Hassan, Bassem A. Institut du Cerveau et de la Moelle Epinière (ICM) - Hôpital Pitié-Salpêtrière, Sorbonne Université, Inserm, CNRS, Paris, France -

23.09.2019

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Developmental Cell. - 2019, vol. 50, no. 6, p. 780-792.e7

English Size trade-offs of visual versus olfactory organs is a pervasive feature of animal evolution. This could result from genetic or functional constraints. We demonstrate that head sensory organ size trade-offs in Drosophila are genetically encoded and arise through differential subdivision of the head primordium into visual versus non- visual fields. We discover that changes in the temporal regulation of the highly conserved eyeless/Pax6 gene expression during development is a conserved mechanism for sensory trade-offs within and between Drosophila species. We identify a natural single nucleotide polymorphism in the cis-regulatory region of eyeless in a binding site of its repressor Cut that is sufficient to alter its temporal regulation and eye size. Because eyeless/Pax6 is a conserved regulator of head sensory placode subdivision, we propose that its temporal regulation is key to define the relative size of head sensory organs.

Faculty

Faculté des sciences et de médecine

Department

Département de Biologie

Language