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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 (2019). Altering the temporal regulation of one transcription factor drives evolutionary trade-offs between head sensory organs. Developmental Cell, 50(6):780-792.

Abstract

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.

Abstract

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.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Scopus Subject Areas:Life Sciences > Molecular Biology
Life Sciences > General Biochemistry, Genetics and Molecular Biology
Life Sciences > Developmental Biology
Life Sciences > Cell Biology
Uncontrolled Keywords:Developmental Biology
Language:English
Date:1 September 2019
Deposited On:14 Feb 2020 14:21
Last Modified:29 Jul 2020 14:28
Publisher:Cell Press (Elsevier)
ISSN:1534-5807
OA Status:Closed
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1016/j.devcel.2019.07.027
PubMed ID:31447264
Project Information:
  • : FunderSNSF
  • : Grant IDPP00P3_133641
  • : Project TitlePopulation Genomic Basis of Evolutionary Change in Drosophila Aging and Life History

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