The macula and fovea located at the optical centre of the retina make primate visual perception unique among mammals. Our current understanding of retina ontogenesis is primarily based on animal models having no macula and no fovea. However, the pigeon retina and the human macula share a number of structural and functional properties that justify introducing the former as a new model system for retina development. Comparative transcriptome analysis of pigeon and chicken retinas at different embryonic stages reveals that the genetic programmes underlying cell differentiation are postponed in the pigeon until the end of the period of cell proliferation. We show that the late onset of neurogenesis has a profound effect on the developmental patterning of the pigeon retina, which is at odds with the current models of retina development. The uncoupling of tissue growth and neurogenesis is shown to result from the fact that the pigeon retinal epithelium is inhibitory to cell differentiation. The sum of these developmental features allows the pigeon to build a retina that displays the structural and functional traits typical of primate macula and fovea.
The authors declare no competing or financial interests.
T.R., L.M.-S. and J.-M.M. carried out experiments. T.R., M.K. and J.-M.M. processed and analysed the data. D.S.-K. provided the ChIP data and participated in data analysis. T.R. and J.-M.M. conceived the study. J.-M.M. and L.M.-S. wrote the manuscript.
The Swiss National Science Foundation (Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung) [grant 31003A-149458], the Gelbert Foundation, the Velux Foundation (Velux Stiftung), the Fonds Suisse pour la prévention et la lutte contre la cécité, and the state of Geneva support our laboratory.
Unpublished histological data concerning the pigeon retina and optic nerve are available at http://www.genes-vision.ch/pigeon. RNA-Seq data have been deposited at Gene Expression Omnibus under accession number GSE89541.
Supplementary information available online at http://dev.biologists.org/lookup/doi/10.1242/dev.138719.supplemental
- Received April 18, 2016.
- Accepted November 1, 2016.