Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila

Evidence for a conserved function in photoreceptors

Guojun Sheng, Eric Thouvenot, Dietmar Schmucker, David S. Wilson, Claude Desplan

Research output: Contribution to journalArticle

Abstract

Pax-6 is a transcription factor containing both a homeodomain (HD) and a Paired domain (PD). It functions as an essential regulator of eye development in both Drosophila and vertebrates, suggesting an evolutionarily conserved origin for different types of metazoan eyes. Classical morphological and phylogenetic studies, however, have concluded that metazoan eyes have evolved many times independently. These apparently contradictory findings may be reconciled if the evolutionarily ancient role of Pax-6 was to regulate structural genes (e.g., rhodopsin) in primitive photoreceptors, and only later did it expand its function to regulate the morphogenesis of divergent and complex eye structures. In support of this, we present evidence that eyeless (ey), which encodes the Drosophila homolog of Pax-6, directly regulates rhodopsin 1 (rh1) expression in the photoreceptor cells. We detect ey expression in both larval and adult terminally differentiated photoreceptor cells. We show that the HD of Ey binds to a palindromic HD binding site P3/RCS1 in the rh1 promoter, which is essential for rh1 expression. We further demonstrate that, in vivo, P3/RCS1 can be replaced by binding sites specific for the PD of Ey. P3/RCS1 is conserved in the promoters of all Drosophila rhodopsin genes as well as in many opsin genes in vertebrates. Mutimerized P3 sites in front of a basal promoter are able to drive the expression of a reporter gene in all photoreceptors. These results suggest that Pax-6/Ey directly regulates rhodopsin 1 gene expression by binding to the conserved P3/RCS1 element in the promoter.

Original languageEnglish (US)
Pages (from-to)1122-1131
Number of pages10
JournalGenes & development
Volume11
Issue number9
StatePublished - May 1 1997

Fingerprint

Rhodopsin
Drosophila
Photoreceptor Cells
Vertebrates
Binding Sites
Genes
Opsins
Morphogenesis
Reporter Genes
Transcription Factors
Gene Expression

Keywords

  • eye evolution
  • eyeless
  • homeodomain
  • Pax-6
  • photoreceptor cell
  • rhodopsin

ASJC Scopus subject areas

  • Genetics
  • Developmental Biology

Cite this

Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila : Evidence for a conserved function in photoreceptors. / Sheng, Guojun; Thouvenot, Eric; Schmucker, Dietmar; Wilson, David S.; Desplan, Claude.

In: Genes & development, Vol. 11, No. 9, 01.05.1997, p. 1122-1131.

Research output: Contribution to journalArticle

Sheng, Guojun ; Thouvenot, Eric ; Schmucker, Dietmar ; Wilson, David S. ; Desplan, Claude. / Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila : Evidence for a conserved function in photoreceptors. In: Genes & development. 1997 ; Vol. 11, No. 9. pp. 1122-1131.
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