Binary cell fate decisions and fate transformation in the Drosophila larval eye

PLoS Genet. 2013;9(12):e1004027. doi: 10.1371/journal.pgen.1004027. Epub 2013 Dec 26.

Abstract

The functionality of sensory neurons is defined by the expression of specific sensory receptor genes. During the development of the Drosophila larval eye, photoreceptor neurons (PRs) make a binary choice to express either the blue-sensitive Rhodopsin 5 (Rh5) or the green-sensitive Rhodopsin 6 (Rh6). Later during metamorphosis, ecdysone signaling induces a cell fate and sensory receptor switch: Rh5-PRs are re-programmed to express Rh6 and become the eyelet, a small group of extraretinal PRs involved in circadian entrainment. However, the genetic and molecular mechanisms of how the binary cell fate decisions are made and switched remain poorly understood. We show that interplay of two transcription factors Senseless (Sens) and Hazy control cell fate decisions, terminal differentiation of the larval eye and its transformation into eyelet. During initial differentiation, a pulse of Sens expression in primary precursors regulates their differentiation into Rh5-PRs and repression of an alternative Rh6-cell fate. Later, during the transformation of the larval eye into the adult eyelet, Sens serves as an anti-apoptotic factor in Rh5-PRs, which helps in promoting survival of Rh5-PRs during metamorphosis and is subsequently required for Rh6 expression. Comparably, during PR differentiation Hazy functions in initiation and maintenance of rhodopsin expression. Hazy represses Sens specifically in the Rh6-PRs, allowing them to die during metamorphosis. Our findings show that the same transcription factors regulate diverse aspects of larval and adult PR development at different stages and in a context-dependent manner.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation / genetics
  • Cell Lineage / genetics*
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Ecdysone / biosynthesis
  • Eye / growth & development*
  • Eye / metabolism
  • Gene Expression Regulation, Developmental
  • Larva / growth & development
  • Larva / metabolism
  • Metamorphosis, Biological / genetics*
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Photoreceptor Cells, Invertebrate / cytology
  • Photoreceptor Cells, Invertebrate / metabolism
  • Rhodopsin / genetics
  • Rhodopsin / metabolism
  • Sensory Receptor Cells / cytology
  • Sensory Receptor Cells / metabolism
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism

Substances

  • Drosophila Proteins
  • Nuclear Proteins
  • Rh5 protein, Drosophila
  • Rh6 protein, Drosophila
  • Transcription Factors
  • sens protein, Drosophila
  • Ecdysone
  • Rhodopsin

Grants and funding

Funding for this project was provided by the Swiss National Science Foundation (project number 31003A_149499) and the “Novartis Foundation for Biomedical Research.” The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.