Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate

Kathryn L Pepple; Mardelle Atkins; Koen Venken; Kari Wellnitz; Mark Harding; Benjamin Frankfort; Graeme Mardon

doi:10.1242/dev.028951

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Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate

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Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate

Kathryn L Pepple, Mardelle Atkins, Koen Venken, Kari Wellnitz, Mark Harding, Benjamin Frankfort and Graeme Mardon

Development (Cambridge), Vol.135(24), pp.4071-4079

12/2008

DOI: 10.1242/dev.028951

PMCID: PMC3135101

PMID: 19004852

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Abstract

Patterning of sensory organs requires precise regulation of neural induction and repression. The neurocrystalline pattern of the adult Drosophila compound eye is generated by ordered selection of single founder photoreceptors (R8s) for each unit eye or ommatidium. R8 selection requires mechanisms that restrict R8 potential to a single cell from within a group of cells expressing the proneural gene atonal ( ato ). One model of R8 selection suggests that R8 precursors are selected from a three-cell ‘R8 equivalence group’ through repression of ato by the homeodomain transcription factor Rough (Ro). A second model proposes that lateral inhibition is sufficient to select a single R8 from an equipotent group of cells called the intermediate group (IG). Here, we provide new evidence that lateral inhibition, but not ro , is required for the initial selection of a single R8 precursor. We show that in ro mutants, ectopic R8s develop from R2,5 photoreceptor precursors independently of ectopic Ato and hours after normal R8s are specified. We also show that Ro directly represses the R8 specific zinc-finger transcription factor senseless ( sens ) in the developing R2,5 precursors to block ectopic R8 differentiation. Our results support a new model for R8 selection in which lateral inhibition establishes a transient pattern of selected R8s that is permanently reinforced by a repressive bistable loop between sens and ro . This model provides new insight into the strategies that allow successful integration of a repressive patterning signal, such as lateral inhibition, with continued developmental plasticity during retinal differentiation.

Eye

Senseless

Lateral inhibition

Drosophila

Rough

Photoreceptor

Details

Title: Subtitle: Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate
Creators: Kathryn L Pepple - Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA
Mardelle Atkins - Program in Developmental Biology, Baylor College of Medicine, Houston, TX 77030, USA
Koen Venken - Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA
Kari Wellnitz - Department of Pathology, Baylor College of Medicine, Houston, TX 77030, USA
Mark Harding - Department of Pathology, Baylor College of Medicine, Houston, TX 77030, USA
Benjamin Frankfort - Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA
Graeme Mardon - Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA
Resource Type: Journal article
Publication Details: Development (Cambridge), Vol.135(24), pp.4071-4079
DOI: 10.1242/dev.028951
PMID: 19004852
PMCID: PMC3135101
ISSN: 0950-1991
eISSN: 1477-9129
Grant note: T32 EY007102-14 || EY / National Eye Institute : NEI
Language: English
Date published: 12/2008
Academic Unit: Critical Care; Stead Family Department of Pediatrics
Record Identifier: 9984093508602771

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