Natural variation in stochastic photoreceptor specification and color preference in Drosophila

Johns Hopkins University, United States
New York University, United States
University of Virginia, United States
Paris-Saclay Institute of Neuroscience, Université Paris Sud, Centre National de la Recherche Scientifque, Université Paris-Saclay, France

Research Article Dec 18, 2017

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Cite this article as: eLife 2017;6:e29593 doi: 10.7554/eLife.29593

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Abstract

Each individual perceives the world in a unique way, but little is known about the genetic basis of variation in sensory perception. In the fly eye, the random mosaic of color-detecting R7 photoreceptor subtypes is determined by stochastic ON/OFF expression of the transcription factor Spineless (Ss). In a genome-wide association study, we identified a naturally occurring insertion in a regulatory DNA element in ss that lowers the ratio of Ss^ON to Ss^OFF cells. This change in photoreceptor fates shifts the innate color preference of flies from green to blue. The genetic variant increases the binding affinity for Klumpfuss (Klu), a zinc finger transcriptional repressor that regulates ss expression. Klu is expressed at intermediate levels to determine the normal ratio of Ss^ON to Ss^OFF cells. Thus, binding site affinity and transcription factor levels are finely tuned to regulate stochastic expression, setting the ratio of alternative fates and ultimately determining color preference.

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Author details

Caitlin Anderson

Department of Biology, Johns Hopkins University, Baltimore, United States

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The authors declare that no competing interests exist.
India Reiss

Department of Biology, Johns Hopkins University, Baltimore, United States

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Cyrus Zhou

Department of Biology, Johns Hopkins University, Baltimore, United States

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Annie Cho

Department of Biology, Johns Hopkins University, Baltimore, United States

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Haziq Siddiqi

Department of Biology, Johns Hopkins University, Baltimore, United States

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Benjamin Mormann

Department of Biology, New York University, New York, United States

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Cameron M Avelis

Department of Biophysics, Johns Hopkins University, Baltimore, United States

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Peter Deford

Department of Biology, Johns Hopkins University, Baltimore, United States

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Alan Bergland

Department of Biology, University of Virginia, Charlottesville, United States

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"This ORCID iD identifies the author of this article:" 0000-0001-7145-7575
Elijah Roberts

Department of Biophysics, Johns Hopkins University, Baltimore, United States

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James Taylor

Department of Biology, Johns Hopkins University, Baltimore, United States

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5079-840X
Daniel Vasiliauskas

Paris-Saclay Institute of Neuroscience, Université Paris Sud, Centre National de la Recherche Scientifque, Université Paris-Saclay, Gif-sur-Yvette, France

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The authors declare that no competing interests exist.
Robert J Johnston

Department of Biology, Johns Hopkins University, Baltimore, United States

For correspondence
robertjohnston@jhu.edu

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5775-6218

Funding

National Eye Institute (R01EY025598)

Robert J Johnston

Pew Charitable Trusts (27373)

Robert J Johnston

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

Simon G Sprecher, University of Fribourg, Switzerland

Publication history

Received: June 14, 2017
Accepted: December 15, 2017
Accepted Manuscript published: December 18, 2017 (version 1)
Accepted Manuscript updated: December 22, 2017 (version 2)
Accepted Manuscript updated: December 23, 2017 (version 3)
Version of Record published: December 27, 2017 (version 4)
Version of Record updated: January 12, 2018 (version 5)
Version of Record updated: April 16, 2018 (version 6)

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.