Ordered patterning of the sensory system is susceptible to stochastic features of gene expression

Sensory neuron numbers and positions are precisely organized to accurately map environmental signals in the brain. This precision emerges from biochemical processes within and between cells that are inherently stochastic. We investigated impact of stochastic gene expression on pattern formation, foc...

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Main Authors: Ritika Giri, Dimitrios K Papadopoulos, Diana M Posadas, Hemanth K Potluri, Pavel Tomancak, Madhav Mani, Richard W Carthew
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/53638
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spelling doaj-6db9f188efc343ad947952776882d9992021-05-05T20:52:10ZengeLife Sciences Publications LtdeLife2050-084X2020-02-01910.7554/eLife.53638Ordered patterning of the sensory system is susceptible to stochastic features of gene expressionRitika Giri0https://orcid.org/0000-0001-8838-0818Dimitrios K Papadopoulos1Diana M Posadas2Hemanth K Potluri3Pavel Tomancak4https://orcid.org/0000-0002-2222-9370Madhav Mani5Richard W Carthew6https://orcid.org/0000-0003-0343-0156Department of Molecular Biosciences, Northwestern University, Evanston, United States; NSF-Simons Center for Quantitative Biology, Northwestern University, Evanston, United StatesMax Planck Institute of Cell Biology and Genetics, Dresden, GermanyDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesMax Planck Institute of Cell Biology and Genetics, Dresden, GermanyDepartment of Molecular Biosciences, Northwestern University, Evanston, United States; NSF-Simons Center for Quantitative Biology, Northwestern University, Evanston, United States; Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, United StatesDepartment of Molecular Biosciences, Northwestern University, Evanston, United States; NSF-Simons Center for Quantitative Biology, Northwestern University, Evanston, United StatesSensory neuron numbers and positions are precisely organized to accurately map environmental signals in the brain. This precision emerges from biochemical processes within and between cells that are inherently stochastic. We investigated impact of stochastic gene expression on pattern formation, focusing on senseless (sens), a key determinant of sensory fate in Drosophila. Perturbing microRNA regulation or genomic location of sens produced distinct noise signatures. Noise was greatly enhanced when both sens alleles were present in homologous loci such that each allele was regulated in trans by the other allele. This led to disordered patterning. In contrast, loss of microRNA repression of sens increased protein abundance but not sensory pattern disorder. This suggests that gene expression stochasticity is a critical feature that must be constrained during development to allow rapid yet accurate cell fate resolution.https://elifesciences.org/articles/53638stochasticitygene expressionsensory developmentmicroRNAstransvection
collection DOAJ
language English
format Article
sources DOAJ
author Ritika Giri
Dimitrios K Papadopoulos
Diana M Posadas
Hemanth K Potluri
Pavel Tomancak
Madhav Mani
Richard W Carthew
spellingShingle Ritika Giri
Dimitrios K Papadopoulos
Diana M Posadas
Hemanth K Potluri
Pavel Tomancak
Madhav Mani
Richard W Carthew
Ordered patterning of the sensory system is susceptible to stochastic features of gene expression
eLife
stochasticity
gene expression
sensory development
microRNAs
transvection
author_facet Ritika Giri
Dimitrios K Papadopoulos
Diana M Posadas
Hemanth K Potluri
Pavel Tomancak
Madhav Mani
Richard W Carthew
author_sort Ritika Giri
title Ordered patterning of the sensory system is susceptible to stochastic features of gene expression
title_short Ordered patterning of the sensory system is susceptible to stochastic features of gene expression
title_full Ordered patterning of the sensory system is susceptible to stochastic features of gene expression
title_fullStr Ordered patterning of the sensory system is susceptible to stochastic features of gene expression
title_full_unstemmed Ordered patterning of the sensory system is susceptible to stochastic features of gene expression
title_sort ordered patterning of the sensory system is susceptible to stochastic features of gene expression
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-02-01
description Sensory neuron numbers and positions are precisely organized to accurately map environmental signals in the brain. This precision emerges from biochemical processes within and between cells that are inherently stochastic. We investigated impact of stochastic gene expression on pattern formation, focusing on senseless (sens), a key determinant of sensory fate in Drosophila. Perturbing microRNA regulation or genomic location of sens produced distinct noise signatures. Noise was greatly enhanced when both sens alleles were present in homologous loci such that each allele was regulated in trans by the other allele. This led to disordered patterning. In contrast, loss of microRNA repression of sens increased protein abundance but not sensory pattern disorder. This suggests that gene expression stochasticity is a critical feature that must be constrained during development to allow rapid yet accurate cell fate resolution.
topic stochasticity
gene expression
sensory development
microRNAs
transvection
url https://elifesciences.org/articles/53638
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