A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.

Sensory neuron diversity is required for organisms to decipher complex environmental cues. In Drosophila, the olfactory environment is detected by 50 different olfactory receptor neuron (ORN) classes that are clustered in combinations within distinct sensilla subtypes. Each sensilla subtype houses s...

Full description

Bibliographic Details
Main Authors: Qingyun Li, Scott Barish, Sumie Okuwa, Abigail Maciejewski, Alicia T Brandt, Dominik Reinhold, Corbin D Jones, Pelin Cayirlioglu Volkan
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC4713227?pdf=render
id doaj-7d9afc91d0d148f6a1cb3b4671a07d80
record_format Article
spelling doaj-7d9afc91d0d148f6a1cb3b4671a07d802020-11-25T02:00:23ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042016-01-01121e100578010.1371/journal.pgen.1005780A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.Qingyun LiScott BarishSumie OkuwaAbigail MaciejewskiAlicia T BrandtDominik ReinholdCorbin D JonesPelin Cayirlioglu VolkanSensory neuron diversity is required for organisms to decipher complex environmental cues. In Drosophila, the olfactory environment is detected by 50 different olfactory receptor neuron (ORN) classes that are clustered in combinations within distinct sensilla subtypes. Each sensilla subtype houses stereotypically clustered 1-4 ORN identities that arise through asymmetric divisions from a single multipotent sensory organ precursor (SOP). How each class of SOPs acquires a unique differentiation potential that accounts for ORN diversity is unknown. Previously, we reported a critical component of SOP diversification program, Rotund (Rn), increases ORN diversity by generating novel developmental trajectories from existing precursors within each independent sensilla type lineages. Here, we show that Rn, along with BarH1/H2 (Bar), Bric-à-brac (Bab), Apterous (Ap) and Dachshund (Dac), constitutes a transcription factor (TF) network that patterns the developing olfactory tissue. This network was previously shown to pattern the segmentation of the leg, which suggests that this network is functionally conserved. In antennal imaginal discs, precursors with diverse ORN differentiation potentials are selected from concentric rings defined by unique combinations of these TFs along the proximodistal axis of the developing antennal disc. The combinatorial code that demarcates each precursor field is set up by cross-regulatory interactions among different factors within the network. Modifications of this network lead to predictable changes in the diversity of sensilla subtypes and ORN pools. In light of our data, we propose a molecular map that defines each unique SOP fate. Our results highlight the importance of the early prepatterning gene regulatory network as a modulator of SOP and terminally differentiated ORN diversity. Finally, our model illustrates how conserved developmental strategies are used to generate neuronal diversity.http://europepmc.org/articles/PMC4713227?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Qingyun Li
Scott Barish
Sumie Okuwa
Abigail Maciejewski
Alicia T Brandt
Dominik Reinhold
Corbin D Jones
Pelin Cayirlioglu Volkan
spellingShingle Qingyun Li
Scott Barish
Sumie Okuwa
Abigail Maciejewski
Alicia T Brandt
Dominik Reinhold
Corbin D Jones
Pelin Cayirlioglu Volkan
A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.
PLoS Genetics
author_facet Qingyun Li
Scott Barish
Sumie Okuwa
Abigail Maciejewski
Alicia T Brandt
Dominik Reinhold
Corbin D Jones
Pelin Cayirlioglu Volkan
author_sort Qingyun Li
title A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.
title_short A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.
title_full A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.
title_fullStr A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.
title_full_unstemmed A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.
title_sort functionally conserved gene regulatory network module governing olfactory neuron diversity.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2016-01-01
description Sensory neuron diversity is required for organisms to decipher complex environmental cues. In Drosophila, the olfactory environment is detected by 50 different olfactory receptor neuron (ORN) classes that are clustered in combinations within distinct sensilla subtypes. Each sensilla subtype houses stereotypically clustered 1-4 ORN identities that arise through asymmetric divisions from a single multipotent sensory organ precursor (SOP). How each class of SOPs acquires a unique differentiation potential that accounts for ORN diversity is unknown. Previously, we reported a critical component of SOP diversification program, Rotund (Rn), increases ORN diversity by generating novel developmental trajectories from existing precursors within each independent sensilla type lineages. Here, we show that Rn, along with BarH1/H2 (Bar), Bric-à-brac (Bab), Apterous (Ap) and Dachshund (Dac), constitutes a transcription factor (TF) network that patterns the developing olfactory tissue. This network was previously shown to pattern the segmentation of the leg, which suggests that this network is functionally conserved. In antennal imaginal discs, precursors with diverse ORN differentiation potentials are selected from concentric rings defined by unique combinations of these TFs along the proximodistal axis of the developing antennal disc. The combinatorial code that demarcates each precursor field is set up by cross-regulatory interactions among different factors within the network. Modifications of this network lead to predictable changes in the diversity of sensilla subtypes and ORN pools. In light of our data, we propose a molecular map that defines each unique SOP fate. Our results highlight the importance of the early prepatterning gene regulatory network as a modulator of SOP and terminally differentiated ORN diversity. Finally, our model illustrates how conserved developmental strategies are used to generate neuronal diversity.
url http://europepmc.org/articles/PMC4713227?pdf=render
work_keys_str_mv AT qingyunli afunctionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT scottbarish afunctionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT sumieokuwa afunctionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT abigailmaciejewski afunctionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT aliciatbrandt afunctionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT dominikreinhold afunctionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT corbindjones afunctionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT pelincayirliogluvolkan afunctionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT qingyunli functionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT scottbarish functionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT sumieokuwa functionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT abigailmaciejewski functionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT aliciatbrandt functionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT dominikreinhold functionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT corbindjones functionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
AT pelincayirliogluvolkan functionallyconservedgeneregulatorynetworkmodulegoverningolfactoryneurondiversity
_version_ 1724960937029402624