A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.
Abstract
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.
Type
Journal articleSubject
AnimalsCadherins
Cell Differentiation
DNA-Binding Proteins
Drosophila Proteins
Drosophila melanogaster
Gene Expression Regulation, Developmental
Gene Regulatory Networks
Imaginal Discs
LIM-Homeodomain Proteins
Nerve Net
Olfactory Receptor Neurons
Smell
Transcription Factors
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https://hdl.handle.net/10161/13274Published Version (Please cite this version)
10.1371/journal.pgen.1005780Publication Info
Li, Qingyun; Barish, Scott; Okuwa, Sumie; Maciejewski, Abigail; Brandt, Alicia T;
Reinhold, Dominik; ... Volkan, Pelin Cayirlioglu (2016). A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron
Diversity. PLoS Genet, 12(1). pp. e1005780. 10.1371/journal.pgen.1005780. Retrieved from https://hdl.handle.net/10161/13274.This is constructed from limited available data and may be imprecise. To cite this
article, please review & use the official citation provided by the journal.
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Show full item recordScholars@Duke
Pelin Cayirlioglu Volkan
Associate Professor of Biology
The long-term goal in the lab is to understand the developmental processes that establish
the basic organizational and functional principles of the neuronal circuits in the
brain. We investigate how the neuronal circuits assemble, functionally mature, remodel
in developmental and evolutionary time scales. To understand these processes the Volkan
lab uses the olfactory system of the genetically tractable Drosophila melanogaster
as a model organism and apply molecular, developmental and systems le

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