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Mechanisms of olfactory receptor neuron specification in Drosophila

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Detection of a broad range of chemosensory signals is necessary for the survival of multicellular organisms. Chemical signals are the main facilitators of foraging, escape, and social behaviors. To increase detection coverage, animal sensory systems have evolved to create a large number of neurons with highly specific functions. The olfactory system, much like the nervous system as a whole, is astonishingly diverse.1‐3 The mouse olfactory system has millions of neurons with over a thousand classes, whereas the more compact Drosophila genome has approximately 80 odorant receptor genes that give rise to 50 neuronal classes and 1300 neurons in the adult.4 Understanding how neuronal diversity is generated remains one of the central questions in developmental neurobiology. Here, we review the current knowledge on the development of the adult Drosophila olfactory system and the progress that has been made toward answering this central question. WIREs Dev Biol 2015, 4:609–621. doi: 10.1002/wdev.197 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Cellular Differentiation Nervous System Development > Flies
Structure of the Drosophila olfactory system. (a) The antenna is covered by sensory hairs called sensilla that can be divided into three classes based upon their morphology, basiconics, trichoids, and coeloconics. (b) Within morphological classes, sensilla can be divided into subtypes defined by the combination of olfactory receptor neurons (ORNs) they house. There are four classes of trichoid sensilla, at1‐4. Each houses a unique set of ORNs. (c) An example of a basiconic sensillum. ORNs project their dendrites into sensillum and express their receptors on the surface of their dendrites where the receptors dimerize with the olfactory coreceptor, Orco, and are exposed to the environment. (d) The antennal lobe of the fly brain is divided into class‐specific glomeruli, where ORN axons synapse with projection neuron (PN) dendrites. Each glomerulus is distinguished by its size position and shape. The glomeruli corresponding to ORNs from panel c are highlighted.
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Development of the Drosophila antennal lobe. Olfactory receptor neuron (ORN) axons enter the antennal lobe around 18 h APF (after puparium formation) via the antennal nerve, guided by Dscam and Robos, and defasciculate into two major bundles based upon Semaphorin‐2b (Sema‐2b)/Plexin‐B signaling. Around 22 h APF ORN axons begin to target their respective glomeruli controlled by Dscam, Robos teneurins, and Sema‐2b, and cross the midline at the commissure to reach the contralateral antennal lobe. Around 30 h APF maxillary palp ORN axons enter the antennal lobe and protoglomerular formation begins, under the control of N‐cadherin (Ncad) and Semaphorin‐1a (Sema‐1a). From 40 h APF, glomeruli segregate and form distinct boundaries and ORN axons synapse with their projection neuron (PN) dendrites, under the guidance of Dscam, teneurins, and Sema2a/2b.
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Generation of a sensillum from a single SOP through the use of Notch signaling. The initial SOP, initial precursor (pI), divides to create two daughter cell pIIa and pIIb, which will generate supporting cells and olfactory receptor neurons (ORNs), respectively. pIIb is Notch‐off and laterally inhibits pIIa from adopting a neural precursor fate through Notch signaling. pIIa and pIIb undergo two more rounds of division each before generating terminally differentiated cells. Blue cells express sens, green cells express cut, and N represents a Notch‐On state. Each ORN within a sensillum can also be defined by the combinatorial expression of elav, ham, and seven‐up (svp).
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Control of olfactory receptor neuron (ORN) identity by larval prepatterning factors. (a) Schematic of morphogen signaling in the antennal disc. Engrailed (En) and Hedgehog (Hh) are expressed in the posterior compartment of the disc and Hh diffuses and signals to the anterior compartment. Wingless (Wg) and Decapentaplegic (Dpp) signaling are activated by Hh and establish the dorsoventral axis. In the center of the disc, where Wg and Dpp signaling events meet, epidermal growth factor receptor (EGFR) is activated to establish the proximal–distal axis. (b) Decision tree of sensory organ precursor (SOP) identity based upon combinatorial expression of prepatterning factors. Each SOP expresses a combination of prepatterning factors that control its fate in a nested and hierarchical fashion. The expression any given factor modifies the fate of a given SOP based upon the previous or concurrent expression of other prepatterning factors. (c) Expression of lozenge (lz), amos, and atonal define sensillar morphological classes. Atonal expressing precursors develop into coeloconic sensilla. Amos expression is required for both basiconic and trichoid sensilla. The level of lz expression then divides out the two classes, with basiconics and trichoids expressing high and low lz, respectively. Rn expression creates two populations of precursors within each morphological class, thereby increasing the number of possible sensilla fates by a factor of 2.
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