Glial and neuronal Semaphorin signaling instruct the development of a functional myotopic map for Drosophila walking

Motoneurons developmentally acquire appropriate cellular architectures that ensure connections with postsynaptic muscles and presynaptic neurons. In Drosophila, leg motoneurons are organized as a myotopic map, where their dendritic domains represent the muscle field. Here, we investigate mechanisms...

Full description

Bibliographic Details
Main Authors: Durafshan Sakeena Syed, Swetha B.M. Gowda, O Venkateswara Reddy, Heinrich Reichert, K VijayRaghavan
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/11572
_version_ 1811227875449241600
author Durafshan Sakeena Syed
Swetha B.M. Gowda
O Venkateswara Reddy
Heinrich Reichert
K VijayRaghavan
author_facet Durafshan Sakeena Syed
Swetha B.M. Gowda
O Venkateswara Reddy
Heinrich Reichert
K VijayRaghavan
author_sort Durafshan Sakeena Syed
collection DOAJ
description Motoneurons developmentally acquire appropriate cellular architectures that ensure connections with postsynaptic muscles and presynaptic neurons. In Drosophila, leg motoneurons are organized as a myotopic map, where their dendritic domains represent the muscle field. Here, we investigate mechanisms underlying development of aspects of this myotopic map, required for walking. A behavioral screen identified roles for Semaphorins (Sema) and Plexins (Plex) in walking behavior. Deciphering this phenotype, we show that PlexA/Sema1a mediates motoneuron axon branching in ways that differ in the proximal femur and distal tibia, based on motoneuronal birth order. Importantly, we show a novel role for glia in positioning dendrites of specific motoneurons; PlexB/Sema2a is required for dendritic positioning of late-born motoneurons but not early-born motoneurons. These findings indicate that communication within motoneurons and between glia and motoneurons, mediated by the combined action of different Plexin/Semaphorin signaling systems, are required for the formation of a functional myotopic map.
first_indexed 2024-04-12T09:48:05Z
format Article
id doaj.art-d0551c3f455c4c2d8db633597fe8803d
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T09:48:05Z
publishDate 2016-02-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-d0551c3f455c4c2d8db633597fe8803d2022-12-22T03:37:53ZengeLife Sciences Publications LtdeLife2050-084X2016-02-01510.7554/eLife.11572Glial and neuronal Semaphorin signaling instruct the development of a functional myotopic map for Drosophila walkingDurafshan Sakeena Syed0Swetha B.M. Gowda1O Venkateswara Reddy2Heinrich Reichert3K VijayRaghavan4https://orcid.org/0000-0002-4705-5629National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, IndiaNational Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India; Manipal University, Manipal, IndiaNational Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, IndiaBiozentrum, University of Basel, Basel, SwitzerlandNational Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, IndiaMotoneurons developmentally acquire appropriate cellular architectures that ensure connections with postsynaptic muscles and presynaptic neurons. In Drosophila, leg motoneurons are organized as a myotopic map, where their dendritic domains represent the muscle field. Here, we investigate mechanisms underlying development of aspects of this myotopic map, required for walking. A behavioral screen identified roles for Semaphorins (Sema) and Plexins (Plex) in walking behavior. Deciphering this phenotype, we show that PlexA/Sema1a mediates motoneuron axon branching in ways that differ in the proximal femur and distal tibia, based on motoneuronal birth order. Importantly, we show a novel role for glia in positioning dendrites of specific motoneurons; PlexB/Sema2a is required for dendritic positioning of late-born motoneurons but not early-born motoneurons. These findings indicate that communication within motoneurons and between glia and motoneurons, mediated by the combined action of different Plexin/Semaphorin signaling systems, are required for the formation of a functional myotopic map.https://elifesciences.org/articles/11572semaphorinmotor neuronsmyotopic mapneuron targetingglia
spellingShingle Durafshan Sakeena Syed
Swetha B.M. Gowda
O Venkateswara Reddy
Heinrich Reichert
K VijayRaghavan
Glial and neuronal Semaphorin signaling instruct the development of a functional myotopic map for Drosophila walking
eLife
semaphorin
motor neurons
myotopic map
neuron targeting
glia
title Glial and neuronal Semaphorin signaling instruct the development of a functional myotopic map for Drosophila walking
title_full Glial and neuronal Semaphorin signaling instruct the development of a functional myotopic map for Drosophila walking
title_fullStr Glial and neuronal Semaphorin signaling instruct the development of a functional myotopic map for Drosophila walking
title_full_unstemmed Glial and neuronal Semaphorin signaling instruct the development of a functional myotopic map for Drosophila walking
title_short Glial and neuronal Semaphorin signaling instruct the development of a functional myotopic map for Drosophila walking
title_sort glial and neuronal semaphorin signaling instruct the development of a functional myotopic map for drosophila walking
topic semaphorin
motor neurons
myotopic map
neuron targeting
glia
url https://elifesciences.org/articles/11572
work_keys_str_mv AT durafshansakeenasyed glialandneuronalsemaphorinsignalinginstructthedevelopmentofafunctionalmyotopicmapfordrosophilawalking
AT swethabmgowda glialandneuronalsemaphorinsignalinginstructthedevelopmentofafunctionalmyotopicmapfordrosophilawalking
AT ovenkateswarareddy glialandneuronalsemaphorinsignalinginstructthedevelopmentofafunctionalmyotopicmapfordrosophilawalking
AT heinrichreichert glialandneuronalsemaphorinsignalinginstructthedevelopmentofafunctionalmyotopicmapfordrosophilawalking
AT kvijayraghavan glialandneuronalsemaphorinsignalinginstructthedevelopmentofafunctionalmyotopicmapfordrosophilawalking