The function of Drosophila larval class IV dendritic arborization sensory neurons in the larval-pupal transition is separable from their function in mechanical nociception responses.

The sensory and physiological inputs which govern the larval-pupal transition in Drosophila, and the neuronal circuity that integrates them, are complex. Previous work from our laboratory identified a dosage-sensitive genetic interaction between the genes encoding the Rho-GEF Trio and the zinc-finge...

Full description

Saved in:
Bibliographic Details
Main Authors: Hannah E Brown, Trishna Desai, Allison J Murphy, Harshida Pancholi, Zachary W Schmidt, Hannah Swahn, Eric C Liebl
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0184950&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850076479547768832
author Hannah E Brown
Trishna Desai
Allison J Murphy
Harshida Pancholi
Zachary W Schmidt
Hannah Swahn
Eric C Liebl
author_facet Hannah E Brown
Trishna Desai
Allison J Murphy
Harshida Pancholi
Zachary W Schmidt
Hannah Swahn
Eric C Liebl
author_sort Hannah E Brown
collection DOAJ
description The sensory and physiological inputs which govern the larval-pupal transition in Drosophila, and the neuronal circuity that integrates them, are complex. Previous work from our laboratory identified a dosage-sensitive genetic interaction between the genes encoding the Rho-GEF Trio and the zinc-finger transcription factor Sequoia that interfered with the larval-pupal transition. Specifically, we reported heterozygous mutations in sequoia (seq) dominantly exacerbated the trio mutant phenotype, and this seq-enhanced trio mutant genotype blocked the transition of third instar larvae from foragers to wanderers, a requisite behavioral transition prior to pupation. In this work, we use the GAL4-UAS system to rescue this phenotype by tissue-specific trio expression. We find that expressing trio in the class IV dendritic arborization (da) sensory neurons rescues the larval-pupal transition, demonstrating the reliance of the larval-pupal transition on the integrity of these sensory neurons. As nociceptive responses also rely on the functionality of the class IV da neurons, we test mechanical nociceptive responses in our mutant and rescued larvae and find that mechanical nociception is separable from the ability to undergo the larval-pupal transition. This demonstrates for the first time that the roles of the class IV da neurons in governing two critical larval behaviors, the larval-pupal transition and mechanical nociception, are functionally separable from each other.
format Article
id doaj-art-55f4d2467f23490a9bf10cb87be81ad3
institution DOAJ
issn 1932-6203
language English
publishDate 2017-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-55f4d2467f23490a9bf10cb87be81ad32025-08-20T02:46:01ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-01129e018495010.1371/journal.pone.0184950The function of Drosophila larval class IV dendritic arborization sensory neurons in the larval-pupal transition is separable from their function in mechanical nociception responses.Hannah E BrownTrishna DesaiAllison J MurphyHarshida PancholiZachary W SchmidtHannah SwahnEric C LieblThe sensory and physiological inputs which govern the larval-pupal transition in Drosophila, and the neuronal circuity that integrates them, are complex. Previous work from our laboratory identified a dosage-sensitive genetic interaction between the genes encoding the Rho-GEF Trio and the zinc-finger transcription factor Sequoia that interfered with the larval-pupal transition. Specifically, we reported heterozygous mutations in sequoia (seq) dominantly exacerbated the trio mutant phenotype, and this seq-enhanced trio mutant genotype blocked the transition of third instar larvae from foragers to wanderers, a requisite behavioral transition prior to pupation. In this work, we use the GAL4-UAS system to rescue this phenotype by tissue-specific trio expression. We find that expressing trio in the class IV dendritic arborization (da) sensory neurons rescues the larval-pupal transition, demonstrating the reliance of the larval-pupal transition on the integrity of these sensory neurons. As nociceptive responses also rely on the functionality of the class IV da neurons, we test mechanical nociceptive responses in our mutant and rescued larvae and find that mechanical nociception is separable from the ability to undergo the larval-pupal transition. This demonstrates for the first time that the roles of the class IV da neurons in governing two critical larval behaviors, the larval-pupal transition and mechanical nociception, are functionally separable from each other.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0184950&type=printable
spellingShingle Hannah E Brown
Trishna Desai
Allison J Murphy
Harshida Pancholi
Zachary W Schmidt
Hannah Swahn
Eric C Liebl
The function of Drosophila larval class IV dendritic arborization sensory neurons in the larval-pupal transition is separable from their function in mechanical nociception responses.
PLoS ONE
title The function of Drosophila larval class IV dendritic arborization sensory neurons in the larval-pupal transition is separable from their function in mechanical nociception responses.
title_full The function of Drosophila larval class IV dendritic arborization sensory neurons in the larval-pupal transition is separable from their function in mechanical nociception responses.
title_fullStr The function of Drosophila larval class IV dendritic arborization sensory neurons in the larval-pupal transition is separable from their function in mechanical nociception responses.
title_full_unstemmed The function of Drosophila larval class IV dendritic arborization sensory neurons in the larval-pupal transition is separable from their function in mechanical nociception responses.
title_short The function of Drosophila larval class IV dendritic arborization sensory neurons in the larval-pupal transition is separable from their function in mechanical nociception responses.
title_sort function of drosophila larval class iv dendritic arborization sensory neurons in the larval pupal transition is separable from their function in mechanical nociception responses
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0184950&type=printable
work_keys_str_mv AT hannahebrown thefunctionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT trishnadesai thefunctionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT allisonjmurphy thefunctionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT harshidapancholi thefunctionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT zacharywschmidt thefunctionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT hannahswahn thefunctionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT ericcliebl thefunctionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT hannahebrown functionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT trishnadesai functionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT allisonjmurphy functionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT harshidapancholi functionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT zacharywschmidt functionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT hannahswahn functionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses
AT ericcliebl functionofdrosophilalarvalclassivdendriticarborizationsensoryneuronsinthelarvalpupaltransitionisseparablefromtheirfunctioninmechanicalnociceptionresponses