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

Abstract

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.

A Multicomponent Neuronal Response Encodes the Larval Decision to Pupariate upon Amino Acid Starvation

“…In this study, we identify them as direct sensors of arginine. Recent reports have described how levels of dietary amino acids affecting their dendritic branching ( Watanabe et al, 2017 ) and subsequently that nutrient-dependent changes in dendritic branching are distinct from their nociceptive function ( Brown et al, 2017 ), thus strengthening the role of multidendritic sensory neurons in nutrient-sensing. We have explored the response to dietary deprivation of amino acids using a semi-intact preparation.…”

Gαq and Phospholipase Cβ signaling regulate nociceptor sensitivity in Drosophila melanogaster larvae

“…While we have hypothesized that NorpA is the major effector of Gαq in larval nociceptors, it is also possible that Gαq signals through other effectors aside from NorpA in the mdIV neurons. In some systems, the Trio rhoGEF is directly activated by Gαq signaling ( Lutz et al, 2005 ; Lutz et al, 2007 ; Rojas et al, 2007 ; Williams et al, 2007 ), and recent studies have demonstrated roles for Trio in regulating mdIV morphogenesis ( Brown et al, 2017 ; Iyer et al, 2012 ). However, Trio loss-of-function larvae do not display mechanical nociception defects, suggesting that Trio may not be an effector of Gαq for the modulation of nociceptor sensitivity ( Brown et al, 2017 ).…”

Fringe-positive Golgi outposts unite temporal Furin 2 convertase activity and spatial Delta signal to promote dendritic branch retraction

“…However, it remains puzzling why C4da dendrites undergo branch retraction in the L3 stage prior to the large-scale pruning in the pupal stage. As late L3 larvae advance to the wandering stage, they crawl out from food substrates to drier places for pupariation (Brown et al, 2017). C4da neurons are nociceptors for strong and harmful stimulations such as heat and UV light (Gorczyca et al, 2014;Xiang et al, 2010).…”