Diverse Roles of Axonemal Dyneins in Drosophila Auditory Neuron Function and Mechanical Amplification in Hearing.

Somdatta Karak,Elena Sivan-Loukianova,Julie S Jacobs,Michael A Schon,Daniel F Eberl,Radoslaw Katana,Maike Kittelmann,Christian Spalthoff,Maurice J Kernan,Martin C Göpfert

doi:10.1038/srep17085

Abstract

Much like vertebrate hair cells, the chordotonal sensory neurons that mediate hearing in Drosophila are motile and amplify the mechanical input of the ear. Because the neurons bear mechanosensory primary cilia whose microtubule axonemes display dynein arms, we hypothesized that their motility is powered by dyneins. Here, we describe two axonemal dynein proteins that are required for Drosophila auditory neuron function, localize to their primary cilia, and differently contribute to mechanical amplification in hearing. Promoter fusions revealed that the two axonemal dynein genes Dmdnah3 (=CG17150) and Dmdnai2 (=CG6053) are expressed in chordotonal neurons, including the auditory ones in the fly’s ear. Null alleles of both dyneins equally abolished electrical auditory neuron responses, yet whereas mutations in Dmdnah3 facilitated mechanical amplification, amplification was abolished by mutations in Dmdnai2. Epistasis analysis revealed that Dmdnah3 acts downstream of Nan-Iav channels in controlling the amplificatory gain. Dmdnai2, in addition to being required for amplification, was essential for outer dynein arms in auditory neuron cilia. This establishes diverse roles of axonemal dyneins in Drosophila auditory neuron function and links auditory neuron motility to primary cilia and axonemal dyneins. Mutant defects in sperm competition suggest that both dyneins also function in sperm motility.

Highlights

The motility of Drosophila auditory neurons cannot be accessed directly but is betrayed by the fly’s auditory mechanics
The mere presence of these arms suggests that Drosophila auditory neurons might use axonemal dyneins to drive mechanical amplification, a possibility that seems supported by genetic evidence: both mechanical amplification and the dynein arms are disrupted by mutations in genes that are implicated in axonemal dynein arm assembly, including for example fd3f (Ref. 20), tilB (Refs 4,21), zmynd[10] (Refs 22,23), dyx1c1 (Refs 22,24), and hmw (Ref. 25)
Whereas mechanical amplification by hair cells involves prestin molecules and, presumably, myosin motors[40,41], amplification by the fly’s auditory chordotonal neurons is shown to involve dyneins: according to our results, axonemal dyneins are expressed in Drosophila chordotonal neurons and are required for their mechanosensory function and mechanical amplification in the ear

Summary

Introduction

The motility of Drosophila auditory neurons cannot be accessed directly but is betrayed by the fly’s auditory mechanics. The mere presence of these arms suggests that Drosophila auditory neurons might use axonemal dyneins to drive mechanical amplification, a possibility that seems supported by genetic evidence: both mechanical amplification and the dynein arms are disrupted by mutations in genes that are implicated in axonemal dynein arm assembly, including for example fd3f (Ref. 20), tilB (Refs 4,21), zmynd[10] (Refs 22,23), dyx1c1 (Refs 22,24), and hmw (Ref. 25). We describe two axonemal dynein subunits, an inner arm heavy chain and a WD-repeat intermediate chain, that are expressed in both males and females, in chordotonal sensory neurons including those of Johnston’s organ. Using mutations of these genes, we tested whether and, if so, how axonemal dyneins and ciliary motility contribute to Drosophila auditory neuron function and mechanical amplification in fly hearing

Methods

Results

Conclusion