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

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.

The Role of the Mechanotransduction Ion Channel Candidate Nanchung-Inactive in Auditory Transduction in an Insect Ear

“…The dendrites of chordotonal organ neurons of Diptera are considerably shorter (∼15 μm; Karak et al, 2015; Andrés et al, 2016) than the dendrites of orthopteran chordotonal neurons, which are ∼50 μm for cricket (Oldfield and Hill, 1986) and ∼110 μm for locust auditory neurons (measured here). Thus, dendritic spikes might not be a general principle of operation of chordotonal organ neurons, but rather a specialization for long dendrites.…”

The evolution of sperm axoneme structure and the dynein heavy chain complement in cecidomid insects

“…In the first case, the defect might be restricted to the germ line, and the gene might be actively expressed in the dendritic cilia of chordotonal organs; our inability to detect by RT-PCR its transcript in the larval or pupal cDNA could be attributable to its extremely low abundance. However, we note that, though sensory cilia have been shown in Drosophila to be endowed with dynein arms [Kavlie et al, 2010;Karak et al, 2015], most of the information that is currently available is limited to this species, and no observations have been reported on the sensory organs in cecidomids. It is thus possible that, similar to sperm cells, cecidomid sensory organs have realized structural adaptations allowing them to accomplish their function in the absence of dynein arms.…”

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis

“…30, 2017; individualization [45], gudu, an Armadillo repeat containing protein [46], and porin (mentioned 330 previously) [39]. Two proteins involved in sperm motility were also identified: dynein axonemal heavy 331 chain 3 (dnah3) [47] and an associated microtubule-binding protein growth arrest specific protein 8 332 (Gas8) [48]. 333…”