Molecular Basis for Cephalic Mechanosensitivity of Drosophila Larvae

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LETTER TO THE EDITOR

Molecular Basis for Cephalic Mechanosensitivity of Drosophila Larvae Zhenyu Zhang1 • Zhiyuan Li1 • Ting Liu1 • Wei Zhang1

Received: 9 December 2019 / Accepted: 3 June 2020 Ó Shanghai Institutes for Biological Sciences, CAS 2020

Dear Editor, For an animal to explore its environment, the mechanosensors on its head are of particular importance. For example, in Drosophila larvae that constantly explore the surrounding substrate during foraging and wandering, the cephalic segments host highly specialized organs with extraordinary mechanical sensitivity [1]. While mechanosensation on the thoracic and abdominal segments has been studied extensively [2], the functions and molecular features of cephalic mechanosensation have not yet been characterized, despite the unambiguous presence of mechanosensors [3]. In Drosophila, there are mainly two types of mechanosensory neuron (Types I and II) in the peripheral nervous system [4]. Type I neurons include external sensory (es) organ neurons and internal chordotonal neurons [5]. In contrast, Type II neurons are characterized by elaborate arborizations and are involved in mechanosensation and proprioception [2]. Moreover, the functions of several genes in the transient receptor potential (TRP) family have been demonstrated in larval abdominal gentle touch, sound, and locomotion [2, 6]. It is still an open question whether these genes function in cephalic mechanosensation [7]. Considering the anatomical differences between larval cephalic, thoracic, and abdominal segmental sensory organs, it is critical to determine the Electronic supplementary material The online version of this article (https://doi.org/10.1007/s12264-020-00555-x) contains supplementary material, which is available to authorized users. & Wei Zhang [email protected] 1

School of Life Sciences, Tsinghua-Peking Joint Center for Life Sciences, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China

expression and function of these genes in larval cephalic sensory organs as well as their functions in mechanotransduction. Fly larvae show stereotyped responses to gentle touch and the behavior pattern depends on the touch location. Previous studies have used a human eyelash to stroke the thoracic segments from posterior to anterior and quantified the touch sensitivity by scoring each response [8]. Given that such stimulation might be too strong for the larval head, we fabricated a U-shaped polypropylene probe to deliver reliable and mild touch stimuli (Fig. 1A). We found that the score in response to head touch was * 10 (summation of 5 trials) in wild-type larvae (Fig. 1B). As a first step to investigate the molecular mechanism underlying the head-touch response, we tested the head touch sensitivity of the mutants from a pool of mechanotransduction channel genes with the above assay (Fig. 1B). Among these genes, nompC and nanchung (nan) mutant larvae showed a significant defect in the head-touch response (Fig. 1B), w