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Published November 2022 | Published + Supplemental Material
Journal Article Open

PEZO-1 and TRP-4 mechanosensors are involved in mating behavior in Caenorhabditis elegans

Abstract

Male mating in Caenorhabditis elegans is a complex behavior with a strong mechanosensory component. C. elegans has several characterized mechanotransducer proteins, but few have been shown to contribute to mating. Here, we investigated the roles of PEZO-1, a piezo channel, and TRP-4, a mechanotransducing TRPN channel, in male mating behavior. We show that pezo-1 is expressed in several male-specific neurons with known roles in mating. We show that, among other neurons, trp-4 is expressed in the Post-Cloacal sensilla neuron type A (PCA) sensory neuron, which monitors relative sliding between the male and the hermaphrodite and inhibits neurons involved in vulva detection. Mutations in both genes compromise many steps of mating, including initial response to the hermaphrodite, scanning, turning, and vulva detection. We performed pan-neuronal imaging during mating between freely moving mutant males and hermaphrodites. Both pezo-1 and trp-4 mutants showed spurious activation of the sensory neurons involved in vulva detection. In trp-4 mutants, this spurious activation might be caused by PCA failure to inhibit vulva-detecting neurons during scanning. Indeed, we show that without functional TRP-4, PCA fails to detect the relative sliding between the male and hermaphrodite. Cell-specific TRP-4 expression restores PCA's mechanosensory function. Our results demonstrate new roles for both PEZO-1 and TRP-4 mechanotransducers in C. elegans mating behavior.

Additional Information

© The Author(s) 2022. Published by Oxford University Press on behalf of the National Academy of Sciences. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. We thank WormBase: Davis P, Zarowiecki M, Arnaboldi V, Becerra A, Cain S, Chan J, Chen WJ, Cho J, da Veiga Beltrame E, Diamantakis S, Gao S, Grigoriadis D, Grove CA, Harris TW, Kishore R, Le T, Lee RYN, Luypaert M, Müller HM, Nakamura C, Nuin P, Paulini M, Quinton-Tulloch M, Raciti D, Rodgers FH, Russell M, Schindelman G, Singh A, Stickland T, Van Auken K, Wang Q, Williams G, Wright AJ, Yook K, Berriman M, Howe KL, Schedl T, Stein L, Sternberg PW. WormBase in 2022-data, processes, and tools for analyzing Caenorhabditis elegans. Genetics. 2022 Apr 4;220(4):iyac003. doi: 10.1093/genetics/iyac003. PMID: 35134929; for genome information, CGC for providing strains, Ian Kimbell for help with data collecting, Xiaofei Bai for providing AG570 pezo-1(av240), Shawn Xu for sharing a plasmid containing trp-4, and Tsui-Fen Chou for providing Cas9 protein. This work was supported by NIH R01-NS113119 (P.W.S. and A.D.T.S.). K.B. was supported by NIH-Training Grant T32GM007616. Authors' Contributions. K.B., V.S., and P.W. designed the project. K.B., V.S., and A.W. performed the experiments. K.B., W.P. and S.N. created essential reagents. K.B. and V.S. collected and analyzed the data. K.B., V.S., A.S., and P.W wrote the manuscript. K.I.B and V.S contributed equally to this work. Data Availability. All data are included in the manuscript and/or Supplementary Material. The authors declare no conflict of interest.

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Additional details

Created:
August 20, 2023
Modified:
December 22, 2023