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Sexually dimorphic architecture and function of a mechanosensory circuit in C. elegans

Author

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  • Hagar Setty

    (Weizmann Institute of Science
    Weizmann Institute of Science)

  • Yehuda Salzberg

    (Weizmann Institute of Science
    Weizmann Institute of Science)

  • Shadi Karimi

    (The Barcelona Institute of Science and Technology)

  • Elisheva Berent-Barzel

    (Weizmann Institute of Science
    Weizmann Institute of Science)

  • Michael Krieg

    (The Barcelona Institute of Science and Technology)

  • Meital Oren-Suissa

    (Weizmann Institute of Science
    Weizmann Institute of Science)

Abstract

How sensory perception is processed by the two sexes of an organism is still only partially understood. Despite some evidence for sexual dimorphism in auditory and olfactory perception, whether touch is sensed in a dimorphic manner has not been addressed. Here we find that the neuronal circuit for tail mechanosensation in C. elegans is wired differently in the two sexes and employs a different combination of sex-shared sensory neurons and interneurons in each sex. Reverse genetic screens uncovered cell- and sex-specific functions of the alpha-tubulin mec-12 and the sodium channel tmc-1 in sensory neurons, and of the glutamate receptors nmr-1 and glr-1 in interneurons, revealing the underlying molecular mechanisms that mediate tail mechanosensation. Moreover, we show that only in males, the sex-shared interneuron AVG is strongly activated by tail mechanical stimulation, and accordingly is crucial for their behavioral response. Importantly, sex reversal experiments demonstrate that the sexual identity of AVG determines both the behavioral output of the mechanosensory response and the molecular pathways controlling it. Our results present extensive sexual dimorphism in a mechanosensory circuit at both the cellular and molecular levels.

Suggested Citation

  • Hagar Setty & Yehuda Salzberg & Shadi Karimi & Elisheva Berent-Barzel & Michael Krieg & Meital Oren-Suissa, 2022. "Sexually dimorphic architecture and function of a mechanosensory circuit in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34661-3
    DOI: 10.1038/s41467-022-34661-3
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    References listed on IDEAS

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    1. Wei Li & Lijun Kang & Beverly J. Piggott & Zhaoyang Feng & X.Z. Shawn Xu, 2011. "The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans," Nature Communications, Nature, vol. 2(1), pages 1-9, September.
    2. Marios Chatzigeorgiou & Sangsu Bang & Sun Wook Hwang & William R. Schafer, 2013. "tmc-1 encodes a sodium-sensitive channel required for salt chemosensation in C. elegans," Nature, Nature, vol. 494(7435), pages 95-99, February.
    3. Jun-Xian Shen & Zhi-Min Xu & Zu-Lin Yu & Shuai Wang & De-Zhi Zheng & Shang-Chun Fan, 2011. "Ultrasonic frogs show extraordinary sex differences in auditory frequency sensitivity," Nature Communications, Nature, vol. 2(1), pages 1-5, September.
    4. Steven J. Cook & Travis A. Jarrell & Christopher A. Brittin & Yi Wang & Adam E. Bloniarz & Maksim A. Yakovlev & Ken C. Q. Nguyen & Leo T.-H. Tang & Emily A. Bayer & Janet S. Duerr & Hannes E. Bülow & , 2019. "Whole-animal connectomes of both Caenorhabditis elegans sexes," Nature, Nature, vol. 571(7763), pages 63-71, July.
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    Cited by:

    1. Rizwanul Haque & Sonu Peedikayil Kurien & Hagar Setty & Yehuda Salzberg & Gil Stelzer & Einav Litvak & Hila Gingold & Oded Rechavi & Meital Oren-Suissa, 2024. "Sex-specific developmental gene expression atlas unveils dimorphic gene networks in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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