IDEAS home Printed from https://ideas.repec.org/a/plo/pgen00/1002587.html
   My bibliography  Save this article

ppk23-Dependent Chemosensory Functions Contribute to Courtship Behavior in Drosophila melanogaster

Author

Listed:
  • Beika Lu
  • Angela LaMora
  • Yishan Sun
  • Michael J Welsh
  • Yehuda Ben-Shahar

Abstract

Insects utilize diverse families of ion channels to respond to environmental cues and control mating, feeding, and the response to threats. Although degenerin/epithelial sodium channels (DEG/ENaC) represent one of the largest families of ion channels in Drosophila melanogaster, the physiological functions of these proteins are still poorly understood. We found that the DEG/ENaC channel ppk23 is expressed in a subpopulation of sexually dimorphic gustatory-like chemosensory bristles that are distinct from those expressing feeding-related gustatory receptors. Disrupting ppk23 or inhibiting activity of ppk23-expressing neurons did not alter gustatory responses. Instead, blocking ppk23-positive neurons or mutating the ppk23 gene delayed the initiation and reduced the intensity of male courtship. Furthermore, mutations in ppk23 altered the behavioral response of males to the female-specific aphrodisiac pheromone 7(Z), 11(Z)-Heptacosadiene. Together, these data indicate that ppk23 and the cells expressing it play an important role in the peripheral sensory system that determines sexual behavior in Drosophila. Author Summary: Insects utilize diverse families of ion channels to respond to environmental cues and control mating, feeding, and the response to threats. Degenerin/epithelial sodium channels (DEG/ENaC) represent one of the largest families of ion channels in Drosophila melanogaster. However, the physiological functions of the majority of these proteins in Drosophila or any other animal are still unknown. We discovered that the DEG/ENaC channel ppk23 is expressed in a subpopulation of sexually dimorphic gustatory-like chemosensory neurons. We show that ppk23 and the neurons expressing it are important for normal male sexual behaviors, possibly via the detection of an aphrodisiac pheromone, but not for feeding decisions. Together, these data indicate that DEG/ENaC signaling plays an important role in the peripheral sensory system that determines sexual behavior in Drosophila.

Suggested Citation

  • Beika Lu & Angela LaMora & Yishan Sun & Michael J Welsh & Yehuda Ben-Shahar, 2012. "ppk23-Dependent Chemosensory Functions Contribute to Courtship Behavior in Drosophila melanogaster," PLOS Genetics, Public Library of Science, vol. 8(3), pages 1-13, March.
    • Handle: RePEc:plo:pgen00:1002587
    DOI: 10.1371/journal.pgen.1002587
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1002587
    Download Restriction: no
    File URL: https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1002587&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pgen.1002587?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Peter A. Brennan & Frank Zufall, 2006. "Pheromonal communication in vertebrates," Nature, Nature, vol. 444(7117), pages 308-315, November.
    2. Koji Sato & Maurizio Pellegrino & Takao Nakagawa & Tatsuro Nakagawa & Leslie B. Vosshall & Kazushige Touhara, 2008. "Insect olfactory receptors are heteromeric ligand-gated ion channels," Nature, Nature, vol. 452(7190), pages 1002-1006, April.
    3. Dieter Wicher & Ronny Schäfer & René Bauernfeind & Marcus C. Stensmyr & Regine Heller & Stefan H. Heinemann & Bill S. Hansson, 2008. "Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels," Nature, Nature, vol. 452(7190), pages 1007-1011, April.
    4. Devanand S. Manoli & Margit Foss & Adriana Villella & Barbara J. Taylor & Jeffrey C. Hall & Bruce S. Baker, 2005. "Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour," Nature, Nature, vol. 436(7049), pages 395-400, July.
    5. Jayaram Chandrashekar & Christina Kuhn & Yuki Oka & David A. Yarmolinsky & Edith Hummler & Nicholas J. P. Ryba & Charles S. Zuker, 2010. "The cells and peripheral representation of sodium taste in mice," Nature, Nature, vol. 464(7286), pages 297-301, March.
    6. Peter Cameron & Makoto Hiroi & John Ngai & Kristin Scott, 2010. "The molecular basis for water taste in Drosophila," Nature, Nature, vol. 465(7294), pages 91-95, May.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Mengjing Sun & Yang Liu & William B Walker & Chengcheng Liu & Kejian Lin & Shaohua Gu & Yongjun Zhang & Jingjiang Zhou & Guirong Wang, 2013. "Identification and Characterization of Pheromone Receptors and Interplay between Receptors and Pheromone Binding Proteins in the Diamondback Moth, Plutella xyllostella," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-14, April.
    2. Yan Li & Mitchell Swerdloff & Tianyu She & Asiyah Rahman & Naveen Sharma & Reema Shah & Michael Castellano & Daniel Mogel & Jason Wu & Asim Ahmed & James San Miguel & Jared Cohn & Nikesh Shah & Raddy , 2023. "Robust odor identification in novel olfactory environments in mice," Nature Communications, Nature, vol. 14(1), pages 1-29, December.
    3. Hao-Ching Jiang & Sung Jin Park & I-Hao Wang & Daniel M. Bear & Alexandra Nowlan & Paul L. Greer, 2024. "CD20/MS4A1 is a mammalian olfactory receptor expressed in a subset of olfactory sensory neurons that mediates innate avoidance of predators," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Jann F Kolter & Markus F Hildenbrand & Sandy Popp & Stephan Nauroth & Julian Bankmann & Lisa Rother & Jonas Waider & Jürgen Deckert & Esther Asan & Peter M Jakob & Klaus-Peter Lesch & Angelika Schmitt, 2021. "Serotonin transporter genotype modulates resting state and predator stress-induced amygdala perfusion in mice in a sex-dependent manner," PLOS ONE, Public Library of Science, vol. 16(2), pages 1-22, February.
    5. Shobha Mummalaneni & Jie Qian & Tam-Hao T Phan & Mee-Ra Rhyu & Gerard L Heck & John A DeSimone & Vijay Lyall, 2014. "Effect of ENaC Modulators on Rat Neural Responses to NaCl," PLOS ONE, Public Library of Science, vol. 9(5), pages 1-18, May.
    6. Ziyu Liang & Courtney E. Wilson & Bochuan Teng & Sue C. Kinnamon & Emily R. Liman, 2023. "The proton channel OTOP1 is a sensor for the taste of ammonium chloride," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Ashkan A. Shahbandi & Ezen Choo & Robin Dando, 2018. "Receptor Regulation in Taste: Can Diet Influence How We Perceive Foods?," J, MDPI, vol. 1(1), pages 1-10, October.
    8. Jean-Pierre Rospars & Alexandre Grémiaux & David Jarriault & Antoine Chaffiol & Christelle Monsempes & Nina Deisig & Sylvia Anton & Philippe Lucas & Dominique Martinez, 2014. "Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons," PLOS Computational Biology, Public Library of Science, vol. 10(12), pages 1-16, December.
    9. Jody Pacalon & Guillaume Audic & Justine Magnat & Manon Philip & Jérôme Golebiowski & Christophe J. Moreau & Jérémie Topin, 2023. "Elucidation of the structural basis for ligand binding and translocation in conserved insect odorant receptor co-receptors," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    10. María de la Paz Fernández & Yick-Bun Chan & Joanne Y Yew & Jean-Christophe Billeter & Klaus Dreisewerd & Joel D Levine & Edward A Kravitz, 2010. "Pheromonal and Behavioral Cues Trigger Male-to-Female Aggression in Drosophila," PLOS Biology, Public Library of Science, vol. 8(11), pages 1-11, November.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pgen00:1002587. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosgenetics (email available below). General contact details of provider: https://journals.plos.org/plosgenetics/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.