A host beetle pheromone regulates development and behavior in the nematode Pristionchus pacificus

  1. Jessica K Cinkornpumin
  2. Dona R Wisidagama
  3. Veronika Rapoport
  4. James L Go
  5. Christoph Dieterich
  6. Xiaoyue Wang
  7. Ralf J Sommer
  8. Ray L Hong  Is a corresponding author
  1. California State University, Northridge, United States
  2. University of Utah, United States
  3. Max Planck Institute for Biology of Ageing, Germany
  4. Max-Planck Institute for Developmental Biology, Germany

Abstract

Nematodes and insects are the two most speciose animal phyla and nematode-insect associations encompass widespread biological interactions. To dissect the chemical signals and the genes mediating this association, we investigated the effect of an oriental beetle sex pheromone on the development and behavior of the nematode Pristionchus pacificus. We found that while the beetle pheromone is attractive to P. pacificus adults, the pheromone arrests embryo development, paralyzes J2 larva, and inhibits exit of dauer larvae. To uncover the mechanism that regulate insect pheromone sensitivity, a newly identified mutant, Ppa-obi-1, is used to reveal the molecular links between altered attraction toward the beetle pheromone, as well as hypersensitivity to its paralyzing effects. Ppa-obi-1 encodes lipid-binding domains and reaches its highest expression in various cell types, including the amphid neuron sheath and excretory cells. Our data suggests that the beetle host pheromone may be a species-specific volatile synomone that coevolved with necromeny.

Article and author information

Author details

  1. Jessica K Cinkornpumin

    California State University, Northridge, Northridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Dona R Wisidagama

    University of Utah, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Veronika Rapoport

    California State University, Northridge, Northridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. James L Go

    California State University, Northridge, Northridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Christoph Dieterich

    Max Planck Institute for Biology of Ageing, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Xiaoyue Wang

    Max-Planck Institute for Developmental Biology, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Ralf J Sommer

    Max-Planck Institute for Developmental Biology, Tuebingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Ray L Hong

    California State University, Northridge, Northridge, United States
    For correspondence
    ray.hong@csun.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Oliver Hobert, Columbia University, United States

Version history

  1. Received: May 4, 2014
  2. Accepted: October 14, 2014
  3. Accepted Manuscript published: October 15, 2014 (version 1)
  4. Version of Record published: November 25, 2014 (version 2)

Copyright

© 2014, Cinkornpumin et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jessica K Cinkornpumin
  2. Dona R Wisidagama
  3. Veronika Rapoport
  4. James L Go
  5. Christoph Dieterich
  6. Xiaoyue Wang
  7. Ralf J Sommer
  8. Ray L Hong
(2014)
A host beetle pheromone regulates development and behavior in the nematode Pristionchus pacificus
eLife 3:e03229.
https://doi.org/10.7554/eLife.03229

Share this article

https://doi.org/10.7554/eLife.03229

Further reading

  1. A beetle pheromone that lures nematode worms to an insect host can also stop their development or even kill them outright.

    1. Developmental Biology
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    Inhibitory G alpha (GNAI or Gαi) proteins are critical for the polarized morphogenesis of sensory hair cells and for hearing. The extent and nature of their actual contributions remains unclear, however, as previous studies did not investigate all GNAI proteins and included non-physiological approaches. Pertussis toxin can downregulate functionally redundant GNAI1, GNAI2, GNAI3, and GNAO proteins, but may also induce unrelated defects. Here, we directly and systematically determine the role(s) of each individual GNAI protein in mouse auditory hair cells. GNAI2 and GNAI3 are similarly polarized at the hair cell apex with their binding partner G protein signaling modulator 2 (GPSM2), whereas GNAI1 and GNAO are not detected. In Gnai3 mutants, GNAI2 progressively fails to fully occupy the sub-cellular compartments where GNAI3 is missing. In contrast, GNAI3 can fully compensate for the loss of GNAI2 and is essential for hair bundle morphogenesis and auditory function. Simultaneous inactivation of Gnai2 and Gnai3 recapitulates for the first time two distinct types of defects only observed so far with pertussis toxin: (1) a delay or failure of the basal body to migrate off-center in prospective hair cells, and (2) a reversal in the orientation of some hair cell types. We conclude that GNAI proteins are critical for hair cells to break planar symmetry and to orient properly before GNAI2/3 regulate hair bundle morphogenesis with GPSM2.