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.

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.

Metrics

  • 3,150
    views
  • 197
    downloads
  • 35
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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. Cell Biology
    2. Developmental Biology
    Pavan K Nayak, Arul Subramanian, Thomas F Schilling
    Research Article Updated

    Mechanical forces play a critical role in tendon development and function, influencing cell behavior through mechanotransduction signaling pathways and subsequent extracellular matrix (ECM) remodeling. Here, we investigate the molecular mechanisms by which tenocytes in developing zebrafish embryos respond to muscle contraction forces during the onset of swimming and cranial muscle activity. Using genome-wide bulk RNA sequencing of FAC-sorted tenocytes we identify novel tenocyte markers and genes involved in tendon mechanotransduction. Embryonic tendons show dramatic changes in expression of matrix remodeling associated 5b (mxra5b), matrilin 1 (matn1), and the transcription factor kruppel-like factor 2a (klf2a), as muscles start to contract. Using embryos paralyzed either by loss of muscle contractility or neuromuscular stimulation we confirm that muscle contractile forces influence the spatial and temporal expression patterns of all three genes. Quantification of these gene expression changes across tenocytes at multiple tendon entheses and myotendinous junctions reveals that their responses depend on force intensity, duration, and tissue stiffness. These force-dependent feedback mechanisms in tendons, particularly in the ECM, have important implications for improved treatments of tendon injuries and atrophy.