1. Neuroscience

Stepwise wiring of the Drosophila olfactory map requires specific Plexin B levels

  1. Jiefu Li
  2. Ricardo Guajardo
  3. Chuanyun Xu
  4. Bing Wu
  5. Hongjie Li
  6. Tongchao Li
  7. David J Luginbuhl
  8. Xiaojun Xie
  9. Liqun Luo  Is a corresponding author
  1. Howard Hughes Medical Institute, Stanford University, United States
  2. Howard Hughes Medical Institute, The Johns Hopkins University School of Medicine, United States
https://doi.org/10.7554/eLife.39088
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  1. Jiefu Li
  2. Ricardo Guajardo
  3. Chuanyun Xu
  4. Bing Wu
  5. Hongjie Li
  6. Tongchao Li
  7. David J Luginbuhl
  8. Xiaojun Xie
  9. Liqun Luo
(2018)
Stepwise wiring of the Drosophila olfactory map requires specific Plexin B levels
eLife 7:e39088.
https://doi.org/10.7554/eLife.39088
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Abstract

The precise assembly of a neural circuit involves many consecutive steps. The conflict between a limited number of wiring molecules and the complexity of the neural network impels each molecule to execute multiple functions at different steps. Here, we examined the cell-type specific distribution of endogenous levels of axon guidance receptor Plexin B (PlexB) in the developing antennal lobe, the first olfactory processing center in Drosophila. We found that different classes of olfactory receptor neurons (ORNs) express PlexB at different levels in two wiring steps - axonal trajectory choice and subsequent target selection. In line with its temporally distinct patterns, the proper levels of PlexB control both steps in succession. Genetic interactions further revealed that the effect of high-level PlexB is antagonized by its canonical partner Sema2b. Thus, PlexB plays a multifaceted role in instructing the assembly of the Drosophila olfactory circuit through temporally-regulated expression patterns and expression level-dependent effects.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Jiefu Li

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Ricardo Guajardo

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Chuanyun Xu

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Bing Wu

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Hongjie Li

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Tongchao Li

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. David J Luginbuhl

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. Xiaojun Xie

    The Solomon H Snyder Department of Neuroscience, Howard Hughes Medical Institute, The Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3459-6095

  9. Liqun Luo

    Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, United States
    For correspondence
    lluo@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5467-9264

Funding

National Institutes of Health (R01-DC005982)

  • Liqun Luo

Howard Hughes Medical Institute

  • Liqun Luo

Stanford University (Vanessa Kong Kerzner Graduate Fellowship)

  • Jiefu Li

Genentech Foundation (Genentech Foundation Predoctoral Fellowship)

  • Jiefu Li

Stanford University (Stanford Neuroscience Institute Interdisciplinary Scholar)

  • Hongjie Li

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Kristin Scott, University of California, Berkeley, Berkeley, United States

Version history

  1. Received: June 10, 2018
  2. Accepted: August 22, 2018
  3. Accepted Manuscript published: August 23, 2018 (version 1)
  4. Version of Record published: August 31, 2018 (version 2)

Copyright

© 2018, Li 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. Jiefu Li
  2. Ricardo Guajardo
  3. Chuanyun Xu
  4. Bing Wu
  5. Hongjie Li
  6. Tongchao Li
  7. David J Luginbuhl
  8. Xiaojun Xie
  9. Liqun Luo
(2018)
Stepwise wiring of the Drosophila olfactory map requires specific Plexin B levels
eLife 7:e39088.
https://doi.org/10.7554/eLife.39088

Share this article

https://doi.org/10.7554/eLife.39088

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Further reading

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    Functional divergence of Plexin B structural motifs in distinct steps of Drosophila olfactory circuit assembly

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    Plexins exhibit multitudinous, evolutionarily conserved functions in neural development. How Plexins employ their diverse structural motifs in vivo to perform distinct roles is unclear. We previously reported that Plexin B (PlexB) controls multiple steps during the assembly of the Drosophila olfactory circuit (Li et al., 2018b). Here, we systematically mutagenized structural motifs of PlexB and examined the function of these variants in these multiple steps: axon fasciculation, trajectory choice, and synaptic partner selection. We found that the extracellular Sema domain is essential for all three steps, the catalytic site of the intracellular RapGAP is engaged in none, and the intracellular GTPase-binding motifs are essential for trajectory choice and synaptic partner selection, but are dispensable for fasciculation. Moreover, extracellular PlexB cleavage serves as a regulatory mechanism of PlexB signaling. Thus, the divergent roles of PlexB motifs in distinct steps of neural development contribute to its functional versatility in neural circuit assembly.

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