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

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.

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.

Metrics

  • 2,225
    views
  • 374
    downloads
  • 18
    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. 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

Further reading

    1. Neuroscience
    Francesco Longo
    Insight

    The neurotransmitter dopamine helps form long-term memories by increasing the production of proteins through a unique signaling pathway.

    1. Neuroscience
    John P Veillette, Fan Gao, Howard C Nusbaum
    Research Article

    Sensory signals from the body’s visceral organs (e.g. the heart) can robustly influence the perception of exteroceptive sensations. This interoceptive–exteroceptive interaction has been argued to underlie self-awareness by situating one’s perceptual awareness of exteroceptive stimuli in the context of one’s internal state, but studies probing cardiac influences on visual awareness have yielded conflicting findings. In this study, we presented separate grating stimuli to each of subjects’ eyes as in a classic binocular rivalry paradigm – measuring the duration for which each stimulus dominates in perception. However, we caused the gratings to ‘pulse’ at specific times relative to subjects’ real-time electrocardiogram, manipulating whether pulses occurred during cardiac systole, when baroreceptors signal to the brain that the heart has contracted, or in diastole when baroreceptors are silent. The influential ‘Baroreceptor Hypothesis’ predicts the effect of baroreceptive input on visual perception should be uniformly suppressive. In contrast, we observed that dominance durations increased for systole-entrained stimuli, inconsistent with the Baroreceptor Hypothesis. Furthermore, we show that this cardiac-dependent rivalry effect is preserved in subjects who are at-chance discriminating between systole-entrained and diastole-presented stimuli in a separate interoceptive awareness task, suggesting that our results are not dependent on conscious access to heartbeat sensations.