Modular transcriptional programs separately define axon and dendrite connectivity

  1. Yerbol Z Kurmangaliyev
  2. Juyoun Yoo
  3. Samuel A LoCascio
  4. Lawrence Zipursky  Is a corresponding author
  1. Howard Hughes Medical Institute, University of California, Los Angeles, United States
  2. University of California, Los Angeles, United States

Abstract

Patterns of synaptic connectivity are remarkably precise and complex. Single-cell RNA sequencing has revealed a vast transcriptional diversity of neurons. Nevertheless, a clear logic underlying the transcriptional control of neuronal connectivity has yet to emerge. Here, we focused on Drosophila T4/T5 neurons, a class of closely related neuronal subtypes with different wiring patterns. Eight subtypes of T4/T5 neurons are defined by combinations of two patterns of dendritic inputs and four patterns of axonal outputs. Single-cell profiling during development revealed distinct transcriptional programs defining each dendrite and axon wiring pattern. These programs were defined by the expression of a few transcription factors and different combinations of cell surface proteins. Gain and loss of function studies provide evidence for independent control of different wiring features. We propose that modular transcriptional programs for distinct wiring features are assembled in different combinations to generate diverse patterns of neuronal connectivity.

Data availability

Raw sequencing data, single-cell expression matrix and cell clustering results were deposited to NCBI GEO under accession: GSE126139.

The following data sets were generated

Article and author information

Author details

  1. Yerbol Z Kurmangaliyev

    Department of Biological Chemistry, Howard Hughes Medical Institute, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Juyoun Yoo

    Neuroscience Interdepartmental Program, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Samuel A LoCascio

    Department of Biological Chemistry, Howard Hughes Medical Institute, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Lawrence Zipursky

    Department of Biological Chemistry, Howard Hughes Medical Institute, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    LZipursky@mednet.ucla.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5630-7181

Funding

Howard Hughes Medical Institute

  • Lawrence Zipursky

G Harold and Leila Y. Mathers Foundation

  • Lawrence Zipursky

National Institute of Neurological Disorders and Stroke (T32NS048004)

  • Samuel A LoCascio

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

Reviewing Editor

  1. Graeme W Davis, University of California, San Francisco, United States

Publication history

  1. Received: August 3, 2019
  2. Accepted: November 4, 2019
  3. Accepted Manuscript published: November 5, 2019 (version 1)
  4. Version of Record published: November 14, 2019 (version 2)

Copyright

© 2019, Kurmangaliyev 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. Yerbol Z Kurmangaliyev
  2. Juyoun Yoo
  3. Samuel A LoCascio
  4. Lawrence Zipursky
(2019)
Modular transcriptional programs separately define axon and dendrite connectivity
eLife 8:e50822.
https://doi.org/10.7554/eLife.50822

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