Extrinsic Activin signaling cooperates with an intrinsic temporal program to increase mushroom body neuronal diversity

  1. Anthony M Rossi  Is a corresponding author
  2. Claude Desplan  Is a corresponding author
  1. New York University, United States

Abstract

Temporal patterning of neural progenitors leads to the sequential production of diverse neuronal types. To better understand how extrinsic cues interact with intrinsic temporal programs to contribute to temporal patterning, we studied the Drosophila mushroom body neural progenitors (neuroblasts). Each of these four neuroblasts divides ~250 times to sequentially produce only three main neuronal types over the course of ~9 days of development: g, followed by α'β', and finally αβ neurons. The intrinsic temporal clock is composed of two RNA-binding proteins, IGF-II mRNA binding protein (Imp) and Syncrip (Syp), that are expressed in opposing temporal gradients. Activin signaling affects the production of α'β' neurons but whether and how this extrinsic cue interacts with the intrinsic temporal program was not known. We show that the Activin ligand Myoglianin produced from glia downregulates the levels of the intrinsic temporal factor Imp in mushroom body neuroblasts. In neuroblasts mutant for the Activin signaling receptor baboon, Imp levels are higher than normal during the α'β' temporal window, leading to the specific loss of the α'β' neurons. The intrinsic temporal clock still progresses but with a delay, skipping the α'β' window without affecting the total number of neurons produced: The number of g neurons likely increases, α'β' disappear, and the number of αβ neurons decreases. Our results illustrate that an extrinsic cue modifies an intrinsic temporal program to increase neuronal diversity.

Data availability

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

The following previously published data sets were used

Article and author information

Author details

  1. Anthony M Rossi

    Biology, New York University, New York, United States
    For correspondence
    amr808@nyu.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9345-7939
  2. Claude Desplan

    Center for Developmental Genetics, Department of Biology, New York University, New York, United States
    For correspondence
    cd38@nyu.edu
    Competing interests
    Claude Desplan, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6914-1413

Funding

National Eye Institute (R01 EY017916)

  • Claude Desplan

National Institute of Neurological Disorders and Stroke (R21 NS095288)

  • Claude Desplan

National Institutes of Health (T32 HD007520)

  • Anthony M Rossi

New York University (GSAS MacCracken Program)

  • Anthony M Rossi

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

Copyright

© 2020, Rossi & Desplan

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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https://doi.org/10.7554/eLife.58880

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