1. Developmental Biology
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Multi-view light-sheet imaging and tracking with the MaMuT software reveals the cell lineage of a direct developing arthropod limb

  1. Carsten Wolff  Is a corresponding author
  2. Jean-Yves Tinevez
  3. Tobias Pietzsch
  4. Evangelia Stamataki
  5. Benjamin Harich
  6. Léo Guignard
  7. Stephan Preibisch
  8. Spencer Shorte
  9. Philipp J Keller
  10. Pavel Tomancak  Is a corresponding author
  11. Anastasios Pavlopoulos  Is a corresponding author
  1. Humboldt- Universität zu Berlin, Germany
  2. Institut Pasteur, France
  3. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  4. Janelia Farm Research Campus, Howard Hughes Medical Institute, United States
  5. Max Delbrück Center for Molecular Medicine, Germany
  6. Max Planck Institute of Cell Biology and Genetics, Germany
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Cite this article as: eLife 2018;7:e34410 doi: 10.7554/eLife.34410

Abstract

During development, coordinated cell behaviors orchestrate tissue and organ morphogenesis. Detailed descriptions of cell lineages and behaviors provide a powerful framework to elucidate the mechanisms of morphogenesis. To study the cellular basis of limb development, we imaged transgenic fluorescently-labeled embryos from the crustacean Parhyale hawaiensis with multi-view light-sheet microscopy at high spatiotemporal resolution over several days of embryogenesis. The cell lineage of outgrowing thoracic limbs was reconstructed at single-cell resolution with new software called Massive Multi-view Tracker (MaMuT). In silico clonal analyses suggested that the early limb primordium becomes subdivided into anterior-posterior and dorsal-ventral compartments whose boundaries intersect at the distal tip of the growing limb. Limb-bud formation is associated with spatial modulation of cell proliferation, while limb elongation is also driven by preferential orientation of cell divisions along the proximal-distal growth axis. Cellular reconstructions were predictive of the expression patterns of limb development genes including the BMP morphogen Decapentaplegic.

Article and author information

Author details

  1. Carsten Wolff

    Institut für Biologie, Humboldt- Universität zu Berlin, Berlin, Germany
    For correspondence
    carsten.wolff@rz.hu-berlin.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5926-7338
  2. Jean-Yves Tinevez

    Center for Innovation and Technological Research, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Tobias Pietzsch

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Evangelia Stamataki

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Benjamin Harich

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Léo Guignard

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Stephan Preibisch

    Berlin Institute for Medical Systems Biology, Max Delbrück Center for Molecular Medicine, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Spencer Shorte

    Center for Innovation and Technological Research, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Philipp J Keller

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2896-4920
  10. Pavel Tomancak

    Max Planck Institute of Cell Biology and Genetics, Dresden, Germany
    For correspondence
    tomancak@mpi-cbg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2222-9370
  11. Anastasios Pavlopoulos

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    pavlopoulosa@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0230-5815

Funding

Howard Hughes Medical Institute

  • Evangelia Stamataki
  • Léo Guignard
  • Philipp J Keller
  • Anastasios Pavlopoulos

European Commission Marie Sklodowska-Curie Actions (FP7-IEF 302235)

  • Anastasios Pavlopoulos

Max-Planck-Institute of Molecular Cell Biology and Genetics

  • Tobias Pietzsch
  • Benjamin Harich
  • Pavel Tomancak

European Research Council (260746)

  • Tobias Pietzsch
  • Pavel Tomancak

Einstein Stiftung Berlin (A-2012_114)

  • Carsten Wolff

Institut Pasteur

  • Jean-Yves Tinevez
  • Spencer Shorte

Agence Nationale de la Recherche

  • Jean-Yves Tinevez
  • Spencer Shorte

Helmholtz-Gemeinschaft

  • Stephan Preibisch

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

Reviewing Editor

  1. Alejandro Sánchez Alvarado, Stowers Institute for Medical Research, United States

Publication history

  1. Received: December 15, 2017
  2. Accepted: March 26, 2018
  3. Accepted Manuscript published: March 29, 2018 (version 1)
  4. Version of Record published: May 1, 2018 (version 2)

Copyright

© 2018, Wolff 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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