Using positional information to provide context for biological image analysis with MorphoGraphX 2.0

  1. Sören Strauss
  2. Adam Runions
  3. Brendan Lane
  4. Dennis Eschweiler
  5. Namrata Bajpai
  6. Nicola Trozzi
  7. Anne-Lise Routier-Kierzkowska
  8. Saiko Yoshida
  9. Sylvia Rodrigues da Silveira
  10. Athul Vijayan
  11. Rachele Tofanelli
  12. Mateusz Majda
  13. Emillie Echevin
  14. Constance Le Gloanec
  15. Hana Bertrand-Rakusova
  16. Milad Adibi
  17. Kay Schneitz
  18. George Bassel
  19. Daniel Kierzkowski
  20. Johannes Stegmaier
  21. Miltos Tsiantis
  22. Richard S Smith  Is a corresponding author
  1. Max Planck Institute for Plant Breeding Research, Germany
  2. John Innes Centre, United Kingdom
  3. RWTH Aachen University, Germany
  4. Université de Montréal, Canada
  5. University of Montreal, Canada
  6. Technical University of Munich, Germany
  7. University of Warwick, United Kingdom

Abstract

Positional information is a central concept in developmental biology. In developing organs, positional information can be idealized as a local coordinate system that arises from morphogen gradients controlled by organizers at key locations. This offers a plausible mechanism for the integration of the molecular networks operating in individual cells into the spatially-coordinated multicellular responses necessary for the organization of emergent forms. Understanding how positional cues guide morphogenesis requires the quantification of gene expression and growth dynamics in the context of their underlying coordinate systems. Here we present recent advances in the MorphoGraphX software (Barbier de Reuille et al., 2015)⁠ that implement a generalized framework to annotate developing organs with local coordinate systems. These coordinate systems introduce an organ-centric spatial context to microscopy data, allowing gene expression and growth to be quantified and compared in the context of the positional information thought to control them.

Data availability

Datasets and software are available at www.MorphoGraphX.org and Dryad

The following data sets were generated

Article and author information

Author details

  1. Sören Strauss

    Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Adam Runions

    Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7758-7423
  3. Brendan Lane

    John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Dennis Eschweiler

    Institute of Imaging and Computer Vision, RWTH Aachen University, Aachen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Namrata Bajpai

    Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Nicola Trozzi

    John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3951-6533
  7. Anne-Lise Routier-Kierzkowska

    Department of Biological Sciences, Université de Montréal, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0383-0811
  8. Saiko Yoshida

    Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Sylvia Rodrigues da Silveira

    Department of Biological Sciences, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  10. Athul Vijayan

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1837-6359
  11. Rachele Tofanelli

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5196-1122
  12. Mateusz Majda

    John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  13. Emillie Echevin

    Department of Biological Sciences, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  14. Constance Le Gloanec

    Department of Biological Sciences, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7959-6307
  15. Hana Bertrand-Rakusova

    Department of Biological Sciences, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  16. Milad Adibi

    Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  17. Kay Schneitz

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6688-0539
  18. George Bassel

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  19. Daniel Kierzkowski

    Department of Biological Sciences, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1947-8691
  20. Johannes Stegmaier

    Institute of Imaging and Computer Vision, RWTH Aachen University, Aachen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4072-3759
  21. Miltos Tsiantis

    Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  22. Richard S Smith

    John Innes Centre, Norwich, United Kingdom
    For correspondence
    Richard.Smith@jic.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9220-0787

Funding

Deutsche Forschungsgemeinschaft (Forschunggruppe 2581)

  • Kay Schneitz
  • Miltos Tsiantis
  • Richard S Smith

Human Frontiers Science Program (RGP0002/2020)

  • George Bassel

Max Planck Society (Core grant)

  • Miltos Tsiantis

Fonds Nature et Technologies (282285)

  • Anne-Lise Routier-Kierzkowska
  • Daniel Kierzkowski

Deutsche Forschungsgemeinschaft (ERA-CAPS V-Morph)

  • Richard S Smith

Biotechnology and Biological Sciences Research Council (ISP to John Innes Centre)

  • Richard S Smith

Bundesministerium für Bildung und Forschung (031A494 & 031A492)

  • Richard S Smith

Deutsche Forschungsgemeinschaft (STE2802/2-1)

  • Dennis Eschweiler

New Frontiers in Research Fund (2018-00953)

  • Anne-Lise Routier-Kierzkowska
  • Daniel Kierzkowski

Natural Sciences and Engineering Research Council of Canada (RGPIN-2018-04897)

  • Daniel Kierzkowski

Natural Sciences and Engineering Research Council of Canada (RGPIN-2018-05762)

  • Anne-Lise Routier-Kierzkowska

Leverhulme Trust (RPG-2019-267)

  • George Bassel

Biotechnology and Biological Sciences Research Council (BB/S002804/1)

  • George Bassel

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

Copyright

© 2022, Strauss 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

  • 4,046
    views
  • 630
    downloads
  • 64
    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. Sören Strauss
  2. Adam Runions
  3. Brendan Lane
  4. Dennis Eschweiler
  5. Namrata Bajpai
  6. Nicola Trozzi
  7. Anne-Lise Routier-Kierzkowska
  8. Saiko Yoshida
  9. Sylvia Rodrigues da Silveira
  10. Athul Vijayan
  11. Rachele Tofanelli
  12. Mateusz Majda
  13. Emillie Echevin
  14. Constance Le Gloanec
  15. Hana Bertrand-Rakusova
  16. Milad Adibi
  17. Kay Schneitz
  18. George Bassel
  19. Daniel Kierzkowski
  20. Johannes Stegmaier
  21. Miltos Tsiantis
  22. Richard S Smith
(2022)
Using positional information to provide context for biological image analysis with MorphoGraphX 2.0
eLife 11:e72601.
https://doi.org/10.7554/eLife.72601

Share this article

https://doi.org/10.7554/eLife.72601

Further reading

    1. Developmental Biology
    Anastasiia Lozovska, Ana Casaca ... Moises Mallo
    Research Article

    During the trunk to tail transition the mammalian embryo builds the outlets for the intestinal and urogenital tracts, lays down the primordia for the hindlimb and external genitalia, and switches from the epiblast/primitive streak (PS) to the tail bud as the driver of axial extension. Genetic and molecular data indicate that Tgfbr1 is a key regulator of the trunk to tail transition. Tgfbr1 has been shown to control the switch of the neuromesodermal competent cells from the epiblast to the chordoneural hinge to generate the tail bud. We now show that in mouse embryos Tgfbr1 signaling also controls the remodeling of the lateral plate mesoderm (LPM) and of the embryonic endoderm associated with the trunk to tail transition. In the absence of Tgfbr1, the two LPM layers do not converge at the end of the trunk, extending instead as separate layers until the caudal embryonic extremity, and failing to activate markers of primordia for the hindlimb and external genitalia. The vascular remodeling involving the dorsal aorta and the umbilical artery leading to the connection between embryonic and extraembryonic circulation was also affected in the Tgfbr1 mutant embryos. Similar alterations in the LPM and vascular system were also observed in Isl1 null mutants, indicating that this factor acts in the regulatory cascade downstream of Tgfbr1 in LPM-derived tissues. In addition, in the absence of Tgfbr1 the embryonic endoderm fails to expand to form the endodermal cloaca and to extend posteriorly to generate the tail gut. We present evidence suggesting that the remodeling activity of Tgfbr1 in the LPM and endoderm results from the control of the posterior PS fate after its regression during the trunk to tail transition. Our data, together with previously reported observations, place Tgfbr1 at the top of the regulatory processes controlling the trunk to tail transition.

    1. Developmental Biology
    2. Neuroscience
    Odessa R Yabut, Jessica Arela ... Samuel J Pleasure
    Research Article

    Mutations in Sonic Hedgehog (SHH) signaling pathway genes, for example, Suppressor of Fused (SUFU), drive granule neuron precursors (GNP) to form medulloblastomas (MBSHH). However, how different molecular lesions in the Shh pathway drive transformation is frequently unclear, and SUFU mutations in the cerebellum seem distinct. In this study, we show that fibroblast growth factor 5 (FGF5) signaling is integral for many infantile MBSHH cases and that FGF5 expression is uniquely upregulated in infantile MBSHH tumors. Similarly, mice lacking SUFU (Sufu-cKO) ectopically express Fgf5 specifically along the secondary fissure where GNPs harbor preneoplastic lesions and show that FGFR signaling is also ectopically activated in this region. Treatment with an FGFR antagonist rescues the severe GNP hyperplasia and restores cerebellar architecture. Thus, direct inhibition of FGF signaling may be a promising and novel therapeutic candidate for infantile MBSHH.