Using positional information to provide context for biological image analysis with MorphoGraphX 2.0
- Max Planck Institute for Plant Breeding Research, Germany
- John Innes Centre, United Kingdom
- RWTH Aachen University, Germany
- Université de Montréal, Canada
- University of Montreal, Canada
- Technical University of Munich, Germany
- 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
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MorphoGraphX2: Datasets that demostrate how to create positional information with local coordinate systemsDryad Digital Repository, doi:10.5061/dryad.m905qfv1r.
Article and author information
Author details
Anne-Lise Routier-Kierzkowska
Constance Le Gloanec
Daniel Kierzkowski
Johannes Stegmaier
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.
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Using positional information to provide context for biological image analysis with MorphoGraphX 2.0
eLife 11:e72601.
https://doi.org/10.7554/eLife.72601
Further reading
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- Developmental Biology
Rhythmic and sequential segmentation of the growing vertebrate body relies on the segmentation clock, a multi-cellular oscillating genetic network. The clock is visible as tissue-level kinematic waves of gene expression that travel through the presomitic mesoderm (PSM) and arrest at the position of each forming segment. Here, we test how this hallmark wave pattern is driven by culturing single maturing PSM cells. We compare their cell-autonomous oscillatory and arrest dynamics to those we observe in the embryo at cellular resolution, finding similarity in the relative slowing of oscillations and arrest in concert with differentiation. This shows that cell-extrinsic signals are not required by the cells to instruct the developmental program underlying the wave pattern. We show that a cell-autonomous timing activity initiates during cell exit from the tailbud, then runs down in the anterior-ward cell flow in the PSM, thereby using elapsed time to provide positional information to the clock. Exogenous FGF lengthens the duration of the cell-intrinsic timer, indicating extrinsic factors in the embryo may regulate the segmentation clock via the timer. In sum, our work suggests that a noisy cell-autonomous, intrinsic timer drives the slowing and arrest of oscillations underlying the wave pattern, while extrinsic factors in the embryo tune this timer’s duration and precision. This is a new insight into the balance of cell-intrinsic and -extrinsic mechanisms driving tissue patterning in development.
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- Developmental Biology
- Genetics and Genomics
Repurposing of pleiotropic factors during execution of diverse cellular processes has emerged as a regulatory paradigm. Embryonic development in metazoans is controlled by maternal factors deposited in the egg during oogenesis. Here, we explore maternal role(s) of Caspar (Casp), the Drosophila orthologue of human Fas-associated factor-1 (FAF1) originally implicated in host-defense as a negative regulator of NF-κB signaling. Maternal loss of either Casp or it’s protein partner, transitional endoplasmic reticulum 94 (TER94) leads to partial embryonic lethality correlated with aberrant centrosome behavior, cytoskeletal abnormalities, and defective gastrulation. Although ubiquitously distributed, both proteins are enriched in the primordial germ cells (PGCs), and in keeping with the centrosome problems, mutant embryos display a significant reduction in the PGC count. Moreover, the total number of pole buds is directly proportional to the level of Casp. Consistently, it’s ‘loss’ and ‘gain’ results in respective reduction and increase in the Oskar protein levels, the master determinant of PGC fate. To elucidate this regulatory loop, we analyzed several known components of mid-blastula transition and identify the translational repressor Smaug, a zygotic regulator of germ cell specification, as a potential critical target. We present a detailed structure-function analysis of Casp aimed at understanding its novel involvement during PGC development.
