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Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation

Nature Methods volume 6, pages 458–464 (2009)Cite this article

Abstract

The dynamic reshaping of tissues during morphogenesis results from a combination of individual cell behaviors and collective cell rearrangements. However, a comprehensive framework to unambiguously measure and link cell behavior to tissue morphogenesis is lacking. Here we introduce such a kinematic framework, bridging cell and tissue behaviors at an intermediate, mesoscopic, level of cell clusters or domains. By measuring domain deformation in terms of the relative motion of cell positions and the evolution of their shapes, we characterized the basic invariant quantities that measure fundamental classes of cell behavior, namely tensorial rates of cell shape change and cell intercalation. In doing so we introduce an explicit definition of cell intercalation as a continuous process. We mapped strain rates spatiotemporally in three models of tissue morphogenesis, gaining insight into morphogenetic mechanisms. Our quantitative approach has broad relevance for the precise characterization and comparison of morphogenetic phenotypes.

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Figure 1: Measuring tissue strain rates in simulated data.
Figure 2: Cellular simulations of tissue morphogenesis.
Figure 3: Measuring strain rates for a domain of zebrafish neuroectoderm.
Figure 4: Tissue, cell shape and intercalation strain rate patterns in Drosophila and zebrafish ectoderm.
Figure 5: Patterns in data pooled from multiple embryos.

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Acknowledgements

We acknowledge financial support from the Medical Research Council (R.J.A.) and the Harvard Materials Research Science and Engineering Center (L.M.). Additional financial support was from a Wellcome Trust studentship to N.L.S. (zebrafish trunk studies); a Human Frontier Science Program grant to B.S. and a Wellcome Trust studentship to L.C.B. (Drosophila germband extension studies); and a Biotechnology and Biological Sciences Research Council grant to Alfonso Martinez Arias and N.G. (Drosophila dorsal closure studies). We thank N.J. Lawrence, who initiated Drosophila germband extension imaging, S.J. England and S.R. Young for fruitful discussions. This paper is dedicated to the memory of Locke G. Nolan Blanchard.

Author information

Authors and Affiliations

  1. Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK

    Guy B Blanchard, Nora L Schultz, Lucy C Butler, Benedicte Sanson & Richard J Adams

  2. Engineering Department, University of Cambridge, Cambridge, UK

    Alexandre J Kabla

  3. Department of Genetics, University of Cambridge, Cambridge, UK

    Nicole Gorfinkiel

  4. Division of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts, USA

    L Mahadevan

  5. Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, USA

    L Mahadevan

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  1. Guy B Blanchard
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  6. Nicole Gorfinkiel
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  7. L Mahadevan
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Contributions

G.B.B., A.J.K., L.M. and R.J.A. conceived and developed the project and wrote the manuscript. G.B.B. and A.J.K. analyzed data and developed the code. N.L.S. (zebrafish trunk), L.C.B., B.S. (Drosophila germband extension) and N.G. (Drosophila dorsal closure) all collaborated to develop the analyses and contributed time-lapse movies and expertise on their models.

Corresponding authors

Correspondence to L Mahadevan or Richard J Adams.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4, Supplementary Note (PDF 974 kb)

Supplementary Software

Zip file of code written in IDL for calculating strain rates in a domain of tissue. (ZIP 8 kb)

Supplementary Video 1

Tracked cell trajectories and membrane shapes in Drosophila amnioserosa. Video to accompany Figure 4a. Video duration is 50 min, with frames at 2 min intervals. Details are as in Figure 4. (MOV 198 kb)

Supplementary Video 2

Tracked cell trajectories and membrane shapes in Drosophila germband. Video to accompany Figure 4i. Video duration is 15 mins, with frames at 30s intervals. Details are as in Figure 4. (MOV 576 kb)

Supplementary Video 3

Tracked cell trajectories and membrane shapes in zebrafish trunk ectoderm. Video to accompany Figure 4q. Video duration is 50 mins, with frames at 2 min intervals. Details are as in Figure 4. (MOV 590 kb)

Supplementary Video 4

Cellular simulation of a domain dominated by cell shape change. Video to accompany Figure 2a simulation. Video duration is 50 mins, with frames every minute. (MOV 38 kb)

Supplementary Video 5

Cellular simulation of a domain dominated by cell intercalation. Video to accompany Figure 2b simulation. Video duration is 50 mins, with frames every minute. (MOV 37 kb)

Supplementary Video 6

Tissue deformations and rotations in Drosophila amnioserosa. Video to accompany Figure 4c. Video duration is 50 mins, with frames at 2 min intervals. Details are as in Figure 4. (MOV 114 kb)

Supplementary Video 7

Cell shape deformations in Drosophila amnioserosa. Video to accompany Figure 4e. Video duration is 50 mins, with frames at 2 min intervals. Details are as in Figure 4. (MOV 110 kb)

Supplementary Video 8

Cell intercalation deformations in Drosophila amnioserosa. Video to accompany Figure 4g. Video duration is 50 mins, with frames at 2 min intervals. Details are as in Figure 4. (MOV 45 kb)

Supplementary Video 9

Tissue deformations and rotations in Drosophila germband. Video to accompany Figure 4k. Video duration is 15 mins, with frames at 30s intervals. Details are as in Figure 4. (MOV 425 kb)

Supplementary Video 10

Cell shape deformations in Drosophila germband. Video to accompany Figure 4m. Video duration is 15 mins, with frames at 30s intervals. Details are as in Figure 4. (MOV 313 kb)

Supplementary Video 11

Cell intercalation deformations in Drosophila germband. Video to accompany Figure 4o. Video duration is 15 mins, with frames at 30s intervals. Details are as in Figure 4. (MOV 325 kb)

Supplementary Video 12

Tissue deformations and rotations in zebrafish trunk ectoderm. Video to accompany Figure 4s. Video duration is 50 mins, with frames at 2 min intervals. Details are as in Figure 4. (MOV 297 kb)

Supplementary Video 13

Cell shape deformations in zebrafish trunk ectoderm. Video to accompany Figure 4u. Video duration is 50 mins, with frames at 2 min intervals. Details are as in Figure 4. (MOV 231 kb)

Supplementary Video 14

Cell intercalation deformations in zebrafish trunk ectoderm. Video to accompany Figure 4w. Video duration is 50 mins, with frames at 2 min intervals. Details are as in Figure 4. (MOV 232 kb)

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Blanchard, G., Kabla, A., Schultz, N. et al. Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation. Nat Methods 6, 458–464 (2009). https://doi.org/10.1038/nmeth.1327

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