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Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension

Nature Cell Biology volume 11, pages 859–864 (2009)Cite this article

Abstract

Drosophila germ-band extension (GBE) is an example of the convergence and extension movements that elongate and narrow embryonic tissues. To understand the collective cell behaviours underlying tissue morphogenesis, we have continuously quantified cell intercalation and cell shape change during GBE. We show that the fast, early phase of GBE depends on cell shape change in addition to cell intercalation. In antero-posterior patterning mutants such as those for the gap gene Krüppel, defective polarized cell intercalation is compensated for by an increase in antero-posterior cell elongation, such that the initial rate of extension remains the same. Spatio-temporal patterns of cell behaviours indicate that an antero-posterior tensile force deforms the germ band, causing the cells to change shape passively. The rate of antero-posterior cell elongation is reduced in twist mutant embryos, which lack mesoderm. We propose that cell shape change contributing to germ-band extension is a passive response to mechanical forces caused by the invaginating mesoderm.

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Figure 1: Relative contribution of cell shape change and cell intercalation to germ-band extension in wild-type and Krüppel− embryos.
Figure 2: Spatio-temporal analysis of cell behaviours in the ectoderm of wild-type and AP patterning mutant embryos.
Figure 3: Spatio-temporal analysis of cell shape and cell area change in the ectoderm of wild-type and Krüppel− embryos.
Figure 4: Relationship between mesoderm invagination and germ-band extension.

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Acknowledgements

We thank Claire Lye, Bruno Monier and Daniel St Johnston for comments on the manuscript and discussions. We thank the Bloomington Drosophila Stock Centre for fly strains. This work was supported by a Human Frontier Science Program grant to B.S., a Wellcome Trust studentship to L.C.B., a Medical Research Council grant to R.J.A. and a Harvard–National Science Foundation Materials Research Science and Engineering Center award to M.L.

Author information

Author notes

  1. Lucy C. Butler and Guy B. Blanchard: These two authors contributed equally to the work.

Authors and Affiliations

  1. Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, CB2 3DY, Cambridge, UK

    Lucy C. Butler, Guy B. Blanchard, Richard J. Adams & Benedicte Sanson

  2. Engineering Department, University of Cambridge, Trumpington Street, CB2 1PZ, Cambridge, UK

    Alexandre J. Kabla

  3. Gurdon Institute, University of Cambridge, Tennis Court Road, CB2 1QN, Cambridge, UK

    Nicola J. Lawrence

  4. Global Health Institute, École Polytechnique Fédérale de Lausanne, CH-1015, Lausanne, Switzerland

    David P. Welchman

  5. School of Engineering and Applied Sciences, Harvard University, Cambridge, 02138, Massachusetts, USA

    L. Mahadevan

  6. Department of Systems Biology, Harvard Medical School, Boston, 02115, Massachusetts, USA

    L. Mahadevan

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Contributions

This project grew from a close collaboration between the groups of B.S. and R.J.A. L.C.B. performed the experiments and analysed the data with G.B.B., R.J.A. and B.S. N.J.L. performed the initial experiments and developed the time-lapse methods. D.P.W. contributed to experiments and manuscript preparation. Strain rate analyses were developed by G.B.B., A.J.K., R.J.A. and L.M., building on a tracking and quantification framework of G.B.B. and R.J.A. B.S. and L.C.B. designed the Drosophila experiments and prepared the manuscript. All authors contributed to data interpretation and editing of the manuscript.

Corresponding author

Correspondence to Benedicte Sanson.

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The authors declare no competing financial interests.

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Butler, L., Blanchard, G., Kabla, A. et al. Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nat Cell Biol 11, 859–864 (2009). https://doi.org/10.1038/ncb1894

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