Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows

Abstract

Asymmetric cell divisions are essential for the development of multicellular organisms. To proceed, they require an initially symmetric cell to polarize1. In Caenorhabditis elegans zygotes, anteroposterior polarization is facilitated by a large-scale flow of the actomyosin cortex2,3,4, which directs the asymmetry of the first mitotic division. Cortical flows appear in many contexts of development5, but their underlying forces and physical principles remain poorly understood. How actomyosin contractility and cortical tension interact to generate large-scale flow is unclear. Here we report on the subcellular distribution of cortical tension in the polarizing C. elegans zygote, which we determined using position- and direction-sensitive laser ablation. We demonstrate that cortical flow is associated with anisotropies in cortical tension and is not driven by gradients in cortical tension, which contradicts previous proposals5. These experiments, in conjunction with a theoretical description of active cortical mechanics, identify two prerequisites for large-scale cortical flow: a gradient in actomyosin contractility to drive flow and a sufficiently large viscosity of the cortex to allow flow to be long-ranged. We thus reveal the physical requirements of large-scale intracellular cortical flow that ensure the efficient polarization of the C. elegans zygote.

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Figure 1: Orthogonal cortical tension in the anterior and posterior domain of C. elegans zygotes measured by COLA.
Figure 2: COLA response.
Figure 3: Orthogonal cortical tension is under control of the Rho-GTPase cycle.
Figure 4: Flow and density profiles demonstrate long-ranged flow.

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Acknowledgements

We thank C. Cowan, N. Goehring, P. Gönczy, J. Howard, T. Hyman, M. Loose, F. Nédélec and K. Oegema for advice and suggestions on the manuscript. We are grateful to E. Munro for scientific advice, worm strains and discussions. M.M. is supported by a predoctoral fellowship from the Boehringer Ingelheim Fonds, and J.S.B. by a postdoctoral fellowship from the Human Frontier Science Program.

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Contributions

M.M. performed the experiments; the presented ideas and the theory were developed together by all authors.

Corresponding author

Correspondence to Stephan W. Grill.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-14 with legends, Supplementary Materials and Methods, Supplementary Tables 1-2, Supplementary Notes, Text and Equations, legends for Supplementary Movies 1-14 and additional references. (PDF 11089 kb)

Supplementary Movie 1

This movie shows anterior COLA along the AP-axis in a polarising NMY-2::GFP Zygote - see Supplementary Information file for full legend. (MOV 4503 kb)

Supplementary Movie 2

This movie shows posterior COLA along the AP-axis in a polarising NMY 2::GFPZygote - see Supplementary Information file for full legend. (MOV 2165 kb)

Supplementary Movie 3

This movie shows anterior COLA along the AP-axis in a polarising GFP::MOE zygote - see Supplementary Information file for full legend. (MOV 4653 kb)

Supplementary Movie 4

This movie shows anterior COLA along the AP-axis in an NMY-2::GFP, spd 5(RNAi) zygote - see Supplementary Information file for full legend. (MOV 4007 kb)

Supplementary Movie 5

This movie shows posterior COLA along the AP-axis in a NMY-2::GFP, spd 5(RNAi) zygot - see Supplementary Information file for full legend e. (MOV 2791 kb)

Supplementary Movie 6

This movie shows anterior COLA along the AP-axis in a polarising NMY-2::GFP, ect-2(RNAi) zygote - see Supplementary Information file for full legend. (MOV 6554 kb)

Supplementary Movie 7

This movie shows anterior COLA along the AP-axis in a polarising NMY-2::GFP, rga 3(RNAi) zygote - see Supplementary Information file for full legend. (MOV 4448 kb)

Supplementary Movie 8

This movie shows anterior COLA orthogonal to the AP-axis in a polarizing NMY- 2::GFP zygote - see Supplementary Information file for full legend. (MOV 3547 kb)

Supplementary Movie 9

This movie shows anterior COLA orthogonal to the AP-axis in a NMY-2::GFP, spd-5(RNAi) zygote - see Supplementary Information file for full legend. (MOV 2833 kb)

Supplementary Movie 10

This movie shows posterior COLA orthogonal to the AP-axis in a NMY-2::GFP, spd- 5(RNAi) zygote - see Supplementary Information file for full legend. (MOV 1970 kb)

Supplementary Movie 11

This movie shows PIV of NMY-2::GFP during polarity establishment – see Supplementary Information file for full legend. (MOV 6355 kb)

Supplementary Movie 12

This movie shows posterior COLA orthogonal to the AP-axis in a polarising NMY-2::GFP zygote - see Supplementary Information file for full legend. (MOV 2660 kb)

Supplementary Movie 13

This movie shows external friction, internal viscosity and the hydrodynamic length scale - see Supplementary Information file for full legend. (MOV 566 kb)

Supplementary Movie 14

This movie shows the period of cortical flow in a GFP::MOE zygote treated with Cytochalasin D - see Supplementary Information file for full legend. (MOV 2226 kb)

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Mayer, M., Depken, M., Bois, J. et al. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467, 617–621 (2010). https://doi.org/10.1038/nature09376

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