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A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis

Abstract

Multicellular development requires coordinated cell polarization relative to body axes, and translation to oriented cell division1,2,3. In plants, it is unknown how cell polarities are connected to organismal axes and translated to division. Here, we identify Arabidopsis SOSEKI proteins that integrate apical–basal and radial organismal axes to localize to polar cell edges. Localization does not depend on tissue context, requires cell wall integrity and is defined by a transferrable, protein-specific motif. A Domain of Unknown Function in SOSEKI proteins resembles the DIX oligomerization domain in the animal Dishevelled polarity regulator. The DIX-like domain self-interacts and is required for edge localization and for influencing division orientation, together with a second domain that defines the polar membrane domain. Our work shows that SOSEKI proteins locally interpret global polarity cues and can influence cell division orientation. Furthermore, this work reveals that, despite fundamental differences, cell polarity mechanisms in plants and animals converge on a similar protein domain.

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Fig. 1: The SOSEKI family of polarly localized proteins.
Fig. 2: Diverse polar patterns of SOSEKI proteins.
Fig. 3: Regulation of SOSEKI localization.
Fig. 4: Protein determinants for SOK localization and activity.

Data availability

The data that support the findings of this study are available from the corresponding authors upon reasonable request.

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Acknowledgements

We thank D. Hagemans and V. Mol for support with experiments and E. Benkova for supporting P.M. This work was supported by the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007-2013) under REA grant agreement number 291734, and a Marie Curie Fellowships (contract 753138) to S.Y. by a European Research Council grant (ERC-StG CELLPATTERN; contract 281573) and ALW Open Competition grant (820.02.019) and an ALW-VIDI grant (864.06.012) from the Netherlands Organization for Scientific Research (NWO) to D.W., an ALW-VENI grant (863.21.010) from the Netherlands Organization for Scientific Research (NWO) to C.A.t.H., a grant (831.13.001) from the Netherlands Organization for Scientific Research (NWO) to M.v.D. and a FEBS long-term fellowship to P.M.

Author information

Authors and Affiliations

Authors

Contributions

D.W. conceived the study. S.Y. performed most of the experiments under the supervision of D.W. and with help from A.v.d.S., L.v.G. and S.S. M.v.D. carried out the BiFC and FRET-FLIM experiments, SOK1 localization in ground tissue and in shr and scr mutants (together with C.A.t.H.) and SOK1/SOK5 swaps. B.M. initiated the project and identified the SOK1 gene. M.A. and R.S. performed 3D SOK1 localization analysis. P.M. helped to perform live imaging under J.F.’s supervision. S.Y. and D.W. wrote the manuscript with input from all authors.

Corresponding authors

Correspondence to Saiko Yoshida or Dolf Weijers.

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Competing interests

The authors declare no competing interests.

Additional information

Journal peer review Information Nature Plants thanks Marie Barberon, Dominique Bergmann, Juan Dong and Markus Grebe for their contribution to the peer review of this work

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Supplementary information

Supplementary Information

Supplementary Figures 1–9, Supplementary Tables 1–3 and Supplementary Video Legends.

Reporting Summary

Supplementary Video 1

Localization of SOK1-YFP in heart stage embryo. Embryo was stained with Renaissance RS2200 (white), observed by confocal microscopy and 3D reconstructed.

Supplementary Video 2

A time-lapse series of SOK1-YFP during lateral root initiation. Root was stained with propidium iodide and observed by confocal microscopy. Time (hours) is indicated. The experiment was repeated in seven lateral roots with similar results.

Supplementary Video 3

A time-lapse series of SOK1-YFP during root growth. Root was stained with propidium iodide and observed by vertical confocal microscopy. Time (hours) is indicated. The experiment was repeated in three roots with similar results.

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Yoshida, S., van der Schuren, A., van Dop, M. et al. A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis. Nature Plants 5, 160–166 (2019). https://doi.org/10.1038/s41477-019-0363-6

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