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

Nature Plants volume 5, pages 160–166 (2019)Cite this article

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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.

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Data availability

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

References

  1. Butler, M. T. & Wallingford, J. B. Planar cell polarity in development and disease. Nat. Rev. Mol. Cell Biol. 18, 375–388 (2017).

    Article  CAS  Google Scholar 

  2. Nakamura, M., Kiefer, C. S. & Grebe, M. Planar polarity, tissue polarity and planar morphogenesis in plants. Curr. Opin. Plant. Biol. 15, 593–600 (2012).

    Article  CAS  Google Scholar 

  3. St Johnston, D. & Ahringer, J. Cell polarity in eggs and epithelia: parallels and diversity. Cell 141, 757–774 (2010).

    Article  Google Scholar 

  4. Chiou, J.-G., Balasubramanian, M. K. & Lew, D. J. Cell polarity in yeast. Annu. Rev. Cell. Dev. Biol. 33, 77–101 (2017).

    Article  CAS  Google Scholar 

  5. St. Johnston, D. Establishing and transducing cell polarity: common themes and variations. Curr. Opin. Cell Biol. 51, 33–41 (2018).

    Article  CAS  Google Scholar 

  6. Yoshida, S. et al. Genetic control of plant development by overriding a geometric division rule. Dev. Cell. 29, 75–87 (2014).

    Article  CAS  Google Scholar 

  7. De Rybel, B. et al. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev. Cell. 24, 426–437 (2013).

    Article  Google Scholar 

  8. Gälweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998).

    Article  Google Scholar 

  9. Müller, A. et al. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903–6911 (1998).

    Article  Google Scholar 

  10. Friml, J., Wiŝniewska, J., Benková, E., Mendgen, K. & Palme, K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002).

    Article  Google Scholar 

  11. Friml, J. et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 (2003).

    Article  CAS  Google Scholar 

  12. Langowski, L. et al. Cellular mechanisms for cargo delivery and polarity maintenance at different polar domains in plant cells. Cell Discov. 2, 16018 (2016).

    Article  Google Scholar 

  13. Dong, J., MacAlister, C. A. & Bergmann, D. C. BASL controls asymmetric cell division in Arabidopsis.Cell 137, 1320–1330 (2009).

    Article  Google Scholar 

  14. Takano, J. et al. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl Acad. Sci. 107, 5220–5225 (2010).

    Article  CAS  Google Scholar 

  15. Pillitteri, L. J., Peterson, K. M., Horst, R. J. & Torii, K. U. Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis. Plant Cell 23, 3260–3275 (2011).

    Article  CAS  Google Scholar 

  16. Kania, U., Fendrych, M. & Friml, J. Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biol. 4, 140017 (2014).

    Article  Google Scholar 

  17. Moller, B. & Weijers, D. Auxin control of embryo patterning. Cold Spring Harb. Perspect. Biol. 1, a001545 (2009).

    Article  Google Scholar 

  18. Hardtke, C. S. & Berleth, T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405–1411 (1998).

    Article  CAS  Google Scholar 

  19. Berleth, T. & Jürgens, G. The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118, 575–587 (1993).

    Google Scholar 

  20. Möller, B. K. et al. Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo. Proc. Natl Acad. Sci. USA 114, E2533–E2539 (2017).

    Article  Google Scholar 

  21. Schlereth, A. et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913–916 (2010).

    Article  CAS  Google Scholar 

  22. Weijers, D. et al. An arabidopsis minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128, 4289–4299 (2001).

    CAS  PubMed  Google Scholar 

  23. Scheres, B. et al. Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121, 53–62 (1995).

    CAS  Google Scholar 

  24. Benfey, P. N. et al. Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119, 57–70 (1993).

    CAS  PubMed  Google Scholar 

  25. Radoeva, T., ten Hove, C. A., Saiga, S. & Weijers, D. Molecular characterization of Arabidopsis GAL4/UAS enhancer trap lines identifies novel cell type-specific promoters. Plant Physiol. 171, 1169–1181 (2016).

    PubMed  PubMed Central  Google Scholar 

  26. Alassimone, J.., Naseer, S. & Geldner, N. . A developmental framework for endodermal differentiation and polarity. Proc. Natl Acad. Sci. USA 107, 5214–5219 (2010).

  27. Liao, C. Y. & Weijers, D. A toolkit for studying cellular reorganization during early embryogenesis in Arabidopsis thaliana. Plant J. 93, 963–976 (2018).

    Article  CAS  Google Scholar 

  28. Traverso, J. A. et al. Roles of N-terminal fatty acid acylations in membrane compartment partitioning: Arabidopsis h-type thioredoxins as a case study. Plant Cell 25, 1056–1077 (2013).

    Article  CAS  Google Scholar 

  29. Bienz, M. Signalosome assembly by domains undergoing dynamic head-to-tail polymerization. Trends. Biochem. Sci. 10, 487–495 (2014).

    Article  Google Scholar 

  30. Ehebauer, M. T. & Arias, A. M. The structural and functional determinants of the Axin and Dishevelled DIX domains. BMC Struct. Biol. 9, 70 (2009).

    Article  Google Scholar 

  31. Schwarz-Romond, T. et al. The DIX domain of Dishevelled confers Wnt signaling by dynamic polymerization. Nat. Struct. Mol. Biol. 14, 484–492 (2007).

    Article  CAS  Google Scholar 

  32. Mansfield, C. et al. Ectopic BASL reveals tissue cell polarity throughout leaf development in Arabidopsis thaliana. Curr. Biol. 28, 2638–2646 (2018).

    Article  CAS  Google Scholar 

  33. Fukaki, H. et al. Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J. 14, 425–430 (1998).

    Article  CAS  Google Scholar 

  34. Helariutta, Y. et al. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555–567 (2000).

    Article  CAS  Google Scholar 

  35. De Rybel, B. et al. A versatile set of ligation-independent cloning vectors for functional studies in plants. Plant Physiol. 156, 1292–1299 (2011).

    Article  Google Scholar 

  36. Weijers, D., Van Hamburg, J. P., Van Rijn, E., Hooykaas, P. J. & Offringa, R. Diphtheria toxin-mediated cell ablation reveals interregional communication during Arabidopsis seed development. Plant Physiol. 133, 1882–1892 (2003).

    Article  CAS  Google Scholar 

  37. Llavata-Peris, C., Lokerse, A., Moller, B., De Rybel, B. & Weijers, D. Imaging of phenotypes, gene expression, and protein localization during embryonic root formation in Arabidopsis. Methods Mol. Biol. 959, 137–148 (2013).

    Article  CAS  Google Scholar 

  38. Marhavý, P. et al. Targeted cell elimination reveals an auxin-guided biphasic mode of lateral root initiation. Genes Dev. 30, 471–483 (2016).

    Article  Google Scholar 

  39. von Wangenheim, D. et al. Live tracking of moving samples in confocal microscopy for vertically grown roots. eLife 6, e26792 (2017).

    Article  Google Scholar 

  40. de Reuille, P. B. et al. MorphoGraphX: A platform for quantifying morphogenesis in 4D. eLife 4, 05864 (2015).

    Google Scholar 

  41. Rios, A. F., Radoeva, T., De Rybel, B., Weijers, D. & Borst, J. W. FRET-FLIM for visualizing and quantifying protein interactions in live plant cells. Methods Mol. Biol. 1497, 135–146 (2017).

    Article  CAS  Google Scholar 

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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.

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Author notes

  1. Saiko Yoshida

    Present address: Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany

  2. Alja van der Schuren & Peter Marhavy

    Present address: Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland

  3. Shunsuke Saiga

    Present address: Department of Plant and Microbial Biology, University of Zürich, Zürich, Switzerland

  4. Barbara Möller

    Present address: VIB-UGent Center for Plant Systems Biology, Ghent, Belgium

  5. These authors contributed equally: Alja van der Schuren, Maritza van Dop.

Authors and Affiliations

  1. Laboratory of Biochemistry, Wageningen University, Wageningen, The Netherlands

    Saiko Yoshida, Alja van der Schuren, Maritza van Dop, Luc van Galen, Shunsuke Saiga, Barbara Möller, Colette A. ten Hove & Dolf Weijers

  2. Institute of Science and Technology, Klosterneuburg, Austria

    Saiko Yoshida, Peter Marhavy & Jiri Friml

  3. Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany

    Milad Adibi & Richard Smith

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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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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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