Letter | Published:

Diffusible repression of cytokinin signalling produces endodermal symmetry and passage cells

Nature volume 555, pages 529533 (22 March 2018) | Download Citation

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Abstract

In vascular plants, the root endodermis surrounds the central vasculature as a protective sheath that is analogous to the polarized epithelium in animals, and contains ring-shaped Casparian strips that restrict diffusion1. After an initial lag phase, individual endodermal cells suberize in an apparently random fashion to produce ‘patchy’ suberization that eventually generates a zone of continuous suberin deposition2. Casparian strips and suberin lamellae affect paracellular and transcellular transport, respectively. Most angiosperms maintain some isolated cells in an unsuberized state3 as so-called ‘passage cells’, which have previously been suggested to enable uptake across an otherwise-impermeable endodermal barrier3,4. Here we demonstrate that these passage cells are late emanations of a meristematic patterning process that reads out the underlying non-radial symmetry of the vasculature. This process is mediated by the non-cell-autonomous repression of cytokinin signalling in the root meristem, and leads to distinct phloem- and xylem-pole-associated endodermal cells. The latter cells can resist abscisic acid-dependent suberization to produce passage cells. Our data further demonstrate that, during meristematic patterning, xylem-pole-associated endodermal cells can dynamically alter passage-cell numbers in response to nutrient status, and that passage cells express transporters and locally affect the expression of transporters in adjacent cortical cells.

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Change history

  • 20 June 2018

    In this Letter, the two centre panels in Extended Data Fig. 7a were identical. The original, incorrect Extended Data Fig. 7 is shown in the Supplementary Information to the accompanying Amendment. The original Letter has been corrected.

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Acknowledgements

This work was supported by funds to N.G. from an ERC Consolidator Grant (GA-N°: 616228 – ENDOFUN), an SNSF grant (31003A_156261), an IEF Marie Curie fellowship (T.G.A.) and an EMBO Long-term postdoctoral fellowship (R.U.). B.D.R., W.S. and B.W. were funded by the Netherlands Organisation for Scientific Research (NWO; VIDI-864.13.001) and The Research Foundation - Flanders (FWO; Odysseus II G0D0515N). We thank A. Paradis and the Central Imaging Facility of the University of Lausanne for support; M. Yamazaki for providing constructs; B. Müller, D. Weijers and T. Vernoux for sharing material; A. Bishopp, A. P. Mähönen, D. Weijers, S. Sabatini, V. Grieneisen, Y. Helariutta and Y. Poirier for discussions; and A. Vjestica, C. Drapek, M. Marek and M. Barberon for input to the manuscript.

Author information

Author notes

    • Joop E. M. Vermeer

    Present address: Department of Plant and Microbial Biology, University of Zürich, 8008 Zürich, Switzerland.

Affiliations

  1. Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne, Switzerland

    • Tonni Grube Andersen
    • , Sadaf Naseer
    • , Robertas Ursache
    • , Joop E. M. Vermeer
    •  & Niko Geldner
  2. Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium

    • Brecht Wybouw
    • , Wouter Smet
    •  & Bert De Rybel
  3. VIB Center for Plant Systems Biology, 9052 Ghent, Belgium

    • Brecht Wybouw
    • , Wouter Smet
    •  & Bert De Rybel
  4. Wageningen University, Laboratory of Biochemistry, 6708 WE Wageningen, The Netherlands

    • Wouter Smet
    •  & Bert De Rybel

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Contributions

T.G.A. planned and conducted all experiments with input from N.G. and J.E.M.V. S.N. conducted initial experiments on PHO1 localization, R.U. created and tested inducible vectors, J.E.M.V. created and tested shy2-2 lines, and B.D.R, W.S. and B.W. created and selected all ARR reporter lines. T.G.A and N.G. wrote the manuscript. All authors commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Tonni Grube Andersen or Niko Geldner.

Reviewer Information Nature thanks H. Fukuda, Y. Helariutta and A. P. Mähönen for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Supplementary information

PDF files

  1. 1.

    Life Sciences Reporting Summary

Excel files

  1. 1.

    Supplementary Table 1

    This file contains a list of primers.

  2. 2.

    Supplementary Table 2

    This table contains individual P-values for all statistical analyses.

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DOI

https://doi.org/10.1038/nature25976

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