Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Brief Communication
  • Published:

Early developmental plasticity of lateral roots in response to asymmetric water availability

Nature Plants volume 6, pages 73–77 (2020)Cite this article

Subjects

Abstract

Root branching is influenced by the soil environment and exhibits a high level of plasticity. We report that the radial positioning of emerging lateral roots is influenced by their hydrological environment during early developmental stages. New lateral root primordia have both a high degree of flexibility in terms of initiation and development angle towards the available water. Our observations reveal how the external hydrological environment regulates lateral root morphogenesis.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Arabidopsis branching is influenced by the position of the root in the agar.
Fig. 2: Lateral root development is flexible during all developmental stages.

Similar content being viewed by others

Data availability

The data for Fig. 1f is shown in Supplementary Video 1. Other datasets can be shared upon reasonable request.

References

  1. Morris, E. C. et al. Shaping 3D root system architecture. Curr. Biol. 27, R919–R930 (2017).

    Article  CAS  Google Scholar 

  2. Drew, M. C. Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. N. Phytol. 75, 479–490 (1975).

    Article  CAS  Google Scholar 

  3. Orman-Ligeza, B. et al. The xerobranching response represses lateral root formation when roots are not in contact with water. Curr. Biol. 28, 3165–3173 (2018).

    Article  CAS  Google Scholar 

  4. Bao, Y. et al. Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc. Natl Acad. Sci. USA 111, 9319–9324 (2014).

    Article  CAS  Google Scholar 

  5. Orosa-Puente, B. et al. Root branching toward water involves posttranslational modification of transcription factor ARF7. Science 362, 1407–1410 (2018).

    Article  CAS  Google Scholar 

  6. von Guttenberg, H. in Handbuch der Pflanzenanatomie (ed. Linsbauer, K.) Band 8 (Gebrüder Bornträger, 1940).

  7. Casero, P. J., Casimiro, I. & Lloret, P. G. Lateral root initiation by asymmetrical transverse divisions of pericycle cells in four plant species: Raphanus sativus, Helianthus annuus, Zea mays, and Daucus carota. Protoplasma 188, 49–58 (1995).

    Article  Google Scholar 

  8. Laskowski, M. J., Williams, M. E., Nusbaum, H. C. & Sussex, I. M. Formation of lateral root meristems is a two-stage process. Development 121, 3303–3310 (1995).

    CAS  PubMed  Google Scholar 

  9. Casimiro, I. et al. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13, 843–852 (2001).

    Article  CAS  Google Scholar 

  10. Dubrovsky, J. G., Rost, T. L., Colón-Carmona, A. & Doerner, P. Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214, 30–36 (2001).

    Article  CAS  Google Scholar 

  11. Lucas, M. et al. Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proc. Natl Acad. Sci. USA 110, 5229–5234 (2013).

    Article  CAS  Google Scholar 

  12. von Wangenheim, D. et al. Rules and self-organizing properties of post-embryonic plant organ cell division patterns. Curr. Biol. 26, 439–449 (2016).

    Article  CAS  Google Scholar 

  13. Casimiro, I. et al. Dissecting Arabidopsis lateral root development. Trends Plant Sci. 8, 165–171 (2003).

    Article  CAS  Google Scholar 

  14. Goh, T., Joi, S., Mimura, T. & Fukaki, H. The establishment of asymmetry in Arabidopsis lateral root founder cells is regulated by LBD16/ASL18 and related LBD/ASL proteins. Development 139, 883–893 (2012).

    Article  CAS  Google Scholar 

  15. Stelzer, E. H. K. Light-sheet fluorescence microscopy for quantitative biology. Nat. Methods 12, 23–26 (2015).

    Article  CAS  Google Scholar 

  16. von Wangenheim, D., Hauschild, R. & Friml, J. Light sheet fluorescence microscopy of plant roots growing on the surface of a gel. J. Vis. Exp. 2017, e55044 (2017).

    Google Scholar 

  17. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    Article  CAS  Google Scholar 

  18. Preibisch, S., Saalfeld, S., Schindelin, J. & Tomancak, P. Software for bead-based registration of selective plane illumination microscopy Data. Nat. Methods 7, 418–419 (2010).

    Article  CAS  Google Scholar 

  19. Preibisch, S. et al. Efficient Bayesian-based multiview deconvolution. Nat. Methods 11, 645–648 (2014).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by awards from the Biotechnology and Biological Sciences Research Council (grant nos. BB/M012212, BB/G023972/1, BB/R013748/1, BB/L026848/1, BB/M018431/1, BB/PO16855/1 and BB/M001806/1), the European Research Council FUTUREROOTS Advanced Investigator (grant no. 294729) and the Leverhulme Trust (grant no. RPG-2016-409). E.H.K.S. is funded by the Deutsche Forschungsgemeinschaft (CEF-MC I/II, DFG Exc 115). Research at the Maizel Lab is supported by the DFG FOR2581, the Land Baden-Württemberg, the Chica und Heinz Schaller Stiftung, the CellNetworks cluster of excellence and the Boehringer Ingelheim Foundation.

Author information

Authors and Affiliations

  1. Plant and Crop Sciences, School of Biosciences, University of Nottingham, Nottingham, UK

    Daniel von Wangenheim, Jason Banda, Anthony Bishopp & Malcolm Bennett

  2. Buchmann Institute for Molecular Life Sciences, Goethe-Universität Frankfurt am Main, Frankfurt am Main, Germany

    Daniel von Wangenheim, Alexander Schmitz & Ernst H. K. Stelzer

  3. Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany

    Jens Boland & Alexis Maizel

Authors
  1. Daniel von Wangenheim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jason Banda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander Schmitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jens Boland
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anthony Bishopp
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alexis Maizel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ernst H. K. Stelzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Malcolm Bennett
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.v.W., J. Banda, A.B., A.M., E.H.K.S. and M.B. designed the experiments. D.v.W. and J. Banda performed the experiments, and D.v.W., J. Banda, A.S., J. Boland, A.B., A.M., E.H.K.S. and M.B. analysed the data. D.v.W., J. Banda and M.B. wrote the manuscript with contributions from all the other authors.

Corresponding authors

Correspondence to Daniel von Wangenheim or Malcolm Bennett.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Figs. 1–4 with legends.

Reporting Summary

Supplementary Video 1

Lateral root angle dataset.

Supplementary Video 2

3D view of Fig. 2d–g.

Supplementary Data 1

Statistical Source Data.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

von Wangenheim, D., Banda, J., Schmitz, A. et al. Early developmental plasticity of lateral roots in response to asymmetric water availability. Nat. Plants 6, 73–77 (2020). https://doi.org/10.1038/s41477-019-0580-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-019-0580-z

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing