Abstract

The root cap protects the stem cell niche of angiosperm roots from damage. In Arabidopsis, lateral root cap (LRC) cells covering the meristematic zone are regularly lost through programmed cell death, while the outermost layer of the root cap covering the tip is repeatedly sloughed. Efficient coordination with stem cells producing new layers is needed to maintain a constant size of the cap. We present a signalling pair, the peptide IDA-LIKE1 (IDL1) and its receptor HAESA-LIKE2 (HSL2), mediating such communication. Live imaging over several days characterized this process from initial fractures in LRC cell files to full separation of a layer. Enhanced expression of IDL1 in the separating root cap layers resulted in increased frequency of sloughing, balanced with generation of new layers in a HSL2-dependent manner. Transcriptome analyses linked IDL1-HSL2 signalling to the transcription factors BEARSKIN1/2 and genes associated with programmed cell death. Mutations in either IDL1 or HSL2 slowed down cell division, maturation and separation. Thus, IDL1-HSL2 signalling potentiates dynamic regulation of the homeostatic balance between stem cell division and sloughing activity.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Additional information

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

References

  1. 1.

    Arnaud, C., Bonnot, Cm, Desnos, T. & Nussaume, L. The root cap at the forefront. Comptes Rendus Biol. 333, 335–343 (2010).

  2. 2.

    Kumpf, R. P. & Nowack, M. K. The root cap: a short story of life and death. J. Exp. Bot. 66, 5651–5662 (2015).

  3. 3.

    Driouich, A., Durand, C., Cannesan, M. A., Percoco, G. & Vicre-Gibouin, M. Border cells versus border-like cells: are they alike? J. Exp. Bot. 61, 3827–3831 (2010).

  4. 4.

    Fendrych, M. et al. Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr. Biol. 24, 931–940 (2014).

  5. 5.

    Lewis, M. W., Leslie, M. E. & Liljegren, S. J. Plant separation: 50 ways to leave your mother. Curr. Opin. Plant Biol. 9, 59–65 (2006).

  6. 6.

    Willemsen, V. et al. The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev. Cell 15, 913–922 (2008).

  7. 7.

    Bennett, T. et al. SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis. Plant Cell 22, 640–654 (2010).

  8. 8.

    Kamiya, M. et al. Control of root cap maturation and cell detachment by BEARSKIN transcription factors in Arabidopsis. Develop 143, 4063–4072 (2016).

  9. 9.

    Sundaresan, S. et al. De novo transcriptome sequencing and development of abscission zone-specific microarray as a new molecular tool for analysis of tomato organ abscission. Front Plant Sci 6, 1258 (2015).

  10. 10.

    Kumpf, R. P. et al. Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. Proc. Natl Acad. Sci. USA 110, 5235–5240 (2013).

  11. 11.

    Aalen, R. B., Wildhagen, M., Sto, I. M. & Butenko, M. A. IDA: a peptide ligand regulating cell separation processes in Arabidopsis. J. Exp. Bot. 64, 5253–5261 (2013).

  12. 12.

    Butenko, M. A. et al. Tools and strategies to match peptide-ligand receptor pairs. Plant Cell 26, 1838–1847 (2014).

  13. 13.

    Estornell, L. H. et al. The IDA peptide controls abscission in Arabidopsis and citrus. Front. Plant Sci 6, 1003 (2015).

  14. 14.

    Santiago, J. et al. Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife 5, e15075 (2016).

  15. 15.

    Patharkar, O. R. & Walker, J. C. Core mechanism regulating developmentally timed and environmentally triggered absission. Plant Physiol. 172, 510–520 (2016).

  16. 16.

    Stenvik, G. E. et al. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20, 1805–1817 (2008).

  17. 17.

    Matsubayashi, Y. Post-translational modifications in secreted peptide hormones in plants. Plant Cell Physiol 52, 5–13 (2011).

  18. 18.

    Butenko, M. A., Vie, A. K., Brembu, T., Aalen, R. B. & Bones, A. M. Plant peptides in signalling: looking for new partners. Trends Plant Sci. 14, 255–263 (2009).

  19. 19.

    ten Hove, C. A. et al. Probing the roles of LRR RLK genes in Arabidopsis thaliana roots using a custom T-DNA insertion set. Plant Mol. Biol. 76, 69–83 (2011).

  20. 20.

    Yamada, M. & Sawa, S. The roles of peptide hormones during plant root development. Curr. Opin. Plant Biol. 16, 56–61 (2013).

  21. 21.

    Brand, L. et al. A versatile and reliable two-component system for tissue-specific gene induction in Arabidopsis. Plant Physiol. 141, 1194–1204 (2006).

  22. 22.

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

  23. 23.

    Nawy, T. et al. Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17, 1908–1925 (2005).

  24. 24.

    del Campillo, E., Abdel-Aziz, A., Crawford, D. & Patterson, S. E. Root cap specific expression of an endo-beta-1,4-D-glucanase (cellulase): a new marker to study root development in Arabidopsis. Plant Mol. Biol. 56, 309–323 (2004).

  25. 25.

    Karve, R., Suarez-Roman, F. & Iyer-Pascuzzi, A. S. The transcription factor NIN-LIKE PROTEIN7 controls border-like cell release. Plant Physiol. 171, 2101–2111 (2016).

  26. 26.

    Olvera-Carrillo, Y. et al. A conserved core of programmed cell death indicator genes discriminates developmentally and environmentally induced programmed cell death in plants. Plant Physiol. 169, 2684–2699 (2015).

  27. 27.

    Bollh”ner, B. et al. Post mortem function of AtMC9 in xylem vessel elements. New Phytol. 200, 498–510 (2013).

  28. 28.

    Durand, C. et al. The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiol. 150, 1411–1421 (2009).

  29. 29.

    Zhou, W. et al. Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22, 3692–3709 (2010).

  30. 30.

    Bennett, T., van den Toorn, A., Willemsen, V. & Scheres, B. Precise control of plant stem cell activity through parallel regulatory inputs. Develop 141, 4055–4064 (2014).

  31. 31.

    Somssich, M., Bleckmann, A. & Simon, R. Shared and distinct functions of the pseudokinase CORYNE (CRN) in shoot and root stem cell maintenance of Arabidopsis. J. Exp. Bot. 67, 4901–4915 (2016).

  32. 32.

    Sto, I. M. et al. Conservation of the abscission signaling peptide IDA during angiosperm evolution: withstanding genome duplications and gain and loss of the receptors HAE/HSL2. Front. Plant Sci. 6, 931, https://doi.org/10.3389/fpls.2015.00931 (2015).

  33. 33.

    Vie, A. K. et al. The IDA/IDA-LIKE and PIP/PIP-LIKE gene families in Arabidopsis: phylogenetic relationship, expression patterns, and transcriptional effect of the PIPL3 peptide. J. Exp. Bot. 66, 5351–5365 (2015).

  34. 34.

    Fauser, F., Schiml, S. & Puchta, H. Both CRISPR/Cas-based nucleases and nickases can be used efficiently for genome engineering in Arabidopsis thaliana. Plant J. 79, 348–359 (2014).

  35. 35.

    Yamaguchi, Y. L. et al. A collection of mutants for CLE-peptide-encoding genes in Arabidopsis generated by CRISPR/Cas9-mediated gene targeting. Plant Cell Physiol 58, 1848–1856 (2017).

Download references

Acknowledgements

We want to thank K. Nakajima for pRCPG:nYG, pBRN1:BRN1-GFP and pBRN2:BRN2-GFP and M. Bennett for BFN1pro:nGFP seeds; R. Falleth, S. Engebretsen and V. Iversen for technical support in the laboratory and phytotron, J. Blix Knutsen for preparation of RNA for sequencing and M. Koomey for critical reading of the manuscript. This work has been supported by the Research Council of Norway (grant 312785) to the Aalen lab, and by the ERASysApp project “Rootbook” to the R.B.A. and M.C.

Author information

Author notes

    • Daniel von Wangenheim

    Present address: Centre for Plant Integrative Biology, University of Nottingham, Loughborough, UK

    • Ullrich Herrmann

    Present address: Plant Developmental Biology and Plant Physiology, University of Kiel, Kiel, Germany

  1. These authors contributed equally to this work: Daniel von Wangenheim, Ullrich Herrmann, Mari Wildhagen.

Affiliations

  1. Section of Genetics and Evolutionary Biology, Department of Biosciences, University of Oslo, Oslo, Norway

    • Chun-Lin Shi
    • , Ullrich Herrmann
    • , Mari Wildhagen
    • , Vilde Olsson
    • , Mari Kristine Anker
    • , Melinka A. Butenko
    •  & Reidunn B. Aalen
  2. Institute of Science and Technology Austria, Klosterneuburg, Austria

    • Daniel von Wangenheim
    • , Ivan Kulik
    •  & Jiří Friml
  3. ETH Zurich, HPT E 73, Auguste-Piccard-Hof 1, Zürich, Switzerland

    • Andreas Kopf
    •  & Manfred Claassen
  4. International Research Organization for Advanced Science and Technology (IROAST), Kumamoto University, Kumamoto, Japan

    • Takashi Ishida
  5. Center for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany

    • Markus Albert
    •  & Georg Felix
  6. Graduate School of Science and Technology, Kumamoto University, Kumamoto, Japan

    • Shinichiro Sawa

Authors

  1. Search for Chun-Lin Shi in:

  2. Search for Daniel von Wangenheim in:

  3. Search for Ullrich Herrmann in:

  4. Search for Mari Wildhagen in:

  5. Search for Ivan Kulik in:

  6. Search for Andreas Kopf in:

  7. Search for Takashi Ishida in:

  8. Search for Vilde Olsson in:

  9. Search for Mari Kristine Anker in:

  10. Search for Markus Albert in:

  11. Search for Melinka A. Butenko in:

  12. Search for Georg Felix in:

  13. Search for Shinichiro Sawa in:

  14. Search for Manfred Claassen in:

  15. Search for Jiří Friml in:

  16. Search for Reidunn B. Aalen in:

Contributions

C.-L.S., T.I., S.S., U.H., M.A.B., M.W., M.K.A. and V.O. generated Arabidopsis lines. J.F. and D.v.W. designed, D.v.W. and I.K. performed, and D.v.W., I.K. and R.B.A. analysed the live imaging. G.F., M.A. and M.A.B. designed and M.W. performed IDL1-HSL2 interaction studies. M.C. and R.B.A. designed and A.K., M.C. and R.B.A. analysed RNAseq data. The rest of the experiments were designed by C.-L.S. and R.B.A., performed by C.-L.S. together with U.H., M.W. and V.O., and analysed by R.B.A., C.-L.S., M.W. and U.H. C.-L.S. drafted the manuscript. R.B.A. wrote the paper with input from other authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Reidunn B. Aalen.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–6, Supplementary Tables 1 and 3.

  2. Reporting Summary

  3. Supplementary Videos 1, 2 and 3

    Standard root cap sloughing in Col-0, Ovelapping sloughing events in EnhIDL1, Split root cap layers in EnhIDL1hsl2.

  4. Supplementary Table 2

    Genes downregualted in the root tip of the hsl2 mutant.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41477-018-0212-z