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The dynamics of root cap sloughing in Arabidopsis is regulated by peptide signalling

Nature Plants volume 4, pages 596–604 (2018)Cite this article

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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.

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Fig. 1: IDL1 peptide interacts with and activates HSL2.
Fig. 2: Live imaging details the sloughing process in Col-0, the effect of enhanced expression of IDL1 and dependency on HSL2.
Fig. 3: Higher frequency of sloughing is compensated with more stem cell divisions.
Fig. 4: idl1 and hsl2 mutants influence sloughing frequency and LRC division patterns.
Fig. 5: IDL1-HSL2 regulates genes involved in cell wall degradation and PCD.
Fig. 6: Working model for IDL1-HSL2 function in root cap sloughing.

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References

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

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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.

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Author notes

  1. Daniel von Wangenheim

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

  2. Ullrich Herrmann

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

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

Authors and 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

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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.

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Correspondence to Reidunn B. Aalen.

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Supplementary information

Supplementary Information

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

Reporting Summary

Supplementary Videos 1, 2 and 3

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

Supplementary Table 2

Genes downregualted in the root tip of the hsl2 mutant.

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Shi, CL., von Wangenheim, D., Herrmann, U. et al. The dynamics of root cap sloughing in Arabidopsis is regulated by peptide signalling. Nature Plants 4, 596–604 (2018). https://doi.org/10.1038/s41477-018-0212-z

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