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

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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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

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.

Correspondence to Reidunn B. Aalen.

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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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.