Organ regeneration does not require a functional stem cell niche in plants

Abstract

Plants rely on the maintenance of stem cell niches at their apices for the continuous growth of roots and shoots. However, although the developmental plasticity of plant cells has been demonstrated1, it is not known whether the stem cell niche is required for organogenesis. Here we explore the capacity of a broad range of differentiating cells to regenerate an organ without the activity of a stem cell niche. Using a root-tip regeneration system in Arabidopsis thaliana to track the molecular and functional recovery of cell fates, we show that re-specification of lost cell identities begins within hours of excision and that the function of specialized cells is restored within one day. Critically, regeneration proceeds in plants with mutations that fail to maintain the stem cell niche. These results show that stem-cell-like properties that mediate complete organ regeneration are dispersed in plant meristems and are not restricted to niches, which nonetheless seem to be necessary for indeterminate growth. This regenerative reprogramming of an entire organ without transition to a stereotypical stem cell environment has intriguing parallels to recent reports of induced transdifferentiation of specific cell types in the adult organs of animals2,3.

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Figure 1: Root-tip regeneration and cell fate re-specification in wild type.
Figure 2: Columella starch staining and root-tip regeneration in stem cell mutants.
Figure 3: Early auxin distribution in the regenerating root tip.
Figure 4: Regeneration competence markers and leaf regeneration.

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Gene Expression Omnibus

Data deposits

Microarray data have been submitted to GEO (NCBI) under the accession number GSE9996.

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Acknowledgements

We thank B. Scheres and R. Heidstra for mutant and reporter lines and for comments. We thank P. Doerner for the CYCB1;1::GFP reporter, J. Friml for the PINFORMED (PIN) reporter lines, and C. Desplan, T. Nawy, B. Bargmann and M. Gifford for comments. This work was supported by the National Institutes of Health grant 5R01GM078279 (K.D.B.)

Author Contributions G.S. performed all experiments with help from X.W. and H.Y.L. on dissections and microarrays. H.H. generated PLT reporter constructs. K.D.B. and G.S. conceived the project, planned all experiments, performed data analysis and wrote the manuscript.

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Correspondence to Kenneth D. Birnbaum.

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This file contains Supplementary Figures 1-9 with Legends, Supplementary Tables 1-2, Supplementary Methods and Supplementary References (PDF 1937 kb)

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Sena, G., Wang, X., Liu, HY. et al. Organ regeneration does not require a functional stem cell niche in plants. Nature 457, 1150–1153 (2009). https://doi.org/10.1038/nature07597

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