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

Nature volume 457, pages 1150–1153 (2009)Cite this article

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

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

References

  1. Steward, F. C., Ammirato, P. V. & Mapes, M. O. Growth and development of totipotent cells — some problems, procedures, perspectives. Ann. Bot. (Lond.) 34, 761–787 (1970)

    Article  CAS  Google Scholar 

  2. Thowfeequ, S., Myatt, E. J. & Tosh, D. Transdifferentiation in developmental biology, disease, and in therapy. Dev. Dyn. 236, 3208–3217 (2007)

    Article  CAS  Google Scholar 

  3. Zhou, Q., Brown, J., Kanarek, A., Rajagopal, J. & Melton, D. A. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455, 627–632 (2008)

    Article  ADS  CAS  Google Scholar 

  4. van den Berg, C., Willemsen, V., Hendriks, G., Weisbeek, P. & Scheres, B. Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390, 287–289 (1997)

    Article  ADS  CAS  Google Scholar 

  5. Aida, M. et al. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120 (2004)

    Article  CAS  Google Scholar 

  6. Feldman, L. J. De novo origin of quiescent center regenerating root apices of Zea mays . Planta 128, 207–212 (1976)

    Article  CAS  Google Scholar 

  7. Rost, T. L. & Jones, T. J. Pea root regeneration after tip excisions at different levels — polarity of new growth. Ann. Bot. (Lond.) 61, 513–523 (1988)

    Article  Google Scholar 

  8. Xu, J. et al. A molecular framework for plant regeneration. Science 311, 385–388 (2006)

    Article  ADS  CAS  Google Scholar 

  9. Birnbaum, K. et al. A gene expression map of the Arabidopsis root. Science 302, 1956–1960 (2003)

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  11. Lee, J. Y. et al. Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc. Natl Acad. Sci. USA 103, 6055–6060 (2006)

    Article  ADS  CAS  Google Scholar 

  12. Wang, J. W. et al. Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis . Plant Cell 17, 2204–2216 (2005)

    Article  CAS  Google Scholar 

  13. Sack, F. D. Plastids and gravitropic sensing. Planta 203, S63–S68 (1997)

    Article  CAS  Google Scholar 

  14. Blancaflor, E. B., Fasano, J. M. & Gilroy, S. Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol. 116, 213–222 (1998)

    Article  CAS  Google Scholar 

  15. Galinha, C. et al. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449, 1053–1057 (2007)

    Article  ADS  CAS  Google Scholar 

  16. Heidstra, R., Welch, D. & Scheres, B. Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev. 18, 1964–1969 (2004)

    Article  CAS  Google Scholar 

  17. Sabatini, S., Heidstra, R., Wildwater, M. & Scheres, B. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17, 354–358 (2003)

    Article  CAS  Google Scholar 

  18. Sabatini, S. et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472 (1999)

    Article  CAS  Google Scholar 

  19. Grieneisen, V. A., Xu, J., Maree, A. F., Hogeweg, P. & Scheres, B. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449, 1008–1013 (2007)

    Article  ADS  CAS  Google Scholar 

  20. Benkova, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003)

    Article  CAS  Google Scholar 

  21. Che, P., Lall, S., Nettleton, D. & Howell, S. H. Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture. Plant Physiol. 141, 620–637 (2006)

    Article  CAS  Google Scholar 

  22. Beemster, G. T., Vercruysse, S., De Veylder, L., Kuiper, M. & Inze, D. The Arabidopsis leaf as a model system for investigating the role of cell cycle regulation in organ growth. J. Plant Res. 119, 43–50 (2006)

    Article  Google Scholar 

  23. Figdor, W. Uber Restitutionserscheinungen an Blattern von Gesneriaceen. Jahrb. Wiss. Bot. 44, 41–56 (1907)

    Google Scholar 

  24. Tusher, V. G., Tibshirani, R. & Chu, G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl Acad. Sci. USA 98, 5116–5121 (2001)

    Article  ADS  CAS  Google Scholar 

  25. Nemhauser, J. L., Hong, F. & Chory, J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126, 467–475 (2006)

    Article  CAS  Google Scholar 

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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.

Author information

Authors and Affiliations

  1. Department of Biology, New York University, Center for Genomics and Systems Biology, Silver Building, 100 Washington Square East, New York, New York 10003, USA,

    Giovanni Sena, Xiaoning Wang, Hsiao-Yun Liu & Kenneth D. Birnbaum

  2. Department of Biology, Utrecht University, Faculty of Science, Padualaan 8, 3584 CH, Utrecht, The Netherlands,

    Hugo Hofhuis

Authors
  1. Giovanni Sena
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  2. Xiaoning Wang
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  5. Kenneth D. Birnbaum
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Corresponding author

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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