Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

PRC2 represses dedifferentiation of mature somatic cells in Arabidopsis

Abstract

Plant somatic cells are generally acknowledged to retain totipotency, the potential to develop into any cell type within an organism. This astonishing plasticity may contribute to a high regenerative capacity on severe damage, but how plants control this potential during normal post-embryonic development remains largely unknown1,2. Here we show that POLYCOMB REPRESSIVE COMPLEX 2 (PRC2), a chromatin regulator that maintains gene repression through histone modification, prevents dedifferentiation of mature somatic cells in Arabidopsis thaliana roots. Loss-of-function mutants in PRC2 subunits initially develop unicellular root hairs indistinguishable from those in wild type but fail to retain the differentiated state, ultimately resulting in the generation of an unorganized cell mass and somatic embryos from a single root hair. Strikingly, mutant root hairs complete the normal endoreduplication programme, increasing their nuclear ploidy, but subsequently reinitiate mitotic division coupled with successive DNA replication. Our data show that the WOUND INDUCED DEDIFFERENTIATION3 (WIND3) and LEAFY COTYLEDON2 (LEC2) genes are among the PRC2 targets involved in this reprogramming, as their ectopic overexpression partly phenocopies the dedifferentiation phenotype of PRC2 mutants. These findings unveil the pivotal role of PRC2-mediated gene repression in preventing unscheduled reprogramming of fully differentiated plant cells.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: PRC2 represses dedifferentiation of mature root hair cells.
Figure 2: Key developmental regulators are ectopically activated in PRC2 mutant roots.
Figure 3: PRC2 directly targets WIND3.
Figure 4: Overexpression of WIND1, WIND2, WIND3 or LEC2 partly phenocopies the multicellular root hair phenotype of PRC2 mutants.

Similar content being viewed by others

References

  1. Ikeuchi, M., Sugimoto, K. & Iwase, A. Plant callus: mechanisms of induction and repression. Plant Cell 25, 4159–3173 (2013).

    Article  Google Scholar 

  2. Birnbaum, K. D. & Alvarado, A. S. Slicing across kingdoms: regeneration in plants and animals. Cell 132, 697–710 (2008).

    Article  CAS  Google Scholar 

  3. Steward, F. C., Mapes, M. O. & Mears, K. Growth and organized development of cultured cells. II. Organization in cultures grown from freely suspended cells. Am. J. Bot. 45, 705–708 (1958).

    Article  Google Scholar 

  4. Datta, S. et al. Root hairs: development, growth and evolution at the plant-soil interface. Plant Soil 346, 1–14 (2011).

    Article  CAS  Google Scholar 

  5. Chanvivattana, Y. et al. Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131, 5263–5276 (2004).

    Article  CAS  Google Scholar 

  6. Bouyer, D. et al. Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet. 7, e1002014 (2011).

    Article  CAS  Google Scholar 

  7. Mylne, J. S. et al. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl Acad. Sci. USA 103, 5012–5017 (2006).

    Article  CAS  Google Scholar 

  8. Cho, H.-T. & Cosgrove, D. J. Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 14, 3237–3253 (2002).

    Article  CAS  Google Scholar 

  9. Campilho, A. et al. Time-lapse analysis of stem-cell divisions in the Arabidopsis thaliana root meristem. Plant J. 48, 619–627 (2006).

    Article  CAS  Google Scholar 

  10. Chytilova, E. et al. Nuclear dynamics in Arabidopsis thaliana. Mol. Biol. Cell 11, 2733–2741 (2000).

    Article  CAS  Google Scholar 

  11. Sugimoto-Shirasu, K. et al. RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth. Proc. Natl Acad. Sci. USA 102, 18736–18741 (2005).

    Article  CAS  Google Scholar 

  12. Breuer, C., Ishida, T. & Sugimoto, K. Developmental control of endocycles and cell growth in plants. Curr. Opin. Plant Biol. 13, 654–660 (2010).

    Article  CAS  Google Scholar 

  13. Breuer, C. et al. BIN4, a novel component of the plant DNA topoisomerase VI complex, is required for endoreduplication in Arabidopsis. Plant Cell 19, 3655–3668 (2007).

    Article  CAS  Google Scholar 

  14. Iwata, E. et al. GIGAS CELL1, a novel negative regulator of the anaphase-promoting complex/cyclosome, is required for proper mitotic progression and cell fate determination in Arabidopsis. Plant Cell 23, 4382–4393 (2011).

    Article  CAS  Google Scholar 

  15. Lafos, M. et al. Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet. 7, e1002040 (2011).

    Article  CAS  Google Scholar 

  16. Schubert, D. et al. Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 25, 4638–4649 (2006).

    Article  CAS  Google Scholar 

  17. Bemer, M. & Grossniklaus, U. Dynamic regulation of Polycomb group activity during plant development. Curr. Opin. Plant Biol. 15, 523–529 (2012).

    Article  CAS  Google Scholar 

  18. Aichinger, E., Villar, C. B. R., Di Mambro, R., Sabatini, S. & Köhler, C. The CHD3 chromatin remodeler PICKLE and Polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23, 1047–1060 (2011).

    Article  CAS  Google Scholar 

  19. Roudier, F. et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928–1938 (2011).

    Article  CAS  Google Scholar 

  20. Iwase, A. et al. The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr. Biol. 21, 508–514 (2011).

    Article  CAS  Google Scholar 

  21. Deal, R. B. & Henikoff, S. A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev. Cell 18, 1030–1040 (2010).

    Article  CAS  Google Scholar 

  22. Ledwoń, A. & Gaj, M. D. LEAFY COTYLEDON2 gene expression and auxin treatment in relation to embryogenic capacity of Arabidopsis somatic cells. Plant Cell Rep. 28, 1677–1688 (2009).

    Article  Google Scholar 

  23. Atta, R. et al. Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J. 57, 626–644 (2009).

    Article  CAS  Google Scholar 

  24. Sugimoto, K., Jiao, Y. & Meyerowitz, E. M. Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev. Cell 18, 463–471 (2010).

    Article  CAS  Google Scholar 

  25. Sugimoto, K., Gordon, S. P. & Meyerowitz, E. M. Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol. 21, 212–218 (2011).

    Article  CAS  Google Scholar 

  26. Stone, S. L. et al. LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc. Natl Acad. Sci. USA 98, 11806–11811 (2001).

    Article  CAS  Google Scholar 

  27. Yang, C. et al. VAL- and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr. Biol 23, 1324–1329 (2013).

    Article  CAS  Google Scholar 

  28. Wang, D., Tyson, M. D., Jackson, S. S. & Yadegari, R. Partially redundant functions of two SET-domain Polycomb-group proteins in controlling initiation of seed development in Arabidopsis. Proc. Natl Acad. Sci. USA 103, 13244–13249 (2006).

    Article  CAS  Google Scholar 

  29. Choi, J. et al. Resetting and regulation of Flowering Locus C expression during Arabidopsis reproductive development. Plant J. 57, 918–931 (2009).

    Article  CAS  Google Scholar 

  30. Karimi, M., De Meyer, B. & Hilson, P. Modular cloning in plant cells. Trends Plant Sci. 10, 103–105 (2005).

    Article  CAS  Google Scholar 

  31. Nakagawa, T. et al. Development of R4 gateway binary vectors (R4pGWB) enabling high-throughput promoter swapping for plant research. Biosci. Biotechnol. Biochem. 72, 624–629 (2008).

    Article  CAS  Google Scholar 

  32. Breuer, C. et al. Transcriptional repression of the APC/C activator CCS52A1 promotes active termination of cell growth. EMBO J. 31, 4488–4501 (2012).

    Article  CAS  Google Scholar 

  33. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    Article  CAS  Google Scholar 

  34. Ishida, T. et al. SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21, 2284–2297 (2009).

    Article  CAS  Google Scholar 

  35. Hayashi, K., Hasegawa, J. & Matsunaga, S. The boundary of the meristematic and elongation zones in roots: endoreduplication precedes rapid cell expansion. Sci. Rep. 3, 2723 (2013).

    Article  Google Scholar 

  36. Seifert, M. et al. MeDIP-HMM: genome-wide identification of distinct DNA methylation states from high-density tiling arrays. Bioinformatics 28, 2930–2939 (2012).

    Article  CAS  Google Scholar 

  37. Marchive, C. et al. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Commun. 4, 1713 (2013).

    Article  Google Scholar 

  38. Morohashi, K. & Grotewold, E. A systems approach reveals regulatory circuitry for Arabidopsis trichome initiation by the GL3 and GL1 selectors. PLoS Genet. 5, e1000396 (2009).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by Grant-in-Aid for Scientific Research on Priority Areas (22119010) and a grant from Scientific Technique Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry to K.S. M.I. is supported by the RIKEN Special Postdoctoral Researcher Programme. Epigenomic studies were supported by the European Union Seventh Framework Programme Network of Excellence EpiGeneSys and the CNRS to the group of V. Colot (A.K.M. and F.R.). A.K.M. is the recipient of a grant from the French Ministère de la Recherche et de l'Enseignement Supérieur. PRC2 expression studies were supported by a France-Berkeley grant to F.R. and S.M.B., an EMBO LT and Human Frontiers Science Program Postdoctoral Fellowship to M.dL. and a Hellman Junior Faculty Fellowship to S.M.B.

Author information

Authors and Affiliations

Authors

Contributions

A.I. and K.S. conceived the project. M.I., A.I. and K.S. designed the experiments, and M.I., A.I. and M.O. conducted most of genetic and cell biological analyses except ChIP-chip, which was performed by F.R., A.K.M. and J.G., and ploidy analyses, which was performed by L.D.V., H.H., B.R. and M.S. C.B. generated pEXP7:NLS–GFP and pEXP7:GTL1–GFP plants, and M.dL. and S.M.B. generated pEMF2:EMF2–GFP plants. M.I. and K.S. wrote the manuscript with help from the co-authors.

Corresponding author

Correspondence to Keiko Sugimoto.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ikeuchi, M., Iwase, A., Rymen, B. et al. PRC2 represses dedifferentiation of mature somatic cells in Arabidopsis. Nature Plants 1, 15089 (2015). https://doi.org/10.1038/nplants.2015.89

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.89

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing