Letter | Published:

The heterodimeric transcription factor complex ERF115–PAT1 grants regeneration competence

Nature Plants volume 2, Article number: 16165 (2016) | Download Citation

Abstract

Regeneration of a tissue damaged by injury represents a physiological response for organ recovery1,​2,​3. Although this regeneration process is conserved across multicellular taxa, plants appear to display extremely high regenerative capacities, a feature widely used in tissue culture for clonal propagation and grafting4,5. Regenerated cells arise predominantly from pre-existing populations of division-competent cells6,7; however, the mechanisms by which these cells are triggered to divide in response to injury remain largely elusive8. Here, we demonstrate that the heterodimeric transcription factor complex ETHYLENE RESPONSE FACTOR115 (ERF115)–PHYTOCHROME A SIGNAL TRANSDUCTION1 (PAT1) sustains meristem function by promoting cell renewal after stem cell loss. High-resolution time-lapse imaging revealed that cell death promotes ERF115 activity in cells that are in direct contact with damaged cells, triggering divisions that replenish the collapsed stem cells. Correspondingly, the ERF115–PAT1 complex plays an important role in full stem cell niche recovery upon root tip excision, whereas its ectopic expression triggers neoplastic growth, correlated with activation of the putative target gene WOUND INDUCED DEDIFFERENTIATION1 (WIND1)9. We conclude that the ERF115–PAT1 complex accounts for the high regenerative potential of plants, granting them the ability to efficiently replace damaged cells with new ones.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    & Built to rebuild: in search of organizing principles in plant regeneration. Curr. Opin. Genet. Dev. 20, 460–465 (2010).

  2. 2.

    & Slicing across kingdoms: regeneration in plants and animals. Cell 132, 697–710 (2008).

  3. 3.

    & The role of stromal stem cells in tissue regeneration and wound repair. Science 324, 1666–1669 (2009).

  4. 4.

    & Plant grafting. Curr. Biol. 25, R183–R188 (2015).

  5. 5.

    History of plant tissue culture. Mol. Biotechnol. 37, 169–180 (2007).

  6. 6.

    , & Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol. 21, 212–218 (2011).

  7. 7.

    , & Plant callus: mechanisms of induction and repression. Plant Cell 25, 3159–3173 (2013).

  8. 8.

    How does a single somatic cell become a whole plant? Science 309, 86 (2005).

  9. 9.

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

  10. 10.

    , , , & Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390, 287–289 (1997).

  11. 11.

    et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811–814 (2007).

  12. 12.

    et al. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131, 657–668 (2004).

  13. 13.

    & Hypersensitivity to DNA damage in plant stem cell niches. Proc. Natl Acad. Sci. USA 106, 20984–20988 (2009).

  14. 14.

    et al. ERF115 controls root quiescent center cell division and stem cell replenishment. Science 342, 860–863 (2013).

  15. 15.

    et al. TOPOISOMERASE1α acts through two distinct mechanisms to regulate stele and columella stem cell maintenance in the Arabidopsis root. Plant Physiol. 171, 483–493 (2016).

  16. 16.

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

  17. 17.

    , & Two GRAS proteins, SCARECROW-LIKE21 and PHYTOCHROME A SIGNAL TRANSDUCTION1, function cooperatively in phytochrome A signal transduction. Plant Physiol. 161, 291–304 (2013).

  18. 18.

    , , & Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140, 411–432 (2006).

  19. 19.

    et al. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466, 128–132 (2010).

  20. 20.

    , , & The SHORT-ROOT protein acts as a mobile, dose-dependent signal in patterning the ground tissue. Proc. Natl Acad. Sci. USA 109, 13010–13015 (2012).

  21. 21.

    , , , & Organ regeneration does not require a functional stem cell niche in plants. Nature 457, 1150–1153 (2009).

  22. 22.

    et al. Root regeneration triggers an embryo-like sequence guided by hormonal interactions. Cell 165, 1721–1733 (2016).

  23. 23.

    et al. PLETHORA genes control regeneration by a two-step mechanism. Curr. Biol. 25, 1017–1030 (2015).

  24. 24.

    et al. Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev. Cell 17, 279–289 (2009).

  25. 25.

    et al. AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 1, 119–132 (2003).

  26. 26.

    , & ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16, 1091–1104 (2004).

  27. 27.

    et al. A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol. Cell Proteomics 6, 1226–1238 (2007).

  28. 28.

    et al. An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells. Nat. Methods 3, 1013–1019 (2006).

  29. 29.

    , , , Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci. 13, 517–520 (2008).

  30. 30.

    et al. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 6, 397 (2010).

  31. 31.

    et al. Atypical E2F activity restrains APC/CCCS52A2 function obligatory for endocycle onset. Proc. Natl Acad. Sci. USA 105, 14721–14726 (2008).

  32. 32.

    et al. Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 maintains cell division activity by temporal inhibition of the anaphase-promoting complex/cyclosome. Plant Cell 23, 4394–4410 (2011).

  33. 33.

    , , & Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20, 1425 (1992).

  34. 34.

    & Embedding thin plant specimens for oriented sectionings. Biotech. Histochem. 75, 23–26 (2000).

  35. 35.

    et al. An easy and versatile embedding method for transverse sections. J. Microsc. 213, 76–80 (2004).

Download references

Acknowledgements

The authors thank C. Bolle for sharing the pat1-2 mutant and Z. Ding for sharing the pWOX5 sequence used for construct generation, D. Van Damme for fruitful discussion concerning the dual colour confocal set-up, M. Van Durme for technical confocal microscopy assistance, and A. Bleys and M. De Cock for help in preparing the manuscript. This research was supported by the Interuniversity Attraction Poles Programme (IUAP P7/29 ‘MARS’) initiated by the Belgian Science Policy Office. J.H. and T.C. are post-doctoral fellows of the Research Foundation Flanders (F.W.O.).

Author information

Affiliations

  1. Department of Plant Systems Biology, VIB, B-9052 Gent, Belgium

    • Jefri Heyman
    • , Toon Cools
    • , Balkan Canher
    • , Sviatlana Shavialenka
    • , Jan Traas
    • , Ilse Vercauteren
    • , Hilde Van den Daele
    • , Geert Persiau
    • , Geert De Jaeger
    •  & Lieven De Veylder
  2. Department of Plant Biotechnology and Bioinformatics, Ghent University, B-9052 Gent, Belgium

    • Jefri Heyman
    • , Toon Cools
    • , Balkan Canher
    • , Sviatlana Shavialenka
    • , Jan Traas
    • , Ilse Vercauteren
    • , Hilde Van den Daele
    • , Geert Persiau
    • , Geert De Jaeger
    •  & Lieven De Veylder
  3. Laboratoire Reproduction et Développement des Plantes, University of Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, F-69342, Lyon, France

    • Jan Traas
  4. RIKEN Centre for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa 230-0045, Japan

    • Keiko Sugimoto

Authors

  1. Search for Jefri Heyman in:

  2. Search for Toon Cools in:

  3. Search for Balkan Canher in:

  4. Search for Sviatlana Shavialenka in:

  5. Search for Jan Traas in:

  6. Search for Ilse Vercauteren in:

  7. Search for Hilde Van den Daele in:

  8. Search for Geert Persiau in:

  9. Search for Geert De Jaeger in:

  10. Search for Keiko Sugimoto in:

  11. Search for Lieven De Veylder in:

Contributions

J.H., T.C., K.S. and L.D.V. conceived the experiments. J.H., T.C., S.S., J.T., B.C., H.V.d.D., I.V., G.P. and G.D.J. performed the experiments. J.H., T.C. and L.D.V. analysed the data. J.H., T.C. and L.D.V. wrote the manuscript. All authors approved the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Lieven De Veylder.

Supplementary information

PDF files

  1. 1.

    Extended Data

    Extended Data Figures 1–10, Supplementary Video Legends 1–5.

Excel files

  1. 1.

    Supplementary Table 1

    Protein identification details obtained with the 4800 MALDI TOF/TOF Proteomics Analyzer (AB SCIEX) and the GPS Explorer v3.6 (AB SCIEX) software package combined with the search engine Mascot version 2.2 (Matrix Science).

  2. 2.

    Supplementary Table 2

    Primers for cloning and RT-qPCR.

Videos

  1. 1.

    Supplementary Video 1

    Time-lapse movie of a pERF115:TdTomato- and pPAT1:GFP-labelled root tip following recovery from bleomycin treatment.

  2. 2.

    Supplementary Video 2

    Time-lapse of ERF115 expression following laser-induced cell death.

  3. 3.

    Supplementary Video 3

    Time-lapse movie of a wild-type root meristem following recovery from bleomycin treatment.

  4. 4.

    Supplementary Video 4

    Time-lapse movie of a ERF115SRDX mutant root meristem following recovery from bleomycin treatment.

  5. 5.

    Supplementary Video 5

    Time-lapse movie of a pat1-2 mutant root meristem following recovery from bleomycin treatment.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nplants.2016.165

Further reading