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The heterodimeric transcription factor complex ERF115–PAT1 grants regeneration competence

Nature Plants volume 2, Article number: 16165 (2016) Cite this article

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Abstract

Regeneration of a tissue damaged by injury represents a physiological response for organ recovery1–3. 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.

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Figure 1: ERF115 interacts with SCL21 and PAT1.
Figure 2: ERF115 and PAT1 co-expression precedes stress-induced cell division.
Figure 3: ERF115–PAT1 activity is required for root tip regeneration.
Figure 4: ERF115–PAT1 activity triggers uncontrolled cell division.

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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.).

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Authors and 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, 230-0045, Kanagawa, Japan

    Keiko Sugimoto

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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.

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Correspondence to Lieven De Veylder.

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The authors declare no competing financial interests.

Supplementary information

Extended Data

Extended Data Figures 1–10, Supplementary Video Legends 1–5. (PDF 11364 kb)

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). (XLSX 24 kb)

Supplementary Table 2

Primers for cloning and RT-qPCR. (XLSX 12 kb)

Supplementary Video 1

Time-lapse movie of a pERF115:TdTomato- and pPAT1:GFP-labelled root tip following recovery from bleomycin treatment. (AVI 1250 kb)

Supplementary Video 2

Time-lapse of ERF115 expression following laser-induced cell death. (AVI 433 kb)

Supplementary Video 3

Time-lapse movie of a wild-type root meristem following recovery from bleomycin treatment. (MOV 3530 kb)

Supplementary Video 4

Time-lapse movie of a ERF115SRDX mutant root meristem following recovery from bleomycin treatment. (MOV 957 kb)

Supplementary Video 5

Time-lapse movie of a pat1-2 mutant root meristem following recovery from bleomycin treatment. (MOV 1486 kb)

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Heyman, J., Cools, T., Canher, B. et al. The heterodimeric transcription factor complex ERF115–PAT1 grants regeneration competence. Nature Plants 2, 16165 (2016). https://doi.org/10.1038/nplants.2016.165

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