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Research Article

Structure of the Arabidopsis TOPLESS corepressor provides insight into the evolution of transcriptional repression

Raquel Martin-Arevalillo, Max H. Nanao, View ORCID ProfileAntoine Larrieu, Thomas Vinos-Poyo, David Mast, Carlos Galvan-Ampudia, Géraldine Brunoud, View ORCID ProfileTeva Vernoux, Renaud Dumas, and View ORCID ProfileFrançois Parcy
  1. aLaboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, Commissariat à l'Energie Atomique et aux Energies Alternatives/Biosciences and Biotechnology Institute of Grenoble, Institut National de la Recherche Agronomique (INRA), F-38000 Grenoble, France;
  2. bStructural Biology Group, European Synchrotron Radiation Facility, F-38000 Grenoble, France;
  3. cEuropean Molecular Biology Laboratory Grenoble, 38042 Grenoble Cedex 9, France;
  4. dLaboratoire de Reproduction et Développement des Plantes, Université de Lyon, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, F-69364 Lyon, France

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PNAS July 25, 2017 114 (30) 8107-8112; first published July 11, 2017; https://doi.org/10.1073/pnas.1703054114
Raquel Martin-Arevalillo
aLaboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, Commissariat à l'Energie Atomique et aux Energies Alternatives/Biosciences and Biotechnology Institute of Grenoble, Institut National de la Recherche Agronomique (INRA), F-38000 Grenoble, France;
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Max H. Nanao
bStructural Biology Group, European Synchrotron Radiation Facility, F-38000 Grenoble, France;
cEuropean Molecular Biology Laboratory Grenoble, 38042 Grenoble Cedex 9, France;
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  • For correspondence: teva.vernoux@ens-lyon.fr nanao@esrf.fr renaud.dumas@cea.fr
Antoine Larrieu
dLaboratoire de Reproduction et Développement des Plantes, Université de Lyon, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, F-69364 Lyon, France
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  • ORCID record for Antoine Larrieu
Thomas Vinos-Poyo
aLaboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, Commissariat à l'Energie Atomique et aux Energies Alternatives/Biosciences and Biotechnology Institute of Grenoble, Institut National de la Recherche Agronomique (INRA), F-38000 Grenoble, France;
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David Mast
aLaboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, Commissariat à l'Energie Atomique et aux Energies Alternatives/Biosciences and Biotechnology Institute of Grenoble, Institut National de la Recherche Agronomique (INRA), F-38000 Grenoble, France;
dLaboratoire de Reproduction et Développement des Plantes, Université de Lyon, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, F-69364 Lyon, France
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Carlos Galvan-Ampudia
dLaboratoire de Reproduction et Développement des Plantes, Université de Lyon, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, F-69364 Lyon, France
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Géraldine Brunoud
dLaboratoire de Reproduction et Développement des Plantes, Université de Lyon, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, F-69364 Lyon, France
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Teva Vernoux
dLaboratoire de Reproduction et Développement des Plantes, Université de Lyon, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, CNRS, INRA, F-69364 Lyon, France
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  • ORCID record for Teva Vernoux
  • For correspondence: teva.vernoux@ens-lyon.fr nanao@esrf.fr renaud.dumas@cea.fr
Renaud Dumas
aLaboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, Commissariat à l'Energie Atomique et aux Energies Alternatives/Biosciences and Biotechnology Institute of Grenoble, Institut National de la Recherche Agronomique (INRA), F-38000 Grenoble, France;
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  • For correspondence: teva.vernoux@ens-lyon.fr nanao@esrf.fr renaud.dumas@cea.fr
François Parcy
aLaboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, Commissariat à l'Energie Atomique et aux Energies Alternatives/Biosciences and Biotechnology Institute of Grenoble, Institut National de la Recherche Agronomique (INRA), F-38000 Grenoble, France;
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  1. Edited by Mark Estelle, University of California, San Diego, La Jolla, CA, and approved June 13, 2017 (received for review February 22, 2017)

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Significance

In most biological processes, genes have to be activated and/or repressed. In plants, the TOPLESS protein is essential for gene repression through its action as a corepressor bridging transcription factor with chromatin remodeling complexes. Here we combine biochemical and structural studies to describe the structure of TOPLESS, how it tetramerizes, and how it interacts with its protein partners. We show that both the tetramerization interface and the binding site for protein partners have been conserved since algae, highlighting the ancestrality of TOPLESS function. Comparison of this plant protein with one of its animal counterparts also shows how corepressors can use a common domain differently to achieve similar properties, illustrating the tinkering of evolution in transcriptional repression.

Abstract

Transcriptional repression involves a class of proteins called corepressors that link transcription factors to chromatin remodeling complexes. In plants such as Arabidopsis thaliana, the most prominent corepressor is TOPLESS (TPL), which plays a key role in hormone signaling and development. Here we present the crystallographic structure of the Arabidopsis TPL N-terminal region comprising the LisH and CTLH (C-terminal to LisH) domains and a newly identified third region, which corresponds to a CRA domain. Comparing the structure of TPL with the mammalian TBL1, which shares a similar domain structure and performs a parallel corepressor function, revealed that the plant TPLs have evolved a new tetramerization interface and unique and highly conserved surface for interaction with repressors. Using site-directed mutagenesis, we validated those surfaces in vitro and in vivo and showed that TPL tetramerization and repressor binding are interdependent. Our results illustrate how evolution used a common set of protein domains to create a diversity of corepressors, achieving similar properties with different molecular solutions.

  • TOPLESS
  • corepressor
  • auxin signaling
  • crystal structure
  • tetramerization

Footnotes

  • ↵1To whom correspondence may be addressed. Email: teva.vernoux{at}ens-lyon.fr, nanao{at}esrf.fr, or renaud.dumas{at}cea.fr.
  • Author contributions: M.H.N., T.V., R.D., and F.P. designed research; R.M.-A., M.H.N., A.L., T.V.-P., D.M., C.G.-A., G.B., and R.D. performed research; R.M.-A., M.H.N., A.L., T.V.-P., D.M., T.V., R.D., and F.P. analyzed data; and R.M.-A., M.H.N., T.V., R.D., and F.P. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The atomic coordinates have been deposited in the Protein Data Bank, www.wwpdb.org (PDB ID codes 5NQV and 5NQS).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1703054114/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Structure of the TOPLESS corepressor
Raquel Martin-Arevalillo, Max H. Nanao, Antoine Larrieu, Thomas Vinos-Poyo, David Mast, Carlos Galvan-Ampudia, Géraldine Brunoud, Teva Vernoux, Renaud Dumas, François Parcy
Proceedings of the National Academy of Sciences Jul 2017, 114 (30) 8107-8112; DOI: 10.1073/pnas.1703054114

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Structure of the TOPLESS corepressor
Raquel Martin-Arevalillo, Max H. Nanao, Antoine Larrieu, Thomas Vinos-Poyo, David Mast, Carlos Galvan-Ampudia, Géraldine Brunoud, Teva Vernoux, Renaud Dumas, François Parcy
Proceedings of the National Academy of Sciences Jul 2017, 114 (30) 8107-8112; DOI: 10.1073/pnas.1703054114
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