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Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity

Tilak Kumar Gupta, View ORCID ProfileSven Klumpe, Karin Gries, Steffen Heinz, View ORCID ProfileWojciech Wietrzynski, Norikazu Ohnishi, Justus Niemeyer, View ORCID ProfileMiroslava Schaffer, View ORCID ProfileAnna Rast, View ORCID ProfileMike Strauss, View ORCID ProfileJürgen M. Plitzko, View ORCID ProfileWolfgang Baumeister, View ORCID ProfileTill Rudack, View ORCID ProfileWataru Sakamoto, View ORCID ProfileJörg Nickelsen, View ORCID ProfileJan M. Schuller, View ORCID ProfileMichael Schroda, View ORCID ProfileBenjamin D. Engel
doi: https://doi.org/10.1101/2020.08.11.243204
Tilak Kumar Gupta
1Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
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Sven Klumpe
1Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
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Karin Gries
2Molecular Biotechnology and Systems Biology, Technische Universität Kaiserslautern, Paul-Ehrlich Straße 23, 67663 Kaiserslautern, Germany
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Steffen Heinz
3Department of Molecular Plant Sciences, LMU Munich, 82152 Martinsried, Germany
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Wojciech Wietrzynski
1Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
4Helmholtz Pioneer Campus, Helmholtz Zentrum München, Ingolstädter Landstraße 1, 85764 Neuherberg, Germany
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Norikazu Ohnishi
5Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama 710-0046, Japan
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Justus Niemeyer
2Molecular Biotechnology and Systems Biology, Technische Universität Kaiserslautern, Paul-Ehrlich Straße 23, 67663 Kaiserslautern, Germany
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Miroslava Schaffer
1Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
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Anna Rast
1Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
3Department of Molecular Plant Sciences, LMU Munich, 82152 Martinsried, Germany
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Mike Strauss
6Department of Anatomy and Cell Biology, McGill University, 3640 University St, Montreal, H3A 17C, QC, Canada
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Jürgen M. Plitzko
1Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
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Wolfgang Baumeister
1Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
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Till Rudack
7Biospectroscopy, Center for Protein Diagnostics (ProDi), Ruhr University Bochum, 44801 Bochum, Germany
8Department of Biophysics, Faculty of Biology & Biotechnology, Ruhr University Bochum, 44780 Bochum, Germany
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Wataru Sakamoto
5Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama 710-0046, Japan
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  • ORCID record for Wataru Sakamoto
Jörg Nickelsen
3Department of Molecular Plant Sciences, LMU Munich, 82152 Martinsried, Germany
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  • For correspondence: joerg.nickelsen@lrz.uni-muenchen.de jan.schuller@synmikro.uni-marburg.de schroda@bio.uni-kl.de ben.engel@helmholtz-muenchen.de
Jan M. Schuller
9Philipps-University Marburg, SYNMIKRO Research Center and Department of Chemistry, 35032 Marburg, Germany
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  • For correspondence: joerg.nickelsen@lrz.uni-muenchen.de jan.schuller@synmikro.uni-marburg.de schroda@bio.uni-kl.de ben.engel@helmholtz-muenchen.de
Michael Schroda
2Molecular Biotechnology and Systems Biology, Technische Universität Kaiserslautern, Paul-Ehrlich Straße 23, 67663 Kaiserslautern, Germany
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  • For correspondence: joerg.nickelsen@lrz.uni-muenchen.de jan.schuller@synmikro.uni-marburg.de schroda@bio.uni-kl.de ben.engel@helmholtz-muenchen.de
Benjamin D. Engel
1Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
4Helmholtz Pioneer Campus, Helmholtz Zentrum München, Ingolstädter Landstraße 1, 85764 Neuherberg, Germany
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  • For correspondence: joerg.nickelsen@lrz.uni-muenchen.de jan.schuller@synmikro.uni-marburg.de schroda@bio.uni-kl.de ben.engel@helmholtz-muenchen.de
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Abstract

Vesicle-inducing protein in plastids (VIPP1) is essential for the biogenesis and maintenance of thylakoid membranes, which transform light into life. However, it is unknown how VIPP1 performs its vital membrane-shaping function. Here, we use cryo-electron microscopy to determine structures of cyanobacterial VIPP1 rings, revealing how VIPP1 monomers flex and interweave to form basket-like assemblies of different symmetries. Three VIPP1 monomers together coordinate a non-canonical nucleotide binding pocket that is required for VIPP1 oligomerization. Inside the ring’s lumen, amphipathic helices from each monomer align to form large hydrophobic columns, enabling VIPP1 to bind and curve membranes. In vivo point mutations in these hydrophobic surfaces cause extreme thylakoid swelling under high light, indicating an essential role of VIPP1 lipid binding in resisting stress-induced damage. Our study provides a structural basis for understanding how the oligomerization of VIPP1 drives the biogenesis of thylakoid membranes and protects these life-giving membranes from environmental stress.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • One Sentence Highlight: The high-resolution structure of VIPP1 reveals how this conserved essential protein oligomerizes, hydrolyzes nucleotides, and binds lipids, providing mechanistic insights into thylakoid biogenesis and protection from environmental stress.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity
Tilak Kumar Gupta, Sven Klumpe, Karin Gries, Steffen Heinz, Wojciech Wietrzynski, Norikazu Ohnishi, Justus Niemeyer, Miroslava Schaffer, Anna Rast, Mike Strauss, Jürgen M. Plitzko, Wolfgang Baumeister, Till Rudack, Wataru Sakamoto, Jörg Nickelsen, Jan M. Schuller, Michael Schroda, Benjamin D. Engel
bioRxiv 2020.08.11.243204; doi: https://doi.org/10.1101/2020.08.11.243204
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Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity
Tilak Kumar Gupta, Sven Klumpe, Karin Gries, Steffen Heinz, Wojciech Wietrzynski, Norikazu Ohnishi, Justus Niemeyer, Miroslava Schaffer, Anna Rast, Mike Strauss, Jürgen M. Plitzko, Wolfgang Baumeister, Till Rudack, Wataru Sakamoto, Jörg Nickelsen, Jan M. Schuller, Michael Schroda, Benjamin D. Engel
bioRxiv 2020.08.11.243204; doi: https://doi.org/10.1101/2020.08.11.243204

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