Structural basis for VIPP1 oligomerization and maintenance of thylakoid 
membrane integrity

Gupta, Tilak Kumar; Klumpe, Sven; Gries, Karin; Heinz, Steffen; Wietrzynski, Wojciech; Ohnishi, Norikazu; Niemeyer, Justus; Spaniol, Benjamin; Schaffer, Miroslava; Rast, Anna; Ostermeier, Matthias; Strauss, Mike; Plitzko, Jürgen M.; Baumeister, Wolfgang; Rudack, Till; Sakamoto, Wataru; Nickelsen, Joerg; Schuller, Jan M.; Schroda, Michael; Engel, Benjamin D.

doi:10.1016/j.cell.2021.05.011

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Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity

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Gupta, Tilak Kumar
Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society;

/persons/resource/persons249307

Klumpe, Sven
Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society;

/persons/resource/persons245332

Wietrzynski, Wojciech
Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society;

/persons/resource/persons86649

Schaffer, Miroslava
Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society;

/persons/resource/persons264193

Rast, Anna
Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society;

/persons/resource/persons78517

Plitzko, Jürgen M.
Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society;

/persons/resource/persons77721

Baumeister, Wolfgang
Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society;

/persons/resource/persons77937

Engel, Benjamin D.
Baumeister, Wolfgang / Molecular Structural Biology, Max Planck Institute of Biochemistry, Max Planck Society;

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Citation

Gupta, T. K., Klumpe, S., Gries, K., Heinz, S., Wietrzynski, W., Ohnishi, N., et al. (2021). Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity. Cell, 184(14), 3643-3659.e23. doi:10.1016/j.cell.2021.05.011.

Cite as: http://hdl.handle.net/21.11116/0000-0008-F3FF-7

Abstract

Vesicle-inducing protein in plastids 1 (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-remodeling functions. 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 on one end of the ring. 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 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. Using cryo-correlative light and electron microscopy (cryo-CLEM), we observe oligomeric VIPP1 coats encapsulating membrane tubules within the Chlamydomonas chloroplast. Our work provides a structural foundation for understanding how VIPP1 directs thylakoid biogenesis and maintenance.