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, Benjamin Spaniol, Miroslava Schaffer, Anna Rast, Matthias Ostermeier, Mike Strauss, Jürgen M. Plitzko, Wolfgang Baumeister, Till Rudack, Wataru Sakamoto, Jörg Nickelsen, Jan M. Schuller, Michael Schroda, Benjamin D. Engel

Research output: Contribution to journalArticlepeer-review

18 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)3643-3659.e23
JournalCell
Volume184
Issue number14
DOIs
Publication statusPublished - Jul 8 2021

Keywords

  • CLEM
  • Chlamydomonas
  • ESCRT-III
  • Synechocystis
  • cryo-EM
  • cryo-electron tomography
  • membrane remodeling
  • nucleotide hydrolysis
  • photosynthesis
  • stress response
  • thylakoid biogenesis

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

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