Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity

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.

SPIRE, Surface Projection Image Recognition Environment for bicontinuous phases: application for plastid cubic membranes

“…Although the role of light-dependent protochlorophyllide oxidoreductase in membrane tubulation was proven recently using electron cryo-tomography techniques (Nguyen et al, 2021;Floris and Kühlbrandt, 2021), factors governing the transition of tubular arrangements into cubic configuration remain elusive (Wietrzynski and Engel, 2021). The role of already recognized structure-remodeling proteins of plastid membranes (CURT1, VIPP1) in this process cannot be excluded and require further investigation (Armbruster et al, 2013;Gupta et al, 2020). PLBs are rare examples of cubic membranes resembling an imbalanced structure, in which the two aqueous channels are geometrically different; the smaller channel is a direct precursor of thylakoid lumen of chloroplasts (Kowalewska et al, 2016).…”

A brief history of how microscopic studies led to the elucidation of the 3D architecture and macromolecular organization of higher plant thylakoids

“…Another chloroplast mutant, vpp1 is also unable to produce IEM-derived vesicles and exhibits a phenotype similar to cpsfl1 (Zhang and Sakamoto 2015). A recent cyro-electron microscopy study has produced high-resolution structures of VPP1 rings produced in vitro, which illustrate how VPP1 monomers interact with each other and how they bind membrane lipid molecules and thereby induce membrane curvature (Gupta et al 2020). Together, these results support the hypothesis that chloroplast vesicles are responsible for the transport of PIPs and PA from the IEM to the thylakoids, whereas the IEM thylakoid contact sites serve the transfer of galactolipids to the thylakoids.…”

“…The most recent advance of cryo-ET research comes from the combination of ion-milling, cryo-ET and improved image analysis methods (Engel et al 2015;Wietrzynski et al 2020). These studies have, for the first time, provided a means for obtaining in situ cryo-ET images of thylakoid membranes in vitrified Chlamydomonas cells (Fig.…”

“…The large, dimeric PSII complexes are limited to the grana membrane domains, whereas the smaller PSI particles are limited to stroma membranes. From Wietrzynski et al (2020)…”

A Structural View on ESCRT-Mediated Abscission

“…The ESCRT machinery is conserved from archaea to humans (Hurley and Emr, 2006;Lindås et al, 2008;Schöneberg et al, 2017;Gupta et al, 2020). The 12 human homologs of ESCRT-III and VPS4 were shown to contribute to cytokinesis (Carlton and Martin-Serrano, 2007;Morita et al, 2007;Caballe and Martin-Serrano, 2011;Schöneberg et al, 2017).…”