VIA1 is a conserved regulator of thylakoid membrane integrity that acts through VIPP1.

Abstract

Thylakoid membranes are indispensable for oxygenic photosynthesis, yet the mechanisms that protect these membranes from photooxidative damage remain poorly understood. By screening poorly characterized proteins induced during the chloroplast unfolded protein response, we identify VIA1 as an essential factor for preserving thylakoid integrity under high light in the model green alga <i>Chlamydomonas reinhardtii</i>. Loss of VIA1 causes hypersensitivity to photo-oxidative stress and rapid thylakoid swelling. VIA1 localizes to thylakoid membranes and directly binds Vesicle-Inducing Protein in Plastids 1 (VIPP1), an ESCRT-III-like protein essential for thylakoid biogenesis and remodeling. Structure-guided mutagenesis shows that this interaction is required for VIA1 function and is mediated by a winged-helix domain interface reminiscent of ESCRT-II/ESCRT-III binding mode. VIA1 orthologs from cyanobacteria and land plants rescue the Chlamydomonas <i>via1</i> mutant phenotype, and disruption of VIA1 in <i>Synechocystis sp</i>. PCC 6803 impairs growth, especially under light stress. Together, these findings establish VIA1 as an evolutionarily conserved protein that contributes to thylakoid membrane homeostasis via its interaction with VIPP1.