A conserved ESCRT-II-like protein participates in the biogenesis and maintenance of thylakoid membranes

Thylakoids are membrane-bound compartments located in cyanobacteria and chloroplasts of plants and algae. They play an indispensable role in the light-driven reactions that enable photosynthetic organisms to convert water and carbon dioxide into oxygen and sugars. The biogenesis and maintenance of thylakoid membranes is a critical yet underappreciated area of research. One of the few known critical regulators of this process, VIPP1 (Vesicle-Inducing Protein in Plastids 1), was recently shown to be structurally similar to ESCRT-III proteins-the first evidence for ESCRT-like (Endosomal Sorting Complex Required for Transport) machinery in chloroplasts. Here, we used an affinity purification approach in two distantly related photosynthetic eukaryotes, the green alga Chlamydomonas reinhardtii and the plant Arabidopsis thaliana, to discover proteins that interact with VIPP1. Among several newly identified proteins, we focused on a highly conserved but uncharacterized protein (VIPP1-Associated protein 1, VIA1) that robustly interacts with VIPP1 in both systems. VIA1 is predicted to contain a winged-helix domain, a characteristic feature of ESCRT-II proteins that mediates the interaction with ESCRT-III proteins. The absence of VIA1 causes thylakoid swelling upon exposure to high light in Chlamydomonas and defective thylakoid biogenesis in the newly emerging leaf tissue in Arabidopsis, thereby delaying chloroplast development in this tissue. We propose that VIA1 is part of a previously unrecognized chloroplast ESCRT-like system that plays a critical role in forming, remodeling, and repairing photosynthetic membranes.