title: Compartmentalization of the protein repair machinery in photosynthetic membranes.
abstract: A crucial component of protein homeostasis in cells is the repair of damaged proteins. The repair of oxygen-evolving photosystem II (PS II) supercomplexes in plant chloroplasts is a prime example of a very efficient repair process that evolved in response to the high vulnerability of PS II to photooxidative damage, exacerbated by high-light (HL) stress. Significant progress in recent years has unraveled individual components and steps that constitute the PS II repair machinery, which is embedded in the thylakoid membrane system inside chloroplasts. However, an open question is how a certain order of these repair steps is established and how unwanted back-reactions that jeopardize the repair efficiency are avoided. Here, we report that spatial separation of key enzymes involved in PS II repair is realized by subcompartmentalization of the thylakoid membrane, accomplished by the formation of stacked grana membranes. The spatial segregation of kinases, phosphatases, proteases, and ribosomes ensures a certain order of events with minimal mutual interference. The margins of the grana turn out to be the site of protein degradation, well separated from active PS II in grana core and de novo protein synthesis in unstacked stroma lamellae. Furthermore, HL induces a partial conversion of stacked grana core to grana margin, which leads to a controlled access of proteases to PS II. Our study suggests that the origin of grana in evolution ensures high repair efficiency, which is essential for PS II homeostasis.
authors.affiliation: Institute of Biological Chemistry, Washington State University, Pullman, WA 99164-6340;
authors.forename: Sujith
authors.initials: S
authors.lastname: Puthiyaveetil
authors.affiliation: Department of Biological Chemistry, Weizmann Institute of Science, 76100 Rehovot, Israel;
authors.forename: Onie
authors.initials: O
authors.lastname: Tsabari
authors.affiliation: Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370; and.
authors.forename: Troy
authors.initials: T
authors.lastname: Lowry
authors.affiliation: Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370; and.
authors.forename: Steven
authors.initials: S
authors.lastname: Lenhert
authors.affiliation: School of Electrical Engineering and Computer Science, Washington State University, Richland, WA 99354.
authors.forename: Robert R
authors.initials: RR
authors.lastname: Lewis
authors.affiliation: Department of Biological Chemistry, Weizmann Institute of Science, 76100 Rehovot, Israel;
authors.forename: Ziv
authors.initials: Z
authors.lastname: Reich
authors.affiliation: Institute of Biological Chemistry, Washington State University, Pullman, WA 99164-6340; kirchhh@wsu.edu.
authors.forename: Helmut
authors.initials: H
authors.lastname: Kirchhoff
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D019143:Evolution, Molecular; D045332:Photosystem II Protein Complex / Q000235:genetics / Q000378:metabolism*; D059748:Proteolysis; D020524:Thylakoids / Q000235:genetics / Q000378:metabolism*
chemical_list: D045332:Photosystem II Protein Complex
keywords: PS II repair cycle; grana margin; photoinhibition; photosynthesis; thylakoid membrane