Compartmentalization of the protein repair machinery in photosynthetic membranes

Sujith Puthiyaveetil; Onie Tsabari; Troy Lowry; Steven Lenhert; Robert R Lewis; Ziv Reich; Helmut Kirchhoff

doi:10.1073/pnas.1413739111

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Compartmentalization of the protein repair machinery in photosynthetic membranes

Journal article

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Compartmentalization of the protein repair machinery in photosynthetic membranes

Sujith Puthiyaveetil, Onie Tsabari, Troy Lowry, Steven Lenhert, Robert R Lewis, Ziv Reich and Helmut Kirchhoff

Proceedings of the National Academy of Sciences - PNAS, Vol.111(44), pp.15839-15844

11/04/2014

DOI: https://doi.org/10.1073/pnas.1413739111

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https://hdl.handle.net/2376/108709

PMCID: PMC4226077

PMID: 25331882

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Abstract

Arabidopsis - genetics

Proteolysis

Photosystem II Protein Complex - genetics

Thylakoids - genetics

Thylakoids - metabolism

Arabidopsis - metabolism

Evolution, Molecular

Photosystem II Protein Complex - metabolism

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.

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Title: Compartmentalization of the protein repair machinery in photosynthetic membranes
Creators: Sujith Puthiyaveetil - Institute of Biological Chemistry, Washington State University, Pullman, WA 99164-6340
Onie Tsabari - Department of Biological Chemistry, Weizmann Institute of Science, 76100 Rehovot, Israel
Troy Lowry - Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370; and
Steven Lenhert - Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370; and
Robert R Lewis - School of Electrical Engineering and Computer Science, Washington State University, Richland, WA 99354
Ziv Reich - Department of Biological Chemistry, Weizmann Institute of Science, 76100 Rehovot, Israel
Helmut Kirchhoff - Institute of Biological Chemistry, Washington State University, Pullman, WA 99164-6340; kirchhh@wsu.edu
Publication Details: Proceedings of the National Academy of Sciences - PNAS, Vol.111(44), pp.15839-15844
Academic Unit: Biological Chemistry, Institute of; Engineering and Applied Sciences (TRIC), School of
Publisher: United States
Identifiers: 99900547200501842
Language: English
Resource Type: Journal article