Identification and Roles of Photosystem II Assembly, Stability, and Repair Factors in Arabidopsis

Abstract

Photosystem II (PSII) is a multi-component pigment-protein complex that is responsible for water splitting, oxygen evolution, and plastoquinone reduction. Components of PSII can be classified into core proteins, low-molecular-mass proteins, extrinsic oxygen-evolving complex (OEC) proteins, and light-harvesting complex II proteins. In addition to these PSII subunits, more than 60 auxiliary proteins, enzymes, or components of thylakoid protein trafficking/targeting systems have been discovered to be directly or indirectly involved in de novo assembly and/or the repair and reassembly cycle of PSII. For example, components of thylakoid-protein-targeting complexes and the chloroplast-vesicle-transport system were found to deliver PSII subunits to thylakoid membranes. Various auxiliary proteins, such as PsbP-like (Psb stands for PSII) and light-harvesting complex-like proteins, atypical short-chain dehydrogenase/reductase family proteins, and tetratricopeptide repeat proteins, were discovered to assist the de novo assembly and stability of PSII and the repair and reassembly cycle of PSII. Furthermore, a series of enzymes were discovered to catalyze important enzymatic steps, such as C-terminal processing of the D1 protein, thiol/disulfide-modulation, peptidylprolyl isomerization, phosphorylation and dephosphorylation of PSII core and antenna proteins, and degradation of photodamaged PSII proteins. This review focuses on the current knowledge of the identities and molecular functions of different types of proteins that influence the assembly, stability, and repair of PSII in the higher plant Arabidopsis thaliana.

Keywords: Arabidopsis thaliana; Photosystem II assembly; Photosystem II repair; Photosystem II stability; identification and roles.

Figure 1

De novo assembly of PSII in Arabidopsis. The major steps include: (1) assembly of precursor D1-PsbI (pD1-PsbI) and D2-cytochrome b₅₅₉ (D2-Cyt b₅₅₉) precomplexes, (2) assembly of the minimal reaction-center complex (RC), which lacks CP47 and CP43, (3) assembly of the reaction-center complex (RC47a) that contains CP47 but lacks CP43, (4) incorporation of LMM subunits, such as PsbH, PsbM, PsbT, and PsbR, to form RC47b, (5) incorporation of CP43, along with LMM subunit PsbK, to form the OEC-less PSII core monomer, (6) assembly of the oxygen-evolving complex (OEC) and additional LMM subunits, such as PsbW and PsbZ, to form the PSII core monomer, and (7) dimerization and formation of the PSII-light-harvesting complex II (LHCII) supercomplex. Proteins that are involved in these steps are listed. Although RBD1 promotes PSII assembly and/or PSII stability, it is not depicted in this figure because it is not clear which step(s) of de novo PSII assembly this protein is involved in. Letters (B, C, D1, D2, E, F, H, I, K, M, O, P, Q, R, T, W, Z) in rectangles represent PSII proteins PsbB (i.e., CP47), PsbC (i.e., CP43), D1, D2, PsbE, PsbF, PsbH, PsbI, PsbK, PsbM, PsbO, PsbP, PsbQ, PsbR, PsbT, PsbW, and PsbZ, respectively. Abbreviations: D2-Cyt b₅₅₉, D2-cytochrome b₅₅₉ precomplex; LHCII, light-harvesting complex II; OEC, oxygen-evolving complex; pD1, precursor D1; pD1-PsbI, precursor D1-PsbI precomplex; PSII, Photosystem II; RC, PSII minimal reaction-center complex; RC47a, PSII reaction-center complex with CP47, without PsbM, PsbH, PsbT, or PsbR; RC47b, PSII reaction-center complex with CP47, PsbM, PsbH, PsbT, and PsbR. For simplicity, only one name is shown for proteins with multiple names (e.g., “THF1” for THF1/PSB29).

Figure 2

Damage, repair, and reassembly of PSII in Arabidopsis. The major steps include: (1) high-light-induced phosphorylation, damage, and disassembly of the PSII-LHCII supercomplex and the PSII core dimer in grana stacks, (2) lateral migration of the PSII core monomer to stroma-exposed thylakoid membranes, (3–5) dephosphorylation, partial disassembly of the PSII core monomer, and degradation of photodamaged D1, (6) synthesis and reassembly of new D1, (7) re-incorporation of CP43, (8) reattachment of OEC, (9) migration of the PSII core monomer back to grana stacks, and (10) dimerization into PSII core dimers and reformation of PSII-LHCII supercomplexes. Proteins that are involved in these steps are listed. Although PPL1 might be involved in PSII repair, it is not depicted in this figure because it is not clear which step(s) of PSII repair this protein is involved in. Letters (B, C, D1, D2, E, F, H, I, K, M, O, P, Q, R, T, W, Z) in rectangles represent PSII proteins PsbB (i.e., CP47), PsbC (i.e., CP43), D1, D2, PsbE, PsbF, PsbH, PsbI, PsbK, PsbM, PsbO, PsbP, PsbQ, PsbR, PsbT, PsbW, and PsbZ, respectively. The letter P in a circle represents phosphate. The yellow lightning bolt represents light. Abbreviations: LHCII, light-harvesting complex II; OEC, oxygen-evolving complex; pD1, precursor D1; PSII, Photosystem II. For simplicity, only one name is shown for proteins with multiple names (e.g., “THF1” for THF1/PSB29).