Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen‐evolving complex show altered PSII super‐complex organization and short‐term adaptive mechanisms

Abstract

These authors contributed equally to this work. SUMMARYThe oxygen-evolving complex of eukaryotic photosystem II (PSII) consists of four extrinsic subunits, PsbO (33 kDa), PsbP (23 kDa), PsbQ (17 kDa) and PsbR (10 kDa), encoded by seven nuclear genes, PsbO1 (At5g66570), PsbO2 (At3g50820), PsbP1 (At1g06680), PsbP2 (At2g30790), PsbQ1 (At4g21280), PsbQ2 (At4g05180) and PsbR (At1g79040). Using Arabidopsis insertion mutant lines, we show that PsbP1, but not PsbP2, is essential for photoautotrophic growth, whereas plants lacking both forms of PsbQ and/or PsbR show normal growth rates. Complete elimination of PsbQ has a minor effect on PSII function, but plants lacking PsbR or both PsbR and PsbQ are characterized by more pronounced defects in PSII activity. Gene expression and immunoblot analyses indicate that accumulation of each of these proteins is highly dependent on the presence of the others, and is controlled at the post-transcriptional level, whereas PsbO stability appears to be less sensitive to depletion of other subunits of the oxygen-evolving complex. In addition, comparison of levels of the PSII super-complex in wild-type and mutant leaves reveals the importance of the individual subunits of the oxygen-evolving complex for the supramolecular organization of PSII and their influence on the rate of state transitions.

PHOTOSYSTEM II SUBUNIT R Is Required for Efficient Binding of LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 to Photosystem II-Light-Harvesting Supercomplexes in Chlamydomonas reinhardtii

“…ami-RNA-psbr-2. Likewise, the data revealed that subunits PSBP and PSBQ were both diminished in amounts in conjunction with PSBR, in agreement with data obtained for Arabidopsis PSBR-deficient plants (Suorsa et al, 2006;Liu et al, 2009;Allahverdiyeva et al, 2013). On the other hand, other PSII core subunits or the minor core PSII light-harvesting proteins, LHCB4 and LHCB5, were not significantly altered in their protein ratios in both ami-RNA-psbr strains.…”

“…On the other hand, the major light-harvesting proteins LHCBM1 and LHCBM3 were slightly diminished in the PSBR knockdown strains, suggesting that PSII-LHCII complex formation is impaired by PSBR depletion. In line with this, it was reported that in PSBR-deficient Arabidopsis plants, the formation of PSII-LHCII supercomplexes was marginally affected (Allahverdiyeva et al, 2013). Interestingly, deletion of LHCBM1 resulted in a significant decrease of NPQ (Elrad et al, 2002) in C. reinhardtii.…”

“…Mass spectrometric analyses of isolated C 2 S 2 M 2 PSII supercomplexes revealed the presence of extrinsic subunits PSBP, PSBQ, and PSBR, while PSBS was not identified, suggesting that PSBS does not influence the association of the PSII core with the outer light-harvesting complex system (Pagliano et al, 2014). In line with the proteomic findings, recent data suggest that subunits PSBP, PSBQ, and PSBR contribute to the stability of PSII-LHCII supercomplexes in vascular plants (Caffarri et al, 2009;Ifuku et al, 2011;Allahverdiyeva et al, 2013). A recent quantitative proteomic study performed with C. reinhardtii identified PSBR as the only PSII subunit to be induced upon the shift from photoheterotrophic to photoautotrophic growth conditions similar to LHCSR3 (Höhner et al, 2013).…”

“…S2C), thus indicating that differences in the amounts of LHCSR3 cannot explain the decrease in NPQ. As already described for a PSBR-deficient mutant in Arabidopsis (Allahverdiyeva et al, 2007(Allahverdiyeva et al, , 2013, the depletion of PSBR Figure 10. PSBR sequence alignment.…”

“…For stable association with the PSII core complex, PSBR needs the presence of PSBJ (Suorsa et al, 2006). Functionally, the depletion of PSBR protein expression decreased rates of oxygen evolution (Allahverdiyeva et al, 2007(Allahverdiyeva et al, , 2013 and quinone reoxidation (Allahverdiyeva et al, 2007). PSBR phosphorylation is known for Arabidopsis (Arabidopsis thaliana; Reiland et al, 2009Reiland et al, , 2011Nakagami et al, 2010) and in the green alga C. reinhardtii (Turkina et al, 2006), although phosphorylation sites are not conserved between the alga and the vascular plant.…”