Cost and benefit of the repair of photodamaged photosystem II in spinach leaves: roles of acclimation to growth light
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When visible light is excess, the photosynthetic machinery is photoinhibited. The extent of net photoinhibition of photosystem II (PSII) is determined by a balance between the rate of photodamage to D1 and some other PSII proteins and the rate of the turnover cycle of these proteins. It is widely believed that the protein turnover requires much energy cost. The aims of this study are to (1) evaluate the energy cost of PSII repair, (2) measure the benefit in terms of photosynthetic gain realized by the repairing of the photodamaged PSII, and (3) know whether acclimation of photosynthesis to growth light affects the rates of the photodamage and repair. We grew spinach in high-light (HL) and low-light (LL) and measured the rates of D1 photodamage and repair in these leaves. We determined the rate constants of photodamage (k pi) and repair (k rec) by the PAM fluorometry in the presence or in the absence of lincomycin, an inhibitor of 70S protein synthesis. HL leaves showed smaller k pi and greater k rec than LL leaves. The energy cost of the repairing of the photodamaged D1 protein was <0.5 % of ATP produced by photophosphorylation at PPFDs ranging from 400 to 1600 μmol m−2 s−1 and was greater in HL leaves than in LL leaves. The benefits brought about by the repair were more than from 35 to 270 times the cost at PPFDs ranging from 400 to 1600 μmol m−2 s−1. The benefits of HL leaves were greater than those of LL leaves because of the higher photosynthesis rates in HL leaves. Running a simple simulation of daily photosynthesis using the parameters obtained in this study, we discuss why the plants need to pay the cost of D1 protein turnover to repair the photodamaged PSII.
KeywordsChlorophyll fluorescence D1 protein turnover Excess energy Light acclimation Photoinhibition Photosystem II
We thank Dr. Riichi Oguchi and Mr. Masaru Kono for kind support and advice. We also thank Prof. Chikahiro Miyake (Kobe University) for a useful discussion concerning the ATP production rate. We are grateful to two anonymous reviewers and the handling editor, Dr. Shizue Matsubara, for their very constructive comments. The last author (IT.) once studies as a postdoctoral fellow under the supervision of Prof. Barry Osmond, and deeply thanks for his continuous encouragement.
- Kato MC, Hikosaka K, Hirotsu N, Makino A, Hirose T (2003) The excess light energy that is neither utilized in photosynthesis nor dissipated by photoprotective mechanisms determines the rate of photoinactivation in photosystem II. Plant Cell Physiol 44:318–325. doi: 10.1093/pcp/pcg045 PubMedCrossRefGoogle Scholar
- Oguchi R, Douwstra P, Fujita T, Chow WS, Terashima I (2011a) Intra-leaf gradients of photoinhibition induced by different color lights: implications for the dual mechanisms of photoinhibition and for the application of conventional chlorophyll fluorometers. New Phytol 191:146–159. doi: 10.1111/j.1469-8137.2011.03669.x PubMedCrossRefGoogle Scholar
- Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44:8494–8499. doi: 10.1021/bi047518q PubMedCrossRefGoogle Scholar
- Osmond CB (1994) What is photoinhibition? Some insights from comparison of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 1–24Google Scholar
- Raven JA, Samuelsson G (1986) Repair of photoinhibitory damage in Anacystis nidulans 625 (Synechococcus 6301): relation to catalytic capacity for, and energy supply to, protein synthesis, and implications for μmax and the efficiency of light-limited growth. New Phytol 103:625–643. doi: 10.1111/j.1469-8137.1986.tb00838.x CrossRefGoogle Scholar
- Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 49–70Google Scholar
- Terashima I, Wong SC, Osmond CB, Farquhar GD (1988) Characterisation of non-uniform photosynthesis induced by abscisic acid in leaves having different mesophyll anatomies. Plant Cell Physiol 29:385–394Google Scholar
- Vass I, Styring S, Hundal T, Koivuniemi A, Aro E, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89:1408–1412. doi: 10.1073/pnas.89.4.1408 PubMedCrossRefGoogle Scholar
- von Caemmerer S (2000) Modelling C3 photosynthesis. In: von Caemmerer S (ed) Techniques in plant science No 2. Biochemical models of leaf photosynthesis. CSIRO Publishing, Collingwood, pp 29–71Google Scholar