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Photoinactivation of functional photosystem II and D1-protein synthesis in vivo are independent of the modulation of the photosynthetic apparatus by growth irradiance

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Abstract

To investigate whether the in-vivo photoinhibition of photosystem II (PSII) function by excess light is an intrinsic property of PSII, the maximal photochemical efficiency of PSII (Fv/Fm) and the content of functional PSII (measured by repetitive flash yield of oxygen evolution) were determined in leaves of pea (Pisum sativum L.), grown in 50 (low light), 250 (medium light), and 650 (high light) μmol photons·m−2·s−1. The modulation of PSII functionality in vivo was induced in 1.1% CO2 by varying either (i) the duration (0–2 h) of light treatment (fixed at 1800 μmol photons· m−2·s−1) or (ii) irradiance (0–3200 μmol photons·m−2·s−1) at a fixed duration (1 h), after infiltration of leaves with water (control), lincomycin (an inhibitor of chloroplast-encoded protein synthesis), or a combination of lincomycin with nigericin (an uncoupler), through the cut petioles of leaves of 22-to 24-d-old plants. The reciprocity law of irradiance and duration of illumination for PSII function in vivo (Park et al. 1995, Planta 196: 401–411) holds in all differently light-grown peas, demonstrating that inactivation of functional PSII depends on photon exposure (mol photons·m−2), not on the rate of photon absorption. In vivo, PSII acts as an intrinsic “photon counter” and at higher photon exposures is inactivated following absorption of about 3 × 107 photons. There is a functional heterogeneity of PSII in vivo with 25% less-stable PSIIs that are inactivated at low photon exposure, compared to 75% more-stable PSIIs regardless of modulation of the photosynthetic apparatus. We suggest that the less-stable PSIIs represent monomers located in the nonappressed granal margins, while the more-stable PSIIs are dimers located in the appressed grana membrane cores. The capacity for D1-protein synthesis was the same in all the light-acclimated peas and saturated at low light, indicating that D1-protein repair is also an intrinsic property of PSII. This accounts for the low intensity required for recovery of photoinhibition in sun and shade plants which is independent of light-harvesting antennae size or PSII/PSI stoichiometries.

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Abbreviations

D1-protein:

psbA gene product

D2 protein:

psbD gene product

Fo:

chlorophyll fluorescence corresponding to open PSII reaction centres

Fv, Fm:

variable and maximum fluorescence after dark incubation, respectively

PS:

photosystem

QB :

secondary quinone electron acceptor

References

  • Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37: 93–136

    Google Scholar 

  • Anderson JM, Aro E-M (1994) Grana stacking and photoprotection of photosystem II in thylakoid membranes of higher plants under sustained high irradiance: an hypothesis. Photosynth Res 41: 315–326

    Google Scholar 

  • Anderson JM, Melis A (1983) Localization of different photosystems in separate regions of chloroplast membranes. Proc Natl Acad Sci USA 80: 745–749

    Google Scholar 

  • Anderson JM, Osmond CB (1987) Shade-sun responses: compromises between acclimation and photoinhibition. In: Kyle DM, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier. Amsterdam, pp 1–38

    Google Scholar 

  • Aro E-M, McCaffery S, Anderson JM (1993) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 103: 835–843

    Google Scholar 

  • Aro E-M, McCaffery S, Anderson JM (1994) Recovery form photoinhibition in peas (Pisium sativum L.) acclimated to varying growth irradiances. Plant Physiol 104: 1033–1041

    Google Scholar 

  • Barbato RJ, Friso G, Rigoni F, Vecchia FD, Giacometti GM (1992) Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids. J Cell Biol 119: 323–335

    Google Scholar 

  • Bell CJ, Rose DA (1981) Light measurement and the terminology of flow. Plant Cell Environ 4: 89–96

    Google Scholar 

  • Bilger W, Björkman O (1994) Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and non-photochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.). Planta 193: 238–246

    Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence at 77 K among vascular plants of diverse origins. Planta 170: 489–504

    Google Scholar 

  • Björkman O, Boardman NK, Anderson JM, Thorne SW, Goodchild DJ, Pyliotis NA (1972) Effect of light intensity during growth of Atriplex patula on the capacity of photosynthetic reactions, chloroplast composition and structure. Carnegie Inst Washington Yearbk 71: 115–135

    Google Scholar 

  • Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J, Rönger M (1995) Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92: 175–179

    Google Scholar 

  • Chow WS (1994) Photoprotection and photoinhibitory damage. Adv Mol Cell Biol 10: 151–196

    Google Scholar 

  • Chow WS, Hope AB (1987) The stoichiometries of supramolecular complexes in the thylakoid membranes from spinach chloroplasts. Aust J Plant Physiol 14: 21–28

    Google Scholar 

  • Chow WS, Hope AB, Anderson JM (1989) Oxygen per flash from leaf discs quantifies photosystem II. Biochim Biophys Acta 937: 105–108

    Google Scholar 

  • Chow WS, Hope AB, Anderson JM (1991) Further studies on quantifying photosystem II in vivo by flash-induced oxygen yield from leaf discs. Aust J Plant Physiol 18: 397–410

    Google Scholar 

  • Danon A, Mayfield SP (1991) Light-regulated translational activators: identification of chloroplast gene specific mRNA bind- ing proteins. EMBO J 10: 3993–4001

    Google Scholar 

  • Danon A, Mayfield SP (1994) Light-regulated translation of messenger RNAs through redox potential. Science 266: 1717–1719

    CAS  PubMed  Google Scholar 

  • Demmig B, Björkman O (1987) Comparision of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants. Planta 171: 171–184

    CAS  Google Scholar 

  • Demmig-Adams B, Adams III WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626

    Article  CAS  Google Scholar 

  • Demmig-Adams, Adams III WW, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Aust J Plant Physiol 22: 249–260

    Google Scholar 

  • Eaglesham ARJ, Ellis RJ (1974) Protein synthesis in chloroplasts. II. Light-driven synthesis of membrane proteins by isolated pea chloroplasts. Biochim Biophys Acta 335: 396–407

    Google Scholar 

  • Greenberg BM, Gaba V, Mattoo AK, Edelman M (1987) Identification of primary in vivo degradation product of the rapidly-turning-over 32 kD protein of photosystem II. EMBO J 6: 2865–2869

    Google Scholar 

  • Greer DH, Berry JA, Björkman O (1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature and requirement for chloroplast-protein synthesis during recovery. Planta 168: 253–260

    Google Scholar 

  • Havaux M, Strasser RJ, Greppin H (1991) A theoretical and experimental analysis of the qP and qN coefficients of chlorophyll fluoresc-nece quenching and their relation to photochemical and nonphotochemical events. Photosynth Res 27: 41–55

    Google Scholar 

  • Jones LW, Kok B (1966) Photoinhibition of chloroplast reactions. Plant Physiol 41: 1037–1043

    Google Scholar 

  • Keren N, Gong H, Ohad I (1995) Oscillations of reaction center II-D1 protein degradation in vivo induced by repetitive light flashes. J Biol Chem 270: 806–814

    Google Scholar 

  • Krause GH, Behrend U (1986) δpH-dependent chlorophyll fluorescence quenching indicating a mechanism of protection against photoinhibition of chloroplasts. FEBS Lett 200: 298–302

    Google Scholar 

  • Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane proteins damage and repair. Selective loss of a quinone protein function in chloroplast membranes. Proc Natl Acad Sci USA 81: 4070–4074

    Google Scholar 

  • Mattoo AK, Hoffman-Falk H, Marer JB, Edelman M (1984) Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci USA 81: 1380–1384

    Google Scholar 

  • Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87–106

    Google Scholar 

  • Melis A, Anderson JM (1983) Structural and functional organization of the photosystems in spinach chloroplasts: antennae size, relative electron transport capacity and chlorophyll composition. Biochim Biophys Acta 724: 473–484

    Google Scholar 

  • Nanba O, Satoh K (1987) Isolation of photosystem II reacton center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112

    Google Scholar 

  • Ohad I, Keren N, Zer H, Gong H, Mor TS, Gal A, Tal S, Domovich Y (1994) Light-induced degradation of the photosystem II reaction centre D1 protein in vivo: an integrative apporach. In: Baker NR, Bowyer JR (eds) Photoinhibition of Photosynthesis. Bios Scientific Pub. Oxford, pp 161–177

    Google Scholar 

  • Ögren O (1991) Prediction of photoinhibition of photosynthesis from measurements of fluorescence quenching components. Planta 184: 538–544

    Google Scholar 

  • Öquist G, Chow WS, Anderson JM (1992) Mechanistic differences in photoinhibition of sun and shade plants. Planta 180: 422–431

    Google Scholar 

  • Ort D, Baker NR (1988) Consideration of photosynthetic efficiency at low light as a major determinant of crop photosynthetic performance. Plant Physiol Biochem 26: 555–565

    Google Scholar 

  • Park Y-I, Chow WS, Anderson JM (1995) Light inactivation of functional photosystem II in leaves of peas grown in medium light depends on photon exposure. Planta 196: 401–411

    Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b with four different solvents: verification of the concentration of chlorophyll by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384–394

    CAS  Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 15–44

    Article  CAS  Google Scholar 

  • Prasil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. Top Photosynth 11: 293–348

    Google Scholar 

  • Rintamäki E, Kettunen R, Tyystjärvi E, Aro E-M (1995) Light-dependent phosphorylation of D1 reaction center protein of photosystem II: hypothesis for the functional role in vivo. Physiol Plant 93: 191–195

    Google Scholar 

  • Russell AW, Critchley C, Robinson SA, Franklin LA, Seaton GGR, Chow WS, Anderson JM, Osmond CB (1995) Photosystem II regulation and dynamics of the chloroplast D1 protein in Arabidopsis leaves during photosynthesis and photoinhibition. Plant Physiol 107: 943–952

    Google Scholar 

  • Santini C, Tidu V, Tognon G, Magaldi AG, Bassi R (1994) Three-dimensional structure of the higher-plant photosystem II reaction centre and evidence for its dimeric organization in vivo. Eur J Biochem 221: 307–315

    Google Scholar 

  • Taniguchi M, Kuroda H, Satoh K (1993) ATP-dependent protein synthesis in isolated pea chloroplasts. Evidence for accumulation of a translation intermediate of D1 protein. FEBS Lett 317: 57–61

    Google Scholar 

  • Tyystjärvi E, Ali-Yrkkö K, Kettunen R, Aro E-M (1992) Slow degradation of the D1 protein is related to the susceptibility of low-light-grown pumpkin plants to photoinhibition. Plant Physiol 100: 1310–1317

    Google Scholar 

  • Walters RG, Horton P (1993) Theoretical assessment of alternative mechanisms for non-photochemical quenching of PSII fluorescence in barley leaves. Photosynth Res 36: 19–139

    Google Scholar 

  • Wollenberger L, Weibull C, Albertsson P-Å (1995) Further characterization of the chloroplast grana margins: the non-detergent preparation of granal photosystem I cannot reduce ferredoxin in the absence of NADP+ reduction. Biochim Biophys Acta 1230: 10–22

    Google Scholar 

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Authors and Affiliations

  1. CSIRO, Division of Plant Industry and Cooperative Research Centre for Plant Science, GPO Box 1600, 2601, Canberra, ACT, Australia

    Youn-Il Park, Jan M. Anderson & Wah Soon Chow

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  1. Youn-Il Park
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  2. Jan M. Anderson
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  3. Wah Soon Chow
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Financial support for this research by the Department of Employment, Education and Training/Australian Research Council International Research Fellowships Program (Korea) is gratefully acknowledged.

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Park, YI., Anderson, J.M. & Chow, W.S. Photoinactivation of functional photosystem II and D1-protein synthesis in vivo are independent of the modulation of the photosynthetic apparatus by growth irradiance. Planta 198, 300–309 (1996). https://doi.org/10.1007/BF00206257

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  • DOI: https://doi.org/10.1007/BF00206257

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