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Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure

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Abstract

To determine the dependence of in vivo photosystem (PS) II function on photon exposure and to assign the relative importance of some photoprotective strategies of PSII against excess light, the maximal photochemical efficiency of PSII (Fv/Fm) and the content of functional PSII complexes (measured by repetitive flash yield of oxygen evolution) were determined in leaves of pea (Pisum satlvum L.) grown in moderate light. The modulation of PSII functionality in vivo was induced by varying either the duration (from 0 to 3 h) of light treatment (fixed at 1200 or 1800 μmol photons · m-2 · s-1) or irradiance (from 0 to 3000 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), nigericin (an uncoupler), or dithiothreitol (an inhibitor of the xanthophyll cycle) through the cut petioles of leaves of 22 to 24-day-old plants. We observed a reciprocity of irradiance and duration of illumination for PSII function, demonstrating that inactivation of functional PSII depends on the total number of photons absorbed, not on the rate of photon absorption. The Fv/Fm ratios from photoinhibitory light-treated leaves, with or without inhibitors, declined pseudo-linearly with photon exposure. The number of functional PSII complexes declined multiphasically with increasing photon exposure, in the following decreasing order of inhibitor effect: lincomycin > nigericin > DTT, indicating the central role of D1 protein turnover. While functional PSII and Fv/Fm ratio showed a linear relationship under high photon exposure conditions, in inhibitor-treated leaves the Fv/Fm ratio failed to reveal the loss of up to 25% of the total functional PSII under low photon exposure. The loss of this 25% of less-stable functional PSII was accompanied by a decrease of excitation-energy trapping capacity at the reaction centre of PSII (revealed by the fluorescence parameter, 1/Fo-1/Fm, where Fo and Fm stand for chlorophyll fluorescence when PSII reaction centres are open and closed, respectively), but not by a loss of excitation energy at the antenna (revealed by the fluorescence parameter, 1/Fm). We conclude that (i) PSII is an intrinsic photon counter under photoinhibitory conditions, (ii) PSII functionality is mainly regulated by D1 protein turnover, and to a lesser extent, by events mediated via the transthylakoid pH gradient, and (iii) peas exhibit PSII heterogeneity in terms of functional stability during photon exposure.

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Abbreviations

D1 protein:

psbA gene product

DTT:

dithiothreitol

Fo:

chlorophyll fluorescence corresponding to open PSII reaction centres

Fv, Fm:

variable and maximum fluorescence after dark incubation, respectively

Fs, Fm′:

steady-state and maximum fluorescence during illumination, respectively

P680:

reactioncentre chlorophyll and primary electron donor of PSII

PS:

photosystem

References

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

    Google Scholar 

  • Anderson, J.M., Osmond, C.B. (1987) Shade-sun responses: compromises between acclimation and photoinhibition. In: Topics in photosynthesis. Photoinhibition, vol. 9, pp. 1–38, Kyle, D.M., Osmond, C.B., Arntzen, C.J., eds. Elsevier, Amsterdam

    Google Scholar 

  • Aro, E.-M., McCaffery, S., Anderson, J.M. (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, J.M. (1994) Recovery from photoinhibition in pea (Pisum sativum L.) acclimated to varying growth irradiances. Plant Physiol. 104, 1033–1041

    Google Scholar 

  • Bell, C.J., Rose, D.A. (1981) Light measurement and the terminology of flow. Plant Cell Environ. 4, 89–96

    Google Scholar 

  • Barber, J. (1995) Molecular basis of the vulnerability of photosystem II to damage by light. Aust. J. Plant Physiol. 22, 201–208

    Google Scholar 

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

    Google Scholar 

  • Bilger, W., Björkman, O., Thayer, S.S. (1989) Light-induced spectral absorbance changes in relation to photosynthesis and the expoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiol. 91, 542–551

    Google Scholar 

  • Björkman, O. (1987) Low-temperature chlorophyll flluorescence in leaves and its relationship to photon yield of photosynthesis in photoinhibition, pp. 123–144, Kyle, D.J., Osmond, C.B., Arntzen, C.J., eds. Elsevier, Amsterdam

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

    Google Scholar 

  • Björkman, O., Boardman, N.K., Anderson, J.M., Thorne, S.W., Goodschild, D.J., Pyliotis, N.A. (1972) Effect of light intensity during growth of Atriplex patula on the capacity of photosynthetic reactions, chloroplast composition and structure. Carnegie Inst. Washington Yearb. 71, 115–135

    Google Scholar 

  • Boekema, E. J., Hankamer, B., Bald, D., Kruip, J. Nield J., Boonstra, A.F., Barber, J., Rogner, 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, W.S. (1994) Photoprotection and photoinhibitory damage. Adv. Mol. Cell Biol. 10, 151–196

    Google Scholar 

  • Chow, W.S., Hope, A.B, Anderson, J.M. (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 

  • Demmig, B., Björkman, O. (1987) Comparison 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, B., Winter, K., Krüger, A., Czygan, F.-C. (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light. Plant Physiol. 84, 218–224

    Google Scholar 

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

    Google Scholar 

  • Eckert, H.-J., Geiken, B., Bernading, J., Napiwotzki, A., Eichler, H.-J., Renger, G. (1991) Two sites of photoinhibition of the electron transfer in oxygen evolving and Tris-treated PSII membrane fragments from spinach. Photosynth. Res. 27, 97–108

    Google Scholar 

  • Franklin, L.A., Lavavasseur, G., Osmond, C.B., Henley, W.J., Ramus, J. (1992) Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 186, 399–408

    Google Scholar 

  • Genty, B., Briantais, J.-M-, Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990, 87–92

    Google Scholar 

  • Gilmore, A.M., Yamamoto, H.Y. (1992) Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching mediated by ATP. Proc. Natl. Acad. Sci. USA 89, 1899–1903

    Google Scholar 

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

    Google Scholar 

  • Hormann, H., Neubauer, C., Schreiber, U. (1994) On the relationship between chlorophyll fluorescence quenching and the quantum yield of electron transport in isolated thylakoids. Photosynth. Res. 40, 93–106

    Google Scholar 

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

    Google Scholar 

  • Krause, G.H., Weiss, E. (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 313–349

    Google Scholar 

  • Mattoo, A.K., Hoffman-Falk, H., Marer, J.B., 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 

  • Mullet, J.E. (1988) Chloroplast development and gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 475–502

    Google Scholar 

  • Ögren, E. (1991) Prediction of photosynthesis in willow leaves under field conditions. Planta 175, 229–236

    Google Scholar 

  • Öquist, G., Chow, W.S. (1992) On the relationship between the quantum yield of photosystem II electron transport, as determined by chlorophyll fluorescence, and the quantum yield of CO2-dependent O2 evolution. Photosynth. Res. 33, 51–62

    Google Scholar 

  • Öquist, G., Chow, W.S., Anderson J.M. (1992) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186, 450–460

    Google Scholar 

  • Osmond, C.B. (1994) What is photoinhibition: some insights from comparisons of shade and sun plants, pp. 1–24, Baker, N.R., Bowyer, J.R., eds. Bios Scientific Publishers, Oxford

  • Porra, R.J., Thompson, W.A., Kriedemann, P.E. (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

    Google Scholar 

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

    Google Scholar 

  • Russell, A.W., Critchley, C., Robinson, S. A., Franklin, L.A., Seaton, G.G.R., Chow, W.S., Anderson, J.M. Osmond, C.B. (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, A.G., 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 

  • Schreiber, U., Hormann, H., Neubauer, C., Klughammer, C. (1995) Assessment of PSII photochemical quantum yield by chlorophyll fluorescence quenching analysis. Aust. J. Plant Physiol. 22, 209–220

    Google Scholar 

  • Seaton, G.G.R., Walker, D. A. (1990) Chlorophyll fluorescence as a measure of photosynthetic carbon assimilation. Proc. R. Soc. B. 242, 29–35

    Google Scholar 

  • Seibert, M. (1995) Reflections on the nature and function of the photosystem II reaction centre. Aust. J. Plant Physiol. 22, 161–166

    Google Scholar 

  • Sonoike, K., Terashima, I. (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194, 287–293

    Google Scholar 

  • Sundby, C., McCaffery, S., Anderson, J.M. (1993) Turnover of the photosystem II D1 protein in higher plants under photoinhibitory and nonphotoinhibitory irradiance. J. Biol. Chem. 268, 25476–25482

    Google Scholar 

  • Trissl, H.-W., Lavergne, J. (1995) Fluorescence induction from photosystem II: analytical equations for the yields of photochemistry and fluorescence derived from analysis of a model including exciton-radical pair equilibrium and restricted energy transfer between photosynthetic units. Aust. J. Plant Physiol. 22, 183–193

    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, R.G., Horton, P. (1993) Theoretical assessment of alternative mechanisms for non-photochemical quenching of PSII fluorescence in barley leaves. Photosynth. Res. 36, 119–139

    Google Scholar 

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Authors and Affiliations

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

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

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

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Park, YI., Chow, W.S. & Anderson, J.M. Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure. Planta 196, 401–411 (1995). https://doi.org/10.1007/BF00203636

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