Photosynthetica 2005, 43(1):13-27 | DOI: 10.1007/s11099-005-3027-x

Experimental and theoretical study on high temperature induced changes in chlorophyll a fluorescence oscillations in barley leaves upon 2 % CO2

D. Lazár1,*, R. Kaňa1, T. Klinkovský2, J. Nauš1
1 Laboratory of Biophysics, Faculty of Science, Palacký University, Olomouc, Czech Republic
2 TK8-Software, Valašské Meziříčí, Czech Republic

Oscillations in many of photosynthetic quantities with a period of about 1 min can be routinely measured with higher plant leaves after perturbation of the steady state by sudden change in gas phase. Among all hypotheses suggested so far to explain the oscillations, an effect of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) activation status to control the oscillations is highly probable, at least upon high temperature (HT) treatment when in vivo RuBPCO activity controlled by RuBPCO activase (RuBPCO-A) decreases. Therefore, we measured the oscillations in fluorescence signal coming from barley leaves (Hordeum vulgare L. cv. Akcent) after their exposure for various time intervals to different HTs in darkness. We also evaluated steady state fluorescence and CO2 exchange parameters to have an insight to functions of electron transport chain within thylakoid membrane and Calvin cycle before initiation of the oscillations. The changes in period of the oscillations induced by moderate HT (up to 43 °C) best correlated with changes in non-photochemical fluorescence quenching (qN) that in turn correlated with changes in gross photosynthetic rate (PG) and rate of RuBPCO activation (kact). Therefore, we suggest that changes in period of the oscillations caused by moderate HT are mainly controlled by RuBPCO activation status. For more severe HT (45 °C), the oscillations disappeared which was probably caused by an insufficient formation of NADPH by electron transport chain within thylakoid membrane as judged from a decrease in photochemical fluorescence quenching (qP). Suggestions made on the basis of experimental data were verified by theoretical simulations of the oscillations based on a model of Calvin cycle and by means of a control analysis of the model.

Additional key words: Hordeum vulgare; model; NADPH; ribulose-1,5-bisphosphate carboxylase, oxygenase and its activase

Received: April 29, 2004; Accepted: November 1, 2004; Published: March 1, 2005  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Lazár, D., Kaňa, R., Klinkovský, T., & Nauš, J. (2005). Experimental and theoretical study on high temperature induced changes in chlorophyll a fluorescence oscillations in barley leaves upon 2 % CO2. Photosynthetica, 43(1), 13-27. doi: 10.1007/s11099-005-3027-x
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Bernacchi, C.J., Singsaas, E.L., Pimentel, C., Portis, A.R., Jr., Long, S.P.: Improved temperature response functions for models of Rubisco-limited photosynthesis. - Plant Cell Environ. 24: 253-259, 2001. Go to original source...
    2. Bilger, W., Schreiber, U.: Energy-dependent quenching of dark-level chlorophyll fluorescence in intact leaves. - Photosynth. Res. 10: 303-308, 1986. Go to original source...
    3. Bilger, W., Schreiber, U., Lange, O.L.: Chlorophyll fluorescence as an indicator of heat induced limitation of photosynthesis in Arbutus unedo L. - In: Tenhunen, J.D., Catarino, F.M., Lange, O.L., Oechel, W.C. (ed.): Plant Response to Stress. Pp. 391-399. Springer-Verlag, Berlin - Heidelberg - New York - London - Paris - Tokyo 1987. Go to original source...
    4. Bukhov, N.G., Boucher, N., Carpentier, R.: Loss of the precise control of photosynthesis and increased yield of non-radiative dissipation of excitation energy after mild heat treatment of barley leaves. - Physiol. Plant. 104: 563-570, 1998. Go to original source...
    5. Bunce, J.A.: Acclimation of photosynthesis to temperature in eight cool and warm climate herbaceous C3 species: Temperature dependence of parameters of a biochemical photosynthesis model. - Photosynth. Res. 63: 59-67, 2000. Go to original source...
    6. Buschmann, P., Gradmann, D.: Minimal model for oscillations of membrane voltage in plant cells. - J. theor. Biol. 188: 323-332, 1997. Go to original source...
    7. Caemmerer, S. von: Biochemical Models of Leaf Photosynthesis. - CSIRO Publishing, Collingwood 2000. Go to original source...
    8. Caemmerer, S. von, Evans, J.R., Hudson, G.S., Andrews, T.J.: The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. - Planta 195: 88-97, 1994. Go to original source...
    9. Caemmerer, S. von, Farquhar, G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. - Planta 153: 376-387, 1981. Go to original source...
    10. Crafts-Brandner, S.J., Law, R.D.: Effect of heat stress on the inhibition and recovery of the ribulose-1,5-bisphosphate carboxylase/ oxygenase activation state. - Planta 212: 67-74, 2000. Go to original source...
    11. Crafts-Brandner, S.J., Salvucci, M.E.: Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. - Proc. nat. Acad. Sci. USA 97: 13430-13435, 2000. Go to original source...
    12. Crafts-Brandner, S.J., van de Loo, F.J., Salvucci, M.E.: The two forms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. - Plant Physiol. 114: 439-444, 1997. Go to original source...
    13. Dau, H.: Molecular mechanisms and quantitative models of variable photosystem II fluorescence. - Photochem. Photobiol. 60: 1-23, 1994. Go to original source...
    14. Delieu, T.J., Walker, D.A.: Simultaneous measurement of oxygen evolution and chlorophyll fluorescence from leaf pieces. - Plant Physiol. 73: 534-541, 1983. Go to original source...
    15. Farquhar, G.D., Caemmerer, S. von, Berry, J.A.: A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. - Planta 149: 78-90, 1980. Go to original source...
    16. Fell, D.A.: Metabolic control analysis: a survey of its theoretical and experimental development. - Biochem. J. 286: 313-330, 1992. Go to original source...
    17. Feller, U., Crafts-Brandner, S.J., Salvucci, M.E.: Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/ oxygenase (Rubisco) activase-mediated activation of Rubisco. - Plant Physiol. 116: 539-546, 1998. Go to original source...
    18. Ferimazova, N., Küpper, H., Nedbal, L., Trtílek, M.: New insights into photosynthetic oscillations revealed by two-dimensional microscopic measurements of chlorophyll fluorescence kinetics in intact leaves and isolated protoplasts. - Photochem. Photobiol. 76: 501-508, 2002. Go to original source...
    19. Fridlyand, L.E., Backhausen, J.E., Holtgrefe, S., Kitzmann, C., Scheibe, R.: Quantitative evaluation of the rate of 3-phosphoglycerate reduction in chloroplasts. - Plant Cell Physiol. 38: 1177-1186, 1997. Go to original source...
    20. Giersch, C.: Oscillatory response of photosynthesis in leaves to environmental perturbations: A mathematical model. - Arch. Biochem. Biophys. 245: 263-270, 1986. Go to original source...
    21. Giersch, C.: Photosynthetic oscillations: Observations and models. - Comments theor. Biol. 3: 339-364, 1994.
    22. Giersch, C., Sivak, M.N.: A mathematical skeleton model of photosynthetic oscillations. - Proc. roy. Soc. London B 245: 77-83, 1991. Go to original source...
    23. Govindjee: Sixty-three years since Kautsky: Chlorophyll a fluorescence. - Aust. J. Plant Physiol. 22: 131-160, 1995. Go to original source...
    24. Gradmann, D: Models for oscillations in plants. - Aust. J. Plant Physiol. 28: 577-590, 2001. Go to original source...
    25. Hahn, B.D.: A mathematical model of the Calvin cycle: analysis of the steady state. - Ann. Bot. 57: 639-653, 1986. Go to original source...
    26. Hammond, E.T., Andrews, TJ., Mott, K.A., Woodrow, I.E.: Regulation of Rubisco activation in antisense plants of tobacco containing reduced levels of Rubisco activase. - Plant J. 14: 101-110, 1998a. Go to original source...
    27. Hammond, E.T., Andrews, TJ., Woodrow, I.E.: Regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase by carbamylation and 2-carboxyarabinitol 1-phosphate in tobacco: Insights from studies of antisense plants containing reduced amounts of Rubisco activase. - Plant Physiol. 118: 1463-1471, 1998b. Go to original source...
    28. Harley, P.S., Weber, J.A., Gates, D.M.: Interactive effects of light, leaf temperature, CO2 and O2 on photosynthesis in soybean. - Planta 165: 249-263, 1985. Go to original source...
    29. Horton, P., Nicholson, H.: Generation of oscillatory behavior in the Laisk model of photosynthetic carbon assimilation. - Photosynth. Res. 12: 129-143, 1987. Go to original source...
    30. Jacquot, J.-P., Lancelin, J.-M., Meyer, Y.: Thioredoxins: structure and function in plant cells. - New Phytol. 136: 543-570, 2000. Go to original source...
    31. Jensen, R.G.: Activation of Rubisco regulates photosynthesis at high temperature and CO2. - Proc. nat. Acad. Sci. USA 97: 12937-12938, 2000. Go to original source...
    32. Kaern, M., Hunding, A.: The effect of slow allosteric transitions in a coupled biochemical oscillator model. - J. theor. Biol. 198: 269-281, 1999. Go to original source...
    33. Karavaev, V.A., Kukushkin, A.K.: A theoretical model of light and dark processes of photosynthesis: the problem of regulation. - Biophysics 38: 958-975, 1993.
    34. Keiller, D.R., Walker, D.A.: The use of chlorophyll fluorescence to predict CO2 fixation during photosynthetic oscillations. - Proc. roy. Soc. London B 241: 59-64, 1990. Go to original source...
    35. Khuznetsova, S.A., Kukushkin, A.K.: A new theoretical approach to the study of regulatory links in photosynthesis. - Biophysics 44: 448-454, 1999.
    36. Kitajama, M., Butler, W.L.: Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. - Biochim. biophys. Acta 376: 105-115, 1975. Go to original source...
    37. Kobza, J., Edwards, G.E.: Influences of leaf temperature on photosynthetic carbon metabolism in wheat. - Plant Physiol. 83: 69-74, 1987. Go to original source...
    38. Kocks, P., Ross, J.: Kinetic model for (damped) oscillations of transthylakoid pH in plants. - J. phys. Chem. 99: 16490-16497, 1995. Go to original source...
    39. Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: The basics. - Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313-349, 1991. Go to original source...
    40. Kukushkin, A.K.: The influence of cyclic electron transport around photosystem II on the dampening oscillations in photosynthesis. - Biophysics 42: 1224-1234, 1997.
    41. Laisk, A., Eichelmann, H.: Towards understanding oscillations: a mathematical model of the biochemistry of photosynthesis. - Phil. Trans. roy. Soc. London B 323: 369-384, 1989. Go to original source...
    42. Laisk, A., Eichelmann, H., Oja, V., Eatherall, A., Walker, D.A.: A mathematical model of the carbon metabolism in photosynthesis. Difficulties in explaining oscillations by fructose 2,6-bisphosphate regulation. - Proc. roy. Soc. London B 237: 389-415, 1989. Go to original source...
    43. Laisk, A., Siebke, K., Gerst, U., Eichelmann, H., Oja, V., Heber, U.: Oscillations in photosynthesis are initiated and supported by imbalances in the supply of ATP and NADPH to the Calvin cycle. - Planta 185: 554-562, 1991. Go to original source...
    44. Laisk, A., Walker, D.A.: Control of phosphate turnover as a rate-limiting factor and possible cause of oscillations in photosynthesis: a mathematical model. - Proc. roy. Soc. London B 227: 281-302, 1986. Go to original source...
    45. Laisk, A., Walker, D.A.: A mathematical model of electron transport. Thermodynamic necessity for photosystem II regulation: 'light stomata'. - Proc. roy. Soc. London B 237: 417-444, 1989. Go to original source...
    46. Law, R.D., Crafts-Brandner, S.J.: Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. - Plant Physiol. 120: 173-181, 1999. Go to original source...
    47. Lazár, D.: Chlorophyll a fluorescence induction. - Biochim. biophys. Acta 1412: 1-28, 1999. Go to original source...
    48. Leegood, R.C., Walker, D.A.: Autocatalysis and light activation of enzymes in relation to photosynthetic induction in wheat chloroplasts. - Arch. Biochem. Biophys. 200: 575-582, 1980. Go to original source...
    49. Leuning, R.: Temperature dependence of two parameters in a photosynthesis model. - Plant Cell Environ. 25: 1205-1210, 2002. Go to original source...
    50. Lieth, J.H., Pasian, C.C.: A model for net photosynthesis of rose leaves as a function of photosynthetically active radiation, leaf temperature, and leaf age. - J. amer. Soc. hort. Sci. 115: 486-491, 1990. Go to original source...
    51. Malkin, S.: Fast photoacoustic transients from dark-adapted intact leaves: oxygen evolution and uptake pulses during photosynthetic induction - a phenomenology record. - Planta 171: 65-72, 1987. Go to original source...
    52. Mate, C.J., Caemmerer, S. von, Evans, J.R., Hudson, G.S., Andrews, T.J.: The relationship between CO2-assimilation rate, Rubisco carbamylation and Rubisco activase content in activase-deficient transgenic tobacco suggests a simple model of activase action. - Planta 198: 604-613, 1996. Go to original source...
    53. Medlyn, B.E., Dreyer, E., Ellsworth, D., Forstreuter, M., Harley, P.C., Kirschbaum, M.U.F., Le Roux, X., Montpied, P., Strassemeyer, J., Walcroft, A., Wang, K., Loustau, D.: Temperature response of parameters of biochemically based model of photosynthesis. II. A review of experimental data. - Plant Cell Environ. 25: 1167-1179, 2002. Go to original source...
    54. Mendes, P.: GEPASI: a software package for modelling the dynamics, steady states and control of biochemical and other systems. - Comput. appl. Biosci. 9: 563-571, 1993. Go to original source...
    55. Motohashi, K., Kondoh, A., Stumpp, M.T., Hisabori, T.: Comprehensive survey of proteins targeted by chloroplast thioredoxin. - Proc. nat. Acad. Sci. USA 98: 11224-11229, 2001. Go to original source...
    56. Mott, K.A., Woodrow, I.E.: Effects of O2 and CO2 on non-steady-state photosynthesis. Further evidence for ribulose-1,5-bisphosphate carboxylase/oxygenase limitation. - Plant Physiol. 102: 859-866, 1993. Go to original source...
    57. Ogawa, T.: Simple oscillations in photosynthesis of higher plants. - Biochim. biophys. Acta 681: 103-109, 1982. Go to original source...
    58. Pastens, C., Horton, P.: Effect of high temperature on photosynthesis in beans. II. Oxygen evolution and chlorophyll fluorescence. - Plant Physiol. 112: 1245-1251, 1996a. Go to original source...
    59. Pastens, C., Horton, P.: Effect of high temperature on photosynthesis in beans. II. CO2 assimilation and metabolite contents. - Plant Physiol. 112: 1253-1260, 1996b. Go to original source...
    60. Peterson, R.B., Sivak, M.N., Walker, D.A.: Carbon dioxide-induced oscillations in fluorescence and photosynthesis. Role of thylakoid membrane energization in regulation of photosystem II activity. - Plant Physiol. 88: 1125-1130, 1988. Go to original source...
    61. Portis, A.R., Jr.: Regulation of ribulose 1,5-bisphosphate carboxylase/ oxygenase activity. - Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 415-437, 1992. Go to original source...
    62. Quick, W.P., Horton, P.: Studies on the induction of chlorophyll fluorescence in barley protoplasts. I. Factor affecting the observation of the oscillations in the yield of chlorophyll fluorescence and the rate of oxygen evolution. - Proc. roy. Soc. London B 220: 361-370, 1984. Go to original source...
    63. Quick, W.P., Horton, P.: Studies on the induction of chlorophyll fluorescence in barley protoplasts. III. Correlation between changes in the level of glycerate 3-phosphate and the pattern of fluorescence quenching. - Biochim. biophys. Acta 849: 1-6, 1986. Go to original source...
    64. Raghavendra, A.S., Gerst, U., Heber, U.: Oscillations in photosynthetic carbon assimilation and chlorophyll fluorescence are different in Amaranthus caudatus, a C4 plant, and Spinacia oleracea, a C3 plant. - Planta 195: 471-477, 1995. Go to original source...
    65. Reijenga, K.A., Westerhoff, H.V., Kholodenko, B.N., Snoep, J.L.: Control analysis for autonomously oscillating biochemical networks. - Biophys. J. 82: 99-108, 2002. Go to original source...
    66. Roháček, K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. - Photosynthetica 40: 13-29, 2002. Go to original source...
    67. Rokka, A., Zhang, L., Aro, E.-M.: Rubisco activase: an enzyme with a temperature-dependent dual function? - Plant J. 25: 463-471, 2001. Go to original source...
    68. Roussel, M.: Slowly reverting enzyme inactivation: a mechanism for generating long-lived damped oscillations. - J. theor. Biol. 19: 233-244, 1998. Go to original source...
    69. Rovers, W., Giersch, C.: Photosynthetic oscillations and the interdependence of photophosphorylation and electron transport as studied by a mathematical model. - BioSystems 35: 63-73, 1995. Go to original source...
    70. Ruuska, S.A., Andrews, T.J., Badger, M.R., Price, G.D., Caemmerer, S. von: The role of chloroplast electron transport and metabolites in modulating Rubisco activity in tobacco. Insights from transgenic plants with reduced amounts of cytochrome b/f complex or glyceraldehyde 3-phosphate dehydrogenase. 3-Plant Physiol. 122: 491-504, 2002. Go to original source...
    71. Ryde-Pettersson, U.: Identification of possible two-reactant sources of oscillations in the Calvin photosynthesis cycle and ancillary pathways. - Eur. J. Biochem. 198: 613-619, 1991. Go to original source...
    72. Salvucci, M.E., Crafts-Brandner, S.J.: Inhibition of photosynthesis by heat stress: the activation of Rubisco as a limiting factor in photosynthesis. - Physiol. Plant. 120: 179-186, 2004. Go to original source...
    73. Salvucci, M.E., Ogren, W.L.: The mechanism of Rubisco activase: Insights from studies of the properties and structure of the enzyme. - Photosynth. Res. 47: 1-11, 1996. Go to original source...
    74. Salvucci, M.E., Osteryoung, K.W., Crafts-Brandner, S.J., Vierling, E.: Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo. - Plant Physiol. 127: 1053-1064, 2001. Go to original source...
    75. Schürmann, P., Jacquot, J.-P.: Plant thioredoxin systems revisited. - Annu. Rev. Plant Physiol. Plant mol. Biol. 51: 371-400, 2000. Go to original source...
    76. Seaton, G.G.R., Walker, D.A.: Chlorophyll fluorescence as a measure of photosynthetic carbon fixation. - Proc. roy. Soc. London B 242: 29-35, 1990. Go to original source...
    77. Sivak, M.N., Walker, D.A.: Chlorophyll a fluorescence: can it shed light on fundamental questions in photosynthetic carbon dioxide fixation? - Plant Cell Environ. 8: 439-448, 1985. Go to original source...
    78. Sivak, M.N., Walker, D.A.: Photosynthesis in vivo can be limited by phosphate supply. - New Phytol. 102: 499-512, 1986. Go to original source...
    79. Sivak, M.N., Walker, D.A.: Oscillations and other symptoms of limitation of in vivo photosynthesis by inadequate phosphate supply to the chloroplast. - Plant Physiol. Biochem. 25: 635-648, 1987.
    80. Spreitzer, R.J., Salvucci, M.E.: Rubisco: Structure, regulatory interactions, and possibilities for a better enzyme. - Annu. Rev. Plant Biol. 53: 449-475, 2002. Go to original source...
    81. Stitt, M.., Grosse, H., Woo, K.-C.: Interactions between sucrose synthesis and CO2 fixation. II. Alterations of fructose 2,6-bis-phosphate during photosynthetic oscillations. - J. Plant Physiol. 133: 138-143, 1988. Go to original source...
    82. Stitt, M., Quick, W.P., Schurr, U., Schulze, E.-D., Rodermel, S.R., Bogorad, L.: Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with 'antisense' rbcS. II. Flux-control coefficients for photosynthesis in varying light, CO2, and air humidity. - Planta 183: 555-566, 1991. Go to original source...
    83. Stitt, M., Schreiber, U.: Interaction between sucrose synthesis and CO2 fixation. III. Response of biphasic induction kinetics and oscillations to manipulation of the relation between electron transport, Calvin cycle, and sucrose synthesis. - J. Plant Physiol. 133: 263-271, 1988. Go to original source...
    84. Teusink, B., Bakker, B.M., Westerhoff, H.V.: Control of frequency and amplitudes is shared by all enzymes in three models of yeast glycolytic oscillations. - Biochim. biophys. Acta 1275: 204-21, 1996. Go to original source...
    85. Veljović-Jovanović, S., Cerović, Z.G.: Induction of oscillations in chlorophyll fluorescence by re-illumination of intact isolated pea chloroplasts. - Planta 185: 39-400, 1991. Go to original source...
    86. Viil, J.: Carboxylation and oxygenation of ribulose-1,5-bisphosphate (RuBP): a model on the level of the partial reactions. - In: Mathis, P. (ed.): Photosynthesis: from Light to Biosphere. Vol. V. Pp. 215-218. Kluwer Academic Publ., Dordrecht - Boston - London 1995. Go to original source...
    87. Viil, J., Ivanova, H., Pärnik, T.: Estimation of rate constants of the partial reactions of carboxylation of ribulose-1,5-bisphosphate in vivo. - Photosynth. Res. 60: 247-256, 1999. Go to original source...
    88. Visser, D., Heijnen, J.: The mathematics of metabolic control analysis revisited. - Metab. Eng. 4: 114-123, 2002. Go to original source...
    89. Walker, D.A.: Concerning oscillations. - Photosynth. Res. 34: 387-395, 1992. Go to original source...
    90. Walker, D.A., Sivak, M.N.: Can phosphate limit photosynthetic carbon assimilation in vivo? - Physiol. vég. 23: 829-841, 1985. Go to original source...
    91. Walker, D.A., Sivak, M.N.: Photosynthesis and phosphate: a cellular affair? - Trends biochem. Sci. 11: 176-179, 1986. Go to original source...
    92. Walker, D.A., Sivak, M.N., Prinsley, R.T., Cheesbrough, J.K.: Simultaneous measurement of oscillations in oxygen evolution in chlorophyll a fluorescence in leaf pieces. - Plant Physiol. 73: 542-549, 1983. Go to original source...
    93. Weis, E.: Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. - Planta 151: 33-39, 1981a. Go to original source...
    94. Weis, E.: The temperature sensitivity of dark-inactivation and light-activation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. - FEBS Lett. 129: 197-200, 1981b. Go to original source...
    95. Weis, E., Berry, J.A.: Plants and high temperature stress. - In: Long, S.P., Woodward, F.I. (ed.): Plants and Temperature. Pp. 329-346. Company of Biologists, Cambridge 1988.
    96. Woodrow, I.E., Mott, K.A.: Rate limitation of non-steady-state photosynthesis by ribulose-1,5-bisphosphate carboxylase in spinach. - Aust. J. Plant Physiol. 16: 487-500, 1989. Go to original source...
    97. Woodrow, I.E., Mott, K.A.: Biphasic activation of ribulose bisphosphate carboxylase in spinach leaves as determined from nonsteady-state CO2 exchange. - Plant Physiol. 99: 298-303, 1992. Go to original source...
    98. Woodrow, I.E., Mott, K.A.: Modelling C3 photosynthesis: A sensitivity analysis of the photosynthetic carbon-reduction cycle. - Planta 191: 421-432, 1993. Go to original source...
    99. Yokota, A., Wadano, A., Murayama, H.: Modelling of continuously and directly analyzed biphasic reaction courses of ribulose-1,5-bisphosphate carboxylase/oxygenase. - J. Biochem. (Tokyo) 119: 487-499, 1996. Go to original source...
    100. Zadoks, J.C., Chang, T.T., Konzak, C.F.: A decimal code for the growth stages of cereals. - Weed Res. 14: 415-421, 1974. Go to original source...
    101. Zhang, N., Kallis, R.P., Ewy, R.G., Portis, A.R.: Light modulation of Rubisco in Arabidopsis requires a capacity of redox regulation of the larger Rubisco activase isoform. - Proc. nat. Acad. Sci. USA 99: 3330-3334, 2002. Go to original source...
    102. Zhang, N., Portis, A.R.: Mechanism of light regulation of Rubisco: A specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. - Proc. nat. Acad. Sci. USA 96: 9438-9443, 1999. Go to original source...

    Return to the content