Abstract
In this study we investigated the basis for the reduction in the quantum yield of carbon assimilation in maize (Zea mays L. cv. LG11) caused by chilling in high light. After chilling attached maize leaves at 5° C for 6 h at high irradiance (1000 μmol photons·m−2·s−1) chlorophyll fluorescence measurements indicated a serious effect on the efficiency of photochemical conversion by photosystem II (PSII) and measurements of [14C]atrazine binding showed that the plastoquinone binding site was altered in more than half of the PSII reaction centres. Although there were no direct effects of the chilling treatment on coupling-factor activity, ATP-formation capacity was affected because the photoinhibition of PSII led to a reduced capacity to energize the thylakoid membranes. In contrast to chilling at high irradiance, no photoinhibition of PSII accompanied the 20% decrease in the quantum yield of carbon assimilation when attached maize leaves were chilled in low light (50 μmol photons·m−2·s−1). Thus it is clear that photoinhibition of PSII is not the sole cause of the light-dependent, chillinduced decrease in the quantum yield of carbon assimilation. During the recovery of photosynthesis from the chilling treatment it was observed that full [14C]atrazinebinding capacity and membrane-energization capacity recovered significantly more slowly than the quantum yield of carbon assimilation. Thus, not only is photoinhibition of PSII not the sole cause for the decreased quantum yield of carbon assimilation, apparently an appreciable population of photoinhibited PSII centres can be tolerated without any reduction in the quantum yield of carbon assimilation.
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Abbreviations
- PPFD:
-
photosynthetically active photon flux density
- PSII:
-
photosystem II
- Fv/Fm :
-
ratio of variable to maximal fluorescence
- Φ :
-
quantum yield of carbon assimilation
References
Baker, N.R., Horton, P. (1987) Chlorophyll fluorescence quenching during photoinhibition. In: Photoinhibition, pp. 145–168, Kyle, D.J., Arntzen, C.J., Osmond, C.B. eds. Elsevier, Amsterdam
Baker, N.R., East, T.M., Long, S.P. (1983) Chilling damage to photosynthesis in young Zea mays. II. Photochemical function of thylakoids in vivo. J. Exp. Bot. 34, 189–197
Baker, N.R., Long, S.P., Ort, D.R. (1988) Photosynthesis and temperature, with particular reference to effects on quantum yield. In: Plants and temperature, pp. 347–375, Long, S.P., Woodward, F.I., eds. The Company of Biologists Ltd., Cambridge, UK
Baker, N.R., Bradbury, M., Farage, P.K., Ireland, C.R., Long, S.P. (1989) Measurements of the quantum yield of carbon assimilation and chlorophyll fluorescence for assessment of photosynthetic performance of crops in the field. Philos. Trans. R. Soc. London Ser. B 323, 295–308
Boyer, J.S., Knipling, E.B. (1965) Isopiestic technique for measuring leaf water potentials with a thermocouple psychrometer. Proc. Natl. Acad. Sci. USA 54, 1044–1051
Butler, W.L., Kitajima, M. (1975) Fluorescence quenching in photosystem II of chloroplasts. Biochim. Biophys. Acta 376, 116–125
Chatterton, N.J., Carlson, G.E., Hungerford, W.E., Lee, D.R. (1972) Effect of tillering and cool nights on photosynthesis and chloroplast starch in Pangola. Crop Sci. 12, 206–208
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
Drake, B.G., Raschke, K. (1974) Prechilling of Xanthium strumarium L. Reduces net photosynthesis and, independently, stomatal conductance, while sensitizing the stomata to CO2. Plant Physiol. 53, 808–812
Downton, W.J.S., Loveys, B.R., Grant, W.J.R. (1988) Stomatal closure fully accounts for the inhibition of photosynthesis by abscisic acid. New Phytol. 108, 263–266
Farage, P.K. (1988) Chilling and freezing effects on photosynthesis and production in field crops with particular reference to photoinhibition. Ph.D. thesis, University of Essex, Colchester, UK
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
Hangarter, R.P., Grandoni, P., Ort, D.R. (1987) The effects of chloroplast coupling factor reduction on the energetics of activation and on the energetics and efficiency of ATP formation. J. Biol. Chem. 262, 13513–13519
Harbinson, J., Genty, B., Baker, N.R. (1989) The relationship between the quantum efficiencies of PS I and PS II in pea leaves. Plant Physiol. 90, 1029–1034
Hayden, D.B., Hopkins, W.G. (1976) Membrane polypeptides and chlorophyll-protein complexes of maize mesophyll chloroplasts. Can. J. Bot. 54, 1684–1689
Hayden, D.B., Baker, N.R., Percival, M.P., Beckwith, P.B. (1986) Modification of the photosystem II light-harvesting chlorophyll a/b protein complex in maize during chill-induced photoinhibition. Biochim. Biophys. Acta 851, 86–92
Horton, P., Hague, A. (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. VI. Resolution of non-photochemical quenching. Biochim. Biophys. Acta 932, 107–115
Ireland, C.R., Long, S.P., Baker, N.R. (1989) An integrated portable apparatus for simultaneous measurement of photosynthetic CO2 and water vapour exchange, light absorption and chlorophyll fluorescence emission of attached leaves. Plant Cell Environ. 12, 947–958
Ketcham, S.R., Davenport, J.W., Warneke, K., McCarty, R.E. (1984) Role of the γ subunit of chloroplast coupling factor 1 in the light-dependent activation of photophosphorylation and ATPase activity by dithiothreitol. J. Biol. Chem. 259, 7286–7293
Kramer, D.M., Crofts, A.R. (1989) Activation of the chloroplast ATPase measured by the electrochromic change in leaves of intact plants. Biochim. Biophys. Acta 976, 28–41
Krause, G.H., Laasch, H., Weis, E. (1988) Regulation of thermal energy dissipation of absorbed light energy in chloroplasts indicated by energy-dependent fluorescence quenching. Plant Physiol. Biochem. 26, 445–452
Kyle, D.J. (1985) The 32,000 dalton protein of photosystem II. Photochem. Photobiol. 41, 107–116
Kyle, D.J., Ohad, L, Arntzen, C.J. (1984) Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc. Natl. Acad. Sci. USA 81, 4070–4074
Long, S.P., East, T.M., Baker, N.R. (1983) Chilling damage to photosynthesis in young Zea mays. I. Effects of light and temperature variation on photosynthetic CO2 assimilation. J. Exp. Bot. 34, 177–188
Martin, B., Ort, D.R., Boyer, J.S. (1981) Impairment of photosynthesis by chilling temperatures in tomato. Plant Physiol. 68, 329–334
Morita, S., Itoh, S., Nishimura, M. (1982) Correlation between the activity of the membrane-bound ATPase and the decay of the flash-induced 515 nm absorbance change in chloroplasts in intact leaves, assayed by means of rapid isolation of chloroplasts. Biochim. Biophys. Acta 679, 125–130
Percival, M.P., Bradbury, M., Hayden, D.B., Baker, N.R. (1987) Modification of the photochemical apparatus in maize by photoinhibitory stress at low temperature. Progr. Photosynth. Res. 4, 47–50
Powles, S.B., Berry, J.A., Björkman, O. (1983) Interactions between light and chilling temperature on inhibition of photosynthesis in chilling sensitive plants. Plant Cell Environ. 6, 117–123
Sassenrath, G.F., Ort, D.R., Portis, Jr., A.R. (1987) Effect of chilling on the activity of enzymes of the photosynthetic carbon reduction cycle. Progr. Photosynth. Res. 4, 103–106
Terashima, I., Wang, S.-C., Osmond, C.B., Farquhar, G.D. (1988) Characterisation of non-uniform photosynthesis induced by abscisic acid in leaves with different mesophyll anatomies. Plant Cell Physiol. 29, 385–394
Tischer, W., Strotmann, H. (1977) Relationship between inhibitor binding by chloroplasts and inhibition of photosynthetic electron transport. Biochim. Biophys. Acta 460, 113–125
Val, J., Baker, N.R. (1989) Light-dependent chilling effects on phosphorylation of thylakoid proteins and consequences for associated photochemical activities in maize. Physiol. Plant. 77, 420–26
Weis, E., Berry, J.A. (1989) Quantum efficiency of photosystem II in relation to ‘energy-dependent’ quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 894, 198–208
Wise, R.R., Ort, D.R. (1989) Photophosphorylation after chilling in the light. Effects on membrane energization and coupling factor activity. Plant Physiol. 90, 657–664
Witt, H.T. (1979) Energy conservation in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field. Biochim. Biophys. Acta 505, 355–427
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This work was supported in part by grants from the UK Agricultural and Food Research Council (AG 84/5) to N.R.B. and from the U.S. Department of Agriculture (Competitive Research Grant 87-CRCR-1-2381) to D.R.O. G.Y.N. was the recipient of a British Council scholarship and N.R.B. received a fellowship from the Organization for Economic Co-operation and Development (Project on Food Production and Preservation).
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Ortiz-Lopez, A., Nie, G.Y., Ort, D.R. et al. The involvement of the photoinhibition of photosystem II and impaired membrane energization in the reduced quantum yield of carbon assimilation in chilled maize. Planta 181, 78–84 (1990). https://doi.org/10.1007/BF00202327
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DOI: https://doi.org/10.1007/BF00202327