Abstract
The possibility of a role for phosphate metabolism in the photosynthetic regulation that occurs during frost hardening was investigated in winter rye (Secale cereale L. cv. Musketeer). Leaves of frost-hardened and non-hardened winter rye were studied during photosynthetic induction, and at steady state after being allowed to take up 20 mM orthophosphate through the transpiration stream for 3 h. At the growth irradiance (350 μmol·m-2·s-1) frost-hardening increased the stationary rate of CO2-dependent O2 evolution by 57% and 25% when measured at 5 and 20° C, respectively. Frosthardening also reduced the lag phase to stationary photosynthesis by 40% at 5° C and decreased the susceptibility of leaves to oscillations during induction and after interruption of the actinic beam during steady-state photosynthesis. These responses are all indicative of increased phosphate availability in frost-hardened leaves. As reported previously by Öquist and Huner (1993, Planta 189, 150–156), frost-hardening also decreased the reduction state of QA, the primary, stable quinone acceptor of PSII, and decreased the sensitivity of winter rye to photoinhibition of photosynthesis. Non-hardened rye leaves fed orthophosphate also showed an increased photosynthetic capacity (25% at 20° C and light saturation), lower reduction state of QA, a reduced sensitivity to photoinhibition and lower susceptibility to oscillations resulting from a brief interruption of the actinic light. Thus, the data indicate that phosphate metabolism plays a key role in photosynthetic acclimation of winter rye to low temperatures.
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Abbreviations
- Fo and F′o :
-
minimal fluorescence when all PSII reaction centres are open in dark-and light-acclimated leaves, respectively
- Fm and F′m :
-
maximal fluorescence when all PSII reaction centres are closed in dark-and light-acclimated leaves, respectively
- Fv :
-
variable fluoresence (Fm -Fo) in dark-acclimated leaves
- F′v :
-
variable fluorescence (F′m-F′o) in light-acclimated leaves
- PCR:
-
photosynthetic carbon reduction
- PPFD:
-
photosynthetic photon flux density
- QA :
-
the primary, stable quinone acceptor of PSII
- qP :
-
photochemical quenching of fluorescence
- qN :
-
non-photochemical quenching of fluorescence
References
Boese, S.R., Huner, N.P.A. (1990) Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis. Plant Physiol. 94, 1830–1836
Cairns, A.J., Pollock, C.J. (1988) Fructan biosynthesis in excised leaves of Lolium temulentum L.I. Chromatographic characterization of oligofructans and their labelling patterns following 14CO2 feeding. New Phytol. 109, 399–405
Chatterton, N.J., Harrison, P.A., Bennett, J.H., Asay, K.H. (1989) Carbohydrate partitioning in 185 accessions of Gramineae grown under warm and cool temperatures. J. Plant Physiol. 134, 169–179
Crespi, M.D., Zabaleta, E.J., Pontis, H.G., Salerno, G.L. (1991) Sucrose synthetase expression during cold acclimation in wheat. Plant Physiol. 96, 887–891
Dietz, K.J., Foyer, C. (1986) The relationship between phosphate status and photosynthesis in leaves. Reversibility of the effects of phosphate deficiency on photosynthesis. Planta 167, 376–381
Foyer, C.H. (1988) Feedback inhibition of photosynthesis through source-sink regulation in leaves. Plant Physiol. Biochem. 26, 483–492
Foyer, C., Furbank, R., Harbinson, J., Horton, P. (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth. Res. 25, 83–100
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
Guy, C.L., Huber, J.L.A., Huber, S.C. (1992) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol. 100, 502–508
Holaday, S.A., Martindale, W., Alred, R., Brooks, A., Leegood, R.C. (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiol. 98, 1105–1114
Horton, P. (1983) Effects of changes in the capacity for photosynthetic electron transfer and photophosphorylation on the kinetics of fluorescence induction in isolated chloroplasts. Biochim. Biophys. Acta 724, 404–410
Huber, J.L., Huber, S.C., Nielsen, T.H. (1989) Protein phosphorylation as a mechanism for regulation of spinach leaf sucrose phosphate synthase. Arc. Biochem. Biophys. 270, 681–690
Huner, N.P.A., Migus, W., Tollenaar, M. (1986) Leaf CO2 exchange rates in winter rye grown at cold-hardening and nonhardening temperatures. Can. J. Plant Sci. 66, 443–452
Hurry, V.M. (1991) Characterisation of the photosynthetic responses of spring and winter wheat to growth at cold-hardening temperatures, Ph.D. thesis, The University of Western Ontario
Hurry, V.M., Huner, N.P.A. (1991) Low growth temperature effects a differential inhibition of photosynthesis in spring and winter wheat. Plant Physiol. 96, 491–497
Hurry, V.M., Huner, N.P.A. (1992) Effect of cold-hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiol. 100, 1283–1290
van Kooten, O., Snel, J.F.H. (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25, 147–150
Krol, M., Griffith, M., Huner, N.P.A. (1984) An appropriate physiological control for environmental temperature studies: comparative growth kinetics of winter rye. Can. J. Bot. 62, 1062–1068
Lapointe, L., Huner, N.P.A. (1993) Photoinhibition of isolated mesophyll cells from cold hardened and nonhardened winter rye. Plant Cell Environ., in press
Lapointe, L., Huner, N.P.A., Carpentier, R., Ottander, C. (1991) Resistance to low temperature photoinhibition is not associated with thylakoid membranes in winter rye. Plant Physiol. 97, 804–810
Leegood, R.C., Furbank, R.T. (1986) Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate. Planta 168, 84–93
Öquist, G., Huner, N.P.A. (1991) Effects of cold acclimation on the susceptibility of photosynthesis to photoinhibition in Scots pine and winter and spring cereals: a fluorescence analysis. Func. Ecol. 5, 91–100
Öquist, G., Huner, N.P.A. (1993) Frost-hardening induced resistance to photoinhibition of photosynthesis in winter rye depends on an increased capacity of photosynthesis. Planta 189, 150–156
Öquist, G., Hurry, V.M., Huner, N.P.A. (1993) Low temperature effects on photosynthesis and correlation with freezing tolerance in spring and winter cultivars of wheat and rye. Plant Physiol. 101, in press
Pollock, C.J. (1986) Fructans and the metabolism of sucrose in vascular plants. New Phytol. 104, 1–24
Pollock, C.J., Chatterton, N.J. (1988) Fructans. In: The biochemistry of plants: Carbohydrates, vol. 14, pp. 109–140, Preiss, J., ed. Academic Press Inc., San Diego
Pollock, C.J., Lloyd, E.J. (1987) The effect of low temperature upon starch, sucrose and fructan synthesis in leaves. Ann. Bot. 60, 231–235
Pollock, C.J., Cairns, A.J., Collis, B.E., Walker, R.P. (1989) Direct effects of low temperature upon components of fructan metabolism in leaves of Lolium temulentum L. J. Plant Physiol. 134, 203–208
Pontis, H.G. (1989) Fructans and cold stress. J. Plant Physiol. 134, 148–150
Prinsley, R.T., Leegood, R.C. (1986) Factors affecting photosynthetic induction in spinach leaves. Biochim. Biophys. Acta 849, 244–253
Quick, W.P., Horton, P. (1984) Studies on the induction of chlorophyll fluorescence in barley protoplasts. I. Factors affecting the observation of oscillations in the yield of chlorophyll fluorescence and the rate of oxygen evolution. Proc. R. Soc. Lond. B. 220, 361–370
Quick, W.P., Horton, P. (1984b) Studies on the induction of chlorophyll fluorescence in barley protoplasts. II. Resolution of fluorescence quenching by redox state and the transthylakoid pH gradient. Proc. R. Soc. Lond. B. 220, 371–382
Quick, W.P., Horton, P. (1986) 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
Sagisaka, S., Matsuda, Y., Okuda, T., Ozeki, S. (1991) Relationship between wintering ability of winter wheat and the extent of depression of carbohydrate reserves: basal metabolic rate under snow determines longevity of plants. Soil Sci. Plant Nutr. 37, 531–541
Sicher, R.C., Sundblad, L.-G., Öquist, G. (1988) Effects of low temperature acclimation upon photosynthetic induction in barley primary leaves. Physiol. Plant. 73, 206–210
Sivak, M.N., Rowell, J. (1988) Phosphate limits photosynthesis in a starchless mutant of Arabidopsis thaliana deficient in chloroplast phosphoglucomutase activity. Plant Physiol. Biochem. 26, 493–501
Sivak, M.N., Walker, D.A. (1986) Photosynthesis in vivo can be limited by phosphate supply. New Phytol. 102, 499–512
Sivak, M.N., Walker, D.A. (1987) Oscillations and other symptoms of limitation of in vivo photosynthesis by inadequate phosphate supply to the chloroplast. Plant Physiol. Biochem. 25, 635–648
Somersalo, S., Krause, G.H. (1990) Reversible photoinhibition of unhardened and cold-acclimated spinach leaves at chilling temperatures. Planta 180, 181–187
Stitt, M. (1986) Limitation of photosynthesis by carbon metabolism: I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiol. 81, 1115–1122
Stitt, M., Grosse, H., Woo, K.-C. (1988) Interactions between sucrose synthesis and CO2 fixation. II. Alterations of fructose 2,6-bisphosphate during photosynthetic oscillations. J. Plant Physiol. 133, 138–143
Stitt, M., Wolke, I., Feil, R., Heldt, H.W. (1988) Coarse control of sucrose-phosphate synthase in leaves: alterations of the kinetic properties in response to the rate of photosynthesis and the accumulation of sucrose. Planta 174, 217–230
Tognetti, J.A., Salerno, G.L., Crespi, M.D., Pontis, H.G. (1990) Sucrose and furctan metabolism of different wheat cultivars at chilling temperatures. Physiol. Plant. 78, 554–559
Walker, D.A., Horton, P., Sivak, M.N., Quick, W.P. (1983) Antiparallel relationship between O2 evolution and slow fluorescence induction kinetics. Photobiochem. Photobiophys. 5, 35–39
Walker, D.A., Sivak, M.N., Prinsley, R.T., Cheesbrough, J.K. (1983) Simultaneous measurement of oscillations in oxygen evolution and chlorophyll a fluorescence in leaf pieces. Plant Physiol. 73, 542–549
Weiner, H., McMichael, R.W., Huber, S.C. (1992) Identification of factors regulating the phosphorylation status of sucrosephosphate synthase in vivo. Plant Physiol. 99, 1435–1442
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This work was supported by the Swedish Natural Sciences Research Council. The authors are indebted to Dr. N. Huner, Department of Plant Sciences, UWO, London, Canada, for helpful discussions during the initiation of this work and for the gift of rye seeds.
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Hurry, V.M., Gardeström, P. & Öquist, G. Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability. Planta 190, 484–490 (1993). https://doi.org/10.1007/BF00224787
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DOI: https://doi.org/10.1007/BF00224787