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Cold-hardening results in increased activity of enzymes involved in carbon metabolism in leaves of winter rye (Secale cereale L.)

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Abstract

Light- and CO2-saturated photosynthesis of nonhardened rye (Secale cereale L. cv. Musketeer) was reduced from 18.10 to 7.17 μmol O2·m−2·s−1 when leaves were transferred from 20 to 5°C for 30 min. Following cold-hardening at 5°C for ten weeks, photosynthesis recovered to 15.05 μmol O2·m−2·s−1,comparable to the nonhardened rate at 20°C. Recovery of photosynthesis was associated with increases in the total activity and activation of enzymes of the photosynthetic carbon-reduction cycle and of sucrose synthesis. The total hexose-phosphate pool increase by 30% and 120% for nonhardened and cold-hardened leaves respectively when measured at 5°C. The large increase in esterified phosphate in coldhardened leaves occurred without a limitation in inorganic phosphate supply. In contrast, the much smaller increase in esterified phosphate in nonhardened leaves was associated with an inhibition of ribulose-1,5-bisphosphate carboxylase/oxygenase and sucrose-phosphate synthase activation. It is suggested that the large increases in hexose phosphates in cold-hardened leaves compensates for the higher substrate threshold concentrations needed for enzyme activation at low temperatures. High substrate concentrations could also compensate for the kinetic limitations imposed by product inhibition from the accumulation of sucrose at 5°C. Nonhardened leaves appear to be unable to compensate in this fashion due to an inadequate supply of inorganic phosphate.

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Abbreviations

DHAP:

dihydroxyacetone phosphate

Fru6P:

fructose-6-phosphate

Fru 1,6BP:

fructose-1,6-bisphosphate

Fru1,6BPase:

fructose-1,6-bisphosphatase

Glc6P:

glucose-6-phosphate

PGA:

3-phosphoglycerate

PPFD:

photosynthetic photon flux density

CH:

cold-hardened rye grown at 5°C

NH:

nonhardened rye grown at 24°C

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

RuBP:

ribulose-1,5-bisphosphate

SPS:

sucrose-phosphate synthase

UDPGlc:

uridine 5′-diphosphoglucose

References

  • Anchordoguy, T.J., Rudolph, A.S., Carpenter, J.F., Crowe, J.H. (1987) Mode of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24, 323–331

    Google Scholar 

  • Arnon, D.L. (1949) Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1–15

    Google Scholar 

  • Badger, M.R., Björkman, O., Armond, P.A. (1982) An analysis of photosynthetic response and adaptation to temperature in higher plants: temperature acclimation in the desert evergreen Nerium oleander L. Plant Cell Environ. 5, 85–99

    Google Scholar 

  • Chatterton, N., Thornley, W., Harrison, P., Bennett, J. (1988) Dynamics of fructan and sucrose biosynthesis in crested wheatgrass. Plant Cell Physiol. 29, 1103–1108

    Google Scholar 

  • Dietz, K.-J., Heber, U. (1986) Light and CO2 limitation of photosynthesis and the states of the reactions regenerating ribulose 1,5-bisphosphate or reducing 3-phosphoglycerate. Biochim. Biophys. Acta 848, 392–401

    Google Scholar 

  • Doncaster, H.D., Adcock, M.D., Leegood, R.C. (1989) Regulation of photosynthesis in leaves of C4 plants following a transition from high to low light. Biochim. Biophys. Acta 973, 176–184

    Google Scholar 

  • Ferrar, P.J., Osmond, C.B. (1986) Nitrogen supply as a factor influencing photoinhibition and photosynthetic acclimation after transfer of shade-grown Solarnum dulcamara to bright light. Planta 168, 563–570

    Google Scholar 

  • Ferrar, P.J., Slatyer, R.O., Vranjic, J.A. (1989) Photosynthetic temperature acclimation in Eucalyptus species from diverse habitats, and a comparison with Nerium oleander. Aust. J. Plant Physiol. 16, 199–217

    Google Scholar 

  • 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

    Google Scholar 

  • Gerhardt, R., Stitt, M. Heldt, H.W. (1987) Subcellular metabolite levels in spinach leaves. Regulation of sucrose synthesis during diurnal alterations in photosynthetic partitioning. Plant Physiol. 83, 399–407

    Google Scholar 

  • 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

    Google Scholar 

  • Heldt, H.W., Chon, C.-J., Lorimer, G.H. (1978) Phosphate requirement for the light activation of ribulose 1,5-bisphosphate carboxylase in intact spinach chloroplasts. FEBS Lett. 92, 234–240

    Google Scholar 

  • Herzog, B., Stitt, M., Heldt, H.W. (1984) Control of photosynthetic sucrose metabolism by fructose 2,6-bisphosphate. III. Properties of the cytosolic fructose-1,6-bisphosphatase. Plant Physiol. 75, 561–565

    Google Scholar 

  • Holaday, A.S., 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

    Google Scholar 

  • Huner, N.P.A. (1985) Morphological, anatomical, and molecular consequences of growth and development at low temperature in Secale cereale L. cv. Puma. Am. J. Bot. 72, 1290–1306

    Google Scholar 

  • Huner, N.P.A., Migus, W., Tollenaar, M. (1986) Leaf CO2 exchange rates in winter rye grown at cold-hardening and non-hardening temperatures. Can. J. Plant Sci. 66, 443–452

    Google Scholar 

  • 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

    Google Scholar 

  • Hurry, V.M., Gardeström, P., Öquist, G. (1993) Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability. Planta 190, 484–490

    Google Scholar 

  • Kobza, J., Edwards, G.E. (1987) Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiol. 83, 69–74

    Google Scholar 

  • Koster, K.L., Lynch, D.V. (1992) Solute accumulation and compartmentation during the cold acclimation of Puma rye. Plant Physiol. 98, 108–113

    Google Scholar 

  • Labate, C.A., Leegood, R.C. (1988) Limitation of photosynthesis by changes in temperature. Factors affecting the response of carbon dioxide assimilation to temperature in barley leaves. Planta 173, 519–527

    Google Scholar 

  • Labate, C.A., Leegood, R.C. (1989) Influence of low temperature on respiration and contents of phosphorylated intermediates in darkened barley leaves. Plant Physiol. 91, 905–910

    Google Scholar 

  • Labate, C.A., Adcock, M.D., Leegood, R.C. (1990) Effects of temperature on the regulation of photosynthetic carbon assimilation in leaves of maize and barley. Planta 181, 547–554

    Google Scholar 

  • Laisk, A.H. (1977) Equipment and methods for the measurements of PCW curves. In: Kinetika fotosinteza i fotodykhaniya u C3 rastenij (Kinetics of photosynthesis and photorespiration of C3plants), pp. 48–71, Nichiporovich, A.A., ed. Nauka, Moscow

    Google Scholar 

  • Leegood, R.C., Furbank, R.T. (1986) Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate. Planta 168, 84–93

    Google Scholar 

  • Livingston, D., Olien, C.R., Freed, R. (1989) Sugar composition and freezing tolerance in barley crowns at varying carbohydrate levels. Crop Sci. 29, 1266–1270

    Google Scholar 

  • Mächler, F., Schnyder, H., Nösberger, J. (1984) Influence of inorganic phosphate on photosynthesis of wheat chloroplasts. I. Photosynthesis and assimilate export at 5°C and 25°C. J. Exp. Bot. 35, 481–487

    Google Scholar 

  • Neuhaus, H.E., Quick, W.P., Siegl, G., Stitt, M. (1990) Control of phosphate partitioning in spinach leaves. Analysis of the interaction between feedforward and feedback regulation of sucrose synthesis. Planta 181, 583–592

    Google Scholar 

  • Oja, V.M. (1983) A quick-operating gas measuring device for studying the kinetics of leaf photosynthesis. Fiziol. Rast. 30, 1045–1052

    Google Scholar 

  • Olien, C.R. (1992) Protective modification of freeze stress in plant tissue. Thermochim. Acta 212, 255–260

    Google Scholar 

  • Olien, C.R., Clark, J.L. (1993) Changes in soluble carbohydrate composition of barley, wheat, and rye during winter. Crop Sci. 85, 21–29

    Google Scholar 

  • Öquist, G., Huner, N.P.A. (1993) Cold-hardening-induced resistance to photoinhibition of photosynthesis in winter rye is dependent upon an increased capacity of photosynthesis. Planta 189, 150–156

    Google Scholar 

  • 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, 245–250

    Google Scholar 

  • Pärnik, T.R., Keerberg, O.F., Jürisma, E.J. (1987) Quick-operating exposition chambers for studying photosynthesis with 14CO2. Fiziol. Rast. 34, 837–845

    Google Scholar 

  • Regehr, D.L., Bazzaz, F.A. (1976) Low temperature photosynthesis in successional winter annuals. Ecology 57, 1297–1303

    Google Scholar 

  • Robinson, S.P., Portis, A.R.J. (1988) Involvement of stromal ATP in the light activation of ribulose 1,5-bisphosphate carboxylase/oxygenase in intact isolated chloroplasts. Plant Physiol. 86, 293–298

    Google Scholar 

  • 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

    Google Scholar 

  • Sharkey, T.D., Stitt, M., Heineke, D., Gerhardt, R., Raschke, K., Heldt, H.W. (1986) Limitation of photosynthesis by carbon metabolism. II. O2-insensitive CO2 uptake results from limitations of triose phosphate utilisation. Plant Physiol. 81, 1123–1129

    Google Scholar 

  • Sharkey, T.D., Savitch, L.V., Butz, N.D. (1991) Photometric method for routine determination of kcat and carbamylation of rubisco. Photosynth. Res. 28, 41–48

    Google Scholar 

  • Stitt, M., Grosse, H. (1988) Interactions between sucrose synthesis and CO2 fixation IV. Temperature-dependent adjustment of the relation between sucrose synthesis and CO2 fixation. J. Plant Physiol. 133, 392–400

    Google Scholar 

  • Stitt, M., Herzog, B., Heldt, H.W. (1984a) Control of photosynthetic sucrose synthesis by fructose 2,6-bisphosphate. I. Coordination of CO2 fixation and sucrose synthesis. Plant Physiol. 75, 548–553

    Google Scholar 

  • Stitt, M., Kürzel, B., Heldt, H.W. (1984b) Control of photosynthetic sucrose synthesis by fructose 2,6-bisphosphate. II. Partitioning between sucrose and starch. Plant Physiol. 75, 554–560

    Google Scholar 

  • Stitt, M., Wilke, L, 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

    Google Scholar 

  • Stitt, M., Lilley, R.M., Gerhardt, R., Heldt, H:W. (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol. 174, 518–552

    Google Scholar 

  • Tognetti, J.A., Salerno, G.L., Crespi, M.D., Pontis, H.G. (1990) Sucrose and fructan metabolism of different wheat cultivars at chilling temperatures. Physiol. Plant. 78, 554–559

    Google Scholar 

  • van Kooten, O., Snel, J.F.H. (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25, 147–150

    Google Scholar 

  • Vernon, L.P. (1960) Spectrophotometric determination of chlorophylls and pheophytins in plant extracts. Anal. Chem. 32, 1144–1150

    Google Scholar 

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This work was supported by operating grants from the Swedish Natural Sciences Research Council to G.Ö. and P.G.

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Hurry, V.M., Keerberg, O., Pärnik, T. et al. Cold-hardening results in increased activity of enzymes involved in carbon metabolism in leaves of winter rye (Secale cereale L.). Planta 195, 554–562 (1995). https://doi.org/10.1007/BF00195715

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