Abstract
Temperatures of more than 25° C adversely affect the activity of soluble starch synthase (SSS), an amyloplastic enzyme, in endosperm of wheat (Triticum aestivum L. cv. Mardler). Enzyme rate was found to have a temperature optimum between 20 and 25°C. This effect was apparently reversible after a short period of exposure to elevated temperature. We also found that with a prolonged period of exposure to elevated temperature there was another temperature-related phenomenon which caused a loss of enzyme activity that appeared to be much slower to reverse. We have termed this effect of temperature on SSS activity “knockdown”. The knockdown in SSS activity also occurred in-vivo. However, elevated temperature did not affect the activities of several other enzymes in the pathway of starch synthesis (ADP-glucose pyrophosphorylase, UDP-glucose pyrophosphorylase, sucrose synthase, phosphoglucomutase, phosphoglucose isomerase, bound starch synthase or hexokinase). Because the knockdown effect appeared to be specific to the enzyme SSS, we quantified the effect of knockdown on flux of carbon into starch and used these data to calculate the flux-control coefficient for SSS. Using data at 10–20°C the flux-control coefficient was CStarch10–20C = 0.50, whereas at 20–30° C the flux-control coefficient was CStarch20–30C = 1.38, and between 30–40°C the flux-control coefficient was CStarch30–40C = 0.69. Using data at 10–30°C the flux-control coefficient was CStarch10–30C = 1.15, and at 10–40°C the flux-control coefficient was CStarch10–40C = 0.82. In conclusion, we suggest that SSS is a major site of regulation of starch synthesis in developing wheat grain. During periods of high temperature the control point in the pathway of starch synthesis is apparently not associated exclusively with ADP-glucose pyrophosphorylase. In field conditions, in which temperatures are fluctuating, there will likely be periods of control of starch synthesis being exerted predominantly by SSS. During periods at lower temperature, control of flux may be exerted by SSS, perhaps in combination with other flux-controlling enzymes in the pathway. Our data point-out a crucial new aspect of quantifying control strengths of enzymes in plants: the determination of enzyme control strengths should be done in carefully regulated temperature conditions. Thus, since temperature is a major determinant of real flux through a pathway and the individual enzymes can respond differently to changing temperature conditions, the control strengths of individual steps in a pathway may vary with changing environmental conditions. This is particularly pronounced in starch deposition, because of the temperature instability of SSS.
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Abbreviations
- ADP-Glc:
-
adenosine diphosphoglucose
- SSS:
-
soluble starch synthase
- UDP-Glc:
-
uridine diphosphoglucose
References
Rees, T., Entwistle, G. (1989) Entry into the amyloplast of carbon for starch synthesis. In: Physiology, biochemistry and gngenetics of nongreen plastids, pp. 49–62, Boyer, C.D., Shannon, C., Harrison R.C., eds. The American Society of Plant Physiologists
Badu-Apraku, B., Hunter, R.B., Tollenaar, M. (1983) Effect of temperature during grain filling on whole plant and grain yield in maize (Zea mays L.). Can. J. Plant Sci. 63, 357–363
Bhullar, S.S., Jenner, C.F. (1986a) Effects of a brief episode of elevated temperature on grain filling in wheat ears cultured on solutions of sucrose. Aust. J. Plant Physiol. 13, 617–626
Bhullar, S.S., Jenner, C.F. (1986b) Effects of temperature on the conversion of sucrose to starch in the developing wheat endosperm. Aust. J. Plant Physiol. 13, 605–615
Brown, D.M. (1977) Response of maize to environmental temperatures: a review. World Meteorological Organization Conference on Agrometeorology of the Maize Crop. World Meteoroligical Organization, No. 481, pp. 15–26
Chang, J-H. (1981) Corn yield in relation to photoperiod, night temperature and solar radiation. Agric. Meteorol. 24, 253–262
Chowdhury, S.I., Wardlaw, I.F. (1978) The effect of temperature on kernel development in cereals. Aust. J. Agric. Res. 29, 205–223
Dale, R.F. (1983) Temperature perturbations in the midwestern and southeastern United States important for corn production. In: Crop reactions to water and temperature stresses in humid and temperate climates, pp. 21–32. Raper, C.D., Kramer P.J., eds. Westview Press, Boulder, USA
Ford, M.A., Pearman, I., Thorne, G.N. (1976) Effects of variation in ear temperature on growth and yield of spring wheat. Ann. Appl. Biol. 82, 317–333
Heinrich, R., Rapoport, T.A. (1974) A linear steady-state treatment of enzymatic chains. Eur. J. Biochem. 42, 89–95
Hochachka, P.W., Somero, G.N. (1984) Biochemical adaptation. Pricetown University Press, Pricetown, N.J. USA
Hunter, R.B., Tollenaar, M., Breuer, C.M. (1977) Effects of photoperiod and temperature on vegetative and reproductive growth of a maize (Zea mays) hybrid. Can. J. Plant Sci. 57, 1127–1133
Jenner, C.F. (1991a) Effects of exposure of wheat ears to high temperature on dry matter accumulation and carbohydrate metabolism in the grain of two cultivars. I. Immediate responses. Aust. J. Plant Physiol. 18, 165–177
Jenner, C.F. (1991b) Effects of exposure of wheat ears to high temperature on dry matter accumulation and carbohydrate metabolism in the grain of two cultivars. II. Carry-over effects. Aust. J. Plant Physiol. 18, 179–190
Jones, R.J., Quattar, S., Crookston, R.K. (1981) Thermal environment during endosperm cell division and grain filling in maize: effects on kernel growth and development in-vitro. Crop Sci. 24, 133–137
Kacser, H., Burns, J.A. (1973) The control of flux. Symp. Soc. Exp. Biol. 27, 65–107
Keeling, P.L. (1989) Evidence against triose phosphate transport into amyloplasts of developing wheat and maize grain. In: Physiology, biochemistry and genetics of nongreen plastids. pp. 63–78, Boyer, C.D., Shannon, J.C., Harrison R.C., eds. The American Society of Plant Physiologists
Keeling, P.L., Woods, J.R., Tyson, R.H., Bridges, I.G. (1988) Starch biosynthesis in developing wheat grain: Evidence against the direct involvement of triose phosphates in the metabolic pathway. Plant Physiol. 87, 311–319
Lavintman, N., Tandecarz, J., Carceller, M., Mendiara, S., Cardini, C.E. (1974) Role of uridine diphosphate glucose in the biosynthesis of starch. Mechanism of formation and enlargement of a glucoproteic acceptor. Eur. J. Biochem. 50, 145–155
MacLeod, L.C., Duffus, C.M. (1988) Reduced starch content and sucrose synthase acivity in developing endosperm of barley plants grown at elevated temperatures. Aust. J. Plant Physiol. 15, 367–375
Mohabir, G., John, P. (1988) Effect of temperature on starch synthesis in potato tuber tissue and in amyloplasts. Plant Physiol. 88, 1222–1228
Neuhaus, H.E., Stitt, M. (1990) Control analysis of photosynthate partitioning: Impact of reduced activity of ADP-Glucose pyrophosphorylase or plastid phosphoglucomutase on the fluxes to starch and sucrose in Arabidopsis thaliana (L.) Heynh. Planta 182, 445–454
Ozbun, J.L., Hawker, J.S., Preiss, J. (1971) Adenosine diphosphoglucose-starch glucosyltransferases from developing kernels of waxy maize. Plant Physiol. 48, 765–769
Ozbun, J.L., Hawker, J.S., Preiss, J. (1972) Soluble adenosine diphosphate glucose-α-1,4-glucan α-4-glucosyltransferases from spinach leaves. Biochem. J. 126, 953–963
Priess, J. (1991) Biology and molecular biology of starch synthesis and its regulation. Oxford Surv. Plant Mol. Cell Biol. 7, 59–114
Priess, J. (1992) Biochemistry and molecular biology of starch synthesis. In: Frontiers in carbohydrate research-2, pp. 208–230. Chandrasekaran, R. ed. Eisevier Science Publishers Ltd., Essex, UK
Rawson, H.M. (1986) High-temperature-tolerant wheat: a description of variation and a search for some limitations to productivity. Field Crops Res. 14, 197–212
Rijven, A.H.G.C. (1986) Heat inactivation of starch synthase in wheat endosperm tissue. Plant Physiol. 81, 449–453
Shaw, R.H. (1983) Estimates of yield reductions in corn by water and temperature stress. In: Crop reactions to water and temperature stresses in humid and temperate climates, pp. 49–65, Raper, C.D., Kramer, P.J., eds. Westview Press, Boulder, USA
Sofield, I., Evans, L.T., Cook, M.G., Wardlaw, I.F. (1977) Factors influencing the rate and duration of grain filling in wheat. Aust. J. Plant Physiol. 4, 785–797
Tashiro, T., Wardlaw, I.F. (1989) A comparison of the effect high temperature on grain development in wheat and rice. Ann. Bot. 64, 59–65
Tashiro, T., Wardlaw, I.F. (1990a) The response to high temperature shock and humidity changes prior to and during the early stages of grain development in wheat. Aust. J. Plant Physiol. 17, 551–561
Tashiro, T., Wardlaw, I.F. (1990b) The effect of high temperature at different stages of ripening on grain set, grain weight and grain dimensions in the semi-dwarf wheat “Banks”. Ann. Bot. 65, 51–61
Tashiro, T., Wardlaw, I.F. (1991) The effect of high temperature on the accumulation of dry matter, carbon and nitrogen in the kernel of rice. Aust. J. Plant Physiol. 18, 250–265
Tollenaar, M. (1989a) Response of dry matter accumulation in maize to temperature: I. Dry matter partitioning. Crop Sci. 29, 1239–1246
Tollenaar, M. (1989b) Response of dry matter accumulation in maize to temperature: II. Leaf photosynthesis. Crop Sci. 29, 1275–1279
Torres, N.U., Mateo, F., Melendez-Hevia, E., Kacser, H. (1986) Kinetics of metabolic pathways. A system in vivo to study the control of flux. Biochem. J. 234, 169–174
Wardlaw, I.F., Sofield, I., Cartwright, P.M. (1980) Factors limiting the rate of dry matter accumulation in the grain of wheat grown at high temperature. Aust J. Plant Physiol. 7, 387–400
Wardlaw, I.F., Dawson, I.A., Munibi, P. (1989a) The tolerance of wheat to high temperatures during reproductive growth. II. Grain development. Aust. J. Agric. Res. 40, 15–24
Wardlaw, I.F., Dawson, I.A., Munibi, P., Fewster, R. (1989b) The tolerance of wheat to high temperatures during reproductive growth. I. Survey procedures and general response patterns. Aust. J. Agric. Res. 40, 1–13
Werner, W, Rey, H.G., Wielinger, H. (1970) Über die Eigenschaften eines neuen Chromogens für die Blutzuckerbestimmung nach der GOD/POD-Methode. Z. Anal. Chem. 252, 224–228
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We wish to thank Dr. Ian Bridges (Zeneca Seeds, Bracknell, UK) and Professor Tom ap Rees (Botany School, Cambridge University, UK) for their constructive criticism during the course of this work. We also wish to thank Dr. Kay Denyer (John Innes Centre, Norich, UK) for her helpful comments on this manuscript.
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Keeling, P.L., Bacon, P.J. & Holt, D.C. Elevated temperature reduces starch deposition in wheat endosperm by reducing the activity of soluble starch synthase. Planta 191, 342–348 (1993). https://doi.org/10.1007/BF00195691
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DOI: https://doi.org/10.1007/BF00195691