The Relationship between Sucrose and Starch during 'Dark' Export from Leaves of Uniculm Barley
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1 Journal of Experimental Botany, Vol. 31, No. 122, pp , June 1980 The Relationship between Sucrose and Starch during 'Dark' Export from Leaves of Uniculm Barley A. J. GORDON, G. J. A. RYLE, AND GILLIAN WEBB The Grassland Research Institute 1, Hurley, Maidenhead, Berkshire Received 11 October 1979 ABSTRACT Uniculm barley plants were grown in 8 h photoperiods at a quantum flux density of 655 //E m~ 2 s~ l. Groups of plants were transferred to four different light environments for one 8 h photoperiod (106, 270, 665, and 975 ^E m" 2 s~') and harvested at intervals throughout the succeeding dark period for subsequent carbohydrate analysis of the youngest mature leaf. Sucrose was the predominant carbohydrate in the leaves (attaining a level of c. 100 mg dm" 2 after 8 h at 975 ^E m~ 2 s~') but starch was also of significance (20 mg dm" 2 after 8 h at 975 fie m~ 2 s"')- During the dark period, following a photoperiod at the three highest light levels (270, 665, and 975 /JE m~ 2 s~'x sucrose was exported first while the starch level remained fairly constant. When rtie' sucrose level fell to mg dm" 2 starch degradation began. This critical sucrose level was reached earlier in those plants subjected to lower quantum flux densities during the preceding photoperiod. The delay in the remobilization of starch suggests an important regulatory mechanism which may be dependent upon the sucrose level. At 106,uE m~ 2 s~' the sucrose level rose to only 10 mg dm~ 2. Here there was no discernible delay in the depletion of sucrose or starch. INTRODUCTION Sucrose was the major carbohydrate accumulated during an 8-5 h photoperiod by young mature leaves of uniculum barley grown in a controlled environment (Gordon, Ryle, Powell, and Mitchell, in press). Starch was a minor, but significant storage carbohydrate (sucrose: starch ratio c. 5 :1). During the dark period sucrose and starch from the leaf contributed to the carbohydrate requirements of the growing regions of the plant. This pattern of remobilization and export of reserve carbohydrates was unlike that found in other plants (Sharkey and Pate, 1976; Challa, 1976). Sucrose was rapidly depleted from the leaf during the first half of the dark period during which time the starch level remained constant. During the second half of the dark period the starch was remobilized and this was accompanied by a reduction in the rate of sucrose depletion. It was suggested that the sucrose concentration might in some way prevent starch remobilization, so that starch was degraded only when the sucrose concentration fell to a low level (Gordon et al., in press). The experiment described in the present paper was designed to explore this possible relationship. Groups of plants were subjected to four different light levels for one photoperiod and the sucrose and starch contents were determined in leaf samples harvested during the subsequent dark period. We expected the carbo- 1 The Grassland Reasearch Institute is financed through the Agricultural Research Council.
2 846 Gordon, Ryle, and Webb 'Dark' Carbohydrate Mobilization in Barley hydrate status of the leaves to be different in each of these four groups of plants and that this difference would affect the pattern of mobilization and export of carbohydrate during darkness. MATERIALS AND METHODS PlanUmaterial and growth conditions Unictilm barley plants (Kindred uniculm 97) were grown from seed in 9-5 cm pots filled with an inert, ; support medium (Perlite) and housed in controlled environment cabinets (Saxcil). Plants were supplied daily with' a complete nutrient solution and illuminated by a mixture of fluorescent tubes and incandescent lamps (655 //E m~ 2 s~' in the spectral region nm) during 8 h photoperiods. Relative humidity and CO 2 concentration were maintained at 60 and 0-3% (v/v) respectively. The initial temperature regime was 23/18 C (day/night) to aid germination and early growth. After 9 d, when the plants were well established (3rd leaf just appearing), the temperature was reduced to 15/10 C (day/night). Plants were used 14 d later as the 3rd leaf reached full expansion. Groups of uniform plants were illuminated for one photoperiod at four different light levels: 106, 270, 665, and 975 //E m~ 2 s~'. Other environmental conditions were unchanged. The 15 cm tip of leaf 3 was harvested at the following times after the beginning of the photoperiod (in parenthesis the number of plants harvested): 0 (6), 8 (4), 9 5 (1), 11 (2), 12 5 (1), 14 (2), 15-5 (1), 17 (2), 18-5 (1), 20 (2), 21-5 (1), 23 (2), 24 (1) h. The areas of harvested leaves were measured and they were then killed by immersion in boiling 80% (v/v) ethanol as described elsewhere (Gordon, Ryle, and Powell, 1977, 1979). Carbohydrates were extracted, fractionated, and their levels estimated by methods reported previously (Gordon et al., 1977, 1979). Leaf net photosynthesis was measured by infrared gas analysis (see Ryle and Powell, 1974, 1975, 1976) and light level by Quantum Sensors (Lambda Instruments Corporation). RESULTS AND DISCUSSION Photosynthesis and export during the photoperiod Plant attributes during the photoperiod at four quantum flux densities are summarized in, Table 1. The rate of accumulation of carbon in the leaf, in the form of sucrose and starch, increased with increasing quantum flux density and net photosynthesis (i> N ). If the rate of carbon accumulation (starch + sucrose) is subtracted from the rate of net gaseous uptake of carbon by the photosynthesizing leaf an estimate of export is obtained. This is likely to be an overestimate since the accumulation of sucrose and starch, although accounting for a large fraction of the stored carbon, does not constitute all the accumulated carbon (cf. Gordon et al., in press). None the less these rates of 'light' export are similar to those reported TABLE 1. Photosynthesis, carbohydrate synthesis and export during the photoperiod Quantum Net Sucrose Starch Estimated flux density photosynthesis accumulation accumulation light export 0 "! s"') mgcdm^h" 1 mg C dm~ 2 h~' mg C dm" 2 h" 1 mg C dm" 2 h~' " See text.
3 Gordon, Ryle, and Webb 'Dark' Carbohydrate Mobilization in Barley 847 elsewhere (Terry and Mortimer 1972; Ho, 1976; Silvius, Kremer, and Lee, 1978; Gordon et ai, 1977, in press), and indicate that the rate of Might' export is higher at higher quantum flux densities. By the end of the photoperiod the leaves contained between 3 and 6 times more sucrose than starch. Carbohydrate export in the dark The diurnal variations in leaf carbohydrate content of plants exposed for one 8 h photoperiod to four different quantum flux densities are illustrated in Fig. 1. During darkness, carbon stored in the leaf during the day was exported. At the three highest quantum flux densities examined, the pattern of carbohydrate depletion was similar; sucrose was exported first whilst the starch level remained fairly constant (Fig. 1). The rate of sucrose depletion was reduced after some hours of darkness. If the sucrose depletion patterns for the four sets of plants are compared it will be noted that the slope A l is similar to slope A 2 \ B,, B 2, and B 3 are similar; and also C x and C 2 are similar. This led us to consider the possibility that all four sets of data might form part of the same leaf sucrose depletion curve. All the data were found to fit the exponential equation y = D e~ kt where y is the sucrose content of the leaf (mg dm~ 2 ) at time t hours after the beginning of the photoperiod. D is a constant for each set of data and depends on the quantity of sucrose in the leaf at the end of the photoperiod. We found no evidence to suggest a statistical difference in the value of the constant, k; the mean value was For all four sets of data the correlation was highly significant (P < 0-001). 20 'E IOO o 00 ~S 80 2 o XI h 975 Quantum flux density during the photoperiod (fie m J s ') FIG. 1. The depletion of starch (A) and sucrose (B) from the youngest mature leaf of uniculm barley plants during darkness. Groups of plants experienced one of the four quantum flux densities for the entire preceding 8 h photoperiod. Arrows indicate the sucrose level when starch degradation began.
4 848 Gordon, Ryle, and Webb 'Dark' Carbohydrate Mobilization in Barley Time (h) after beginning of photoperiod FIG. 2. The theoretical exponential decline in sucrose content of leaves exposed to a quantum flux density of 975 //E m~ 2 s~' during the preceding photoperiod. The solid line is derived from the equation v = 277 e~ l3/. The symbols O, A,, V represent the decline in sucrose level following a photoperiod at 975, 665, 270, and 106 //E m~ 2 s" 1 respectively. The time scale has been shifted so that the points coincide with the appropriate part of the curve. In Fig. 2 the theoretical exponential curve is plotted based on the value of k = and D = 277 (this was the constant for the 975 fie irr 2 s~' data). The four sets of data have also been plotted in Fig. 2 for comparison. The value of y at / 8 for each light-treatment was determined from the best fit of the data and the time scale was then shifted so that this '8 h point' coincided with the predicted curve. The correlation coefficient for the data as shown in Fig. 2 was 0-98 (P < 0-001). The model suggests that foe.the sucrose level to fall from c. 100 mg dm~ 2 (8 h point of 975 /ue m~ 2 s~ l treatment)-to c. 2 mg dm~ 2 (24 h point of 106 //E m~ 2 s~' treatment) it would be necessary to keep-tjie plants, previously illuminated at 975 /ue m~ 2 s~ l, in darkness for c. 32 h. Remobilization of starch Lines fitted by eye have been drawn through the starch data (Fig. 1). In the three higher light treatments, starch level initially remained approximately constant during darkness, but this was followed by rapid breakdown when the sucrose concentration had decreased to mg dm" 2 (indicated by arrows in Fig. 1). In
5 i Gordon, Ryle, and Webb 'Dark' Carbohydrate Mobilization in Barley 849 plants subjected to the lowest light level (106 //E rrr 2 s" 1 )* the sucrose concentration only rose to c. 10 mg dm~ 2. Here no delay was apparent in the depletion of sucrose or starch after the onset of darkness. Although it might be expected that starch remobilization would be delayed longer if the leaf sucrose level were higher, we are not aware of any mechanism which could account for this. Current knowledge about the relationships between metabolites of the chloroplast and cytoplasm suggests that starch is confined to the chloroplast while sucrose is found in the cytoplasm (Walker, 1976; Heber, 1974; Bird, Cornelius, Keys, and Whittingham, 1974). The chloroplast membrane is impermeable to sucrose (Walker, 1976; Heber, 1974), therefore if a feedback mechanism is operating in barley leaves it is unlikely to involve sucrose directly. The situation is complicated further by the possibility that sucrose is present in different compartments in the leaf. Although we have no information about sucrose compartmentation within barley leaves there have been a number of reports about sucrose compartments in other plants, e.g. soyabean (Fisher, 1970) and sugar beet (Outlaw, Fisher, and Christy, 1975; Outlaw and Fisher, 1975; Geiger, Giaquinta, Sovonick, and Fellows, 1973; Giaquinta, 1978). It would be unwise, however, to assume that sucrose compartmentation is similar in all plants especially in the case of barley leaves where the sucrose level is generally much higher than in many other plants (cf. Gordon et ah, in press (barley), Thome and Koller, 1974 (soyabean), Milford and Pearman, 1975; Christy and Swanson, 1976 (sugar beet), Challa, 1976 (cucumber), and Ho, 1977, 1978 (tomato)).the precise location of sucrose in barley leaves could affect its role in any control mechanism. The indirect control of starch metabolism by sucrose might occur as a result of other relationships as yet not investigated. Starch formation in the light is favoured by a combination of relatively high levels of 3-phosphoglycerate (PGA) and relatively low levels of inorganic phosphate (P,) (Preiss, Ghosh, and Wittkop, 1967; Preiss and Kosuge, 1970). Also starch formation has been induced by sequestration of Pi by exogenous mannose in isolated spinach chloroplasts (Herold, Lewis, and Walker, 1976; Chen-She, Sheu-Hwa, Lewis, and Walker, 1975; Heldt etai, 1977). Thus P, seems to be an important effector in this system (Steup, Peavey, and Gibbs, 1976; Levi and Preiss, 1978; Herold and Walker, 1979). If there is an equilibrium between sucrose and its precursors in the cytoplasm such that the concentration of phosphorylated compounds is relatively high when sucrose level is high this may reduce the P, level. Initially in the dark, the level of P, might be insufficient to allow starch degradation since starch phosphorylase requires P, to function (Heldt et ai, 1977; Levi and Preiss, 1978). As the sucrose level falls in uniculm barley leaves in the dark so the level of phosphorylated precursors might also decline, thus liberating P,. In the presence of higher P, levels starch degradiation may occur. In conclusion, we have examined the pattern of carbohydrate supply from mature leaves of uniculm barley during darkness. The apparent relationship between sucrose and starch levels is an interesting finding and further experiments are in progress to study the control of starch metabolism with regard to carbon mobilization during 'dark' export.
6 850 Gordon, Ryle, and Webb 'Dark' Carbohydrate Mobilization in Barley ACKNOWLEDGEMENTS We are grateful to the staff of the Controlled Environment Facility for assistance and to Miss Jane Woledge, Dr. E. L. Leafe and Dr. M. J. Robson for constructive criticism of an earlier version of this manuscript. We also wish to thank Mr. G. W. Morgan and Mr. L. C. Chapas for statistical advice. LITERATURE CITED BIRD, I. F., CORNELIUS, M. J., KEYS, A. J., and WHITTINGHAM, C. P., Phytochemistry. 13, CHALLA, H., An analysis of the diurnal growth, carbon dioxide exchange and carbohydrate reserve content of cucumbers. Publ. No. 20. Centre for Agric. Publ. and Documentation, Wageningen. CHEN-SHE, SHEU-HWA., LEWIS, D. H., and WALKER, D. A., New Phytol. 74, CHRISTY, A. L., and SWANSON, C. A., Transport and transfer processes in plants. Eds. I. F. Wardlaw, and J. B. Passioura, Academic Press. Ch. 27. pp FISHER, D. B., PL Phystol., Lancaster, 45, GEIGER, D. R., GIAQUINTA, R. T., SOVONICK, S. A., and FELLOWS, R. J., Ibid. 52, GIAQUINTA, R. T., Ibid. 61, GORDON, A.J., RYLE, G.J. A., and POWELL, C.E., \911.J.exp.Bot. 28, Ibid. 30, and MITCHELL, D. Ibid, (in press). HEBER, U., A. Rev. PI. Physiol. 25, HELDT, H. W., CHON, C. J., MARONDE, D., HEROLD, A., STANKOVIC, Z. S., WALKER, D. A., KRAMINER, A., KIRK, M. A., HEBER, U., PL Physiol. Lancaster. 59, HEROLD, A., LEWIS, D. H., and WALKER, D. A., New Phytol. 76,397^07. and WALKER, D. A., 1979 In Membrane transport in biology. II. Transport across single biological membranes. Springer-Verlag Berlin, Heidelberg. Eds. G. Giebisch, D. C. Tosteson, and H. H. Ussing, pp Ho, L. C, /. exp. Bot. 27, Ann. appl. Biol. 87, Ann. Bot. 42, LEVI, C, and PREISS, J., PL Physiol., Lancaster, 61, MILFORD, G. F. J., and PEARMAN, I., Photosynthetica, 9 (1), OUTLAW, W. H., and FISHER, D. B., PL Physiol., Lancaster, 55, and CHRISTY, A. L., Ibid. 55, PREISS, J., GHOSH, M. P., and WITTKOP, J Biochemistry of chloroplasts. Ed. T. W. Goodwin, Academic Press. Vol. 2, pp and KOSUGE, T., A. Rev. PL Physiol. 21, RYLE, G. J. A., and POWELL, C. E., Ann. appl. Biol. 77, Ann. Bot. 39, J. exp. Bot. 27, SHARKEY, P. J., and PATE, J. E., Planta, 123, SILVIUS, J. E., KREMER, D. F., and LEE, D. R., PL Physiol., Lancaster, 62,54-8. STEUP, M., PEAVEY, D. G., and GIBBS, M., Biochem. biophys. Res. Commun. 72, TERRY, N., and MORTIMER, D. C, Can. J. Bot. 50, THORNE, J. H., and KOLLER, H. R., PI. Physiol., Lancaster, 54, WALKER, D. A., Encyclopedia of Plant Physiology. New Series, Vol. 3. Transport in Plants HI. Springer-Verlag, Berlin, Heidelberg, N.Y. Eds. C. R. Stocking and U. Heber, pp \
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