Summary
We examine the idea that sucrose plays a central role in control of plant growth beyond that of substrate and product. The extended hypothesis we discuss is that sucrose can regulate source metabolism by down-regulating genes encoding proteins involved with photosynthesis, and sink metabolism by up-regulating genes encoding proteins involved with sucrose hydrolysis and growth. The rates of turnover, and of changes of pool size, of sucrose render it suitable for temporally integrating changes in the environment, or within the plant itself, over a period of hours to a few days. While much evidence can be adduced to support the extended hypothesis, a great deal of it is essentially correlational and we still lack the details of a mechanism by which sucrose status might modulate gene expression.
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References
Alderson A, Sabelli PA, Dickinson Jr, Cole D, Richardson M, Kreis M, Shewry PR and Halford NG (1991) Complementation of snf 1, a mutation affecting global regulation of carbon metabolism in yeast, by a plant protein kinase cDNA. Proc Natl Acad Sci USA 88: 8602–8605
Atherton JG, Harris GP (1986) Flowering. In: Atherton JG, Rudich J (ed) The Tomato Crop, pp 167–200. Chapman and Hall, London
Audus LJ (1972) Plant Growth Substances, Vol I. Leonard Hill. London
Avelange M-H, Sarrey F, Rebille F (1990) Effect of glucose feeding on respiration and photosynthesis in photoautotrophic Dianthus caryophyllus cells. Plant Physiol 94: 157–1162
Avigad G (1982) Sucrose and other disaccharides. In: Loewus FA, Tanner W (ed) Encyclopedia of Plant Physiology 13A, pp 217–347. Springer, Berlin
Azcón-Bieto J (1983) Inhibition of photosynthesis by carbohydrates in wheat leaves. Plant Physiol 73: 681–686
Azumi Y, Miura M and Suzuki H (1993) Analysis of upstream region of radish senescence-associated gene din 1. Abstracts of the 15th International Botanical Congress, Yokohama, 1993, No.6156
Baker DA and Milburn JA (ed) (1989) Transport of Photoassimilates. Longman, Harlow
Barber J and Andersson B (1992) Too much of a good thing: Light can be bad for photosynthesis. TIBS 17: 61–65
Bastow Wilson J (1988) A review of evidence on the control of shoot:root ratio, in relation to models. Ann Bot 61: 433–449
Baysdorfer C, van der Woude WJ (1988) Carbohydrate responsive proteins in the roots of Pennisetum americanum. Plant Physiol 87:566–570
Bernier G (1988) Floral evocation and morphogenesis. Ann Rev Plant Physiol Plant Mol Biol 39: 175–219
Bingham IJ, Farrar JF (1988) Regulation of respiration in roots of barley. Physiol Plant 70: 491–498
Bodson M, Bernier G (1985) Is flowering controlled by the assimilate level? Physiol Veg 23: 491–501
Borland AM and Farrar JF (1989) The partitioning of photosynthetically fixed carbon in the leaf blade and leaf sheath of Poa pratensis L. J Exp Bot 40: 1247–1254
Cairns AJ (1989) Fructan biosynthesis in excised leaves of Lolium tenntlentum L. IV. Cell-free C labelling of specific oligofructans at low sucrose concentration. New Phytol 112: 465–473
Cairns AJ (1992) Fructan biosynthesis in excised leaves of Lolium temulentum L. V. Enzymatic de novo synthesis of large fructans from sucrose. New Phytol 122: 253–259
Cairns AJ and Pollock CJ (1988a) Fructan biosynthesis in excised leaves of Lolium temulentum L. I. Chromatographic characterisation of oligofructans and their labelling patterns following 14CO2 feeding. New Phytol 109: 399–405
Cairns AJ and Pollock CJ (1988b) Fructan biosynthesis in excised leaves of Lolium temulentum L. II. Changes in fructosyl transferase activity following excision and application of inhibitors of gene expression. New Phytol 109: 407–413
Cairns AJ, Winters A and Pollock, CJ (1989) Fructan biosynthesis in excised leaves of Lolium temulentum L. III. A comparison of the in vitroproperties of fructosyl transferase activities with the characteristics of in vivo fructan accumulation. New Phytol 112: 343–352
Carlson M (1987) Regulation of sugar utilisation in Saccharomyces species. J Bacteriol 169: 4873–4877
Catsky J, Tichá I and Solárová J (1976) Ontogenetic changes in the internal limitations to bean leaf photosynthesis. 1. Carbon dioxide exchange and conductances for carbon dioxide transfer. Photosynthetica 10: 394–402
Collis BE and Pollock CJ (1991) The control of sucrose synthesis in leaves of Lolium temulentum L., a fructan-accumulating grass. New Phytol 119: 483–489
Cote GL and Ahlgren JA (1993) Metabolism in micro-organisms Part 1. Levan and levansucrase. In: Suzuki M and Chatterton NJ (eds) Science and Technology of Fructans, pp. 141–168. CRC Press, Boca Raton
Couee I, Jan M. Carde J-P, Brouquisse R, Raymond P and Pradet A (1992) Effects of glucose starvation on mitochondrial subpopulations in the meristematic and submeristematic regions of maize root. Plant Physiol 100: 1891–1900
Crutz AM, Steinmetz M, Aymerich S, Richter R and Le Coq D (1990) Induction of levansucrase in Bacillus subtilis: an anti-termination mechanism negatively controlled by the phosphotransferase system. J. Bacteriol 172: 1043–1050
Delrot S (1989) Loading of photoassimilates In: Baker DA, Milburn JA (ed) Transport of Photoassimilates, pp 167–205. Longman, Harlow
Douce R, Bligny R, Brown D, Dorne A-J, Genix P, Roby C (1991) Autophagy triggered by sucrose deprivation in sycamore (Acer pseudoplatanus) cells. In: Emes MJ (ed) Compartmentation of Plant Metabolism in Non-photosynthetic Tissues, pp 127–146. Cambridge University Press, Cambridge
Erner Y (1989) Citrus fruit set: Carbohydrate, hormone and leaf mineral relationships. In: Wright CJ (ed) Manipulation of Fruiting, pp 233–242. Butterworths, London
Evans PS (1972) Root growth of Loliumperenne III. Investigation of the mechanisms of defoliation-induced suppression of elongation. NZ J Agricult Res 15: 347–355
Farrar JF (1981) Respiration rate of barley roots: Its relation to growth, substrate supply and the illumination of the shoot. Ann Bot 48: 53–63
Farrar JF (1985a) Fluxes of carbon in roots of barley plants. New Phytol 99: 57–69
Farrar JF (1985b) The respiratory source of CO2. Plant Cell Environ 8: 427–438
Farrar JF (1989) Fluxes and turnover of sucrose and fructans in healthy and diseased plants. J Plant Physiol 134: 137–140
Farrar JF (1992) The whole plant: carbon partitioning during development. In: Pollock CJ, Farrar JF and Gordon AJ (eds) Carbon Partitioning Within and Between Organisms, pp 163–179. Bios Scientific Publishers, Oxford
Farrar JF and Jones CL (1986) Modification of respiration and carbohydrate status of barley roots by selective pruning. New Phytol 102:513–521
Farrar JF and Williams JHH (1991a) Control of the rate of respiration in roots: compartmentation, demand and the supply of substrate. In Emes M (ed) Compartmentation of Plant Metabolism in Nono-photosynthetic Tissues, pp 167–188. Cambridge University Press, Cambridge
Farrar JF and Williams ML (1991b) The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source-sink relations and respiration. Plant Cell Environ 14: 819–830
Farrar JF, Minchin PEH and Thorpe MR (1994) Carbon import into barley roots: stimulation by galactose. J Exp Bot 45: 17–22
Farrar SC and Farrar JF (1985) Fluxes of carbon compounds in leaves and roots of barley plants. In Jeffcoat B, Hawkins AF, Stead AD (ed) Regulation of Sources and Sinks in Crop Plants, pp 67–84. British Plant Growth regulator Group, Bristol
Farrar SC and Farrar JF (1987) Effects of photon fluence rate on carbon partitioning in barley source leaves. Plant Physiol Biochem 25: 541–548
Foyer CH (1987) The basis of source-sink interactions in leaves. Plant Physiol Biochem 25: 649–657
Foyer CH (1988) Feedback inhibition of photosynthesis through source-sink regulation in leaves. Plant Physiol Biochem 26: 483–497
Gallie DR (1993) Post-transcriptional regulation of gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 44: 77–105
Gerhardt R and Heldt HW (1984) Measurement of subcellular metabolite levels in leaves by fractionation of freeze-stopped material in non-aqueous media. Plant Physiol 75: 542–547
Gordon AJ and Kessler W (1990) Defoliation-induced stress in nodules of white clover. II. Immunological and enzymic measurements of key proteins. J Exp Bot 41: 255–1262
Gordon AJ, Ryle GJA and Webb, G (1980) The relationship between sucrose and starch during ‘dark’ export from leaves of Uniculm barley. J Exp Bot 31: 845–850
Gordon AJ, Ryle GJA, Mitchell DF, Lowry KH and Powell CE (1986) The effect of defoliation on carbohydrate, protein and leghaemoglobin content of white clover nodules. Ann Bot 58: 141–154
Gordon AJ, Kessler W and Minchin FR (1990) Defoliation induced stress in nodules of white clover I Changes in physiological parameters and protein synthesis. J Exp Bot 41: 1245–1253
Gordon AJ, Ougham HJ and James CL (1993) Changes in levels of gene transcripts and their corresponding proteins in nodules of soybean plants subjected to dark-induced stress. J Exp Bot 44:1453–1460
Graham IA, Derby KJ and Leaver CJ (1994) Carbon catabolite repression regulates glyoxylate cycle gene expression in cucumber. Plant Cell 6: 761–772
Hemerly AS, Ferreira P, Engler Jde A, Montagu Mvan, Engler G and Inze D (1993) cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5: 1711–1723
Herold A (1980) Regulation of photosynthesis by sink activity-the missing link. New Phytol 86: 131–144
Herold A and McNeil PH (1979) Restoration of photosynthesis in pot-bound tobacco plants. J Exp Bot 30: 1187–1194
Hiem U, Weber H, Baumleim H and Wobus U (1993) A sucrose-synthase gene of Viciafaba L.: Expression pattern in developing seeds in relation to starch synthesis and metabolic regulation. Planta 191: 394–401
Ho LC (1978) The regulation of carbon transport and the carbon balance of mature tomato leaves. Ann Bot 42: 155–164
Ho LC (1988) Metabolism and compartmentation of sugars in sink organs. Ann Rev Plant Physiol Plant Mol Biol 39: 355–378
Ho LC and Thornley JHM (1978) Energy requirements for assimilate translocation from mature tomato leaves. Ann Bot 42: 481–483
Houssa S, Bernier G and Kinet JM (1991) Qualitative and quantitative analysis of carbohydrates in leaf exudate of the short-day-plantXanthium strumarium L. during floral transition. J Plant Physiol 138: 24–28
Housley TL and Pollock CJ (1985) Photosynthesis and carbohydrate metabolism in detached leaves of Lolium temulentum L. New Phytol 99: 499–507
Huber SC (1989) Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis. Plant Physiol 91: 656–662
Huber SC, Huber JLA and McMichael Jr RW (1992) The regulation of sucrose synthesis in leaves. In: Pollock CJ, Farrar JF and Gordon AJ (eds) Carbon Partitioning Within and Between Organisms, pp. 1–26. Bios Scientific Publishers, Oxford
Jang JC and Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6: 1665–1679
Jeffs RA and Northcote DH (1967) The influence of indol-3-yl acetic acid and sugar on the pattern of induced differentiation in plant tissue culture. J Cell Sci 2: 77–88
Kaiser G and Heber V (1984) Sucrose transport into vacuoles isolated from barley mesophy ll protoplasts. Planta 161: 562–568
Kholodova VP (1967) Localization of sucrose in tissues of the storage root of sugar beet. Fiziol Rast 14: 444–450
Koch KE, Nolte KD, Duke ER, McCarty DR and Avigne WT (1992) Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 4: 59–69
Krapp A, Hofmann B, Schäfer C and Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the’ sink regulation’ of photosynthesis? Plant J 3: 817–828
Labhart C, Nösberger J and Nelson CJ (1983) Photosynthesis and degree of polymerisation of fructan during reproductive growth of meadow fescue at two temperatures and two photon flux densities. J Exp Bot 34: 1037–1046
Lambers H (1985) Respiration in intact plants and tissues. In: Douce R, Day DA (ed) Encyclopedia of Plant physiology, Vol 18, pp 418–473. Springer, Berlin
Lambers H, van der Werf A and Konings H (1991) Respiratory patterns in roots in relation to their functioning. In: Waisel Y, Eshel A, Kafkafi U (ed) Plant Roots: The Hidden Half, pp 229–263. Dekker, New York
Liu XJ, Pratt S, Willmitzer L and Fromer WB (1990) Cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter/GUS-gene fusion. Mol Gen Genet 223: 401–406
Looney NE (1989) Effects of crop reduction, gibberellin sprays and summer pruning on vegetative growth, yield, and quality of sweet cherries. In: Wright CJ (ed) Manipulation of Fruiting, pp 39–50. Butterworths, London
Mae T, Thomas H, Gay AP, Makino A and Hidema J (1993) Leaf development in Lolium temulentum: Photosynthesis and photosynthetic proteins in leaves senescing under different irradiances. Plant Cell Physiol 34: 391–399
Martinoia E, Kaiser G, Schramm MJ and Heber U (1987) Sugar transport across the plasma lemma and tonoplast of barley meophyll protoplasts. J Plant Physiol 131: 467–478
McDaniel CN, King RW, Evans LT (1991) Floral determination and in-vitro floral differentiation in isolated shoot apices of Lolium temulentum L. Planta 185: 9–16
McDonnell E and Farrar JF (1992) Substrate supply and its effect on mitochondrial and whole-tissue respiration in barley roots. In: Lambers H and van der Plas L (ed) Molecular, Biochemical and Physiological Aspects of Plant Respiration, pp 455–62. SPB, The Hague
McKnight SL, Lane MD and Glueckshon-Waelsch S (1989) Is CCAAT/enhancer-binding protein a central regulator of energy metabolism? Genes Dev 3: 2021–2024
Minchin FR and Pate JS (1974) Diurnal fluctuating of the legume root nodule. J Exp Bot 25: 295–308
Minchin PEH, Farrar JF and Thorpe MR (1994) Partitioning in split root systems of barley: Effect of temperature of the root. JExpBot 45:1103–1109
Minchin PEH and McNaughton G (1984) Exudation of recently fixed carbon by non-sterile roots. J Exp Bot 35: 74–82
Minchin PEH, Thorpe MR and Farrar JF (1993) A simple mechanistic model of phloem transport which explains sink priority. J Exp Bot 44: 947–955
Moorby J and Jarman PD (1976) The use of compartmental analysis in the study of the movement of carbon through leaves. Planta 122: 155–168
Muller-Rober BT, Kossman J, Hannah LC, Willmitzer L, Sonnewald U (1991) ADPG-pyrophosphorylase genes from potato: Mode of RNA expression and its relation to starch synthesis. In: Bonnemain J-L (ed) Phloem Transport and Assimilate Compartmentation, pp 204–208. Ouest, Nantes
Natr L (1967) Time-course for photosynthesis and maximum figures for the accumulation of assimilates in barley leaf segments. Photosynthetica 1: 29–36
Neales TF and Incoll LD (1968) The control of leaf photosynthesis rate by the level of assimilate concentration in the leaf: a review of the hypothesis. Bot Rev 34: 107–124
Obenland DM, Simmen U, Boller T and Wiemken A (1991) Regulation of sucrose-sucrose-fructosyl transferase in barley leaves. Plant Physiol 97: 811–813
Passioura JB, Ashford AE (1974) Rapid translocation in the phloem of wheat roots. Aust J P1 Physiol 1: 521–527
Patrick JW (1990) Sieve-element unloading: cellular pathway, mechanism and control. Physiol Plant 78: 298–308
Penning de Vries FWT, Witlage JM and Kremer D (1979) Rates of respiration and of increase in structural dry matter in young wheat, ryegrass and maize plants in relation to temperature, water stress and to their sugar content. Ann Bot 44: 595–609
Pollock CJ (1986) Fructans and the metabolism of sucrose in vascular plants. New Phytol 104: 1–24
Pollock CJ and Cairns AJ (1991) Fructan metabolism in grasses and cereals. Ann Rev Plant Physiol Plant Mol Biol 42: 77–101
Pollock CJ and Housley TL (1993) The extraction and assay of 1 — kestose: Sucrose fructosyl transferase from leaves of wheat. Plant Physiol 102: 537–539
Pollock CJ, Cairns, AJ, Collis BE and Walker RP (1989) Direct effects of low temperature upon components of fructan metabolism in leaves of Lolium temulentum L. J Plant Physiol 134:203–208
Preiss J (1987) Biosynthesis of starch and its regulation. In: Preiss J (ed) Carbohydrates (The Biochemistry of Plants, Vol 14), pp 181–254. Academic Press, San Diego
Saglio PH, Pradet A (1980) Soluble sugars, respiration and energy charge during ageing of excised maize root tips. Plant Physiol 66: 516–519
Salanoubat M, Belliard G (1989) The steady-state level of potato sucrose synthase mRNA is dependent on wounding, anaerobiosis and sucrose. Gene 84: 181–185
Schäfer C, Simper H and Hofmann B (1992) Glucose feeding results in co-ordinated changes of chlorophyll content, ribulose-1,5-bisphosphate carboxylase-oxygenase activity and photosynthetic potential in photoautotropic suspension cultured cells of Chenopodium rubrum. Plant Cell Environ 15: 343–350
Schweitzer LE and Harper JE (1980) Effect of light, dark and temperature on root nodule activity of soyabeans. Plant Physiol 65: 51–56
Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2: 1027–1038
Sicher RC, Harris WG, Kremer DF and Chatterton NJ (1982) Effects of shortened day length upon translocation and starch accumulation by maize, wheat and pangola grass leaves. Can J Bot 60: 1304–1309
Simpson RJ, Walker RP and Pollock CJ (1991) Fructan exohydrolase activity in leaves of Lolium temulentum L. New Phytol 119:499–507
Smith H (1990) Introduction: Signal perception, differential expression within multigene families and the molecular basis of phenotypic plasticity. Plant Cell Environ. 13: 585–595
Steup M (1987) Starch degradation. In: Preiss J (ed) Carbohydrates. The Biochemistry of Plants, Vol 14. pp 255–296. Academic Press, San Diego
Stitt M (1990) Fructose-2,6-bisphosphate as a regulatory molecule in plants. Ann Rev Plant Physiol Plant Mol Biol 4l: 153–185
Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ. 14: 741–762
Stitt M, Kürzel B and Heldt HW (1984) Control of photosynthetic sucrose synthesis by fructose 2,6-bisphosphate. II. Partitioning between sucrose and starch. Plant Physiol 75: 554–560
Stitt M, Huber S and Kerr S (1987) Control of photosynthetic sucrose formation. In: Hatch MD and Boardman NK (eds) The Biochemistry of Plants, a Comprehensive Treatise, Vol 10, Photosynthesis, pp. 327–409. Academic Press, London
Stitt M, von Schaewen A and Willmitzer L (1990) ’sink’ regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in the cell wall involves a down-regulation of the Calvin cycle and an up-regulation of glycolysis. Planta 183: 40–50
Street HE (1969) Growth in organized and unorganized systems. In: Steward FC (ed) Plant Physiology VB, pp 3–223. Academic Press, New York
Swanson CA and Christy AL (1976) Control of translocation by photosynthesis and carbohydrate concentration of the source leaf. In: Wardlaw IF, Passioura JB (ed) Transport and Transfer Processes in Plants, pp 329–338. Academic Press, New York
Tetlow IJ and Farrar JF (1993) Apoplastic sugar concentration and pH in barley leaves infected with brown rust. J Exp Bot 44: 929–936
Thomas H (1984) Cell senescence and protein metabolism in the photosynthetic tissue of leaves. In: Davies I and Sigee DC (eds) Cell Ageing and Cell Death, pp. 171–188. Cambridge University Press, Cambridge
Thorne JH and Koller HR (1974) Influence of assimilate demand on photosynthesis, diffusive resistance, translocation and carbohydrate levels of soybean leaves. Plant Physiol 54: 201–207
Tomos AD, Leigh RA, Palta, JA and Williams JHH (1992) Sucrose and cell water relations. In: Pollock CJ, Farrar JF and Gordon AJ (eds) Carbon Partitioning Within and Between Organisms, pp 71–89. Bios Scientific Publishers, Oxford
Trewavas A (1991) How do plant growth substances work? II: Opinion. Plant Cell Environ. 14: 1–12
van Bel AJE (1992) Pathways and mechanisms of phloem loading. In: Pollock CJ, Farrar JF, Gordon AJ (ed) Carbon Partitioning, pp 53–70. Bios Scientific Publishers, Oxford
van’t Hof J (1985) Control points within the cell cycle. In: Bryant J A, Francis D (ed) The Cell Division Cycle in Plants, pp 1–13. Cambridge University Press, Cambridge
van’t Hof J, Hoppin DP, Yagi S (1973) Cell arrest in G1 and G2 of the mitotic cycle of Vicia faba root meristems. Am J Bot 60: 889–895
von Schaewen A, Stitt M, Schmidt R, Sonnewald U and Willmitzer L (I990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J 9: 3033–3044
Wagner W, Wiemken A and Matile P (1986) Regulation of fructan metabolism in leaves of barley (Hordeum vulgare L. cv. Gerbel). Plant Physiol 81: 444–447
Wetmore RH and Rier JP (1963) Experimental induction of vascular tissues in callus of angiosperms. Am J Bot 50, 418–430
Williams JHH and Farrar JF (1987) Endogenous control of photosynthesis in leaf blades ofbarley. Plant Physiol Biochem. 26:503–509
Williams JHH and Farrar JF (1990) Control of barley root respiration. Physiol Plant 79: 259–266
Williams JHH, Farrar JF and Minchin PEH (1991) Carbon partitioning in split root systems of barley: Effect of osmotica. J Exp Bot 42: 453–460
Williams JHH, Winters AL and Farrar JF (1992) Sucrose: A novel plant growth regulator. In: Lambers H, van der Plas LHW (ed) Molecular, Biochemical and Physiological Aspects of Plant Respiration, pp 463–469. SPB, The Hague
Williams M, Farrar J and Pollock CJ (1989) Cell specialization within the parenchymatous bundle sheath ofbarley. Plant Cell Environ. 12:909–918
Worrell AC, Bruneau J, Summerfelt K, Boersig M and Voelker TA (1991) Expression of a maize sucrose phosphate synthase in tomato alters leaf carbohydrate partitioning. Plant Cell 3: 1121–1130
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Pollock, C.J., Farrar, J.F. (1996). Source-Sink Relations: The Role of Sucrose. In: Baker, N.R. (eds) Photosynthesis and the Environment. Advances in Photosynthesis and Respiration, vol 5. Springer, Dordrecht. https://doi.org/10.1007/0-306-48135-9_10
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DOI: https://doi.org/10.1007/0-306-48135-9_10
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