[en] We studied the influence of the internal oxygen concentration in seeds of wheat (Triticum aestivum) on storage metabolism and its relation to phloem import of nutrients. Wheat seeds that were developing at ambient oxygen (21%) were found to be hypoxic (2.1%). Altering the oxygen supply by decreasing or increasing the external oxygen concentration induced parallel changes in the internal oxygen tension. However, the decrease in internal concentration was proportionally less than the reduction in external oxygen. This indicates that decreasing the oxygen supply induces short-term adaptive responses to reduce oxygen consumption of the seeds. When external oxygen was decreased to 8%, internal oxygen decreased to approximately 0.5% leading to a decrease in energy production via respiration. Conversely, increasing the external oxygen concentration above ambient levels increased the oxygen content as well as the energy status of the seeds, indicating that under normal conditions the oxygen supply is strongly limiting for energy metabolism in developing wheat seeds. The intermediate metabolites of seed storage metabolism were not substantially affected when oxygen was either increased or decreased. However, at subambient external oxygen concentrations (8%) the metabolic flux of carbon into starch and protein, measured by injecting (14)C-Suc into the seeds, was reduced by 17% and 32%, respectively, whereas no significant effect was observed at superambient (40%) oxygen. The observed decrease in biosynthetic fluxes to storage compounds is suggested to be part of an adaptive response to reduce energy consumption preventing excessive oxygen consumption when oxygen supply is limited. Phloem transport toward ears exposed to low (8%) oxygen was significantly reduced within 1 h, whereas exposing ears to elevated oxygen (40%) had no significant effect. This contrasts with the situation where the distribution of assimilates has been modified by removing the lower source leaves from the plant, resulting in less assimilates transported to the ear in favor of transport to the lower parts of the plant. Under these conditions, with two strongly competing sinks, elevated oxygen (40%) did lead to a strong increase in phloem transport to the ear. The results show that sink metabolism is affected by the prevailing low oxygen concentrations in developing wheat seeds, determining the import rate of assimilates via the phloem.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
van Dongen, Joost T
Roeb, Gerhard W
Dautzenberg, Marco
Froehlich, Anja
Vigeolas, Hélène ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Minchin, Peter E H
Geigenberger, Peter
Language :
English
Title :
Phloem import and storage metabolism are highly coordinated by the low oxygen concentrations within developing wheat seeds.
Publication date :
2004
Journal title :
Plant Physiology
ISSN :
0032-0889
eISSN :
1532-2548
Publisher :
American Society of Plant Biologists, Rockville, United States - Maryland
Aoki N, Whitfield P, Hoeren F, Scofield G, Newell K, Patrick J, Offler C, Clarke B, Rahman S, Furbank RT (2002) Three sucrose transporter genes are expressed in the developing grain of hexaploid wheat. Plant Mol Biol 50: 453-462
Atkinson DE (1977) Cellular Energy Metabolism and Its Regulation. Academic Press, NY
Bagnall N, Wang XD, Scofield GN, Furbank RT, Offler CE, Patrick JW (2000) Sucrose transport-related genes are expressed in both maternal and filial tissues of developing wheat grains. Aust J Plant Physiol 27: 1009-1020
Bechtel DB (1989) How the structure of the wheat caryopsis could be modified to increase its end-use value. In Y Pomeranz, ed, Wheat is Unique. Structure, Composition, Processing, End-use Properties, and Products. American Association of Cereal Chemists, St. Paul, pp 71-84
Bologa KL, Fernie AR, Leisse A, Loureiro ME, Geigenberger P (2003) A bypass of sucrose synthase leads to low internal oxygen and impaired metabolic performance in growing potato tubers. Plant Physiol 132: 2058-2072
Borisjuk L, Rolletschek H, Walenta S, Panitz R, Wobus U, Weber H (2003) Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity. Plant J 36: 318-329
Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD
de Jong A, Borstlap AC (2000) Transport of amino acids (L-valine, L-lysine, L-glutamic acid) and sucrose into plasma membrane vesicles isolated from cotyledons of developing pea seeds. J Exp Bot 51: 1663-1670
de Jong A, Koerselman-Kooij JW, Schuurmans JAMJ, Borstlap AC (1996) Characterization of the uptake of sucrose and glucose by isolated seed coat halves of developing pea seeds. Evidence that a sugar facilitator with diffusional kinetics is involved in seed coat unloading. Planta 199: 486-492
de Jong A, Koerselman-Kooij JW, Schuurmans JAMJ, Borstlap AC (1997) The mechanism of amino acid efflux from seed coats of developing pea seeds as revealed by uptake experiments. Plant Physiol 114: 731-736
Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48: 223-250
Fader GM, Koller HR (1985) Seed growth rate and carbohydrate pool sizes of the soybean fruit. Plant Physiol 79: 663-666
Farrar JF (1996) Sinks - integral parts of a whole plant. J Exp Bot 47: 1273-1279
Gaines RL, Bechtel DB, Pomeranz Y (1985) Endosperm structural and biochemical differences between a high-protein amphiploid wheat and its progenitors. Cereal Chem 62: 25-31
Geigenberger P (2003a) Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot 54: 457-465
Geigenberger P (2003b) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6: 247-256
Geigenberger P, Fernie AR, Gibon Y, Christ M, Stitt M (2000) Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol Chem 381: 723-740
Geigenberger P, Hajirezaei M, Geiger M, Deiting U, Sonnewald U, Stitt M (1998) Overexpression of pyrophosphatase leads to increased sucrose degradation and starch synthesis, increased activities of enzymes for sucrose-starch interconversions, and increased levels of nucleotides in growing potato tubers. Planta 205: 428-437
Geigenberger P, Reimholz R, Geiger M, Merlo L, Canale V, Stitt M (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta 201: 502-518
Gibon Y, Vigeolas H, Tiessen A, Geigenberger P, Stitt M (2002) Sensitive and high throughput metabolite assays for inorganic pyrophosphate, adpglc, nucleotide phosphates, and glycolytic intermediates based on a novel enzymic cycling system. Plant J 30: 221-235
Gifford RM, Bremner PM (1981) Accumulation and conversion of sugars by developing wheat grains. 2. Light requirement for kernels cultured in vitro. Aust J Plant Physiol 8: 631-640
James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6: 215-222
Jelitto T, Sonnewald U, Willmitzer L, Hajirezeai M, Stitt M (1992) Inorganic pyrophosphate content and metabolites in potato and tobacco plants expressing Escherichia coli pyrophosphatase in their cytosol. Planta 188: 238-244
Kuang A, Crispi M, Musgrave ME (1998) Control of seed development in Arabidopsis thaliana by atmospheric oxygen. Plant Cell Environ 21: 71-78
Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant Cell Environ 26: 37-56
Minchin PEH, Thorpe MR (1996) What determines carbon partitioning between competing sinks? J Exp Bot 47: 1293-1296
Münch E (1930) Die stoffbewegungen in der pflanze. Gustav Fisher, Jena, Germany
Okumoto S, Schmidt R, Tegeder M, Fischer WN, Rentsch D, Frommer WB, Koch W (2002) High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J Biol Chem 277: 45338-45346
Patrick JW, Offler CE (2001) Compartmentation of transport and transfer events in developing seeds. J Exp Bot 52: 551-564
Pickard WF, Minchin PEH, Troughton JH (1978) Real-time studies of U-C translocation in moonflower. 1. Effects of cold blocks. J Exp Bot 29: 993-1001
Pomeranz Y, Shellenberg JA (1961) Histochemical characterization of wheat and wheat products. II. Mapping of protein distribution in the wheat kernel. Cereal Chem 38: 109-113
Porterfield DM, Kuang AX, Smith PJS, Crispi ML, Musgrave ME (1999) Oxygen-depleted zones inside reproductive structures of brassicaceae: implications for oxygen control of seed development. Can J Bot 77: 1439-1446
Roeb G, Britz SJ (1991) Short-term fluctuations in the transport of assimilates to the ear of wheat measured with steady-state C-11 CO 2-labeling of the flag leaf. J Exp Bot 42: 469-475
Rolletschek H, Borisjuk L, Koschorreck M, Wobus U, Weber H (2002) Legume embryos develop in a hypoxic environment. J Exp Bot 53: 1099-1107
Rolletschek H, Weber H, Borisjuk L (2003) Energy status and its control on embryogenesis of legumes. Embryo photosynthesis contributes to oxygen supply and is coupled to biosynthetic fluxes. Plant Physiol 132: 1196-1206
Rolletschek H, Weschke W, Weber H, Wobus U, Borisjuk L Energy state and ist control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains. J Exp Bot (in press)
Tegeder M, Offler CE, Frommer WB, Patrick JW (2000) Amino acid transporters are localized to transfer cells of developing pea seeds. Plant Physiol 122: 319-325
van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26: 125-149
van Dongen JT, Laan RGW, Wouterlood M, Borstlap AC (2001) Electro-diffusional uptake of organic cations by pea seed coats. Further evidence for poorly selective pores in the plasma membrane of seed coat parenchyma cells. Plant Physiol 126: 1688-1697
van Dongen JT, Schurr U, Pfister M, Geigenberger P (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 131: 1529-1543
Vigeolas H, van Dongen JT, Waldeck P, Huhn D, Geigenberger P (2003) Lipid storage metabolism is limited by the prevailing low oxygen concentrations within developing seeds of oilseed rape. Plant Physiol 133: 2048-2060
Wang HL, Offler CE, Patrick JW, Ugalde TD (1994) The cellular pathway of photosynthate transfer in the developing wheat-grain. 1. Delineation of a potential transfer pathway using fluorescent dyes. Plant Cell Environ 17: 257-266
Wang N, Fisher DB (1995) Sucrose release into the endosperm cavity of wheat grains apparently occurs by facilitated diffusion across the nucellar cell-membranes. Plant Physiol 109: 579-585
Wardlaw IF (1965) Velocity and pattern of assimilate translocation in wheat plants during grain development. Aust J Biol Sci 18: 269-281
