Dynamic 13C/1H NMR imaging uncovers sugar allocation in the living seed

Plant Biotechnology Journal

Volumn 9, Issue 9, 2011, Pages 1022-1037

  Melkus, Gerd ^a,b,c   Rolletschek, Hardy ^b   Fuchs, Johannes ^a,b   Radchuk, Volodymyr ^b   Grafahrend Belau, Eva ^b   Sreenivasulu, Nese ^b   Rutten, Twan ^b   Weier, Diana ^b   Heinzel, Nicolas ^b   Schreiber, Falk ^b   Altmann, Thomas ^b   Jakob, Peter M ^a   Borisjuk, Ljudmilla ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Barley; FBA; NMR; Seed filling; Sucrose allocation; Transcriptome

Indexed keywords

HORDEUM; HORDEUM VULGARE SUBSP. VULGARE;

CARBON; SUCROSE;

ARTICLE; CARBOHYDRATE METABOLISM; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORDEUM; IMAGE PROCESSING; INSTRUMENTATION; ISOTOPE LABELING; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLANT GENE; PLANT SEED; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CARBOHYDRATE METABOLISM; CARBON ISOTOPES; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HORDEUM; IMAGE PROCESSING, COMPUTER-ASSISTED; ISOTOPE LABELING; MAGNETIC RESONANCE SPECTROSCOPY; SEEDS; SUCROSE;

EID: 80053207269     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2011.00618.x     Document Type: Article

References (88)

1. Babst, B.A., Ferrieri, R.A., Gray, D.W., Lerdau, M., Schlyer, D.J., Schueller, M., Thorpe, M.R. and Orians, C.M. (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol. 167, 63-72.
2. Baud, S., Wuilleme, S., Lemoine, R., Kronenberger, J., Caboche, M., Lepiniec, L. and Rochat, C. (2005) The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Plant J. 43, 824-836.
3. Bewley, D.J., Black, M. and Halmer, P. (eds.) (2006) The Encyclopedia of Seeds: Science, Technology and Uses. Wallingford: CABI. P. 828.
4. Bolstad, B.M., Irizarry, R.A., Astrand, M. and Speed, T.P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics, 19, 185-193.
5. Braun, D.M. and Slewinski, T.L. (2009) Genetic control of carbon partitioning in grasses: roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiol. 149, 71-81.
6. Carpaneto, A., Geiger, D., Bamberg, E., Sauer, N., Fromm, J. and Hedrich, R. (2005) Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. J. Biol. Chem. 280, 21437-21443.
7. Chen, F. and Foolad, M.R. (1997) Molecular organization of a gene in barley which encodes a protein similar to aspartic protease and its specific expression in nucellar cells during degeneration. Plant Mol. Biol. 35, 821-831.
8. Chiou, T.J. and Bush, D.R. (1998) Sucrose is a signal molecule in assimilate partitioning. Proc. Natl Acad. Sci. USA 95, 4784-4788.
9. Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., Giakountis, A., Farrona, S., Gissot, L., Turnbull, C. and Coupland, G. (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science, 316, 1030-1033.
10. Di Ventura, B., Lemerle, C., Michalodimitrakis, K. and Serrano, L. (2006) From in vivo to in silico biology and back. Nature, 443, 527-533.
11. Domínguez, F., Moreno, J. and Cejudo, F.J. (2001) The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development. Planta, 213, 352-360.
12. Endler, A., Meyer, S., Schelbert, S., Schneider, T., Weschke, W., Peters, S.W., Keller, F., Baginsky, S., Martinoia, E. and Schmidt, U.G. (2006) Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 141, 196-207.
13. Ekman, Å.M., Hayden, D., Dehesh, K., Bülow, L. and Stymne, S. (2008) Carbon partitioning between oil and carbohydrates in developing oat (Avena sativa L.) seeds. J. Exp. Bot. 59, 4247-4257.
14. 14C] Sucrose uptake and labeling of starch in developing grains of normal and seg1 barley. Plant Physiol. 74, 43-46.
15. Fisher, D.B. and Cash-Clark, C.E. (2000) Sieve tube unloading and post-phloem transport of fluorescent tracers and proteins injected into sieve tubes via severed aphid stylets. Plant Physiol. 123, 125-138.
16. Fisher, D.B. and Gifford, R.M. (1986) Accumulation and conversion of sugars by developing wheat grains: VI. Gradients along the transport pathway from the peduncle to the endosperm cavity during grain filling. Plant Physiol. 82, 1024-1030.
17. Friis, E.M., Crane, P.R., Pedersen, K.R., Bengtson, S., Donoghue, P.C.J., Grimm, G.W. and Stampanoni, M. (2007) Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature, 450, 549-552.
18. Frommer, W.B. and Sonnewald, U. (2010) Progress in physiological research and its relevance for agriculture and ecology. Curr. Opin. Plant Biol. 13, 227-232.
19. Frommer, W.B., Davidson, M.W. and Campbell, R.E. (2009) Genetically encoded biosensors based on engineered fluorescent proteins. Chem. Soc. Rev. 38, 2833-2841.
20. Furbank, R.T., Scofield, G.N., Hirose, T., Wang, X.D., Patrick, J.W. and Offler, C.E. (2001) Cellular localisation and function of a sucrose transporter OsSUT1 developing rice grains. Aust. J. Plant. Physiol. 28, 1187-1196.
21. Gomez, E., Royo, J., Muniz, L.M., Sellam, O., Paul, W., Gerentes, D., Barrero, C., Lopez, M., Perez, P. and Hueros, G. (2009) The maize transcription factor Myb-related protein-1 is a key regulator of the differentiation of transfer cells. Plant Cell, 21, 2022-2035.
22. Grafahrend-Belau, E., Schreiber, F., Koschützki, D. and Junker, B.H. (2009a) Flux balance analysis of barley seeds: a computational approach to study systemic properties of central metabolism. Plant Physiol. 149, 585-598.
23. Grafahrend-Belau, E., Klukas, C., Junker, B.H. and Schreiber, F. (2009b) FBA-SimVis: interactive visualization of constraint-based metabolic models. Bioinformatics, 25, 2755-2757.
24. 13C NMR spectroscopy of the brain. NMR Biomed. 16, 313-338.
25. Hatsugai, N., Kuroyanagi, M., Nishimura, M. and Hara-Nishimura, I. (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis, 11, 905-911.
26. Haywood, V., Yu, T.S., Huang, N.C. and Lucas, W.J. (2005) Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant J. 42, 49-68.
27. Heidenreich, M., Koeckenberger, W., Kimmich, R., Chandrakumara, N. and Bowtell, R. (1998) Investigation of carbohydrate metabolism and transport in castor bean seedlings by cyclic J cross polarization imaging and spectroscopy. J. Magn. Reson. 132, 109-124.
28. Heim, U., Weber, H., Bäumlein, H. and Wobus, U. (1993) A sucrose synthase gene of Vicia faba L.: expression pattern in developing seeds in relation to starch synthesis and metabolic regulation. Planta, 191, 394-401.
29. Hoad, G.V. (2004) Transport of hormones in the phloem of higher plants. Plant Growth Regul. 16, 173-182.
30. Hurd, R.E. and John, B.K. (1991) Gradient-enhanced proton-detected heteronuclear multiple-quantum coherence spectroscopy. Magn. Reson. 92, 658.
31. Ischida, N., Koizumi, M. and Kano, H. (2000) The NMR microscope: a unique and promising tool for plant science. Ann. Bot. (Lond.) 86, 259-278.
32. Ishimaru, K., Hirose, T., Aoki, N., Takahashi, S., Ono, K., Yamamoto, S., Wu, J., Saji, S., Baba, T., Ugaki, M., Matsumoto, T. and Ohsugi, R. (2001) Antisense expression of a rice sucrose transporter OsSUT1 in rice (Oryza sativa L.). Plant Cell Physiol. 42, 1181-1185.
33. Jahnke, S., Menzel, M.I., Van Dusschoten, D., Roeb, G.W., Bühler, J., Minwuyelet, S., Blümler, P., Temperton, V.M., Hombach, T., Streun, M., Beer, S., Khodaverdi, M., Ziemons, K., Coenen, H.H. and Schurr, U. (2009) Combined MRI-PET dissects dynamic changes in plant structures and functions. Plant J. 59, 634-644.
34. Jenner, C.F., Xia, Y., Eccles, C.D. and Callaghan, P.T. (1988) Circulation of water within wheat grain revealed by nuclear magnetic resonance micro-imaging. Nature, 336, 399-402.
35. 13C-nuclear magnetic resonance spectroscopy in vivo. Planta, 208, 358-364.
36. Kehr, J. and Buhtz, A. (2008) Long-distance transport and movement of RNA through the phloem. J Exp Bot 59, 85-92.
37. Kladnik, A., Chamusco, K., Dermastia, M. and Chourey, P. (2004) Evidence of programmed cell death in post-phloem transport cells of the maternal pedicel tissue in developing caryopsis of maize. Plant Physiol. 136, 3572-3581.
38. Koch, K.E. (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7, 235-246.
39. Koeckenberger, W., De Panfilis, C., Santoro, D., Dahiya, P. and Rawsthorne, S. (2004) High resolution NMR microscopy of plants and fungi. J. Microsc. 214, 182-189.
40. Kühn, C. and Grof, C.P.L. (2010) Sucrose transporters of higher plants. Curr. Opin. Plant Biol. 13, 287-297.
41. Lalonde, S., Wipf, D. and Frommer, W.B. (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu. Rev. Plant Biol. 55, 341-372.
42. Lim, J.D., Cho, J.I., Park, Y., Hahn, T., Choi, S. and Jeon, J. (2006) Sucrose transport from source to sink in rice seeds. Physiol. Plant. 126, 572-584.
43. Lough, T.J. and Lucas, W.J. (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu. Rev. Plant Biol. 57, 203-232.
44. Marcelis, L.F.M. (1996) Sink strength as a determinant of dry matter partitioning in the whole plant. J Exp Bot 47, 1281-1291.
45. Matsukura, C., Saitoh, T., Hirose, T., Ohsugi, R., Perata, P. and Yamaguchi, J. (2000) Sugar uptake and transport in rice embryo. Expression of companion cell-specific sucrose transporter (OsSUT1) induced by sugar and light. Plant Physiol. 124, 85-93.
46. Matsuo, T. and Hoshikawa, K. (1993) Science of the Rice Plant. Morphology, Tokyo: Japanese Ministry of Agriculture, Forestry and Fisheries.
47. McCurdy, D.W., Patrick, J.W. and Offler, C.E. (2008) Wall ingrowth formation in transfer cells: novel examples of localized wall deposition in plant cells. Curr. Opin. Plant Biol. 11, 653-661.
48. Melkus, G., Rolletschek, H., Radchuk, R., Fuchs, J., Rutten, T., Wobus, U., Altmann, T., Jakob, P. and Borisjuk, L. (2009) The metabolic role of legume endosperm: a non-invasive imaging study. Plant Physiol. 151, 1139-1154.
49. Metzler, A., Izquierdo, M., Ziegler, A., Koeckenberger, W., Komor, E., von Kienlin, M., Haase, A. and Decorps, M. (1995) Plant histochemistry by correlation peak imaging. Proc. Natl Acad. Sci. USA 92, 11912-11915.
50. Minchin, P. and Thorpe, M. (1996) What determines carbon partitioning between competing sinks? J Exp Bot 47, 1293-1296.
51. 11C in mechanistic studies of photosynthate transport. Funct. Plant Biol. 30, 831-841.
52. Mullendore, D.l., Carel, L., Windt, C.W., Van As, H. and Knoblauch, M.l. (2010) Sieve tube geometry in relation to phloem flow. Plant Cell, 22, 579-593.
53. Niittylae, T., Chaudhuri, B., Sauer, U. and Frommer, W.B. (2009) Comparison of quantitative metabolite imaging tools and carbon-13 techniques for fluxomics. Methods Mol. Biol. 553, 355-372.
54. Offler, C.E., McCurdy, D.W., Patrick, J.W. and Talbot, M.J. (2002) Transfer cells: cells specialized for a special purpose. Annu. Rev. Plant Biol. 54, 431-454.
55. Patrick, J.W. and Offler, C.E. (2001) Compartmentation of transport and transfer events in developing seeds. J Exp Bot 52, 551-564.
56. Patron, N.J., Greber, B., Fahy, B.F., Laurie, D.A., Parker, M.L. and Denyer, K. (2004) The lys5 mutations of barley reveal the nature and importance of plastidial ADP-Glc transporters for starch synthesis in cereal endosperm. Plant Physiol. 135, 2088-2097.
57. Phelps, M.E. (ed.) (2004) PET: Molecular Imaging and its Biological Application. NY: Springer.
58. Phelps, M.E., Hoffman, E.J., Huang, S.C. and Ter Pogossian, M.M. (1975) Effect of positron range on spatial resolution. J. Nucl. Med. 16, 649-652.
59. Radchuk, V., Borisjuk, L., Radchuk, R., Steinbiss, H.H., Rolletschek, H., Broeders, S. and Wobus, U. (2006) Jekyll encodes a novel protein involved in the sexual reproduction of barley. Plant Cell, 18, 1652-1666.
60. Radchuk, V., Weier, D., Radchuk, R., Weschke, W. and Weber, H. (2010) Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth. J Exp Bot 63, 1217-1227.
61. Ramage, R.T. and Crandall, C.R. (1981) Shrunken endosperm mutant seg8. Barley Genet. Newslett. 11, 34.
62. Ratcliffe, R.G., Roscher, A. and Shachar-Hill, Y. (2001) Plant NMR spectroscopy. Prog. Nucl. Mag. Res. Sp. 39, 267-300.
63. Roberts, J.K.M. (2000) NMR adventures in the metabolic labyrinth within plants. Trends Plant Sci. 5, 30-34.
64. Rolland, F., Baena-Gonzalez, E. and Sheen, J. (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675-709.
65. Rolletschek, H., Weschke, W., Weber, H., Wobus, U. and Borisjuk, L. (2004) Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grain. J Exp Bot 55, 1351-1359.
66. Rolletschek, H., Koch, K., Wobus, U. and Borisjuk, L. (2005) Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. Plant J. 42, 69-83.
67. Royo, J., Gomez, E. and Hueros, G. (2007) Transfer cells. In Plant Cell Monographs (Olsen, O.A., ed), pp. 73-89, Berlin-Heidelberg: Springer.
68. Schwachtje, J., Minchin, P.E.H., Jahnke, S., van Dongen, J.T., Schittko, U. and Baldwin, I.T. (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl Acad. Sci. USA 103, 12935-12940.
69. Scofield, G.N., Hirose, T., Gaudron, J.A., Upadhyaya, N.M., Ohsugi, R. and Furbank, R.T. (2002) Antisense suppression of the rice sucrose transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis. Funct. Plant Biol. 29, 815-826.
70. Sivitz, A.B., Reinders, A. and Ward, J.M. (2005) Analysis of the transport activity of barley sucrose transporter HvSUT1. Plant Cell Physiol. 46, 1666-1673.
71. Sreenivasulu, N., Radchuk, V., Strickert, M., Miersch, O., Weschke, W. and Wobus, U. (2006) Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA-regulated maturation in developing barley seeds. Plant J. 47, 310-327.
72. Sreenivasulu, N., Borisjuk, L., Junker, B.H., Mock, H.P., Rolletschek, H., Seiffert, U., Weschke, W. and Wobus, U. (2010a) Barley grain development: toward an integrative view. Int. Rev. Cell. Mol. Biol. 281, 49-89.
73. Sreenivasulu, N., Radchuk, V., Alawady, A., Borisjuk, L., Weier, D., Staroske, N., Fuchs, J., Miersch, O., Strickert, M., Usadel, B., Wobus, U., Grimm, B., Weber, H. and Weschke, W. (2010b) Deregulation of abscisic acid contents causes abnormal endosperm development in the barley mutant seg8. Plant J. 64, 589-603.
74. Stadler, R., Lauterbach, C. and Sauer, N. (2005) Cell-to-cell movement of GFP reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol. 139, 701-712.
75. Szimtenings, M., Olt, S. and Haase, A. (2003) Flow encoded NMR spectroscopy for quantification of metabolite flow in intact plants. J. Magn. Reson. 161, 70-76.
76. Thompson, R.D., Hueros, G., Becker, H.A. and Maitz, M. (2001) Development and functions of seed transfer cells. Plant Sci. 160, 775-783.
77. 1H NMR spectroscopy of rat brain at 1ms echo time. Magn. Reson. Med. 41, 649-656.
78. Tse, T.Y., Spanswick, R.M. and Jelinski, L.W. (1996) Quantitative evaluation of NMR and MRI methods to measure sucrose concentrations in plants. Protoplasma, 194, 54-62.
79. Van As, H. (2007) Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport. J Exp Bot 58, 743-756.
80. Van As, H. and Schaafsma, T.J. (1984) Noninvasive measurement of plant water flow by nuclear magnetic resonance. Biophys. J. 45, 469-472.
81. Verscht, J., Kalusche, B., Köhler, J., Koeckenberger, W., Metzler, A., Haase, A. and Komor, E. (1998) The kinetics of sucrose concentration in the phloem of individual vascular bundles of the Ricinus communis seedling measured by nuclear magnetic resonance microimaging. Planta, 205, 132-139.
82. Wang, H.L., Offler, C.E., Patrick, J.W. and Ugalde, T.D. (1994) Cellular pathway of photosynthate transfer in the developing wheat grain. I. Delineation of the potential transfer pathway using fluorescent dyes. Plant Cell Environ. 17, 257-266.
83. Weber, H., Borisjuk, L., Heim, U., Sauer, N. and Wobus, U. (1997) A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds. Plant Cell, 9, 895-908.
84. Weschke, W., Panitz, R., Sauer, N., Wang, Q., Neubohn, B., Weber, H. and Wobus, U. (2000) Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. Plant J. 21, 455-467.
85. Weschke, W., Panitz, R., Gubatz, S., Wang, Q., Radchuk, R., Weber, H. and Wobus, U. (2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J. 33, 395-411.
86. Williams, T.C.R., Miguet, L., Masakapalli, S.K., Kruger, N.J., Sweetlove, L.J. and Ratcliffe, R.G. (2008) Metabolic network fluxes in heterotrophic Arabidopsis cells: stability of the flux distribution under different oxygenation conditions. Plant Physiol. 148, 704-718.
87. Zhang, J., Nallamilli, B.R., Mujahid, H. and Peng, Z. (2010) OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J. 64, 604-617.
88. Zhou, Y., Chan, K., Wang, T., Hedley, C., Offler, C.E. and Patrick, J. (2009) Intracellular sucrose communicates metabolic demand to sucrose transporters in developing pea cotyledons. J Exp Bot 60, 71-85.