Carbon conversion efficiency and central metabolic fluxes in developing sunflower (Helianthus annuus L.) embryos

Plant Journal

Volumn 52, Issue 2, 2007, Pages 296-308

  Alonso, Ana P ^a,c   Goffman, Fernando D ^b,c   Ohlrogge, John B ^c   Shachar Hill, Yair ^c  

^a UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

^b PHILIP MORRIS PRODUCTS S A   (Switzerland)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Carbon conversion efficiency; Fatty acid synthesis; Isotopic labeling; Metabolic flux analysis; Oilseed filling; Sunflower embryo

Indexed keywords

BIOCONVERSION; BIOMASS; CARBON MONOXIDE; CELL CULTURE; METABOLISM; SEED; SUBSTRATES;

CARBON CONVERSION EFFICIENCY; ISOTOPIC LABELING; METABOLIC FLUX ANALYSIS; OILSEED FILLING; SUNFLOWER EMBRYO;

PLANTS (BOTANY);

CARBON; FATTY ACID; VEGETABLE OIL;

ARTICLE; BIOSYNTHESIS; METABOLISM; PLANT SEED; PRENATAL DEVELOPMENT; STAINING; SUNFLOWER; TISSUE CULTURE TECHNIQUE;

CARBON; CARBON RADIOISOTOPES; FATTY ACIDS; HELIANTHUS; PLANT OILS; SEEDS; STAINING AND LABELING; TISSUE CULTURE TECHNIQUES;

BRASSICA NAPUS; HELIANTHUS; HELIANTHUS ANNUUS;

EID: 35148880253     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03235.x     Document Type: Article

References (52)

1. Alonso, A.P., Vigeolas, H., Raymond, P., Rolin, D. Dieuaide-Noubhani, M. (2005) A new substrate cycle in plants. evidence for a high glucose-phosphate- to-glucose turnover from in vivo steady-state and pulse-labeling experiments with [C-13] glucose and [C-14] glucose. Plant Physiol. 138, 2220 2232.
2. Bao, X., Focke, M., Pollard, M. Ohlrogge, J. (2000) Understanding in vivo carbon precursor supply for fatty acid synthesis in leaf tissue. Plant J. 22, 39 50.
3. Ben, C., Hewezi, T., Jardinaud, M., Bena, F., Ladouce, N., Moretti, S., Tamborindeguy, C., Liboz, T., Petitprez, M. Gentzbittel, L. (2005) Comparative analysis of early embryonic sunflower cDNA libraries. Plant Mol. Biol. 57, 255 270.
4. Bradford, M.M. (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72, 248 254.
5. Browse, J. Slack, C.R. (1985) Fatty-acid synthesis in plastids from maturing safflower and linseed cotyledons. Planta, 166, 74 80.
6. Converti, A. Perego, P. (2002) Use of carbon and energy balances in the study of the anaerobic metabolism of Enterobacter aerogenes at variable starting glucose concentrations. Appl. Microbiol. Biotechnol. 59, 303 309.
7. Dieuaide-Noubhani, M., Raffard, G., Canioni, P., Pradet, A. Raymond, P. (1995) Quantification of compartmented metabolic fluxes in maize root tips using isotope distribution from 13C- or 14C-labeled glucose. J. Biol. Chem. 270, 13147 13159.
8. Eastmond, P.J. Rawsthorne, S. (2000) Coordinate changes in carbon partitioning and plastidial metabolism during the development of oilseed rape embryo. Plant Physiol. 122, 767 774.
9. Flinn, A.M., Atkins, C.A. Pate, J.S. (1977) Significance of photosynthetic and respiratory exchanges in carbon economy of developing pea fruit. Plant Physiol. 60, 412 418.
10. Garcia-Diaz, M.T., Martinez-Rivas, J.M. Mancha, M. (2002) Temperature and oxygen regulation of oleate desaturation in developing sunflower (Helianthus annuus) seeds. Physiol. Plant. 114, 13 20.
11. Giege, P., Heazlewood, J.L., Roessner-Tunali, U., Millar, A.H., Fernie, A.R., Leaver, C.J. Sweetlove, L.J. (2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell, 15, 2140 2151.
12. Goffman, F.D., Alonso, A.P., Schwender, J., Shachar-Hill, Y. Ohlrogge, J.B. (2005) Light enables a very high efficiency of carbon storage in developing embryos of rapeseed. Plant Physiol. 138, 2269 2279.
13. Hargreaves, J.A. ap Rees, T. (1988) Turnover of starch and sucrose in roots of Pisum sativum. Phytochemistry, 27, 1627 1629.
14. Hatzfeld, W.D. Stitt, M. (1990) A study of the rate of recycling of triose phosphates in heterotrophic Chenopodium rubrum cells, potato-tubers, and maize endosperm. Planta, 180, 198 204.
15. Hewezi, T., Petitprez, M. Gentzbittel, L. (2006) Primary metabolic pathways and signal transduction in sunflower (Helianthus annuus L.): comparison of transcriptional profiling in leaves and immature embryos using cDNA microarrays. Planta, 223, 948 964.
16. Hill, S.A. ap Rees, T. (1994) Fluxes of carbohydrate-metabolism in ripening bananas. Planta, 192, 52 60.
17. Hill, S.A. ap Rees, T. (1995) The effect of hypoxia on the control of carbohydrate-metabolism in ripening bananas. Planta, 197, 313 323.
18. Hill, L.M. Smith, A.M. (1991) Evidence that glucose-6-phosphate is imported as the substrate for starch synthesis by the plastids of developing pea embryos. Planta, 185, 91 96.
19. Hsu, F.C. Obendorf, R.L. (1982) Compositional analysis of in vitro matured soybean seeds. Plant Sci. Lett. 27, 129 135.
20. Kang, F. Rawsthorne, S. (1996) Metabolism of glucose-6-phosphate and utilization of multiple metabolites for fatty acid synthesis by plastids from developing oilseed rape embryos. Planta, 199, 321 327.
21. Kang, F., Ridout, C.J., Morgan, C.L. Rawsthorne, S. (1994) The activity of acetyl-CoA carboxylase is not correlated with the rate of lipid-synthesis during development of oilseed rape (Brassica napus L) embryos. Planta, 193, 320 325.
22. Kleppinger-Sparace, K.F., Stahl, R.J. Sparace, S.A. (1992) Energy-requirements for fatty-acid and glycerolipid biosynthesis from acetate by isolated pea root plastids. Plant Physiol. 98, 723 727.
23. Mantese, A.I., Medan, D. Hall, A.J. (2006) Achene structure, development and lipid accumulation in sunflower cultivars differing in oil content at maturity. Ann. Bot. 97, 999 1010.
24. Moing, A., Escobar-Gutierrez, A. Gaudillere, J.P. (1994) Modeling carbon export out of mature peach leaves. Plant Physiol. 106, 591 600.
25. Mollney, M., Wiechert, W., Kownatzki, D. de Graaf, A.A. (1999) Bidirectional reaction steps in metabolic networks: IV. Optimal design of isotopomer labeling experiments. Biotechnol. Bioeng. 66, 86 103.
26. Neuhaus, H.E., Batz, O., Thom, E. Scheibe, R. (1993) Purification of highly intact plastids from various heterotrophic plant-tissues - analysis of enzymatic equipment and precursor dependency for starch biosynthesis. Biochem. J. 296, 395 401.
27. Novak, L. Loubiere, P. (2000) The metabolic network of Lactococcus lactis: distribution of C-14-labeled substrates between catabolic and anabolic pathways. J. Bacteriol. 182, 1136 1143.
28. Pate, J.S., Sharkey, P.J. Atkins, C.A. (1977) Nutrition of a developing legume fruit - functional economy in terms of carbon, nitrogen, water. Plant Physiol. 59, 506 510.
29. Peoples, M.B., Pate, J.S., Atkins, C.A. Murray, D.R. (1985) Economy of water, carbon, and nitrogen in the developing cowpea fruit. Plant Physiol. 77, 142 147.
30. Pleite, R., Pike, M.J., Garces, R., Martinez-Force, E. Rawsthorne, S. (2005) The sources of carbon and reducing power for fatty acid synthesis in the heterotrophic plastids of developing sunflower (Helianthus annuus L.) embryos. J. Exp. Bot. 56, 1297 1303.
31. Ploschuk, E.L. Hall, A.J. (1997) Maintenance respiration coefficient for sunflower grains is less than that for the entire capitulum. Field Crops Res. 49, 147 157.
32. Qi, Q.G., Kleppinger-Sparace, K.F. Sparace, S.A. (1995) The utilization of glycolytic-intermediates as precursors for fatty-acid biosynthesis by pea root plastids. Plant Physiol. 107, 413 419.
33. Ratcliffe, R.G. Shachar-Hill, Y. (2005) Revealing metabolic phenotypes in plants: inputs from NMR analysis. Biol. Rev. 80, 27 43.
34. Ratcliffe, R.G. Shachar-Hill, Y. (2006) Measuring multiple fluxes through plant metabolic networks. Plant J. 45, 490 511.
35. Rawsthorne, S. (2002) Carbon flux and fatty acid synthesis in plants. Progr. Lipid Res. 41, 182 196.
36. Rontein, D., Dieuaide-Noubhani, M., Dufourc, E.J., Raymond, P. Rolin, D. (2002) The metabolic architecture of plant cells. Stability of central metabolism and flexibility of anabolic pathways during the growth cycle of tomato cells. J. Biol. Chem. 277, 43948 43960.
37. Roughan, P.G., Holland, R. Slack, C.R. (1979) Control of long-chain fatty acid synthesis in isolated intact spinach (Spinacia oleracea) chloroplasts. Biochem. J. 184, 193 202.
38. Ruuska, S.A., Schwender, J. Ohlrogge, J.B. (2004) The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol. 136, 2700 2709.
39. Saez, J.C., Schell, D.J., Tholudur, A., Farmer, J., Hamilton, J., Colucci, J.A. McMillan, J.D. (2002) Carbon mass balance evaluation of cellulase production on soluble and insoluble substrates. Biotechnol. Prog. 18, 1400 1407.
40. Salon, C., Raymond, P. Pradet, A. (1988) Quantification of carbon fluxes through the tricarboxylic-acid cycle in early germinating lettuce embryos. J. Biol. Chem. 263, 12278 12287.
41. Schwender, J., Ohlrogge, J.B. Shachar-Hill, Y. (2003) A flux model of glycolysis and the oxidative pentosephosphate pathway in developing Brassica napus embryos. J. Biol. Chem. 278, 29442 29453.
42. Schwender, J., Goffman, F., Ohlrogge, J.B. Shachar-Hill, Y. (2004a) Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature, 432, 779 782.
43. Schwender, J., Ohlrogge, J. Shachar-Hill, Y. (2004b) Understanding flux in plant metabolic networks. Curr. Opin. Plant Biol. 7, 309 317.
44. Schwender, J., Shachar-Hill, Y. Ohlrogge, J.B. (2006) Mitochondrial metabolism in developing embryos of Brassica napus. J. Biol. Chem. 281, 34040 34047.
45. Smith, R.G., Gauthier, D.A., Dennis, D.T. Turpin, D.H. (1992) Malate-dependent and pyruvate-dependent fatty-acid synthesis in leukoplastids from developing castor endosperm. Plant Physiol. 98, 1233 1238.
46. Sriram, G., Fulton, D.B., Iyer, V.V., Peterson, J.M., Zhou, R.L., Westgate, M.E., Spalding, M.H. Shanks, J.V. (2004) Quantification of compartmented metabolic fluxes in developing soybean embryos by employing biosynthetically directed fractional C-13 labeling, [C-13, H-1] two-dimensional nuclear magnetic resonance, and comprehensive isotopomer balancing. Plant Physiol. 136, 3043 3057.
47. Weaire, P.J. Kekwick, R.G.O. (1975) Fractionation of fatty-acid synthetase activities of avocado mesocarp plastids. Biochem. J. 146, 439 445.
48. Wiechert, W. de Graaf, A.A. (1997) Bidirectional reaction steps in metabolic networks. 1. Modeling and simulation of carbon isotope labeling experiments. Biotechnol. Bioeng. 55, 101 117.
49. Wiechert, W., Siefke, C., de Graaf, A.A. Marx, A. (1997) Bidirectional reaction steps in metabolic networks. 2. Flux estimation and statistical analysis. Biotechnol. Bioeng. 55, 118 135.
50. Wiechert, W., Mollney, M., Isermann, N., Wurzel, W. de Graaf, A.A. (1999) Bidirectional reaction steps in metabolic networks: III. Explicit solution and analysis of isotopomer labeling systems. Biotechnol. Bioeng. 66, 69 85.
51. Wiechert, W., Mollney, M., Petersen, S. de Graaf, A.A. (2001) A universal framework for C-13 metabolic flux analysis. Metab. Eng. 3, 265 283.
52. Zaitseva, M.G., Kasumova, I.V., Kasumov, E.A., Borisova, M.A. Il'chishina, N.V. (2002) Respiration of mitochondria in developing sunflower seeds. Biol. Bulletin, 29, 555 558.