A kinetic model describes metabolic response to perturbations and distribution of flux control in the benzenoid network of Petunia hybrida

Plant Journal

Volumn 62, Issue 1, 2010, Pages 64-76

  Colón, Amy Marshall ^a   Sengupta, Neelanjan ^a   Rhodes, David ^a   Dudareva, Natalia ^a   Morgan, John ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Benzenoid network; Floral volatiles; Kinetic modeling; Metabolic control analysis; Petunia

Indexed keywords

BRANCH POINTS; CAPTURE FLUX; CONCENTRATION OF; CONTROLLING FACTORS; FLUX CONTROL; FLUX CONTROL COEFFICIENTS; GENETIC MANIPULATIONS; GENETIC MODIFICATIONS; IN-VIVO; KINETIC MODELING; KINETIC MODELS; METABOLIC CONTROL ANALYSIS; METABOLIC NETWORK; NETWORK CONTROL; NETWORK DECOMPOSITION; NETWORK DYNAMICS; NETWORK RESPONSE; NON-LINEAR LEAST SQUARES; OXIDATIVE PATHWAYS; PETUNIA HYBRIDA; PHENYLACETALDEHYDE; PLANT METABOLISM; PREDICTIVE INFORMATION; REGULATORY PROPERTIES; SYNTHASES; TRANSGENIC PETUNIA PLANTS;

AMINO ACIDS; IGNEOUS ROCKS; KINETIC PARAMETERS; KINETIC THEORY; METABOLISM; PLANTS (BOTANY);

GENETIC ENGINEERING;

ESSENTIAL OIL; PHENYLALANINE;

ARTICLE; BIOLOGICAL MODEL; FLOWER; GENE EXPRESSION REGULATION; METABOLISM; PETUNIA; TRANSGENIC PLANT;

FLOWERS; GENE EXPRESSION REGULATION, PLANT; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; OILS, VOLATILE; PETUNIA; PHENYLALANINE; PLANTS, GENETICALLY MODIFIED;

PETUNIA; PETUNIA X HYBRIDA;

EID: 77951844002     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04127.x     Document Type: Article

References (63)

1. Affourtit, C., Krab, K. Moore, A.L. (2001) Control of plant mitochondrial respiration. Biochim. Biophys. Acta. 1504, 58 69.
2. Aluru, M., Xu, Y., Guo, R., Wang, Z., Li, S., White, W., Wang, K. Rodermel, S. (2008) Generation of transgenic maize with enhanced provitamin A content. J. Exp. Bot. 59, 3551 3562.
3. Antoniewicz, M.R., Kelleher, J.K. Stephanopoulos, G. (2006) Determination of confidence intervals of metabolic fluxes estimated from stable isotope measurements. Met. Eng. 8, 324 337.
4. Atanassova, R., Favet, N., Martz, F., Chabbert, B., Tollier, M-T., Monties, B., Fritig, B. Legrand, M. (1995) Altered lignin composition in transgenic tobacco expression O-methyltransferase sequence in sense and antisense orientation. Plant J. 8, 465 477.
5. Boatright, J., Negre, F., Chen, X., Kish, C.M., Wood, B., Peel, G., Orlova, I., Gang, D., Rhodes, D. Dudareva, N. (2004) Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol. 135, 1993 2011.
6. Camm, E.L. Towers, G.H.N. (1973) Phenylalanine ammonia lyase. Phytochemistry, 12, 961 973.
7. Colon, A.J.M., Morgan, J.A., Dudareva, N. Rhodes, D. (2009) Application of dynamic flux analysis in plant metabolic networks. In Plant Metabolic Networks (Schwender, J., ed).
8. Curien, G., Ravanel, S. Dumas, R. (2003) A kinetic model of the branch-point between the methionine and threonine biosynthesis pathways in Arabidopsis thaliana. Eur. J. Biochem. 270, 4615 4627.
9. Daae, E.B., Dunhill, P., Mitsky, T.A., Padgette, S.R., Taylor, N.B., Valentin, H.E. Gruys, K.J. (1999) Metabolic modeling as a tool for evaluating polyhydroxyalkanoate copolymer production in plants. Metab. Eng. 1, 243 254.
10. Dauwe, R., Morreel, K., Goeminne, G. et al. (2007) Molecular phenotyping of lignin-modified tobacco reveals associated changes in cell-wall metabolism, primary metabolism, stress metabolism and photorespiration. Plant J. 52, 263 285.
11. Donath, J. Boland, W. (1995) Biosynthesis of acyclic homoterpenes: enzyme selectivity and absolute configuration of the nerolidol precursor. Phytochemistry, 39, 785 790.
12. Dubery, I.A. Smit, F. (1994) Phenylalanine ammonia-lyase from cotton (Gossypium hirsutum) hypocotyls: properties of the enzyme induced by a Verticillium dahliae phytotoxin. Biochim. Biophys. Acta. 1207, 24 30.
13. Dudareva, N. Pichersky, E. (2006) Floral scent metabolic pathways: their regulation and evolution. In Biology of Floral Scent (Dudareva, N. Pichersky, E., eds).
14. Dudareva, N., Andersson, S., Orlova, I., Gatto, N., Reichelt, M., Rhodes, D., Boland, W. Gershenzon, J. (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc. Natl Acad. Sci. USA, 102, 933 938.
15. Dwivedi, U.N., Campbell, W.H., Yu, J., Datla, R.S., Bugos, R.C., Chiang, V.L. Podila, G.K. (1994) Modification of lignin biosynthesis in transgenic Nicotiana through expression of an antisense O-methyltransferase gene from Populus. Plant Mol. Biol. 26, 61 71.
16. Fell, D. (1997) Understanding the Control of Metabolism.
17. 2 fixation as an example for general control mechanisms in metabolic cycles. Biosystems, 51, 79 93.
18. Fridlyand, L.E., Backhausen, J.E. Scheibe, R. (1998) Flux control of the malate valve in leaf cells. Arch. Biochem. Biophys. 349, 290 298.
19. Halpin, C., Knight, M.E., Foxon, G.A., Campbell, M.M., Boudet, A.M., Boon, J.J., Chabbert, B., Tollier, M. Schuch, W. (1994) Manipulation of lignin quality by down regulation of cinnamyl alcohol dehydrogenase. Plant J. 6, 339 350.
20. Hanson, K.R. Havir, E.A. (1970) l-Phenylalanine ammonia-lyase. IV. Evidence that the prosthetic group contains a dehydroalanyl residue and mechanism of action. Arch. Biochem. Biophys. 141, 1 17.
21. Heinzle, E., Matsuda, F., Miyagawa, H., Wakasa, K. Nishioka, T. (2007) Estimation of metabolic fluxes, expression levels and metabolite dynamics of a secondary metabolic pathway in potato using label pulse-feeding experiments combined with kinetic network modeling and simulation. Plant J. 50, 176 187.
22. Jorrin, J. Dixon, R. (1990) Stress response in alfalfa (Medicago sativa L.): II. Purification, characterization, and induction of phenylalanine ammonia-lyase isoforms from elicitor-treated cell suspension cultures. Plant Physiol. 92, 447 455. (Pubitemid 120029703)
23. Kacser, H. Burns, J. (1973) The control of flux. Symp. Soc. Exp. Biol. 27, 65 104.
24. Kaminaga, Y., Schnepp, J., Peel, G. et al. (2006) Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J. Biol. Chem. 281, 23357 23366.
25. Kebeish, R., Niessen, M., Thiruveedhi, K., Bari, R., Hirsch, H.J., Rosenkranz, R., Stabler, N., Schonfeld, B., Kreuzaler, F. Peterhansel, C. (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat. Biotechnol. 25, 593 599.
26. Khan, N.U., Kamath, A.V. Vaidyanathan, C.S. (1987) Study of interfering substances in a simple, new spectrophotometric assay for phenylalanine ammonia-lyase. Biochem. Int. 14, 451 455.
27. Knudsen, J.T. Gershenzon, J. (2006) The chemical diversity of floral scent. In Biology of Floral Scent (Dudareva, N. Pichersky, E., eds).
28. Koeduka, T., Fridman, E., Gang, D.R. et al. (2006) Eugenol and isoeugenol, characteristic aromatic constituents of spices, are biosynthesized via reduction of a coniferyl alcohol ester. Proc. Natl Acad. Sci. USA, 103, 10128 10133.
29. Koeduka, T., Orlova, I., Baiga, T.J., Noel, J.P., Dudareva, N. Pichersky, E. (2009) The lack of floral synthesis and emission of isoeugenol in Petunia axillaries subsp. parodii is due to a mutation in the isoeugenol synthase gene. Plant J. 58, 961 969.
30. Kolosova, N., Gorenstein, N., Kish, C.M. Dudareva, N. (2001) Regulation of circadian methylbenzoate emission in diurnally and nocturnally emitting plants. Plant Cell, 13, 2333 2347.
31. Koukol, J. Conn, E.E. (1961) The metabolism of aromatic compounds in higher plants: IV Purification and properties of the phenylalanine deaminase of Hordeum vulgare. J. Biol. Chem. 236, 2692 2698.
32. Krab, K. (1995) Kinetic and regulatory aspects of the function of the alternative oxidase in plant respiration. J. Bioenerg. Biomembr. 27, 387 396.
33. Libourel, I.G. Shachar-Hill, Y. (2008) Metabolic flux analysis in plants: from intelligent design to rational engineering. Annu. Rev. Plant Biol. 59, 625 650.
34. MacDonald, M.J. D'Cunha, G.B. (2007) A modern view of phenylalanine ammonia lyase. Biochem. Cell Biol. 85, 273 282.
35. Mavandad, M., Edwards, R., Liang, X., Lamb, C.J. Dixon, R. (1990) Effects of trans-cinnamic acid on expression of the bean phenylalanine ammonia-lyase gene family. Plant Physiol. 94, 671 680.
36. McNeil, S.D., Nuccio, M.L., Rhodes, D., Shachar-Hill, Y. Hanson, A.D. (2000a) Radiotracer and computer modeling evidence that phosphor-base methylation is the main route of choline synthesis in tobacco. Plant Physiol. 123, 371 380.
37. McNeil, S.D., Rhodes, D., Russell, B.L., Nuccio, M.L., Shachar-Hill, Y. Hanson, A.D. (2000b) Metabolic modeling identifies key constraints on an engineered glycine betaine synthesis pathway in tobacco. Plant Physiol. 124, 153 162.
38. McNeil, S.D., Nuccio, M.L., Ziemak, M.J. Hanson, A.D. (2001) Enhanced synthesis of choline and glycine betaine synthesis pathway in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferse. Proc. Natl Acad. Sci. USA, 98, 10001 10005.
39. Morgan, J.A. Rhodes, D. (2002) Mathematical modeling of plant metabolic pathways. Metab. Eng. 4, 80 89.
40. 31P NMR. Biochem. J. 342, 567 580.
41. Napier, J.A. (2007) The production of unusual fatty acids in transgenic plants. Annu. Rev. Plant Biol. 58, 295 319.
42. Negre, F., Kish, C.M., Boatright, J., Underwood, B., Shibuya, K., Wagner, C., Clark, D.G. Dudareva, N. (2003) Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowers. Plant Cell, 15, 2992 3006.
43. Nuccio, M.L., McNeil, S.D., Ziemak, M.J., Hanson, A.D., Jain, R.K. Selvaraj, G. (2000) Choline import into chloroplasts limits glycine betaine synthesis in tobacco: analysis of plants engineered with a chloroplastic or a cytosolic pathway. Metab. Eng. 2, 300 311.
44. Orlova, I., Marshall Colon, A., Schnepp, J. et al. (2006) Reduction of benzenoid synthesis in petunia flowers reveals multiple pathways to benzoic acid and enhancement in auxin transport. Plant Cell, 18, 3458 3475.
45. Pearcy, R.W., Gross, L.J. He, D. (1997) An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes. Plant Cell Environ. 20, 411 424.
46. Pichersky, E., Noel, J.P. Dudareva, N. (2006) Biosynthesis of plant volatiles: nature's diversity and ingenuity. Science, 311, 808 811.
47. Poolman, M.G., Fell, D.A. Thomas, S. (2000) Modelling photosynthesis and its control. J. Exp. Bot. 51, 319 328.
48. Reed, M.C., Nijhout, H.F., Sparks, R. Ulrich, C.M. (2004) A mathematical model of the methionine cycle. J. Theor. Biol. 226, 33 43.
49. Rios-Estepa, R., Turner, G.W., Lee, J.M., Croteau, R.B. Lange, B.M. (2008) A systems biology approach identifies the biochemical mechanisms regulating monoterpenoid essential oil composition in peppermint. Proc. Natl Acad. Sci. USA, 105, 2818 2823.
50. Rizzi, M., Baltes, M., Theobald, U. Reuss, M. (1997) In vivo analysis of metabolic dynamics in Saccharomyces cerevisiae: II Mathematical model. Biotech. Bioeng. 55, 592 608. (Pubitemid 27318173)
51. Sato, T., Kiuchi, F. Sankawa, U. (1982) Inhibition of phenylalanine ammonia lyase by cinnamic acid derivatives and related compounds. Phytochemistry, 21, 845 850.
52. Schwender, J. (2009) Kinetic properties of metabolic networks. In Plant Metabolic Networks (Schwender, J., ed).
53. Sewalt, V., Ni, W., Blount, J.W., Jung, H.G., Masoud, S.A., Howles, P.A., Lamb, C. Dixon, R.A. (1994) Reduced lignin content and altered lignin composition in transgenic tobacco down-regulated in expression of l-phenylalanine ammonia-lyase or cinnamate 4-hydroxylase. Plant Physiol. 115, 41 50.
54. Stephanopoulos, G.N., Aristidou, A.A. Nielsen, J. (1998) Metabolic Engineering: principles and Methodologies.
55. Thomas, S., Mooney, P.J.F., Burrell, M.M. Fell, D.A. (1997a) Finite change analysis of glycolytic intermediates in tuber tissue of lines of transgenic potato (Solanum tuberosum) overexpression phophofructokinase. Biochem. J. 322, 111 117.
56. Thomas, S., Mooney, P.J.F., Burrell, M.M. Fell, D.A. (1997b) Metabolic control analysis of glycolysis in tuber tissue of potato (Solanum tuberosum): explanation for the low control coefficient of phosphofructokinase over respiratory flux. Biochem. J. 322, 119 127.
57. Uys, L., Botha, F.C., Hofmeyr, J.H. Rohwer, J.M. (2007) Kinetic model of sucrose accumulation in maturing sugarcane culm tissue. Phytochemistry, 68, 2375 2392.
58. Van Doorsselaere, J., Baucher, M., Chognot, E. et al. (1995) A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J. 8, 855 864.
59. Verdonk, J.C., Ric de Vos, C.H., Verhoeven, H.A., Haring, M.A., van Tunen, A.J. Schuurink, R.C. (2003) Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry, 62, 997 1008.
60. Von Caemmerer, S. (2000) Biochemical Models of Photosynthesis.
61. Wu, S., Schalk, M., Clark, A., Miles, R.B., Coates, R. Chappell, J. (2006) redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat. Biotech. 24, 1359 1361.
62. Ye, X., Al-Babili, S., Kloti, A., Zhang, J., Lucca, P., Beyer, P. Potrykus, I. (2000) Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science, 287, 303 305.
63. Zhu, X.-G., de Struler, E. Long, S. (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol. 145, 513 526.