DOI: 10.1046/j.1432-1033.2003.03851.x. A kinetic model of the branch‐point between the methionine and threonine biosynthesis pathways in <i>Arabidopsis thaliana</i>

A kinetic model of the branch‐point between the methionine and threonine biosynthesis pathways in Arabidopsis thaliana

10.1046/j.1432-1033.2003.03851.x

Crossref journal-article

Wiley

European Journal of Biochemistry (311)

Abstract

This work proposes a model of the metabolic branch‐point between the methionine and threonine biosynthesis pathways in Arabidopsis thaliana which involves kinetic competition for phosphohomoserine between the allosteric enzyme threonine synthase and the two‐substrate enzyme cystathionine γ‐synthase. Threonine synthase is activated by S‐adenosylmethionine and inhibited by AMP. Cystathionine γ‐synthase condenses phosphohomoserine to cysteine via a ping‐pong mechanism. Reactions are irreversible and inhibited by inorganic phosphate. The modelling procedure included an examination of the kinetic links, the determination of the operating conditions in chloroplasts and the establishment of a computer model using the enzyme rate equations. To test the model, the branch‐point was reconstituted with purified enzymes. The computer model showed a partial agreement with the in vitro results. The model was subsequently improved and was then found consistent with flux partition in vitro and in vivo. Under near physiological conditions, S‐adenosylmethionine, but not AMP, modulates the partition of a steady‐state flux of phosphohomoserine. The computer model indicates a high sensitivity of cystathionine flux to enzyme and S‐adenosylmethionine concentrations. Cystathionine flux is sensitive to modulation of threonine flux whereas the reverse is not true. The cystathionine γ‐synthase kinetic mechanism favours a low sensitivity of the fluxes to cysteine. Though sensitivity to inorganic phosphate is low, its concentration conditions the dynamics of the system. Threonine synthase and cystathionine γ‐synthase display similar kinetic efficiencies in the metabolic context considered and are first‐order for the phosphohomoserine substrate. Under these conditions outflows are coordinated.

Bibliography

Curien, G., Ravanel, S., & Dumas, R. (2003). A kinetic model of the branchâpoint between the methionine and threonine biosynthesis pathways in Arabidopsis thaliana. European Journal of Biochemistry, 270(23), 4615â4627. Portico.

Authors 3

Gilles Curien (first)
Stéphane Ravanel (additional)
Renaud Dumas (additional)

References 47 Referenced 54

10.1042/bst0110035
10.1016/S0021-9258(18)89857-X
10.1111/j.1432-1033.1990.tb15406.x
10.1016/S0021-9258(17)42750-5 / J. Biol. Chem. / Determination of flux through the branch point of two metabolic cycles. The tricarboxylic acid cycle and the glyoxylate shunt by Walsh K. (1984)
10.1016/S0021-9258(17)39492-9 / J. Biol. Chem. / Branch point control by the phosphorylation state of isocitrate dehydrogenase. A quantitative examination of fluxes during a regulatory transition by Walsh K. (1985)
10.1046/j.1432-1327.1999.00534.x
10.1099/00221287-148-4-1003
10.3109/10409238809083374
{'key': 'e_1_2_26_10_2', 'first-page': '1139', 'article-title': 'Homocysteine biosynthesis in green plants. O‐phosphorylhomoserine as the physiological substrate for cystathionine gamma‐synthase', 'volume': '249', 'author': 'Datko A.H.', 'year': '1974', 'journal-title': 'J. Biol. Chem.'} / J. Biol. Chem. / Homocysteine biosynthesis in green plants. O‐phosphorylhomoserine as the physiological substrate for cystathionine gamma‐synthase by Datko A.H. (1974)
10.1016/0006-291X(76)90842-1
10.1104/pp.71.4.780
10.1042/bj3310639
10.1104/pp.76.2.285
10.1016/0014-5793(96)00633-3
10.1021/bi980068f
10.1046/j.1432-1327.1999.00487.x
10.1104/pp.81.2.577
10.1042/bj3200383
10.1021/bi001625c
10.1016/0003-2697(74)90034-7
10.1111/j.1432-1033.1976.tb10186.x
10.1104/pp.116.2.547
10.1016/S0764-4469(00)01242-7
10.1104/pp.123.1.101
10.1046/j.1365-313X.2002.01221.x
10.1074/jbc.273.49.32739
10.1016/S0021-9258(19)40016-1 / J. Biol. Chem. / 31P NMR studies of spinach leaves and their chloroplasts by Bligny R. (1990)
10.1006/abbi.1995.1077
10.1016/S0065-2296(08)60087-7
10.1104/pp.86.2.369
{'key': 'e_1_2_26_32_2', 'first-page': '33', 'volume-title': 'Sulfur Nutrition and Sulfur Assimilation in Higher Plants.', 'author': 'Giovanelli J.', 'year': '1990'} / Sulfur Nutrition and Sulfur Assimilation in Higher Plants. by Giovanelli J. (1990)
10.1104/pp.75.2.474
10.1007/BF02411558
10.1104/pp.70.4.971
{'key': 'e_1_2_26_36_2', 'first-page': '65', 'article-title': 'The control of flux', 'volume': '27', 'author': 'Kacser H.', 'year': '1973', 'journal-title': 'Symp Soc. Exp. Biol.'} / Symp Soc. Exp. Biol. / The control of flux by Kacser H. (1973)
10.1111/j.1432-1033.1974.tb03320.x
10.1111/j.1574-6968.1986.tb01863.x
10.1042/bj2860313
{'key': 'e_1_2_26_40_2', 'volume-title': 'NATO ASI Series A: Life Sciences', 'author': 'Cornish‐Bowden A.', 'year': '1990'} / NATO ASI Series A: Life Sciences by Cornish‐Bowden A. (1990)
{'key': 'e_1_2_26_41_2', 'volume-title': 'Understanding the Control of Metabolism', 'author': 'Fell D.A.', 'year': '1997'} / Understanding the Control of Metabolism by Fell D.A. (1997)
10.1042/bj1990155
10.1038/287357a0
10.1074/jbc.M207379200
10.1126/science.286.5443.1371
10.1093/pcp/pce146
10.1104/pp.010819
10.1073/pnas.1831512100

Dates

Type	When
Created	21 years, 9 months ago (Nov. 13, 2003, 7:03 p.m.)
Deposited	1 year, 10 months ago (Oct. 16, 2023, 10:19 a.m.)
Indexed	1 year, 3 months ago (May 23, 2024, 9:49 p.m.)
Issued	21 years, 9 months ago (Nov. 28, 2003)
Published	21 years, 9 months ago (Nov. 28, 2003)
Published Online	21 years, 9 months ago (Nov. 28, 2003)
Published Print	21 years, 8 months ago (Dec. 1, 2003)

Funders 0

None

BibTeX

@article{Curien_2003, title={A kinetic model of the branch‐point between the methionine and threonine biosynthesis pathways in Arabidopsis thaliana}, volume={270}, ISSN={1432-1033}, url={http://dx.doi.org/10.1046/j.1432-1033.2003.03851.x}, DOI={10.1046/j.1432-1033.2003.03851.x}, number={23}, journal={European Journal of Biochemistry}, publisher={Wiley}, author={Curien, Gilles and Ravanel, Stéphane and Dumas, Renaud}, year={2003}, month=nov, pages={4615–4627} }

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