Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: A numerical simulation using an evolutionary algorithm

Plant Physiology

Volumn 145, Issue 2, 2007, Pages 513-526

  Zhu, Xin Guang ^a   De Sturler, Eric ^b   Long, Stephen P ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; COMPUTER SIMULATION; EVOLUTIONARY ALGORITHMS; MAXIMUM LIKELIHOOD; METABOLISM; PHOTOSYNTHETIC MEMBRANES;

CARBON METABOLISM; PHOTOSYNTHETIC CARBON METABOLISM; PHOTOSYNTHETIC PRODUCTIVITY; PHOTOSYNTHETIC RATES;

ENZYMES;

EID: 35348928051     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.107.103713     Document Type: Article

References (73)

1. Badger MR, Lorimer G (1981) Interaction of sugar phosphate with the catalytic site of RuBP-carboxylase. Biochemistry 20: 2219-2225
2. 2 record from the Vostok ice core. In Trends: A Compendium of Data on Global Change. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, Department of Energy, Oak Ridge, TN
3. Bassham JA, Krause GH (1969) Free energy changes and metabolic regulation in steady state photosynthetic carbon reduction. Biochim Biophys Acta 189: 207-221
4. Bernacchi CJ, Singsaas EL, Pimentel C, Portis JAR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24: 253-259
5. Cleland WW (1963) The kinetics of enzyme-catalyzed reactions with two or more substrates or products. Biochim Biophys Acta 67: 104-137
6. Dietz KJ, Heber U (1984) Rate-limiting factors in leaf photosynthesis. 1. Carbon fluxes in the Calvin cycle. Biochim Biophys Acta 767: 432-443
7. Douce R, Bourguignon J, Neuburger M, Rébeillé F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6: 167-176
8. Eckardt NA, Snyder GW, Portis AR, Ogren WL (1997) Growth and photosynthesis under high and low irradiance of Arabidopsis thaliana antisense mutants with reduced ribulose-1,5-bisphosphate carboxylase/ oxygenase activase content. Plant Physiol 113: 575-586
9. Farquhar GD (1979) Models describing the kinetics of ribulose biphosphate carboxylase-oxygenase. Arch Biochem Biophys 193: 456-468
10. 3 species. Planta 149: 78-90
11. Farquhar GD, von Caemmerer S, Berry JA (2001) Models of photosynthesis. Plant Physiol 125: 42-45
12. Fliege R, Flugge U-I, Werner K, Heldt HW (1978) Specific transport of inorganic phosphate, 3-phosphoglycerate and triose phosphates across the inner membrane of the envelope in spinach chloroplasts. Biochim Biophys Acta 502: 232-247
13. Fridlyand L, Backhausen J, Scheibe R (1999) Homeostatic regulation upon changes of enzyme activities in the Calvin cycle as an example for general mechanisms of flux control. What can we expect from transgenic plants? Photosynth Res 61: 227-239
14. Fridlyand LE, Scheibe R (1999a) Controlled distribution of electrons between acceptors in chloroplasts: a theoretical consideration. Biochim Biophys Acta 1413: 31-42
15. 2 fixation as an example for general control mechanism in metabolic cycles. Biosystems 51: 79-93
16. Giersch C (2000) Mathematical modelling of metabolism. Curr Opin Plant Biol 3: 249-253
17. 2 fixation. Photosynth Res 42: 75-86
18. Goldberg DE (1989) Genetic Algorithms in Search, Optimization and Machine Learning. Addison-Wesley, Reading, MA
19. Harris GC, Koniger M (1997) The 'high' concentration of enzymes within the chloroplast. Photosynth Res 54: 5-23
20. Harrison EP, Olcer H, Lloyd JC, Long SP, Raines CA (2001) Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity. J Exp Bot 52: 1779-1784
21. Heinrich R, Klipp E (1996) Control analysis of unbranched enzymatic chains in states of maximal activity. J Theor Biol 182: 243-252
22. Howitz KT, McCarty RE (1985a) Kinetic characteristics of the chloroplast envelope glycolate transporter. Biochemistry 24: 2645-2652
23. Howitz KT, McCarty RE (1985b) Substrate specificity of the pea chloroplast glycolate transporter. Biochemistry 24: 3645-3650
24. 2 evolution. Plant Physiol 80: 390-395
25. Kacser H, Burns JA, Fell DA (1995) The control of flux. Biochem Soc Trans 23: 341-366
26. 2 in NADP-malic enzyme type species. Photosynth Res 66: 199-224
27. Laisk A, Eichelmann H, Oja V, Eatherall A, Walker DA (1989) A mathematical model of the carbon metabolism in photosynthesis. Difficulties in explaining oscillations by fructose 2,6-bisphosphate regulation. Proc R Soc Lond B Biol Sci 237: 389-415
28. Laisk A, Oja V, Heber U (1992a) Steady-state and induction kinetics of the photosynthetic electron-transport related to donor side oxidation and acceptor side reduction of photosystem-1 in sunflower leaves. Photosynthetica 27: 449-463
29. Laisk A, Oja V, Walker D, Heber U (1992b) Oscillations in photosynthesis and reduction of photosystem-1 acceptor side in sunflower leaves - functional cytochrome b6/f-photosystem 1 ferredoxin-NADP reductase supercomplexes. Photosynthetica 27: 465-479
30. Laisk A, Siebke K, Gerst U, Eichelmann H, Oja V, Heber U (1991) Oscillations in photosynthesis are initiated and supported by imbalances in the supply of ATP and NADPH to the Calvin cycle. Planta 185: 554-562
31. Laisk A, Walker DA (1986) Control of phosphate turnover as a rate-limiting factor and possible cause of oscillations in photosynthesis: a mathematical model. Proc R Soc Lond B Biol Sci 227: 281-302
32. Laisk A, Walker DA (1989) A mathematical model of electron transport. Thermodynamics necessity for photosystem II regulation: 'Light stroma'. Proc R Soc Lond B Biol Sci 237: 417-444
33. Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138: 451-460
34. Leidreiter K, Kruse A, Heineke D, Robinson DG, Heldt HW (1995) Subcellular volumes and metabolite concentrations in potato (Solanum tuberosum cv Desiree) leaves. Bot Acta 108: 439-444
35. 3 sedge, Scripus olneyi. Plant Physiol 96: 221-226
36. 2 exchange in the field. J Exp Bot 47: 1629-1642
37. Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29: 315-330
38. Niklas K (1999) Evolutionary walks through a land plant morphospace. J Exp Bot 50: 39-52
39. Oliver DJ, Raman R (1995) Glycine decarboxylase: protein chemistry and molecular biology of the major protein in leaf mitochondria. J Bioenerg Biomembr 27: 407-414
40. 4 tree species in the understory of a Hawaiian forest. Oecologia 58: 19-25
41. Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41: 421-453
42. Pearcy RW, Gross LJ, He D (1997) An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes. Plant Cell Environ 20: 411-424
43. Pettersson G (1997) Control properties of the Calvin photosynthesis cycle at physiological carbon dioxide concentrations. Biochim Biophys Acta 1322: 173-182
44. Pettersson G, Ryde-Pettersson U (1988) A mathematical model of the Calvin photosynthesis cycle. Eur J Biochem 175: 661-672
45. Poolman MG (1999) Computer modeling applied to the Calvin cycle. PhD thesis. Oxford Brookes University, Oxford
46. Poolman MG, Fell DA, Thomas S (2000) Modelling photosynthesis and its control. J Exp Bot 51: 319-328
47. Poolman MG, Olcer H, Lloyd JC, Raines CA, Fell DA (2001) Computer modelling and experimental evidence for two steady states in the photosynthetic Calvin cycle. Eur J Biochem 268: 2810-2816
48. Portis AR (1995) The regulation of Rubisco by Rubisco activase. J Exp Bot 46: 1285-1291
49. Portis AR (2003) Rubisco activase - Rubisco's catalytic chaperone. Photosynth Res 75: 11-27
50. Prentice IC, Farquhar GD, Fasham MJR, Goulden ML, Heimann M, Jaramillo VJ, Kheshgi HS, Le Quéré C, Scholes RJ, Wallace DWR (2001) The carbon cycle and atmospheric carbon dioxide. In JT Houghton, Y Ding, DJ Griggs, M Noguer, PJ van der Linden, X Dai, K Maskell, C Johnson, eds, Climate Change 2001: The Scientific Basis. Cambridge University Press, Cambridge, UK, pp 183-237
51. Price GD, von Caemmerer S, Evans JR, Siebke K, Anderson JM, Badger MR (1998) Photosynthesis is strongly reduced by antisense suppression of chloroplastic cytochrome bf complex in transgenic tobacco. Aust J Plant Physiol 25: 445-452
52. Pyke KA, Leech RM (1987) The control of chloroplast number in wheat mesophyll cells. Planta 170: 416-420
53. Raines CA (2003) The Calvin cycle revisited. Photosynth Res 75: 1-10
54. Raines CA, Harrison EP, Olcer H, Lloyd JC (2000) Investigating the role of the thiol-regulated enzyme sedoheptulose-1,7-bisphosphatase in the control of photosynthesis. Physiol Plant 110: 303-308
55. Raines CA, Lloyd JC, Dyer TA (1999) New insights into the structure and function of sedoheptulose-1,7-bisphosphatase; an important but neglected Calvin cycle enzyme. J Exp Bot 50: 1-8
56. Schimkat D, Heineke D, Heldt HW(1990) Regulation of sedoheptulose-1,7-bisphosphatase by sedoheptulose-7-phosphate and glycerate, and of fructose-1,6-bisphosphatase by glycerate in spinach chloroplasts. Planta 181: 97-103
57. Segel IH (1975) Enzyme Kinetics. John Wiley & Sons, New York
58. 3 plants. Plant Physiol 78: 71-75
59. Schurmann P, Jacquot JP (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51: 371-400
60. 2, and air humidity. Planta 183: 555-566
61. Tamoi M, Nagaoka M, Miyagawa Y, Shigeoka S (2006) Contribution of fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the Calvin cycle in transgenic plants. Plant Cell Physiol 47: 380-390
62. von Caemmerer S (2000) Biochemical Models of Leaf Photosynthesis. Techniques in Plant Sciences Series. CSIRO Publishing, Victoria, Australia, pp 1-28
63. Walker D (1992) Concerning oscillations. Photosynth Res 34: 387-395
64. Wingler A, Ann VJ, Lea PJ, Leegood RC (1999) Serine:glyoxylate aminotransferase exerts no control on photosynthesis. J Exp Bot 50: 719-722
65. Wingler A, Lea PJ, Leegood RC (1997) Control of photosynthesis in barley plants with reduced activities of glycine decarboxylase. Planta 202: 171-178
66. Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191: 180-190
67. Winter H, Robinson DG, Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193: 530-535
68. Wong S-C, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282: 424-426
69. 3 plants. Annu Rev Plant Physiol Plant Mol Biol 39: 533-594
70. 3 photosynthesis - a sensitivity analysis of the photosynthetic carbon reduction cycle. Planta 191: 421-432
71. i curves from 109 species. J Exp Bot 44: 907-920
72. Zhu X-G, Ort DR, Whitmarsh J, Long SP (2004a) The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies. A theoretical analysis. J Exp Bot 55: 1167-1175
73. 3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27: 155-165