Slow deactivation of ribulose 1,5-bisphosphate carboxylase/oxygenase elucidated by mathematical models

FEBS Journal

Volumn 277, Issue 4, 2010, Pages 931-950

  Witzel, Franziska ^a,b   Götze, Jan ^c   Ebenhöh, Oliver ^a,d,e  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF POTSDAM   (Germany)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Carbon fixation; Enzyme kinetics; Fallover; Mathematical model; RuBisCO

Indexed keywords

PHOSPHATE; RIBULOSEBISPHOSPHATE CARBOXYLASE; UNCLASSIFIED DRUG; XYLULOSE 1,5 BISPHOSPHATE;

AMINO ACID SEQUENCE; ARTICLE; CARBON DIOXIDE FIXATION; CARBOXYLATION; CHEMICAL STRUCTURE; CONCEPTUAL FRAMEWORK; ENZYME INACTIVATION; ENZYME SUBSTRATE COMPLEX; KINETICS; MATHEMATICAL MODEL; OXYGENATION; PRIORITY JOURNAL;

CATALYTIC DOMAIN; KINETICS; MODELS, MOLECULAR; MODELS, THEORETICAL; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 76149101232     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07541.x     Document Type: Article

References (48)

1. Portis AR Parry MAJ (2007) Discoveries in Rubisco (Ribulose 1,5-bisphosphate carboxylase/oxygenase): A historical perspective. Photosynth Res 94, 121 143.
2. Jensen RG Bahr JT (1977) Ribulose 1,5-bisphosphate carboxylase-oxygenase. Annu Rev Plant Physiol 28, 379 400.
3. Tabita F (1999) Microbial ribulose 1,5-bisphosphate carboxylase/ oxygenase: a different perspective. Photosynth Res 60, 1 28. (Pubitemid 29384472)
4. Andersson I Taylor TC (2003) Structural framework for catalysis and regulation in ribulose-1,5-bisphosphate carboxylase/oxygenase. Arch Biochem Biophys 414, 130 140.
5. Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59, 1555 1568.
6. Andersson I Backlund A (2008) Structure and function of Rubisco. Plant Physiol Biochem 46, 275 291.
7. Edmondson DL, Badger MR Andrews TJ (1990) A kinetic characterization of slow inactivation of ribulosebisphosphate carboxylase during catalysis. Plant Physiol 93, 1376 1382.
8. Edmondson DL, Badger MR Andrews TJ (1990) Slow inactivation of ribulosebisphosphate carboxylase during catalysis is not due to decarbamylation of the catalytic site. Plant Physiol 93, 1383 1389.
9. Edmondson DL, Badger MR Andrews TJ (1990) Slow inactivation of ribulosebisphosphate carboxylase during catalysis is caused by accumulation of a slow, tight-binding inhibitor at the catalytic site. Plant Physiol 93, 1390 1397.
10. Kim K Portis AR (2006) Kinetic analysis of the slow inactivation of Rubisco during catalysis: effects of temperature, O2 and Mg(++). Photosynth Res 87, 195 204.
11. Pearce FG (2006) Catalytic by-product formation and ligand binding by ribulose bisphosphate carboxylases from different phylogenies. Biochem J 399, 525 534.
12. Schrader SM, Kane HJ, Sharkey TD von Caemmerer S (2006/10/02) High temperature enhances inhibitor production but reduces fallover in tobacco. Rubisco Funct Plant Biol 33, 921 929.
13. Robinson SP Portis AR (1989) Ribulose-1,5-bisphosphate carboxylase/oxygenase activase protein prevents the in vitro decline in activity of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol 90, 968 971.
14. Portis AR (2003) Rubisco activase - rubisco's catalytic chaperone. Photosynth Res 75, 11 27.
15. Pearce FG Andrews TJ (2003) The relationship between side reactions and slow inhibition of ribulosebisphosphate carboxylase revealed by a loop 6 mutant of the tobacco enzyme. J Biol Chem 278, 32526 32536.
16. Farquhar GD (1979) Models describing the kinetics of ribulose biphosphate carboxylase-oxygenase. Arch Biochem Biophys 193, 456 468.
17. Yokota A, Wadano A Murayama H (1996) Modeling of continuously and directly analyzed biphasic reaction courses of ribulose 1,5-bisphosphate carboxylase/oxygenase. J Biochem 119, 487 499.
18. King WA, Gready JE Andrews TJ (1998) Quantum chemical analysis of the enolization of ribulose bisphosphate: the first hurdle in the fixation of CO2 by Rubisco. Biochemistry 37, 15414 15422.
19. Mauser H, King WA, Gready JE Andrews TJ (2001) CO(2) fixation by Rubisco: computational dissection of the key steps of carboxylation, hydration, and C-C bond cleavage. J Am Chem Soc 123, 10821 10829.
20. McNevin D, von Caemmerer S Farquhar G (2006) Determining RuBisCO activation kinetics and other rate and equilibrium constants by simultaneous multiple non-linear regression of a kinetic model. J Exp Bot 57, 3883 3900.
21. Kannappan B Gready JE (2008) Redefinition of Rubisco carboxylase reaction reveals origin of water for hydration and new roles for active-site residues. J Am Chem Soc 130, 15063 15080.
22. Edmondson DL (1990) Substrate isomerization inhibits ribulosebisphosphate carboxylase-oxygenase during catalysis. FEBS Lett 260, 62 66.
23. Lorimer B (1976) The activation of ruibulose-1,5-bisphosphate carboxylase by carbon-dioxide and Magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. Biochemistry 15, 529 536.
24. Zhu G Jensen RG (1991) Fallover of ribulose 1,5-bisphosphate carboxylase/oxygenase activity: decarbamylation of catalytic sites depends on pH. Plant Physiol 97, 1354 1358.
25. McCurry SD Tolbert NE (1977) Inhibition of ribulose-1,5-bisphosphate carboxylase/oxygenase by xylulose 1,5-bisphosphate. J Biol Chem 252, 8344 8346.
26. Harpel MR, Serpersu EH, Lamerdin JA, Huang ZH, Gage DA Hartman FC (1995) Oxygenation mechanism of ribulose-bisphosphate carboxylase/oxygenase. Structure and origin of 2-carboxytetritol 1,4-bisphosphate, a novel O2-dependent side product generated by a site-directed mutant. Biochemistry 34, 11296 11306.
27. von Caemmerer, S (2000) Biochemical Models of Leaf Photosynthesis - Techniques in Plant Sciences Series Number 2. CSIRO PUBLISHING, Collingwood, Australia.
28. Frank J (1998) Thermodynamics and kinetics of sugar phosphate binding to D-ribulose 1,5-bisphosphate carboxylase/oxygenase (RUBISCO). J Chem Soc, Faraday Trans. 94, 2127 2133.
29. Tcherkez GGB, Farquhar GD Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci U S A 103, 7246 7251.
30. Gutteridge S Pierce J (2006) A unified theory for the basis of the limitations of the primary reaction of photosynthetic CO(2) fixation: was Dr. Pangloss right? Proc Natl Acad Sci U S A 103, 7203 7204.
31. Kane H, Wilkin J, Portis A Andrews T (1998) Potent inhibition of ribulose-bisphosphate carboxylase by an oxidized impurity in ribulose-1,5-bisphosphate. Plant Physiol 117, 1059 1069.
32. Zhu G, Bohnert H, Jensen R Wildner G (1998) Formation of the tight-binding inhibitor, 3-ketoarabinitol-1,5-bisphosphate by ribulose-1,5-bisphosphate carboxylase/oxygenase is O-2-dependent. Photosynth Res 55, 67 74.
33. Portis AR, Lilley RM Andrews TJ (1995) Subsaturating ribulose-1,5- bisphosphate concentration promotes inactivation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) (Studies using continuous substrate addition in the presence and absence of Rubisco activase). Plant Physiol 109, 1441 1451.
34. Yokota A (1991) Carboxylation and detoxification of Xylulose bisphosphate by Spinach ribulose bisphosphate carboxylase oxygenase. Plant Cell physiol 32, 755 762.
35. Zhu G Jensen RG (1991) Xylulose 1,5-bisphosphate synthesized by ribulose 1,5-bisphosphate carboxylase/oxygenase during catalysis binds to decarbamylated enzyme. Plant Physiol 97, 1348 1353.
36. Whitney SM, Baldet P, Hudson GS Andrews TJ (2001) Form I Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J 26, 535 547.
37. Kim K Portis AR (2004) Oxygen-dependent H2O2 production by Rubisco. FEBS Lett 571, 124 128.
38. 2 specificty of ribulose 1,5-bisphosphate carboxylase oxygenase - dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161, 308 313.
39. Lee EH, Harpel MR, Chen YR Hartman FC (1993) Perturbation of reaction-intermediate partitioning by a site-directed mutant of ribulose-bisphosphate carboxylase/oxygenase. J Biol Chem 268, 26583 26591.
40. Parry MAJ, Andralojc PJ, Mitchell RAC, Madgwick PJ Keys AJ (2003) Manipulation of Rubisco: the amount, activity, function and regulation. J Exp Bot 54, 1321 1333.
41. Laing WA (1974) Regulation of soybean net photosynthetic CO(2) fixation by the interaction of CO(2), O(2), and ribulose 1,5-diphosphate carboxylase. Plant Physiol 54, 678 685.
42. Heinrich R Schuster S (1996) The Regulation of Cellular Systems. Chapman & Hall, London, UK.
43. Morell MK, Paul K, O'Shea NJ, Kane HJ Andrews TJ (1994) Mutations of an active site threonyl residue promote beta elimination and other side reactions of the enediol intermediate of the ribulosebisphosphate carboxylase reaction. J Biol Chem 269, 8091 8098.
44. Read BA Tabita FR (1994) High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial RubiSCO containing ''algal'' residue modifications. Arch Biochem Biophys 312, 210 218.
45. Morell MK, Kane HJ, Hudson GS Andrews TJ (1992) Effects of mutations at residue 309 of the large subunit of ribulosebisphosphate carboxylase from Synechococcus PCC 6301. Arch Biochem Biophys 299, 295 301.
46. Terzaghi BE, Laing WA, Christeller JT, Petersen GB Hill DF (1986) Ribulose 1,5-bisphosphate carboxylase. Effect on the catalytic properties of changing methionine-330 to leucine in the Rhodospirillum rubrum enzyme. Biochem J 235, 839 846.
47. 2 specificity of ribulosebisphosphate carboxylase-cxygenase. Aust J Plant Physiol 21, 449 461.
48. Taylor TC, Backlund A, Bjorhall K, Spreitzer RJ Andersson I (2001) First crystal structure of Rubisco from a green algae, Chlamydomonas reinhardtii. J Biol Chem 276, 48159 48164.