Rubisco activase – Rubisco's catalytic chaperone

Abstract

The current status of research on the structure, regulation, mechanism and importance of Rubisco activase is reviewed. The activase is now recognized to be a member of the AAA+ family, whose members participate in macromolecular complexes that perform diverse chaperone-like functions. The conserved nucleotide-binding domain of AAA+ family members appears to have a common fold that when applied to the activase is generally consistent with previous site-directed mutagenesis studies of the activase. Regulation of the activase in species containing both isoforms can occur via redox changes in the carboxy-terminus of the larger isoform, mediated by thioredoxin-f, which alters the response of activase to the ratio of ADP to ATP in the stroma. Studies of Rubisco activation in transgenic Arabidopsis plants demonstrated that light modulation is dependent on redox regulation of the larger isoform, providing a model for the regulation in other species. Further insights into the mechanism of the activase have emerged from an analysis of the crystal structures of Rubisco conformational variants and the identification of Rubisco residues that confer specificity in its interaction with the activase. The physiological importance of the activase is reinforced by recent studies indicating that it plays a vital role in the response of photosynthesis to temperature. Rubisco activase is one of a new type of chaperone, which in this case functions to promote and maintain the catalytic activity of Rubisco.

This is a preview of subscription content, access via your institution.

References

  1. Andrews TJ, Hudson GS, Mate CJ, von Caemmerer S, Evans JR and Arvidsson YBC (1995) Rubisco – the consequences of altering its expression and activation in transgenic plants. J Exp Bot 46: 1293–1300

    Google Scholar 

  2. Berry JA and Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31: 491–543

    Google Scholar 

  3. Buef L, Kurano N and Miyachi S (1999) Rubisco activase transcript (rca) abundance increases when the marine unicellular green alga Chlorococcum littorale is grown under high-CO2 stress. Plant Mol Biol 41: 627–635

    Google Scholar 

  4. Büchen-Osmond C, Portis AR Jr and Andrews TJ (1992) Rubisco activase modifies the appearance of Rubisco in the electron microscope. In: Murata N (ed) Research in Photosynthesis, Vol III, pp 653–656. IXth International Congress On Photosynthesis, Nagoya, Japan, August 30–September 4, 1992. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  5. Cleland WW, Andrews TJ, Gutteridge S, Hartman FC and Lorimer GH (1998) Mechanism of Rubisco: the carbamate as general base. Chem Rev 98: 549–561

    Google Scholar 

  6. Crafts-Brandner SJ and Law RD (2000) Effect of heat stress on the inhibition and recovery of the ribulose-1,5-bisphosphate carboxylase/oxygenase activation state. Planta 212: 67–74

    Google Scholar 

  7. Crafts-Brandner SJ and Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97: 13430–13435

    Google Scholar 

  8. Crafts-Brandner SJ, van de Loo FJ and Salvucci ME (1997) The two forms of ribulose-1,5-bisphosphate carboxylase-oxygenase activase differ in sensitivity to elevated temperature. Plant Physiol 114: 439–344

    Google Scholar 

  9. Duff AP, Andrews TJ and Curmi PMG (2000) The transition between the open and closed states of Rubisco is triggered by the inter-phosphate distance of the bound bisphosphate. J Mol Biol 298: 903–916

    Google Scholar 

  10. Eckardt NA and Portis AR Jr (1997) Heat denaturation profiles of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase and the inability of Rubisco activase to restore activity of heat-denatured Rubisco. Plant Physiol 113: 243–248

    Google Scholar 

  11. Eckardt NA, Snyder GW, Portis AR Jr and 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

    Google Scholar 

  12. Edmondson DL, Badger MR and Andrews TJ (1990a) 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

    Google Scholar 

  13. Edmondson DL, Badger MR and Andrews TJ (1990b) Slow inactivation of ribulosebisphosphate carboxylase is not due to decarbamylation of the catalytic site. Plant Physiol 93: 1383–1389

    Google Scholar 

  14. Esau BD, Snyder GW and Portis AR Jr (1996) Differential effects of N-and C-terminal deletions on the two activities of Rubisco activase. Arch Biochem Biophys 326: 100–105

    Google Scholar 

  15. Esau BD, Snyder GW and Portis AR Jr (1998) Activation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) with chimeric activase proteins. Photosynth Res 58: 175–181

    Google Scholar 

  16. Feller U, Crafts-Brandner SJ and Salvucci ME (1998) Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiol 116: 539–546

    Google Scholar 

  17. Friedberg D, Jager KM, Kessel M, Silman NJ and Bergman B (1993) Rubisco but not Rubisco activase is clustered in the carboxysomes of the cyanobacterium Synechococcus sp. PCC 7942: Mud-induced carboxysomeless mutants. Mol Microbiol 9: 1193–1201

    Google Scholar 

  18. Guenther B, Onrust R, Sali A, O'Donnell M and Kuriyan J (1997) Crystal structure of the δ' subunit of the clamp-loader complex of E. coli DNA polymerase III. Cell 91: 335–345

    Google Scholar 

  19. Hammond ET, Andrews TJ, Mott KA and Woodrow IE (1998a) Regulation of Rubisco activation in antisense plants of tobacco containing reduced levels of Rubisco activase. Plant J 14: 10l–110

    Google Scholar 

  20. Hammond ET, Andrews TJ and Woodrow IE (1998b) Regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase by carbamylation and 2-carboxyarabinitol 1-phosphate in tobacco: insights from studies of antisense plants containing reduced amounts of Rubisco activase. Plant Physiol 118: 1463–1471

    Google Scholar 

  21. Hartman FC and Harpel MR (1994) Structure, function, regulation, and assembly of D-ribulose-1,5-bisphosphate carboxylaseoxygenase. Annual Review of Biochemistry 63: 197–234

    Google Scholar 

  22. He ZL, von Caemmerer S, Hudson GS, Price GD, Badger MR and Andrews TJ (1997) Ribulose-1,5-bisphosphate carboxylase/oxygenase activase deficiency delays senescence of ribulose-1,5-bisphosphate carboxylase/oxygenase but progressively impairs its catalysis during tobacco leaf development. Plant Physiol 115: 1569–1580

    Google Scholar 

  23. Kallis RP, Ewy RG and Portis AR Jr (2000) Alteration of the adenine nucleotide response and increased Rubisco activation activity of Arabidopsis Rubisco activase by site-directed mutagenesis. Plant Physiol 123: 1077–1086

    Google Scholar 

  24. Kobza J and Edwards GE (1987) Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiol 83: 69–74

    Google Scholar 

  25. Komatsu S, Masuda T and Hirano H (1996) Rice gibberellinbinding phosphoprotein structurally related to ribulose-1,5-bisphosphate carboxylase-oxygenase activase. FEBS Lett 384: 167–171

    Google Scholar 

  26. Lan Y and Mott KA (1991) Determination of apparent Km values for ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase using the spectrophotometric assay of Rubisco activity. Plant Physiol 95: 604–609

    Google Scholar 

  27. Lan Y, Mott KA and Woodrow IE (1992) Light-dependent activation of Rubisco activase. Plant Physiology Suppl 99: 104

    Google Scholar 

  28. Larson EM, O'Brien CM, Zhu GH, Spreitzer RJ and Portis AR Jr (1997) Specificity for activase is changed by a Pro-89 to Arg substitution in the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 272: 17033–17037

    Google Scholar 

  29. Law RD and Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol 120: 173–181

    Google Scholar 

  30. Law RD and Crafts-Brandner SJ (2001) High temperature stress increases the expression of wheat leaf ribulose-1,5-bisphosphate carboxylase/oxygenase activase protein. Arch Biochem Biophys 386: 261–267

    Google Scholar 

  31. Law RD, Crafts-Brandner SJ and Salvucci ME (2001) Heat stress induces the synthesis of a new form of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in cotton leaves. Planta 214: 117–125

    Google Scholar 

  32. Li L-A, Gibson JL and Tabita FR (1993) The Rubisco activase (rca) gene is located downstream from rbcS in Anabaena sp. strain CA and is detected in other Anabaena/Nostoc strains. Plant Mol Biol 21: 753–764

    Google Scholar 

  33. Li L-A, Zianni MR and Tabita FR (1999) Inactivation of the monocistronic rca gene in Anabaena variabilis suggests a physiological ribulose bisphosphate carboxylase oxygenase activase-like function in heterocystous cyanobacteria. Plant Mol Biol 40: 467–478

    Google Scholar 

  34. Lilley RM and Portis AR Jr (1990) Activation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) by Rubisco activase: effects of some sugar phosphates. Plant Physiol 94: 245–250

    Google Scholar 

  35. Lilley RM and Portis AR Jr (1997) ATP hydrolysis activity and polymerization state of ribulose-1,5-bisphosphate carboxylase oxygenase activase: do the effects of Mg2+, K+, and activase concentrations indicate a functional similarity to actin? Plant Physiol 114: 606–613

    Google Scholar 

  36. Lorimer GH, Badger MR and Andrews TJ (1976) The activation of ribulose-1,-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. Biochemistry 15: 529–536

    Google Scholar 

  37. Ludwig M, Sültemeyer D and Price GD (2000) Isolation of ccmKLMN genes from the marine cyanobacterium, Synechococcus sp. PCC7002 (Cyanophyceae), and evidence that CcmM is essential for carboxysome assembly. J Phycol 36: 1109–1118

    Google Scholar 

  38. MacIntyre HL, Sharkey TD and Geider RJ (1997) Activation and deactivation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) in three marine microalgae. Photosynth Res 51: 93–106

    Google Scholar 

  39. Mächler F and Nösberger J (1980) Regulation of ribulose bisphosphate carboxylase activity in intact wheat leaves by light, CO2, and temperature. J Expt Bot 31: 1485–1491

    Google Scholar 

  40. Mate CJ, von Caemmerer S, Evans JR, Hudson GS and Andrews TJ (1996) The relationship between CO2-assimilation rate, Rubisco carbamylation and Rubisco activase content in activase-deficient transgenic tobacco suggests a simple model of activase action. Planta 198: 604–613

    Google Scholar 

  41. McKay RML, Gibbs SP and Vaughn KC (1991) RuBisCo activase is present in the pyrenoid of green algae. Protoplasma 162: 38–45

    Google Scholar 

  42. Mott KA and Woodrow IE (2000) Modelling the role of Rubisco activase in limiting non-steady-state photosynthesis. J Expt Bot 51: 399–406

    Google Scholar 

  43. Mott KA, Snyder GW and Woodrow IE (1997) Kinetics of Rubisco activation as determined from gas-exchange measurements in antisense plants of Arabidopsis thaliana containing reduced levels of Rubisco activase. Aust J Plant Physiol 24: 811–818

    Google Scholar 

  44. Murakami Y, Tsuyama M, Kobayashi Y, Kodama H and Iba K (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287: 476–479

    Google Scholar 

  45. Neuwald AF, Aravind L, Spouge JL and Koonin EV (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9: 27–43

    Google Scholar 

  46. Ogura T and Wilkinson AJ (2001) AAA+ superfamily ATPases: common structure – diverse function. Genes Cells 6: 575–597

    Google Scholar 

  47. Ott CM, Smith BD, Portis AR Jr and Spreitzer RJ (2000) Activase region on chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase: nonconservative substitution in the large subunit alters species specificity of protein interaction. J Biol Chem 275: 26241–26244

    Google Scholar 

  48. Parry MAJ, Andralojc PJ, Parmar S, Keys AJ, Habash D, Paul MJ, Alred R, Quick WP and Servaites JC (1997) Regulation of Rubisco by inhibitors in the light. Plant Cell Environ 20: 528–534

    Google Scholar 

  49. Perchorowicz JT, Raynes DA and Jensen RG (1981) Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proc Natl Acad Sci USA 78: 2985–2989

    Google Scholar 

  50. Portis AR Jr (1990) Rubisco activase. Biochim Biophys Acta 1015: 15–28

    Google Scholar 

  51. Portis AR Jr (1992) Regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activity. Annu Rev Plant Physiol Plant Mol Biol 43: 415–437

    Google Scholar 

  52. Portis AR Jr (1995) The regulation of Rubisco by Rubisco activase. J Expt Bot 46: 1285–1291

    Google Scholar 

  53. Portis AR Jr (2001) The Rubisco activase-Rubisco system: an ATPase-dependent association that regulates photosynthesis. In: McManus MT, Laing WL and Allen AC (eds) Protein – Protein Interactions in Plant Biology, pp 30–52. Sheffield Academic Press, Sheffield, England

    Google Scholar 

  54. Portis AR Jr, Salvucci ME and Ogren WL (1986) Activation of ribulosebisphosphate carboxylase/oxygenase at physiological CO2 and ribulosebisphosphate concentrations by Rubisco activase. Plant Physiol 82: 967–971

    Google Scholar 

  55. Portis AR Jr, Lilley RM and 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

    Google Scholar 

  56. Price GD, Howitt SM, Harrison K and Badger MR (1993) Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function. J Bacteriol 175: 2871–2879

    Google Scholar 

  57. Quick WP, Schurr U, Scheibe R, Schulze ED, Rodermel SR, Bogorad L and Stitt M (1991) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with 'antisense' rbcS: I. Impact on photosynthesis in ambient growth conditions. Planta 183: 542–554

    Google Scholar 

  58. Robinson SP and Portis AR Jr (1988a) Involvement of stromal ATP in the light activation of ribulose-1,5-bisphosphate carboxylase/oxygenase in intact isolated chloroplasts. Plant Physiol 86: 293–298

    Google Scholar 

  59. Robinson SP and Portis AR Jr (1988b) Release of the nocturnal inhibitor, carboxyarabinitol-1-phosphate, from ribulose bisphosphate carboxylase/oxygenase by Rubisco activase FEBS Lett 233: 413–416

    Google Scholar 

  60. Robinson SP and Portis AR Jr (1989a) Adenosine triphosphate hydrolysis by purified Rubisco activase. Arch Biochem Biophys 268: 93–99

    Google Scholar 

  61. Robinson SP and Portis AR Jr (1989b) 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

    Google Scholar 

  62. Robinson SP, Streusand VJ, Chatfield JM and Portis AR Jr (1988) Purification and assay of Rubisco activase from leaves. Plant Physiol 88: 1008–1014

    Google Scholar 

  63. Roesler KR and Ogren WL (1990) Primary structure of Chlamydomonas reinhardtii ribulose-1,5-bisphosphate carboxylase/oxygenase activase and evidence for a single polypeptide. Plant Physiol 95: 1837–1841

    Google Scholar 

  64. Rokka A, Zhang LX and Aro EM (2001) Rubisco activase: an enzyme with a temperature-dependent dual function? Plant J 25: 463–471

    Google Scholar 

  65. Rundle SJ and Zielinski RE (1991) Organization and expression of two tandemly oriented genes encoding ribulosebisphosphate carboxylase/oxygenase activase in barley. J Biol Chem 266: 4677–4685

    Google Scholar 

  66. Ruuska SA, Andrews TJ, Badger MR, Price GD and von Caemmerer 5 (2000) The role of chloroplast electron transport and metabolites in modulating Rubisco activity in tobacco. Insights from transgenic plants with reduced amounts of cytochrome b/f complex or glyceraldehyde 3-phosphate dehydrogenase. Plant Physiol 122: 491–504

    Google Scholar 

  67. Salvucci ME (1992) Subunit interactions of Rubisco activase-polyethylene glycol promotes self-association, stimulates ATPase and activation activities, and enhances interactions with Rubisco. Arch Biochem Biophys 298: 688–696

    Google Scholar 

  68. Salvucci ME (1993) Covalent modification of a highly reactive and essential lysine residue of ribulose-1,5-bisphosphate carboxylase-oxygenase activase. Plant Physiol 103: 501–508

    Google Scholar 

  69. Salvucci ME and Klein RR (1994) Site-directed mutagenesis of a reactive lysyl residue (Lys-247) of Rubisco activase. Arch Biochem Biophys 314: 178–185

    Google Scholar 

  70. Salvucci ME and Ogren WL (1996) The mechanism of Rubisco activase: insights from studies of the properties and structure of the enzyme. Photosynth Res 47: 1–11

    Google Scholar 

  71. Salvucci ME, Portis AR Jr and Ogren WL (1985) A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase/oxygenase activation in vivo. Photosynth Res 7: 193–201

    Google Scholar 

  72. Salvucci ME, Portis AR Jr and Ogren WL (1986) Light and CO2 response of ribulose-1,5-bisphosphate carboxylase/oxygenase activation in Arabidopsis leaves. Plant Physiol 80: 655–659

    Google Scholar 

  73. Salvucci ME, Werneke JM, Ogren WL and Portis AR Jr. (1987) Purification and species distribution of Rubisco activase. Plant Physiol 84: 930–936

    Google Scholar 

  74. Salvucci ME, Rajagopalan K, Sievert G, Haley BE and Watt DS (1993) Photoaffinity labeling of ribulose-1,5-bisphosphate carboxylase/oxygenase activase with ATP γ-benzophenone: identification of the ATP γ-phosphate binding domain. J Biol Chem 268: 14239–14244

    Google Scholar 

  75. Salvucci ME, Chavan AJ, Klein RR, Rajagopolan K and Haley BE (1994) Photoaffinity labeling of the ATP binding domain of Rubisco activase and a separate domain involved in the activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Biochemistry 33: 14879–14886

    Google Scholar 

  76. Salvucci ME, Osteryoung KW, Crafts-Brandner SJ amd Vierling E (2001) Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiol 127: 1053–1064

    Google Scholar 

  77. Sánchez de Jiménez E, Medrano L and Martínez-Barajas E (1995) Rubisco activase, a possible new member of the molecular chaperone family. Biochemistry 34: 2826–2831

    Google Scholar 

  78. Sánchez R, Pieper U, Mirkovic N, de Bakker PIW, Wittenstein E and Sali A (2000) MODBASE, a database of annotated comparative protein structure models. Nucleic Acids Res 28: 250–253

    Google Scholar 

  79. Schreuder HA, Knight S, Curmi PMG, Andersson I, Cascio D, Brändén CI and Eisenberg D (1993) Formation of the active site of ribulose-1,5-bisphosphate carboxylase-oxygenase by a disorder-order transition from the unactivated to the activated form. Proc Natl Acad Sci USA 90: 9968–9972

    Google Scholar 

  80. Schürmann P and Jacquot J-P (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51: 371–400

    Google Scholar 

  81. Seemann JR, Berry JA, Freas SM and Krump MA(1985) Regulation of ribulose bisphosphate carboxylase activity in vivo by a lightmodulated inhibitor of catalysis. Proc Natl Acad Sci USA 82: 8024–8028

    Google Scholar 

  82. Servaites JC (1985) Binding of a phosphorylated inhibitor to ribulose bisphosphate carboxylase/oxygenase during the night. Plant Physiol 78: 834–843

    Google Scholar 

  83. Sharkey TD (1989) Evaluating the role of Rubisco regulation in photosynthesis of C3 plants. Phil Trans R Soc London 323: 434–448

    Google Scholar 

  84. Sharkey TD (1990) Feedback limitation of photosynthesis and the physiological role of ribulose bisphosphate carboxylase carbamylation. Bot Mag Tokyo Special Issue 2: 87–105

    Google Scholar 

  85. Sharkey TD (2000) Plant biology – some like it hot. Science 287: 435–437

    Google Scholar 

  86. Sharkey TD, Stitt M, Heineke D, Gerhardt R, Raschke K and Heldt HW (1986) Limitation of photosynthesis by carbon metabolism. II. O2 insensitive CO2 uptake results from limitation of triose phosphate utilization. Plant Physiol 81: 1123–1129

    Google Scholar 

  87. Sharkey TD, Badger MR, von Caemmerer S and Andrews TJ (2001) Increased heat sensitivity of photosynthesis in tobacco plants with reduced Rubisco activase. Photosynth Res 67: 147–156

    Google Scholar 

  88. Sharma A and Komatsu S (2002) Involvement of a Ca2+-dependent protein kinase component downstream to the gibberellin-binding phosphoprotein, RuBisCO activase, in rice. Biochem Biophys Res Commun 290: 690–695

    Google Scholar 

  89. Shen JB and Ogren WL (1992) Alteration of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase activase activities by sitedirected mutagenesis. Plant Physiol 99: 1201–1207

    Google Scholar 

  90. Shen JB, Orozco EM and Ogren WL (1991) Expression of the two isoforms of spinach ribulose 1,5-bisphosphate carboxylase activase and essentiality of the conserved lysine in the consensus nucleotide-binding domain. J Biol Chem 266: 8963–8968

    Google Scholar 

  91. Somerville CR, Portis AR Jr and Ogren WL (1982) A mutant of Arabidopsis thaliana which lacks activation of RuBP carboxylase in vivo. Plant Physiol 70: 381–387

    Google Scholar 

  92. Spreitzer RJ (1999) Questions about the complexity of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase. Photosynth Res 60: 29–42

    Google Scholar 

  93. Spreitzer RJ and Salvucci ME (2002) RUBISCO: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53: 449–485

    Google Scholar 

  94. Taylor TC and Andersson I (1996) Structural transitions during activation and ligand binding in hexadecameric Rubisco inferred from the crystal structure of the activated unliganded spinach enzyme. Nature Struct Biol 3: 95–101

    Google Scholar 

  95. Taylor TC and Andersson I (1997) The structure of the complex between Rubisco and its natural substrate ribulose 1,5-bisphosphate. J Mol Biol 265: 432–444

    Google Scholar 

  96. To KY, Suen DF and Chen SCG (1999) Molecular characterization of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in rice leaves. Planta 209: 66–76

    Google Scholar 

  97. van de Loo FJ and Salvucci ME (1996) Activation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) involves Rubisco activase Trp16. Biochemistry 35: 8143–8148

    Google Scholar 

  98. van de Loo FJ and Salvucci ME (1998) Involvement of two aspartate residues of Rubisco activase in coordination of the ATP γ-phosphate and subunit cooperativity. Biochemistry 37: 4621– 4625

    Google Scholar 

  99. Walker DA (1973) Photosynthetic induction phenomena and the light activation of ribulose diphosphate carboxylase. New Phytol 72: 209–235

    Google Scholar 

  100. Wang ZY and Portis AR Jr (1992) Dissociation of ribulose-1,5-bisphosphate bound to ribulose-1,5-bisphosphate carboxylase/oxygenase and its enhancement by ribulose-1,5-bisphosphate carboxylase/oxygenase activase-mediated hydrolysis of ATP. Plant Physiol 99: 1348–1353

    Google Scholar 

  101. Wang ZY, Ramage RT and Portis AR Jr (1993) Mg2+ and ATP or adenosine 5?-[γ-thio]-triphosphate (ATPγ S) enhances intrinsic fluorescence and induces aggregation which increases the activity of spinach Rubisco activase. Biochim Biophys Acta 1202: 47–55

    Google Scholar 

  102. Wang ZY, Synder GW, Esau BD, Portis AR Jr and Ogren WL (1992) Species-dependent variation in the interaction of substrate-bound ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase. Plant Physiol 100: 1858–1862

    Google Scholar 

  103. Weis E (1981a) Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151: 33–39

    Google Scholar 

  104. Weis E (1981b) The temperature-sensitivity of dark-inactivation and light-activation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. FEBS Lett 129: 197–200

    Google Scholar 

  105. Weis E and Berry JA (1988) Plants and high temperature stress. In: Long SP and Woodward FI (eds) Plants and Temperature, pp 327–346. Society of Experimental Botany, Cambridge, UK

    Google Scholar 

  106. Werneke JM, Zielinski RE and Ogren WL (1988) Structure and expression of spinach leaf complementary DNA encoding ribulose bisphosphate carboxylase-oxygenase activase. Proc Natl Acad Sci USA 85: 787–791

    Google Scholar 

  107. Werneke JM, Chatfield JM and Ogren WL (1989) Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis. Plant Cell 1: 815–825

    Google Scholar 

  108. Woodrow IE, Kelly ME and Mott KA (1996) Limitation of the rate of ribulosebisphosphate carboxylase activation by carbamylation and ribulosebisphosphate carboxylase activase activity – development and tests of a mechanistic model. Aust J Plant Physiol 23: 141–149

    Google Scholar 

  109. Yokota A and Tsujimoto N (1992) Characterization of ribulose-1,5-bisphosphate carboxylase/oxygenase carrying ribulose 1,5-bisphosphate at its regulatory sites and the mechanism of interaction of this form of the enzyme with ribulose-1,5-bisphosphatecarboxylase/ oxygenase activase. Eur J Biochem 204: 901–909

    Google Scholar 

  110. Zhang N and Portis AR Jr (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci USA 96: 9438–9443

    Google Scholar 

  111. Zhang N, Kallis RP, Ewy RG and Portis AR Jr (2002) Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc Natl Acad Sci USA 99: 3330–3334

    Google Scholar 

  112. Zhang N, Schürmann P and Portis AR Jr (2001) Characterization of the regulatory function of the 46-kDa isoform of Rubisco activase from Arabidopsis. Photosynth Res 68: 29–37

    Google Scholar 

  113. Zhang ZL and Komatsu S (2000) Molecular cloning and characterization of cDNAs encoding two isoforms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in rice (Oryza sativa L.). J Biochem 128: 383–389

    Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Portis, A.R. Rubisco activase – Rubisco's catalytic chaperone. Photosynthesis Research 75, 11–27 (2003). https://doi.org/10.1023/A:1022458108678

Download citation

  • activase
  • chaperone
  • enzyme regulation
  • photosynthesis
  • protein-protein interaction
  • Rubisco
  • temperature stress