Abstract
Rubisco, the primary carboxylating enzyme in photosynthesis, must be activated to catalyze CO2 fixation. The concept of an ‘activase’, a specific protein for activating Rubisco, was first introduced in 1985 based largely on biochemical and genetic studies of a high CO2-requiring mutant of Arabidopsis (Salvucci et al. (1985) Photosynth Res 7: 193–201). Over the past ten years, details about the occurrence, structure, and properties of Rubisco activase have been elucidated. However, the mechanism of action of Rubisco activase remains elusive. This review discusses the need for and function of Rubisco activase and summarizes information about the properties and structure of Rubisco activase. The information is evaluated in the context of the mechanism of Rubisco activase.
Similar content being viewed by others
Abbreviations
- CA1-P:
-
carboxyarabinitol 1-phosphate
- PS:
-
photosystem
- Rubisco:
-
ribulose 1,5-bisphosphate carboxylase/oxygenase
- RuBP:
-
ribulose 1,5-bisphosphate
- XuBP:
-
xylulose 1,5-bisphosphate
References
Andrews TJ and Lorimer GH (1987) Rubisco: Structure, mechanisms, and prospects for improvement. In: Stumpf PK and Conn EE (eds) The Biochemistry of Plants, Vol 10, pp 131–219. Academic Press Publishers, London
Andrews TJ, Hudson GS, Mate CJ, vonCaemmerer S, Evans JR and Avridsson YBC (1995) Rubisco, the consequence of altering its expression and activation in transgenic plants. J Expt Bot 46: 1293–1300
Bahr JT and Jensen RG (1974) Ribulose diphosphate carboxylase from freshly ruptured spinach chloroplasts having an in vivo KM[CO2]. Plant Physiol 53: 39–44
Berry JA, Lorimer GH, Pierce J, Seemann JR, Meek J and Freas S (1987) Isolation, identification, and synthesis of 2-carboxyarabinitol 1-phosphate, a diurnal regulator of ribulose-bisphosphate carboxylase activity. Proc Natl Acad Sci USA 84: 734–738
Brooks A and Portis ARJr (1988) Protein-bound ribulose bisphosphate correlates with deactivation of ribulose bisphosphate carboxylase in leaves. Plant Physiol 87: 244–249
Campbell WJ and Ogren WL (1990) Electron transport through Photosystem I stimulates light activation of ribulose bisphosphate carboxylase/oxygenase (Rubisco) by Rubisco activase. Plant Physiol 94: 479–484
Campbell WJ and Ogren WL (1992) Light activation of Rubisco by Rubisco activase and thylakoid membranes. Plant Cell Physiol 33: 751–756
Campbell WJ and Ogren WL (1995) Rubisco activase activity in spinach leaf extracts. Plant Cell Physiol 36: 215–220
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
Edmondson DL, Kane HJ and Andrews TJ (1990b) Substrate isomerization inhibits ribulosebisphospate carboxylase-oxygenase during catalysis. FEBS Lett 260: 62–66
Esau BD, Snyder GE, Portis ARJr, Ogren WL (1992) Chimeric Rubisco activase proteins. Plant Physiol 99: S106
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
Gutteridge S, Parry MAJ, Burton S, Keys AJ, Mudd A, Feeney J, Servaites JC and Pierce J (1986) A nocturnal inhibitor of carboxylation in leaves. Nature 324: 274–276
Hartman FC and Harpel MR (1994) Structure, function, regulation, and assembly of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Annu Rev Biochem 63: 197–234
Hatch AL and Jensen RG (1980) Regulation of ribulose-1,5-bisphosphate carboxylase from tobacco: Changes in pH response and affinity for CO2 and Mg2+ induced by chloroplast intermediates. Arch Biochem Biophys 205: 587–594
Hayer-Hartl MK, Martin J and Hartl F-U (1995) Asymmetrical interaction of GroEL and GroES in the ATPase cycle of assisted protein folding. Science 269: 836–841
Heber U, Takahama U, Neimanis S and Shimizu-Takahama M (1982) Transport as the basis of the Kok effect. Levels of some photosynthetic intermediates and activation of light regulated enzymes during photosynthesis of chloroplasts and green leaf protoplasts. Biochim Biophys Acta 679: 289–299
Hendrick JP and Hartl F-U (1993) Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62: 349–384
Hudson GS, Dengler RE, Hattersley PW and Dengler NG (1992) Cell-specific expression of Rubisco small subunit and Rubisco activase genes in C3 and C4 species of Atriplex. Aust J Plant Physiol 19: 89–96
Jiménez ESD, Medrano L and Martínez-Barajas E (1995) Rubisco activase, a possible new member of the molecular chaperone family. Biochemistry 34: 2826–2831
Jordan DB and Chollet R (1983) Inhibition of ribulose bisphosphate carboxylase by substrate ribulose 1,5-bisphosphate. J Biol Chem 258: 13752–13758
Jordan DB and Ogren WL (1981) Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291: 513–515
Klein RR and Salvucci ME (1995) Rubisco, rubisco activase and ribulose-5-phosphate kinase gene expression and polypeptide accumulation in a tobacco mutant defective in chloroplast protein synthesis. Photosynth Res 43: 213–223
Kobza J and Edwards GE (1987) Control of photosynthesis in wheat by CO2, O2 and light intensity. Plant Cell Physiol 28: 1141–1152
Lan Y, Woodrow IE, Mott KA (1992) Light-dependent changes in ribulose bisphosphate carboxylase activase activity in leaves. Plant Physiol 99: 304–309
Li LA and Tabita FR (1994) Transcriptional control of ribulose bisphosphate carboxylase/oxygenase activase and adjacent genes in Anabaena species. J Bacter 176: 6697–6706
Li LA, 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
Lorimer GH (1979) Evidence for the existence of discrete activator and substrate sites for CO2 on ribulose-1,5-bisphosphate carboxylase. J Biol Chem 254: 5599–5601
Lorimer GH (1981) Ribulosebisphosphate carboxylase: Amino acid sequence of a peptide bearing the activator carbon dioxide. Biochemistry 20: 1236–1240
Lorimer GH and Miziorko HM (1980) Carbamate formation on the ε-amino group of a lysyl residue as the basis for the activation of ribulosebisphosphate carboxylase by CO2 and Mg2+. Biochemistry 19: 5321–5328
Lorimer GH, Badger MR and Andrews TJ (1976) The activation of ribulose-1,5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. Biochemistry 15: 529–536
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
Martino-Catt S and Ort DL (1992) Low temperature interrupts circadian regulation of transcriptional activity in chilling-sensitive plants. Proc Natl Acad USA 89: 3731–3735
Mate CJ, Hudson GS, vonCaemmerer S, Evans JR and Andrews TJ (1993) Reduction of ribulose bisphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose bisphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiol 102: 1119–1128
McKay RML, Gibbs SP and Vaughn KC (1991) RuBisCo activase is present in the pyrenoid of green algae. Protoplasma 162: 38–45
Moore BD, Kobza J and Seemann JR (1991) Measurement of 2-carboxyarabinitol 1-phosphate in plant leaves by isotope dilution. Plant Physiol 96: 208–213
Orozco BM, McClung CR, Werneke JM and Ogren WL (1993) Molecular basis of the ribulose-1,5-bisphosphate carboxylase/oxygenase activase mutation in Arabidopsis thaliana is a guanine-to-adenine transition at the 5,-splice junction of intron 3. Plant Physiol 102: 227–232
Parry MAJ, Delgado E, Vadell J, Keys AJ, Lawlor DW and Medrano H (1993) Water stress and the diurnal activity of ribulose-1,5-bisphosphate carboxylase in field grown Nicotiana tabacum genotypes selected for survival at low CO2 concentrations. Plant Physiol Biochem 31: 113–120
Perchorowicz JT and Jensen RG (1983) Photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Regulation by CO2 and O2. Plant Physiol 71: 955–960
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
Pilgrim ML and McClung CR (1993) Differential involvement of the circadian clock in the expression of genes required for ribulose-1,5-bisphosphate carboxylase/oxygenase synthesis, assembly, and activation in Arabidopsis thaliana. Plant Physiol 103: 553–564
Pon NG, Rabin BR and Calvin M (1963) Mechanism of the carboxydismutase reaction. I. The effect of preliminary incubation of substrates, metal ions, and enzyme on activity. Biochem J 338: 7–19
Portis ARJr (1990) Rubisco activase. Biochim Biophys Acta 1015: 15–28
Portis ARJr (1992) Regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activity. Annu Rev Plant Physiol Plant Mol Biol 43: 415–437
Portis ARJr, 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
Read BA and Tabita FR (1992) A hybrid ribulosebisphosphate carboxylase/oxygenase enzyme exhibiting a substantial increase in substrate specificity factor. Biochemistry 31: 5553–5560
Robinson SP and Portis ARJr (1988) Involvement of stromal ATP in the light activation of ribulose-1,5-bisphosphate carboxylase/oxygenase in intact isolated chloroplasts. Plant Physiol 86: 293–298
Robinson SP and Portis ARJr (1989) Adenosine triphosphate hydrolysis by purified Rubisco activase. Arch Biochem Biophys 268: 93–99
Robinson SP, Streusand VJ, Chatfield JM and Portis ARJr (1988) Purification and assay of Rubisco activase from leaves. Plant Physiol 88: 1008–1014
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 94: 1837–1841
Sage RF, Sharkey TD and Seemann JR (1989) Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiol 89: 590–596
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
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
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
Salvucci ME, Portis ARJr, Ogren WL (1985) A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase/oxygenase activation in vivo. Photosynth Res 7: 193–201
Salvucci ME, Portis ARJr and Ogren WL (1986) Light and CO2 response of ribulose-1,5-bisphosphate carboxylase/oxygenase activation in Arabidopsis leaves. Plant Physiol 80: 655–659
Salvucci ME, Portis ARJr, Heber U and Ogren WL (1987a) Stimulation of thylakoid energization and ribulose-bisphosphate carboxylase/oxygenase activation in Arabidopsis leaves by methyl viologen. FEBS Lett 221: 215–220
Salvucci ME, Werneke JM, Ogren WL and Portis ARJr (1987b) Purification and species distribution of Rubisco activase. Plant Physiol 84: 930–936
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. J Biol Chem 268: 14239–14244
Salvucci ME, Chavan AJ, Klein RR, Rajagoplan K, Haley BE (1994) Photoaffinity labeling of the ATP binding domain of Rubisco activase and a separate domain involved in the activation of Rubisco. Biochemistry 33: 14879–14886
Schmieden-Kompalla U, Hartmann U, Korthals S and Wild A (1989) Activity and activation state of ribulose-1,5-bisphosphate carboxylase of spruce trees with varying degrees of damage relative to the occurrence of novel forest decline. Photosynth Res 21: 161–169
Schneider G, Lindqvist Y and Branden CI (1992) RUBISCO: Structure and mechanism. Annu Rev. Biophys Biomol Struct 21: 119–143
Schreuder HA, Knight S, Curmi PMG, Andersson I, Cascio D, Brändén C-I 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
Sharkey TD, Seemann JR and Berry JA (1986) Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to changing partial pressure of O2 and light in Phaseolus vulgaris. Plant Physiol 81: 788–791
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
Shen JB, Orozco EMJr 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
Sicher RC, Hatch AL, Stumpf DK and Jensen RG (1981) Ribulose 1,5-bisphosphate and activation of the carboxylase in the chloroplast. Plant Physiol 68: 252–255
Somerville CR, Portis ARJr and Ogren WL (1982) A mutant of Arabidopsis thaliana which lacks activation of RuBP carboxylase in vivo. Plant Physiol 70: 381–387
Streusand VJ and Portis ARJr (1987) Rubisco activase mediates ATP-dependent activation of ribulose bisphosphate carboxylase. Plant Physiol 85: 152–154
van deLoo FJ and Salvucci ME (1985) Identification of the Rubisco activase site of interaction with Rubisco. Plant Physiol 108: S90
vonCaemmerer S and Edmondson DL (1986) Relationship between steady-state gas exchange, in vivo ribulose bisphosphate carboxylase activity and some carbon reduction cycle intermediates in Raphanus sativus. Aust J Plant Physiol 13: 669–688
Wang ZY and Portis ARJr (1991) A fluorometric study with 1-anilinonaphthalene-8-sulfonic acid (ANS) of the interactions of ATP and ADP with rubisco activase. Biochim Biophys Acta 1079: 263–267
Wang ZY and Portis ARJr (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
Wang ZY, Snyder GW, Esau BD, Portis ARJr 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
Wang ZY, Ramage RT and Portis ARJr (1993) Mg2+ and ATP or adenosine 5′-[γ-thio]-triphosphate (ATPγS) enhances intrinsic fluorescence and induces aggregation which increases the activity of spinach Rubisco activase. Biochim Biophys Acta 1202: 47–55
Werneke JM, Chatfield JM and Ogren WL (1988a) Catalysis of ribulosebisphosphate carboxylase/oxygenase activation by the product of a Rubisco activase cDNA clone expressed in Escherichia coli. Plant Physiol 87: 917–920
Werneke JM, Zielinski RE and Ogren WL (1988b) Structure and expression of spinach leaf cDNA encoding ribulosebisphosphate carboxylase/oxygenase activase. Proc Natl Acad Sci USA 85: 787–791
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
Yokota A (1991) Carboxylation and detoxification of xylulose bisphosphate by spinach ribulose bisphosphate carboxylate/oxygenase. Plant Cell Physiol 32: 755–762
Zhu G and Jensen RG (1991a) Xylulose 1,5-bisphosphate synthesized by ribulose 1,5-bisphosphate carboxylase/oxygenase during catalysis binds to decarbamylated enzyme. Plant Physiol 97: 1348–1353
Zhu G and Jensen RG (1991b) Fallover of ribulose 1,5-bisphosphate carboxylase/oxygenase activity. Decarbamylation of catalytic sites depends on pH. Plant Physiol 97: 1354–1358
Zielinski RE, Werneke JM and Jenkins ME (1989) Coordinate expression of Rubisco activase and Rubisco during barley leaf cell development. Plant Physiol 90: 516–521
Author information
Authors and Affiliations
Additional information
The US Government right to retain a non-exclusive, royalty-free licence in and to any copyright is acknowledged.
Rights and permissions
About this article
Cite this article
Salvucci, M.E., Ogren, W.L. The mechanism of Rubisco activase: Insights from studies of the properties and structure of the enzyme. Photosynth Res 47, 1–11 (1996). https://doi.org/10.1007/BF00017748
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00017748