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Award Review

Revisiting RuBisCOFootnote

Pages 2039-2049 | Received 08 Jun 2017, Accepted 21 Aug 2017, Published online: 27 Sep 2017

References

  • Benson AA, Bassham JA, Calvin M, et al. The path of carbon in photosynthesis. V. Paper chromatography and radioautography of the products. J Assoc Chem Soc. 1950; 72(4): 1710–1718.10.1021/ja01160a080
  • Paulsen JM, Lane MD. Spinach ribulose diphosphate carboxylase. I. Purification and properties of the enzyme. Biochemistry. 1966;5(7):2350–2357.10.1021/bi00871a025
  • Ogren WL, Bowes G. Ribulose diphosphate carboxylase regulates soybean photorespiration. Nat New Biol. 1971;230(13):159–160.10.1038/newbio230159a0
  • Laign WA, Ogren WL, Hageman RH. Bicarbonate stabilization of ribulose 1,5-diphosphate carboxylase. Biochemistry. 1975;14(10):2269–2275.
  • Lorimer GH, Badger MR, Andrews TJ. The activation of ribulose-1,5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. Biochemistry. 1976;15(3):529–536.10.1021/bi00648a012
  • Farquhar GD, von Caemmerer S, Berry JA. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta. 1980;149(1):78–90.10.1007/BF00386231
  • Boyer JS. Plant productivity and environment. Science. 1982;218(4571):443–448.10.1126/science.218.4571.443
  • Tcherkez GG1, Farquhar GD, Andrews TJ. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA. 2006;103(19):7246–7251.10.1073/pnas.0600605103
  • Yokota A, Shigeoka S. Engineering photosynthetic pathways. In: Bohnert HJ, Nguyen HT, editors. Bioengineering and molecular biology of plant pathways, Volume 1. In: Lewis NG, executive editor. Advances in plant biochemistry and molecular biology. Dordrecht: Elsevier; 2008. p. 81–105.10.1016/S1755-0408(07)01004-1
  • Bowes G, Ogren WL, Hageman RH. Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem Biophys Res Commun. 1971;45(3):716–722.10.1016/0006-291X(71)90475-X
  • Ku SB, Edwards GE. Oxygen inhibition of photosynthesis: I. temperature dependence and relation to O2/CO2 solubility ratio. Plant Physiol. 1977;59(5):986–990.10.1104/pp.59.5.986
  • Ashida H, Yokota A. Increasing photosynthesis/RuBisCO and CO2-concentrating mechanisms. In: Murray M-Y, editor. Comprehensive biotechnology. 2nd ed. Vol. 4. Dordrecht: Elsevier; 2011. p. 165–176.10.1016/B978-0-08-088504-9.00243-9
  • Roy H, Andrews TJ. Rubisco: assembly and mechanism. In: Leegood RC, Sharkey TD, von Caemmerer S, editors. Photosynthesis: physiology and metabolism. Dordrecht: Kluwer, Elsevier; 2000. p. 53–83.10.1007/0-306-48137-5
  • Jordan DB, Ogren WL. Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase. Nature. 1981;291(5815):513–515.10.1038/291513a0
  • Uemura K, Anwaruzzaman MS, Yokota A. Ribulose-1,5-bisphosphate carboxylase/oxygenase from thermophilic red algae with a strong specificity for CO2 fixation. Biochem Biophys Res Commun. 1997;233(2):568–571.10.1006/bbrc.1997.6497
  • Wang Y, Stessman DJ, Spalding MH. The CO2 concentrating mechanism and photosynthetic carbon assimilation in limiting CO2: how Chlamydomonas works against the gradient. Plant J. 2015;82(3):429–448.10.1111/tpj.12829
  • Andrews TJ, Whitney SM. Manipulating ribulose bisphosphate carboxylase/oxygenase in the chloroplasts of higher plants. Arch Biochem Biophys. 2003;414(2):159–169.
  • Lorimer GH, Miziorko HM. Carbamate formation on the epsilon-amino group of a lysyl residue as the basis for the activation of ribulosebisphosphate carboxylase by CO2 and Mg2+. Biochemistry. 1980;19(23):5321–5328.10.1021/bi00564a027
  • Taylor TC, Andersson I. Structural transitions during activation and ligand binding in hexadecameric Rubisco inferred from the crystal structure of the activated unliganded spinach enzyme. Nat Struct Biol. 1996;3(1):95–101.10.1038/nsb0196-95
  • Cleland WW, Andrews TJ, Gutteridge S, et al. Mechanism of Rubisco: the carbamate as general base. Chem Rev. 1998;98(2):549–562.10.1021/cr970010r
  • Habash DZ1, Parry MA, Parmar S, et al. The regulation of component processes of photosynthesis in transgenic tobacco with decreased phosphoribulokinase activity. Photosynth Res. 1996;49(2):159–167.10.1007/BF00117666
  • Somerville CR, Portis AR, Ogren WL. A mutant of Arabidopsis thaliana which lacks activation of RuBp carboxylase in vivo. Plant Physiol. 1982;70(2):381–387.10.1104/pp.70.2.381
  • Portis AR Jr, Li C, Wang D, et al. Regulation of Rubisco activase and its interaction with Rubisco. J Exp Bot. 2008;59(7):1597–1604.
  • Yamori W, Nagai T, Makino A, The rate-limiting step for CO2 assimilation at different temperatures is influenced by the leaf nitrogen content in several C3 crop species. Plant Cell Environ. 2011;34(5):764–777.
  • Makino A, Sage RF. Temperature response of photosynthesis in transgenic rice transformed with ‘sense’ or ‘antisense’ rbcS. Plant Cell Physiol. 2007;48(10):1472–1483.10.1093/pcp/pcm118
  • Kubien DS, Sage RF. The temperature response of photosynthesis in tobacco with reduced amounts of Rubisco. Plant Cell Environ. 2008;31(4):407–418.10.1111/j.1365-3040.2008.01778.x
  • Fukayama H, Ueguchi C, Nishikawa K, et al. Overexpression of Rubisco activase decreases the photosynthetic CO2 assimilation rate by reducing Rubisco content in rice leaves. Plant Cell Physiol. 2012 Jun;53(6):976–986.10.1093/pcp/pcs042
  • McCann N, Phan D, Wang X, et al. Kinetics and mechanism of carbamate formation from CO2(aq), carbonate species, and monoethanolamine in aqueous solution. J Phys Chem A. 2009;113(17):5022–5029.10.1021/jp810564z
  • Vater S, Salnikow J, Kleinkauf H. A fluorimetric study of substrate and effector binding of D-ribulose-1,5-biphosphate carboxylase/oxygenase from spinach. Biochem Biophys Res Commun. 1977;74(4):1618–1625.10.1016/0006-291X(77)90628-3
  • Stotz M, Mueller-Cajar O, Ciniawsky S, et al. Structure of green-type Rubisco activase from tobacco. Nat Struct Mol Biol. 2011;18(12):1366–1370.10.1038/nsmb.2171
  • Mueller-Cajar O, Stotz M, Wendler P, et al. Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase. Nature. 2011;479(7372):194–199.10.1038/nature10568
  • Salvucci ME, Portis AR Jr, Ogren WL, A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase/oxygenase activation in vivo. Photosynth Res. 1985;7(2):193–201.
  • Eckardt NA1, Snyder GW, Portis AR Jr, et al, 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. 1997;113(2):575–586.10.1104/pp.113.2.575
  • Mate CJ, von Caemmerer S, Evans JR, et al. 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. 1996;198(4):604–613.10.1007/BF00262648
  • Hammond ET, Andrews TJ, Mott KA, et al. Regulation of Rubisco activation in antisense plants of tobacco containing reduced levels of Rubisco activase. Plant J. 1998;14(1):101–110.10.1046/j.1365-313X.1998.00103.x
  • Lan Y, Mott KA. Determination of apparent km values for ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase using the spectrophotometric assay of Rubisco activity. Plant Physiol. 1991;95(2):604–609.10.1104/pp.95.2.604
  • McCurry SD, Pierce J, Tolbert NE, et al. On the mechanism of effector-mediated activation of ribulose bisphosphate carboxylase/oxygenase. J Biol Chem. 1981 Jul 10;256(13):6623–6628.
  • Gutteridge S, Parry MA, Schmidt CN. The reactions between active and inactive forms of wheat ribulosebisphosphate carboxylase and effectors. Eur J Biochem. 1982;126(3):597–602.10.1111/ejb.1982.126.issue-3
  • Jordan DB, Chollet R, Ogren WL. Binding of phosphorylated effectors by active and inactive forms of ribulose- 1, s, -bisphosphate carboxylase. Biochemistry. 1983;22(14):3410–3418.10.1021/bi00283a017
  • Zhu G, Jensen RG. Fallover of ribulose 1,5-bisphosphate carboxylase/oxygenase activity : decarbamylation of catalytic sites depends on pH. Plant Physiol. 1991;97(4):1354–1358.10.1104/pp.97.4.1354
  • Badger MR, Lorimer GH. Interaction of sugar phosphates with the catalytic site of ribulose-1,5-bisphosphate carboxylase. Biochemistry. 1981;20(8):2219–2225.10.1021/bi00511a023
  • Matsumura H, Mizohata E, Ishida H, et al. Crystal structure of rice Rubisco and implications for activation induced by positive effectors NADPH and 6-phosphogluconate. J Mol Biol. 2012;422(1):75–86.10.1016/j.jmb.2012.05.014
  • Heineke D, Riens B, Grosse H. Redox transfer across the inner chloroplast envelope membrane. Plant Physiol. 1991 Apr;95(4):1131–1137.10.1104/pp.95.4.1131
  • Buchanan BB. Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development. Arch Biochem Biophys. 1991;288(1):1–9.10.1016/0003-9861(91)90157-E
  • Badger MR, Sharkey TD, von Caemmerer S. The relationship between steady-state gas exchange of bean leaves and the levels of carbon-reduction-cycle intermediates. Planta. 1984 Mar;160(4):305–313.10.1007/BF00393411
  • Dumas R, Joyard J, Douce R. Effect of sulphate on glutamate synthesis by intact spinach (Spinacia oleracea) chloroplasts. Biochem J. 1989;259(3):769–774.10.1042/bj2590769
  • Martin W, Scheibe R, Schnarrenberger C, The Calvin cycle and its regulation. In Leegood RC, Sharkey TD, von Caemmerere S, editors. Photosynthesis: physiology and metabolism. Alphen aan den Rijn: Kluwer; 2000. p. 9–51, 10.1007/0-306-48137-5
  • Price GD, Evans JR, von Caemmerer S, et al. Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta. 1995;195(3):369–378.10.1007/BF00202594
  • Banks FM, Driscoll SP, Parry MA, et al. Decrease in phosphoribulokinase activity by antisense RNA in transgenic tobacco. relationship between photosynthesis, growth, and allocation at different nitrogen levels. Plant Physiol. 1999;119(3):1125–1136.10.1104/pp.119.3.1125
  • Haake V, Zrenner R, Sonnewald U, et al. A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant J. 1998;14(2):147–157.10.1046/j.1365-313X.1998.00089.x
  • Quick WP, Schurr U, Scheibe R. Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS : I. Impact on photosynthesis in ambient growth conditions. Planta. 1991;183(4):542–554.
  • Hudson GS1, Evans JR, von Caemmerer S, Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiol. 1992;98(1):294–302.10.1104/pp.98.1.294
  • Kossmann J, Uwe Sonnewald U, Willmitzer L. Reduction of the chloroplastic fructose-1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J. 1994;6(5):637–650.10.1046/j.1365-313X.1994.6050637.x
  • Harrison EP, Olcer H, Lloyd JC, et al. Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity. J Exp Bot. 2001;52(362):1779–1784.10.1093/jexbot/52.362.1779
  • Tamoi M, Murakami A, Takeda T, et al. Acquisition of a new type of fructose-1,6-bisphosphatase with resistance to hydrogen peroxide in cyanobacteria: molecular characterization of the enzyme from Synechocystis PCC 6803. Biochim Biophys Acta. 1998;1383(2):232–244.10.1016/S0167-4838(97)00208-2
  • Miyagawa Y, Tamoi M, Shigeoka S. Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat Biotechnol. 2001 Oct;19(10):965–969.10.1038/nbt1001-965
  • Yabuta Y, Tamoi M, Yamamoto K, et al. Molecular design of photosynthesis-elevated chloroplasts for mass accumulation of a foreign protein. Plant Cell Physiol. 2008;49(3):375–385.10.1093/pcp/pcn014
  • Portis AR1, Salvucci ME, Ogren WL, Activation of ribulosebisphosphate carboxylase/cxygenase at physiological CO2 and ribulosebisphosphate concentrations by Rubisco activase. Plant Physiol. 1986;82(4):967–971.10.1104/pp.82.4.967
  • Yokota A. Ribulose bisphosphate-induced, slow conformational changes of spinach ribulose bisphosphate carboxylase cause the two types of inflections in the course of its carboxylase reaction. J Biochem. 1991;110(2):246–252.10.1093/oxfordjournals.jbchem.a123565
  • Yokota A, Higashioka M, Wadano A. Cooperative binding of carboxyarabinitol bisphosphate to the regulatory sites of ribulose bisphosphate carboxylase/oxygenase from spinach. J Biochem. 1991;110(2):253–256.10.1093/oxfordjournals.jbchem.a123566
  • Yokota A, Higashioka M, Wadano A. Regulation of the activity of ribulose-1,5-bisphosphate carboxylase/oxygenase through cooperative binding of 6-phosphogluconate to its regulatory sites. Eur J Biochem. 1992;208(3):721–727.10.1111/ejb.1992.208.issue-3
  • Perchorowicz JT, Jensen RG. Photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings : regulation by CO2 and O2. Plant Physiol. 1983;71(4):955–960.10.1104/pp.71.4.955
  • Takahara K, Kasajima I, Takahashi H. Metabolome and photochemical analysis of rice plants overexpressing Arabidopsis NAD kinase gene. Plant Physiol. 2010;152(4):1863–1873.10.1104/pp.110.153098
  • Cardona T, Murray JW, Rutherford AW. Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Mol Biol Evol. 2015;32(5):1310–1328.10.1093/molbev/msv024
  • Ezaki S, Maeda N, Kishimoto T, et al. Presence of a structurally novel type ribulose-bisphosphate carboxylase/oxygenase in the hyperthermophilic archaeon, Pyrococcus kodakaraensis KOD1. J Biol Chem. 1999 Feb 19;274(8):5078–5082.10.1074/jbc.274.8.5078
  • Tabita FR. Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a different perspective. Photosynth Res. 1999;60(1):1–28.10.1023/A:1006211417981
  • Sato T, Atomi H, Imanaka T. Archaeal Type III RuBisCOs function in a pathway for AMP metabolism. Science. 2007;315(5814):1003–1006.10.1126/science.1135999
  • Hanson TE, Tabita FR. A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci USA. 2001;98(8):4397–4402.10.1073/pnas.081610398
  • Ashida H, Saito Y, Kojima C. A functional link between RuBisCO-like protein of bacillus and photosynthetic RuBisCO. Science. 2003;302(5643):286–290.10.1126/science.1086997
  • Ashida H, Saito Y, Nakano T, et al. RuBisCO-like proteins as the enolase enzyme in the methionine salvage pathway: functional and evolutionary relationships between RuBisCO-like proteins and photosynthetic RuBisCO. J Exp Bot. 2008;59(7):1543–1554.
  • Tabita FR, Hanson TE, Li H, et al. Function, structure, and evolution of the rubisco-like proteins and their RubisCO homologs. Microbiol Mol Biol Rev. 2007 Dec;71(4):576–599.10.1128/MMBR.00015-07
  • Mueller-Cajar O, Badger MR. New roads lead to Rubisco in archaebacteria. BioEssays. 2007 Aug;29(8):722–724.10.1002/bies.v29:8
  • Kono T, Mehrotra S, Endo C, et al. A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea. Nat Commun. 2017;8:14007. doi:10.1038/ncomms14007.
  • Kasting JF, Pollack JB, Effects of high CO2 levels on surface temperature and atmospheric oxidation state of the early Earth. J Atmos Chem. 1984(4);1:403–428.10.1007/BF00053803
  • Bartoschek S, Vorholt JA, Thauer RK, et al. N-Carboxymethanofuran (carbamate) formation from methanofuran and CO2 in methanogenic archaea: Thermodynamics and kinetics of the spontaneous reaction. Eur J Biochem. 2000;267(11):3130–3138.10.1046/j.1432-1327.2000.01331.x

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