Rubisco: structure, regulatory interactions, and possibilities for a better enzyme.

Ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco) catalyzes the first step in net photosynthetic CO2 assimilation and photorespiratory carbon oxidation. The enzyme is notoriously inefficient as a catalyst for the carboxylation of RuBP and is subject to competitive inhibition by O2, inactivation by loss of carbamylation, and dead-end inhibition by RuBP. These inadequacies make Rubisco rate limiting for photosynthesis and an obvious target for increasing agricultural productivity. Resolution of X-ray crystal structures and detailed analysis of divergent, mutant, and hybrid enzymes have increased our insight into the structure/function relationships of Rubisco. The interactions and associations relatively far from the Rubisco active site, including regulatory interactions with Rubisco activase, may present new approaches and strategies for understanding and ultimately improving this complex enzyme.

[1]  M. Salvucci,et al.  Factors affecting the activation state and the level of total activity of ribulose bisphosphate carboxylase in tobacco protoplasts. , 1987, Plant physiology.

[2]  D. Eisenberg,et al.  Crystal structure of activated tobacco rubisco complexed with the reaction‐intermediate analogue 2‐carboxy‐arabinitol 1, 5‐bisphosphate , 1993, Protein science : a publication of the Protein Society.

[3]  I. Andersson,et al.  The structure of the complex between rubisco and its natural substrate ribulose 1,5-bisphosphate. , 1997, Journal of molecular biology.

[4]  S. Komatsu,et al.  Molecular cloning and characterization of cDNAs encoding two isoforms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in rice (Oryza sativa L.). , 2000, Journal of biochemistry.

[5]  F. Tabita.  Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: A different perspective , 1999, Photosynthesis Research.

[6]  G. W. Snyder,et al.  Differential effects of N- and C-terminal deletions on the two activities of rubisco activase. , 1996, Archives of Biochemistry and Biophysics.

[7]  I. Andersson,et al.  A Common Structural Basis for the Inhibition of Ribulose 1,5-Bisphosphate Carboxylase by 4-Carboxyarabinitol 1,5-Bisphosphate and Xylulose 1,5-Bisphosphate* , 1996, The Journal of Biological Chemistry.

[8]  T. Andrews,et al.  The CO2/O2 specificity of single-subunit ribulose-bisphosphate carboxylase from the dinoflagellate, Amphidinium carterae , 1998 .

[9]  S. Ruuska,et al.  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. , 2000, Plant physiology.

[10]  I. Andersson,et al.  Crystallographic analysis of ribulose 1,5-bisphosphate carboxylase from spinach at 2.4 A resolution. Subunit interactions and active site. , 1990, Journal of molecular biology.

[11]  F. C. Hartman,et al.  Role of asparagine-111 at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase from Rhodospirillum rubrum as explored by site-directed mutagenesis. , 1992, The Journal of biological chemistry.

[12]  T. Andrews,et al.  Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. , 1992, Plant physiology.

[13]  G. W. Snyder,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 , 1997, Plant physiology.

[14]  A. Portis,et al.  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?) , 1997, Plant physiology.

[15]  T. Andrews,et al.  Directed mutation of the Rubisco large subunit of tobacco influences photorespiration and growth. , 1999, Plant physiology.

[16]  R. Horgan,et al.  Abscisic acid biosynthesis in roots , 1992, Planta.

[17]  I. Khrebtukova,et al.  Elimination of the Chlamydomonas gene family that encodes the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  B. Read,et al.  Catalytic properties of recombinant octameric, hexadecameric, and heterologous cyanobacterial/bacterial ribulose- 1,5-bisphosphate carboxylase/oxygenase. , 1991, Archives of biochemistry and biophysics.

[19]  S. Gutteridge.  The relative catalytic specificities of the large subunit core of Synechococcus ribulose bisphosphate carboxylase/oxygenase. , 1991, The Journal of biological chemistry.

[20]  K. Andersen.  Mutations altering the catalytic activity of a plant-type ribulose biphosphate carboxylase/oxygenase in Alcaligenes eutrophus. , 1979, Biochimica et biophysica acta.

[21]  Y. Kai,et al.  Crystal Structure of Carboxylase Reaction-oriented Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase from a Thermophilic Red Alga, Galdieria partita * , 1999, The Journal of Biological Chemistry.

[22]  G. Lorimer,et al.  Carbamate formation on the epsilon-amino group of a lysyl residue as the basis for the activation of ribulosebisphosphate carboxylase by CO2 and Mg2+. , 1980, Biochemistry.

[23]  M. Salvucci.  Subunit interactions of Rubisco activase: polyethylene glycol promotes self-association, stimulates ATPase and activation activities, and enhances interactions with Rubisco. , 1992, Archives of biochemistry and biophysics.

[24]  Lih-Ann Li,et al.  The Rubisco activase (rca) gene is located downstream from rbcS in Anabaena sp. strain CA and is detected in other Anabaena/Nostoc strains , 1993, Plant Molecular Biology.

[25]  A. Portis,et al.  Ribulose-1,5-bisphosphate carboxylase/oxygenase activase protein prevents the in vitro decline in activity of ribulose-1,5-bisphosphate carboxylase/oxygenase. , 1989, Plant physiology.

[26]  A. Yokota,et al.  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-bisphosphate-carboxylase/oxygenase activase. , 1992, European journal of biochemistry.

[27]  F. C. Hartman,et al.  Mechanistic insights provided by deletion of a flexible loop at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase. , 1995, Biochemistry.

[28]  F. C. Hartman,et al.  Evidence supporting lysine 166 of Rhodospirillum rubrum ribulosebisphosphate carboxylase as the essential base which initiates catalysis. , 1988, The Journal of biological chemistry.

[29]  A. Portis,et al.  Mg2+ and ATP or adenosine 5′-[γ-thio]-triphosphate (ATPγS) enhances intrinsic fluorescence and induces aggregation which increases the activity of spinach Rubisco activase , 1993 .

[30]  M. Morell,et al.  Side Reactions Catalyzed by Ribulose-bisphosphate Carboxylase in the Presence and Absence of Small Subunits* , 1997, The Journal of Biological Chemistry.

[31]  R. J. Spreitzer,et al.  C172S Substitution in the Chloroplast-encoded Large Subunit Affects Stability and Stress-induced Turnover of Ribulose-1,5-bisphosphate Carboxylase/Oxygenase* , 1999, The Journal of Biological Chemistry.

[32]  R. J. Spreitzer,et al.  Directed mutagenesis of chloroplast ribulosebisphosphate carboxylase/oxygenase. Substitutions at large subunit asparagine 123 and serine 379 decrease CO2/O2 specificity. , 1994, The Journal of biological chemistry.

[33]  I. Andersson,et al.  First Crystal Structure of Rubisco from a Green Alga,Chlamydomonas reinhardtii * , 2001, The Journal of Biological Chemistry.

[34]  R. J. Spreitzer,et al.  Complementing substitutions within loop regions 2 and 3 of the alpha/beta-barrel active site influence the CO2/O2 specificity of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase. , 1994, Biochemistry.

[35]  D. Jordan,et al.  Inhibition of ribulose bisphosphate carboxylase by substrate ribulose 1,5-bisphosphate. , 1983, The Journal of biological chemistry.

[36]  T. Andrews,et al.  Substrate isomerization inhibits ribulosebisphospate carboxylase‐oxygenase during catalysis , 1990 .

[37]  R. J. Spreitzer,et al.  Directed Mutagenesis of Chloroplast Ribulose-1,5-bisphosphate Carboxylase/Oxygenase , 1996, The Journal of Biological Chemistry.

[38]  S. Parmar,et al.  Effect of mutations of residue 340 in the large subunit polypeptide of Rubisco from Anacystis nidulans. , 1998, European journal of biochemistry.

[39]  F. Tabita,et al.  Expression of glnB and aglnB-Like Gene (glnK) in a Ribulose Bisphosphate Carboxylase/Oxygenase-Deficient Mutant of Rhodobacter sphaeroides , 1998, Journal of bacteriology.

[40]  Kensaku Suzuki.  Phosphoglycolate Phosphatase-Defident Mutants of Chlamydomonas reinhardtii Capable of Growth under Air , 1995 .

[41]  S. Hemmingsen,et al.  Co-expression of plastid chaperonin genes and a synthetic plant Rubisco operon in Escherichia coli , 1993, Plant Molecular Biology.

[42]  F. C. Hartman,et al.  A Signature of the Oxygenase Intermediate in Catalysis by Ribulose-bisphosphate Carboxylase/Oxygenase as Provided by a Site-directed Mutant(*) , 1995, The Journal of Biological Chemistry.

[43]  G. Farquhar,et al.  Reduction of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase by Antisense RNA in the C4 Plant Flaveria bidentis Leads to Reduced Assimilation Rates and Increased Carbon Isotope Discrimination , 1997, Plant physiology.

[44]  T. Andrews,et al.  The Gene for the Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (Rubisco) Small Subunit Relocated to the Plastid Genome of Tobacco Directs the Synthesis of Small Subunits That Assemble into Rubisco , 2001, Plant Cell.

[45]  W. Laing,et al.  Regulation of Soybean Net Photosynthetic CO(2) Fixation by the Interaction of CO(2), O(2), and Ribulose 1,5-Diphosphate Carboxylase. , 1974, Plant physiology.

[46]  S. Rothstein,et al.  Co-expression of both the maize large and wheat small subunit genes of ribulose-bisphosphate carboxylase in Escherichia coli. , 1987, European journal of biochemistry.

[47]  M. Edelman,et al.  A point mutation in the gene for the large subunit of ribulose 1,5‐bisphosphate carboxylase/oxygenase affects holoenzyme assembly in Nicotiana tabacum. , 1989, The EMBO journal.

[48]  H. Bohnert,et al.  Identification of an assembly domain in the small subunit of ribulose-1,5-bisphosphate carboxylase. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[49]  A. Fersht,et al.  Mutation of asparagine 111 of rubisco from Rhodospirillum rubrum alters the carboxylase/oxygenase specificity. , 1992, Journal of molecular biology.

[50]  E. M. Larson,et al.  Specificity for Activase Is Changed by a Pro-89 to Arg Substitution in the Large Subunit of Ribulose-1,5-bisphosphate Carboxylase/Oxygenase* , 1997, The Journal of Biological Chemistry.

[51]  P. Maliga,et al.  Plastome engineering of ribulose-1,5-bisphosphate carboxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. , 1999, Plant physiology.

[52]  Y. Du,et al.  RbcS suppressor mutations improve the thermal stability and CO2/O2 specificity of rbcL- mutant ribulose-1,5-bisphosphate carboxylase/oxygenase. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[53]  B. Read,et al.  Alteration of the alpha helix region of cyanobacterial ribulose 1,5-bisphosphate carboxylase/oxygenase to reflect sequences found in high substrate specificity enzymes. , 1998, Archives of biochemistry and biophysics.

[54]  A. Portis,et al.  Activase Region on Chloroplast Ribulose-1,5-bisphosphate Carboxylase/Oxygenase , 2000, The Journal of Biological Chemistry.

[55]  F. C. Hartman,et al.  Multiple catalytic roles of His 287 of Rhodospirillum rubrum ribulose 1,5‐bisphosphate carboxylase/oxygenase , 1998, Protein science : a publication of the Protein Society.

[56]  R. J. Spreitzer,et al.  How various factors influence the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase , 1992, Photosynthesis Research.

[57]  M. Salvucci,et al.  Activation of Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (Rubisco) Involves Rubisco Activase Trp16 , 1996 .

[58]  R. Jensen,et al.  Xylulose 1,5-Bisphosphate Synthesized by Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase during Catalysis Binds to Decarbamylated Enzyme. , 1991, Plant physiology.

[59]  T. N. Bhat,et al.  The Protein Data Bank , 2000, Nucleic Acids Res..

[60]  J. Rochaix,et al.  The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas , 1998, Advances in Photosynthesis and Respiration.

[61]  T. Andrews,et al.  Rubisco: Assembly and Mechanism , 2000 .

[62]  T. Andrews.  The bait in the Rubisco mousetrap , 1996, Nature Structural Biology.

[63]  R. Ellis.  The most abundant protein in the world , 1979 .

[64]  D. Suen,et al.  Molecular characterization of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in rice leaves , 1999, Planta.

[65]  I. Andersson,et al.  Structural transitions during activation and ligand binding in hexadecameric Rubisco inferred from the crystal structure of the activated unliganded spinach enzyme , 1996, Nature Structural Biology.

[66]  W. Ogren,et al.  Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis. , 1989, The Plant cell.

[67]  G. Lorimer,et al.  Catalytic properties of a hybrid between cyanobacterial large subunits and higher plant small subunits of ribulose bisphosphate carboxylase-oxygenase. , 1985, The Journal of biological chemistry.

[68]  F. Tabita,et al.  Inactivation of the monocistronic rca gene in Anabaena variabilis suggests a physiological ribulose bisphosphate carboxylase/oxygenase activase-like function in heterocystous cyanobacteria , 1999, Plant Molecular Biology.

[69]  W. Ogren,et al.  Catalysis of Ribulosebisphosphate Carboxylase/Oxygenase Activation by the Product of a Rubisco Activase cDNA Clone Expressed in Escherichia coli. , 1988, Plant physiology.

[70]  M. Salvucci,et al.  Purification and species distribution of rubisco activase. , 1987, Plant physiology.

[71]  S. Lindquist,et al.  Subunit interactions influence the biochemical and biological properties of Hsp104. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[72]  G. Lorimer,et al.  Reaction intermediate partitioning by ribulose-bisphosphate carboxylases with differing substrate specificities. , 1986, The Journal of biological chemistry.

[73]  E. Kellogg,et al.  The structure and function of RuBisCO and their implications for systematic studies. , 1997, American journal of botany.

[74]  T. Andrews,et al.  Reduction of Ribulose Bisphosphate Carboxylase Activase Levels in Tobacco (Nicotiana tabacum) by Antisense RNA Reduces Ribulose Bisphosphate Carboxylase Carbamylation and Impairs Photosynthesis , 1993, Plant physiology.

[75]  I. Andersson,et al.  Structure of a product complex of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase. , 1997, Biochemistry.

[76]  I. Major,et al.  Is there another player in the game of Rubisco regulation , 1995 .

[77]  H. Medrano,et al.  Photosynthesis, Ribulose-1,5-bisphosphate Carboxylase and Leaf Characteristics of Nicotiana tabacum L. Genotypes Selected by Survival at Low CO2 Concentrations , 1993 .

[78]  A. Fersht,et al.  Role of phenylalanine-327 in the closure of loop 6 of ribulosebisphosphate carboxylase/oxygenase from Rhodospirillum rubrum. , 1993, Biochemistry.

[79]  G. W. Snyder,et al.  Activation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) with chimeric activase proteins , 1998, Photosynthesis Research.

[80]  R. J. Spreitzer,et al.  Chloroplast intragenic suppression enhances the low CO2/O2 specificity of mutant ribulose-bisphosphate carboxylase/oxygenase. , 1989, The Journal of biological chemistry.

[81]  R. J. Spreitzer.  Genetic Dissection of Rubisco Structure and Function , 1993 .

[82]  R. Zielinski,et al.  Organization and expression of two tandemly oriented genes encoding ribulosebisphosphate carboxylase/oxygenase activase in barley. , 1991, The Journal of biological chemistry.

[83]  A. Portis,et al.  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. , 1992, Plant physiology.

[84]  G. W. Snyder,et al.  Species-dependent variation in the interaction of substrate-bound ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) and rubisco activase. , 1992, Plant physiology.

[85]  F. C. Hartman,et al.  Mechanism of Rubisco: The Carbamate as General Base , 1998 .

[86]  R. Furbank,et al.  MOLECULAR ENGINEERING OF C4 PHOTOSYNTHESIS. , 2003, Annual review of plant physiology and plant molecular biology.

[87]  K. Roesler,et al.  Primary Structure of Chlamydomonas reinhardtii Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase Activase and Evidence for a Single Polypeptide. , 1990, Plant physiology.

[88]  M. Salvucci,et al.  Light and CO(2) Response of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Activation in Arabidopsis Leaves. , 1986, Plant physiology.

[89]  M. Salvucci,et al.  Moderately High Temperatures Inhibit Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (Rubisco) Activase-Mediated Activation of Rubisco , 1998, Plant physiology.

[90]  D. Jordan,et al.  Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase , 1981, Nature.

[91]  Y. Kai,et al.  The role of structural intersubunit microheterogeneity in the regulation of the activity in hysteresis of ribulose 1, 5-bisphosphate carboxylase/oxygenase. , 2000, Journal of biochemistry.

[92]  C. Mann.  Genetic Engineers Aim to Soup Up Crop Photosynthesis , 1999, Science.

[93]  M. Salvucci,et al.  The mechanism of Rubisco activase: Insights from studies of the properties and structure of the enzyme , 2004, Photosynthesis Research.

[94]  R. J. Spreitzer,et al.  Proteolysis and transition-state-analogue binding of mutant forms of ribulose-1,5-bisphosphate carboxylase/oxygenase from Chlamydomonas reinhardtii , 1991, Planta.

[95]  E. Hough,et al.  The crystal structure of rubisco from Alcaligenes eutrophus reveals a novel central eight-stranded beta-barrel formed by beta-strands from four subunits. , 1999, Journal of molecular biology.

[96]  A. Vázquez,et al.  Effects of hydroxy-benzaldehydes on rooting and indole-3-acetic acid-oxidase activity in bean cuttings , 1991 .

[97]  F. Tabita,et al.  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 , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[98]  M. Salvucci,et al.  Involvement of two aspartate residues of Rubisco activase in coordination of the ATP gamma-phosphate and subunit cooperativity. , 1998, Biochemistry.

[99]  M T Clegg,et al.  The evolution of plant nuclear genes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[100]  W. Ogren,et al.  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. , 1991, The Journal of biological chemistry.

[101]  G. Schneider,et al.  Crystal structure of the active site of ribulose-bisphosphate carboxylase , 1989, Nature.

[102]  A. Fersht,et al.  Role of isoleucine-164 at the active site of rubisco from Rhodospirillum rubrum. , 1997, Biochemical and biophysical research communications.

[103]  D. Jordan,et al.  The CO2/O 2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase : Dependence on ribulosebisphosphate concentration, pH and temperature. , 1984, Planta.

[104]  C. Small,et al.  Mutations in a sequence near the N-terminus of the small subunit alter the CO2/O2specificity factor for ribulose bisphosphate carboxylase/oxygenase , 1997, Photosynthesis Research.

[105]  A. Portis,et al.  Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[106]  E V Koonin,et al.  AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. , 1999, Genome research.

[107]  C. Foyer,et al.  A point mutation in the gene encoding the Rubisco large subunit interferes with holoenzyme assembly , 1996, Plant Molecular Biology.

[108]  A. Portis,et al.  Adenosine triphosphate hydrolysis by purified rubisco activase. , 1989, Archives of biochemistry and biophysics.

[109]  H. Bohnert,et al.  Replacement of a conserved arginine in the assembly domain of ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit interferes with holoenzyme formation. , 1992, The Journal of biological chemistry.

[110]  R. J. Spreitzer,et al.  Complementing amino acid substitutions within loop 6 of the alpha/beta-barrel active site influence the CO2/O2 specificity of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase. , 1991, Biochemistry.

[111]  G. Lorimer,et al.  Details of the reactions catalysed by mutant forms of rubisco , 1988 .

[112]  S. Miyachi,et al.  Ribulose-1,5-bisphosphate carboxylase/oxygenase from thermophilic red algae with a strong specificity for CO2 fixation. , 1997, Biochemical and biophysical research communications.

[113]  S. Al-Abed,et al.  Reduced CO2/O2 specificity of ribulose-bisphosphate carboxylase/oxygenase in a temperature-sensitive chloroplast mutant of Chlamydomonas. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[114]  F. C. Hartman,et al.  Structure, Function, Regulation, and Assembly of D-Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase , 1994 .

[115]  R. J. Spreitzer,et al.  Pseudoreversion Substitution at Large-Subunit Residue 54 Influences the CO2/O2 Specificity of Chloroplast Ribulose-Bisphosphate Carboxylase/Oxygenase , 1995, Plant physiology.

[116]  M. Morell,et al.  An Improved Method for Measuring the CO2/O2 Specificity of Ribulosebisphosphate Carboxylase-Oxygenase , 1994 .

[117]  P. Curmi,et al.  The transition between the open and closed states of rubisco is triggered by the inter-phosphate distance of the bound bisphosphate. , 2000, Journal of Molecular Biology.

[118]  S. Howitt,et al.  Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function , 1993, Journal of bacteriology.

[119]  J. Williams,et al.  A cyanobacterial mutant requiring the expression of ribulose bisphosphate carboxylase from a photosynthetic anaerobe. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[120]  F. C. Hartman,et al.  Chemical rescue by exogenous amines of a site-directed mutant of ribulose 1,5-bisphosphate carboxylase/oxygenase that lacks a key lysyl residue. , 1994, Biochemistry.

[121]  F. Tabita,et al.  Expression of endogenous and foreign ribulose 1,5-bisphosphate carboxylase-oxygenase (RubisCO) genes in a RubisCO deletion mutant of Rhodobacter sphaeroides , 1991, Journal of bacteriology.

[122]  I. Andersson,et al.  Large structures at high resolution: the 1.6 A crystal structure of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase complexed with 2-carboxyarabinitol bisphosphate. , 1996, Journal of molecular biology.

[123]  J. Pitts,et al.  Effect of mutation of lysine-128 of the large subunit of ribulose bisphosphate carboxylase/oxygenase from Anacystis nidulans. , 1998, The Biochemical journal.

[124]  Y. Du,et al.  Alanine-scanning mutagenesis of the small-subunit beta A-beta B loop of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase: substitution at Arg-71 affects thermal stability and CO2/O2 specificity. , 2001, Biochemistry.

[125]  A. Portis,et al.  Alteration of the adenine nucleotide response and increased Rubisco activation activity of Arabidopsis rubisco activase by site-directed mutagenesis. , 2000, Plant physiology.

[126]  F. C. Hartman,et al.  Beta-elimination of phosphate from reaction intermediates by site-directed mutants of ribulose-bisphosphate carboxylase/oxygenase. , 1994, The Journal of biological chemistry.

[127]  A. Portis,et al.  Release of the nocturnal inhibitor, car☐yarabinitol‐1 ‐phosphate, from ribulose bisphosphate car☐ylase/oxygenase by rubisco activase , 1988 .

[128]  Andrews Tj,et al.  Quantum chemical analysis of the enolization of ribulose bisphosphate: the first hurdle in the fixation of CO2 by Rubisco. , 1998 .

[129]  M. Salvucci,et al.  The Two Forms of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Activase Differ in Sensitivity to Elevated Temperature , 1997, Plant physiology.

[130]  R. J. Spreitzer,et al.  Complementing Substitutions at the Bottom of the Barrel Influence Catalysis and Stability of Ribulose-bisphosphate Carboxylase/Oxygenase* , 1997, The Journal of Biological Chemistry.

[131]  M T Clegg,et al.  Chloroplast gene sequences and the study of plant evolution. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[132]  R. J. Spreitzer.  Questions about the complexity of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase , 1999, Photosynthesis Research.

[133]  M. Salvucci,et al.  Rubisco, rubisco activase and ribulose-5-phosphate kinase gene expression and polypeptide accumulation in a tobacco mutant defective in chloroplast protein synthesis , 1995, Photosynthesis Research.

[134]  A. Portis,et al.  Rubisco Activase Mediates ATP-Dependent Activation of Ribulose Bisphosphate Carboxylase. , 1987, Plant physiology.

[135]  Garrett J. Lee,et al.  Leucine 332 influences the CO2/O2 specificity factor of ribulose‐1, 5‐bisphosphate carboxylase/oxygenase from Anacystis nidulans , 1993, Protein science : a publication of the Protein Society.

[136]  E. Vierling,et al.  Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo. , 2001, Plant physiology.

[137]  H. Bohnert,et al.  Mutations in the Small Subunit of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Increase the Formation of the Misfire Product Xylulose-1,5-Bisphosphate , 1997, Plant physiology.

[138]  R. Furbank,et al.  MOLECULAR ENGINEERING OF C 4 PHOTOSYNTHESIS , 2001 .

[139]  S. Gutteridge,et al.  Site-specific mutations in a loop region of the C-terminal domain of the large subunit of ribulose bisphosphate carboxylase/oxygenase that influence substrate partitioning. , 1993, The Journal of biological chemistry.

[140]  B. Read,et al.  A hybrid ribulosebisphosphate carboxylase/oxygenase enzyme exhibiting a substantial increase in substrate specificity factor. , 1992, Biochemistry.

[141]  M. Morell,et al.  Effects of mutations at residue 309 of the large subunit of ribulosebisphosphate carboxylase from Synechococcus PCC 6301. , 1992, Archives of biochemistry and biophysics.

[142]  D. Morse,et al.  A nuclear-encoded form II RuBisCO in dinoflagellates. , 1995, Science.

[143]  J. Gready,et al.  Quantum chemical analysis of the enolization of ribulose bisphosphate: the first hurdle in the fixation of CO2 by Rubisco. , 1998, Biochemistry.

[144]  W. Ogren.  Photorespiration: Pathways, Regulation, and Modification , 1984 .

[145]  Z. Adam.  A mutation in the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase that reduces the rate of its incorporation into holoenzyme , 1995, Photosynthesis Research.

[146]  A. Kaplan,et al.  CO2 CONCENTRATING MECHANISMS IN PHOTOSYNTHETIC MICROORGANISMS. , 1999, Annual review of plant physiology and plant molecular biology.

[147]  D. Jordan,et al.  The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase , 1984, Planta.

[148]  G. Lorimer,et al.  Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. , 1994, Science.

[149]  A. Portis.  The regulation of Rubisco by Rubisco activase , 1995 .

[150]  T. Fukui,et al.  Ribulose bisphosphate carboxylase/oxygenase from the hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1 is composed solely of large subunits and forms a pentagonal structure. , 1999, Journal of molecular biology.

[151]  A study of conserved in-loop and out-of-loop glycine residues in the large subunit of ribulose bisphosphate carboxylase/oxygenase by directed mutagenesis. , 1998, Protein engineering.

[152]  T. Andrews,et al.  Rubisco Activase Modifies the Appearance of Rubisco in the Electron Microscope , 1992 .

[153]  R. J. Spreitzer,et al.  Suppressor Mutations in the Chloroplast-encoded Large Subunit Improve the Thermal Stability of Wild-type Ribulose-1,5-bisphosphate Carboxylase/Oxygenase* , 2000, The Journal of Biological Chemistry.

[154]  F. C. Hartman,et al.  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. , 1995, Biochemistry.

[155]  G. Lorimer,et al.  Ribulose-1,5-bisphosphate carboxylase-oxygenase. , 1983, Annual review of biochemistry.

[156]  S. Parmar,et al.  Mutations in loop six of the large subunit of ribulose-1,5-bisphosphate carboxylase affect substrate specificity , 1992, Planta.

[157]  S. Gutteridge,et al.  The X-ray structure of Synechococcus ribulose-bisphosphate carboxylase/oxygenase-activated quaternary complex at 2.2-A resolution. , 1993, The Journal of biological chemistry.

[158]  B. McFadden,et al.  Activity and carboxylation specificity factor of mutant ribulose 1,5‐bisphosphate carboxylase/oxygenase from Anacystis Nidulans , 1997, Biochemistry and molecular biology international.

[159]  T. Andrews.  Catalysis by cyanobacterial ribulose-bisphosphate carboxylase large subunits in the complete absence of small subunits. , 1988, The Journal of biological chemistry.

[160]  H. Bohnert,et al.  Chimeric Arabidopsis thaliana ribulose-1,5-bisphosphate carboxylase/oxygenase containing a pea small subunit protein is compromised in carbamylation. , 1998, Plant physiology.

[161]  B. Read,et al.  High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial RubiSCO containing "algal" residue modifications. , 1994, Archives of biochemistry and biophysics.

[162]  M. Salvucci,et al.  Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[163]  R. J. Spreitzer.  Genetic Engineering of Rubisco , 1998 .

[164]  M. Badger,et al.  CO 2 concentrating mechanisms in cyanobacteria : molecular components , their diversity and evolution , 2022 .

[165]  J. Seemann,et al.  Metabolism of 2-carboxyarabinitol 1-phosphate and regulation of ribulose-1,5-bisphosphate carboxylase activity , 1990, Photosynthesis Research.

[166]  C. Dean,et al.  Structure, evolution and regulation of RbcS genes in higher plants , 1989 .

[167]  F. C. Hartman,et al.  Facilitation of the terminal proton transfer reaction of ribulose 1,5-bisphosphate carboxylase/oxygenase by active-site Lys166. , 1996, Biochemistry.