ࡱ> Y QbjbjWW .==M]ZZZZZZZ8,;\(\$SGZ;aZZMaaaZZnZZZZa.aZZLUþaCarbon Metabolism in Photosynthesis David J. Oliver Department of Botany Iowa State University Ames, IA 50011 Rubisco I. Key Features A. Catalyzed the oxygenation and carboxylation of RuBP B. Enzymatically very inefficient (low turnover number) C. Catalytic activity is carefully controlled by metabolites, light, and other enzymes D. Functional enzyme requires expression of nuclear and chloroplast genome E. Synthesis of proteins is regulated by light and other signals F. Assembly requires post translational modification, transport, chaperonins G. Rubisco is the most abundant protein in the biosphere 50% of soluble protein in leaf, about 10 kg per person II. The reactions of Rubisco A. Rubisco catalyzes two competing reactions - carboxylase and oxygenase  B. Competition between CO2 and O2 each looks like a competitive inhibitor of the other neither O2 nor CO2 forms a Michaelis complex with the enzyme  C. Physiological - CO2 fixation results in C fixation into carbohydrates O2 fixation results in CO2 loss through photorespiration  D. The ratio of carboxylase to oxygenase is expressed by the specificity factor (() ( = VcKo/VoKc Vc = Vmax carboxylase Ko = Km oxygenase Vo = Vmax oxygenase Kc = Km carboxylase vc/vo = ( ([CO2]/[O2]) There is a natural difference in ( between different Rubisco sources C3 plants ( = 80 C4 plants ( = 50 Anaerobic bacteria ( = 10 E. Other reactions of Rubisco Xylulose 1,5 bisphosphate (XuBP) results from about 1/400 of the turnovers when RuBP is misprotonated on C3. 3-keto-arabinitol 1,5 bisphosphate results from the protonation of the enediol at C2. Both of these bind to and inhibit the enzyme called FALLOVER III. Control of Rubisco Activity A. Rubisco occurs in two forms, inactivated and activated Activation requires the carbamylation of lys191  1. The carbamylation is slow, the addition of Mg is rapid. 2. The tertiary Enz-CO2-Mg complex forms the active site. 3. The activating CO2 is different from the substrate CO2 4. The oxygenase activity also requires activation. 5. The activated enzyme binds RuBP and then the next substrate (O2 or CO2) that arrives is the one that reacts (competition). 6. 2-carboxyarabinitol 1,5 bisphosphate (CABP) is an analogue of the carboxylation reaction that will bind to the activated enzyme. It can be used to titrate the number of activated active sites.  B. Problems with in vitro activation 1. While carbamylation occurs in vitro the Km for the activation is about 25 uM while the concentration of CO2 in the chloroplast is 10 uM. 2. Sugar phosphates can affect the activation by preferentially binding E or E-CO2  3. Ogren and Portis discovered that an Arabidopsis mutant that would only grow in the presence of high [CO2] had Rubisco that had normal activity in vitro but would not activate in vivo. C. Rubisco Activase 1. 200 kDa tetramer in Arabidopsis that is composed of 41 & 45 kDa subunits. Subunits arise from alternative splicing 2. Uses MgATP and catalyzes the activation of Rubisco 3. The hydrolysis of ATP is not stoichiometrically coupled to activation. AMP - PNP does not work. Some site directed mutants have different ratios of ATPase to activation. Inhibiting ATPase will kill activation. Probably uses energy to change conformation of Rubisco. 4. [Rubisco] = 3 mM active sites [activase] = 0.04 mM  5. Plants use sugar phosphates (RuBP and 2-carboxyarabinitol) to inhibit Rubisco. Activase reverses this inactivation. II. Rubisco synthesis requires the coordinated expression of nuclear and chloroplast genome A. In land plants the small subunit of Rubisco (SSU - 14 kDa) is encoded by a small family (5 - 7 members) of nuclear-encoded genes (rbcS) Expression of these genes transcriptionally controlled by Light - both blue light and phytochrome Biological clock - circadian rhythm Unknown signal from mature chloroplasts Metabolite control by sugars B. The large subunit (LSU - 53 kDa) is encoded on the chloroplast genome (rbcL). Control of LSU expression is post-transcriptional. C. Expression of rbcS and rbcL are coordinated. D. In higher plants Rubisco is a hexadecamer L8S8 In purple nonsulfur bacteria (Rhodospirillum rubrum) L2 form shows that large subunit has active site E. Structure - see Hartman and Harpel 1994 F. The assembly requires chaperonins 1. cpn60 (hsp60 or groEL) and 2. cpn10 (hsp10 or groES) and 3. rubisco-binding protein 4. Work together with to assist protein folding in an ATP-coupled process to inhibit incorrect assembly pathways. Coordination of Nuclear and Plastid Genomes a unique form of control How does a plant control equal expression of the large and small subunit to allow for assembly of an active Rubisco in the chloroplast? This was addressed by using antisense tobacco plants with reduced ability to make small subunit. As the amount of small subunit mRNA decreases so does the amount of small subunit protein. While the amount of large subunit mRNA remained constant, the amount of large subunit protein decreased. Large subunit mRNA is not on polysomes and is not translated. References: Fred C. Hartman and Mark R. Harpel (1994) Structure, Function, Regulation, and Assembly of D-Ribulose-1,5-bisphosphate carboxylase/Oxygenase. Annu. Rev. Biochem. 63: 197-234 Archie R. Portis (1992) Regulation of Ribulose 1,5 Bisphosphate Carboxylase/Oxygenase Activity. Ann. Rev. Plant Physiol. Plant Mol. Biol. 43: 415-437 Wilhelm Gruissem (1989) Chloroplast Gene Expression: How Plants Turn Their Plastids On. Cell 56: 161-170 Rodermel et al. (1996) A mechanism of intergenomic integration: Abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA. PNAS 93: 3881-3885 Mark Stitt and D. Schulze (1994) Doses Rubicso control the rate of photosynthesis and plant growth? An excercise in molecular exophysiology. Plant, Cell, and Environment 17: 465-487 Kim J et al. Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 278:1954-7 (1997) Rochaix JD Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas reinhardtii. Plant Mol Biol 32:327-41 (1996) Parry MA et al.The localisation of 2-carboxy-D-arabinitol 1-phosphate and inhibition of Rubisco in leaves of Phaseolus vulgaris L. FEBS Lett 444:106-10 (1999) Hammond ET et al. 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 118:1463-71 (1998) Calvin - Bassham - Benson Cycle C3 Photosynthetic Carbon Reduction (PCR) Cycle I. Introduction - early work Melvin Calvin won the Nobel prize for working out this cycle. At the time this involved several new technologies including the use of radioisotope tracers (14CO2 was available because of proximity to Lawrence labs) and paper chromatography and autoradiography for the identification of the metabolites. The first work was done by labeling Chlorella with pulses of 14CO2 and then quenching the reaction by dropping it into hot ethanol. Paper chromatography identified the first labeled compound as a three carbon organic acid, thus the C3 cycle. II. The reaction mechanism - PGA converted to triose-P by the reactions of gluconeogenesis and then the sugars are converted to ribulose 5-P by the pentose phosphate pathway. See attached figure of C3 cycle. III. Regulation of the C3 cycle. A. Chloroplast enzymes exist for both carbohydrate synthesis and degradation so regulation is essential to avoid futile cycles 1. The biosynthetic enzymes are light-activated 2. Regulated steps appear to include a. Rubisco b. Fructose 1,6 bisphosphatase* c. Sedoheptulose 1,7 bisphosphatase* d. Phosphoribulokinase* e. NADP-glyceraldehyde 3-phosphate dehydrogenase* 3. These 4 steps of the C3 cycle (*) are regulated by the ferredoxin/thioredoxin system a. Ferredoxin (Fd) - soluble iron sulfur protein of the electron transport chain b. Thioredoxin is a small protein with an active disulfide bond c. Ferredoxin-thioredoxin reductase is an iron sulfur protein d. Activation of the electron transport chain reduces ferredoxin which in turn reduces thioredoxin (catalyzed by reductase). Thioredoxin undergoes a disulfide exchange reaction with several enzymes and activates (or inactivates) them. 4. The ferredoxin/thioredoxin system also activates CF1 and NADP+-malate dehydrogenase and inactivates glucose 6-phosphate dehydrogenase, an important control step in oxidative pentose phosphate pathway.  Carbohydrate control of Photosynthesis a universal regulation? Researchers have long known that when the carbohydrate level in leaves increases (as happens in elevated CO2) the rate of photosynthesis decreases. Analysis has shown that as carbohydrates accumulate the rate of transcription of photosynthetic genes is repressed. Jang et al. have shown that the flux of carbon through hexose kinase is important in measuring the amount of carbohydrate. Effect of carbohydrates on cab promoter CarbohydrateCab promoter activityNone100%D-glucose15%L-glucose100%2-deoxyglucose20%6-deoxyglucose110%Glucose 6-phosphate110%Glucose + mannoheptulose 70% Overexpression of hexose kinase produces plants that are hypersensitive to carbohydrate repression while under expression of hexose kinase makes plants that are less sensitive to carbohydrate repression. References: James A. Bassham (1979) The reductive pentose phosphate cycle and its regulation. In Encyclopedia of Plant Physiology (M. Gibbs and E. Latzko, eds) Vol. 6: 9-30 Ulf-Ingo Flugge and Hans Walter Heldt (1991) Metabolite translocators of the chloroplast envelope. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 129-144 R.G. Jensen (1990) Ribulose 1,5-bisphosphate carboxylase/oxygenase: mechanisms, activation, and regulation. In Plant Physiology, Biochemistry, and Molecular Biology (D.T. Dennis and D.H. Turpin, eds) pg. 224-238 R.C. Leegood (1993) The Calvin cycle and photorespiration. In Plant Biochemistry and Molecular Biology (P.J. Lea and R.C. Leegood, eds) pg. 27-45 Fraser D. MacDonald and Bob B. Buchanan (1990) The reductive pentose phosphate pathway and its regulation. In Plant Physiology, Biochemistry, and Molecular Biology (D.T. Dennis and D.H. Turpin, eds) pg. 224-238 Jang et al. (1997) Hexokinase as a sugar sensor in higher plants. The Plant Cell 9: 5-19 Jeff R. Seeman, J. Kabza and Brandon d. Moore (1990) Metabolism of 2-carboxyarabinitol 1-phosphate and regulation of ribulose - 1,5 - bisphosphate carboxylase activity. Photosynthesis Research 23: 119-130 Hirasawa M, et al. Oxidation-reduction properties of chloroplast thioredoxins, ferredoxin:thioredoxin reductase, and thioredoxin f-regulated enzymes. Biochemistry 38:5200-5 (1999) Brandes HK et al.. Efficient expression of the gene for spinach phosphoribulokinase in Pichia pastoris and utilization of the recombinant enzyme to explore the role of regulatory cysteinyl residues by site-directed mutagenesis. J Biol Chem 271:6490-6 (1996) Glycolate pathway - C2 cycle - photorespiration - Photosynthetic Carbon Oxidation (PCO) Cycle I. Physiological measurements and early observations A. post illumination burst - the first measurement of photorespiration was made by Decker in the early 1950's - observed rapid rates of respiration for the first minute or so after plants darkened. Determined that there was a rapid rate of respiration occurring in the dark. O2 enhances the reaction and CO2 represses it. B. CO2 compensation point - plants that exhibit photorespiration (C3 plants) are placed in a closed container and illuminated they will lower the [CO2] to about 50 to 60 ppm. At this point photorespiration + dark respiration (small) = photosynthesis. C. Warburg effect - inhibition of CO2 fixation by elevated O2 concentrations. II. Biochemistry A. Zelitch showed that the [glycolate] correlates with amount of post-illumination burst. B. Tolbert resolved photorespiration pathway (all except glycolate synthesis reaction that was discovered by Bowes and Ogren in 1971). See separate sheet showing C2 cycle. C. Enzymes 1. Phosphoglycolate phosphatase - chloroplastic and highly specific for phosphoglycolate. One of first biochemical mutants identified using Arabidopsis. 2. Glycolate oxidase - flavoprotein (FMN), reduces O2 to H2O2 Major source of H2O2 production in plants - implications in H2O2-linked Reactions 3. Catalase - mutants in barley only lethal under photorespiratory conditions suggest that photorespiration is the major H2O2 source Glyoxylate + H2O2 ( formate + CO2 (only when N-limited) 4. Transaminases - prevent other glyoxylate reactions One prefers glutamate the other serine (will use other amino acids) Serine:glyoxylate transaminase mutant obtained in Arabidopsis 5. Glycine decarboxylase - the worlds most interesting protein a. Proteins - amount of proteins CharacteristicP-proteinH-proteinT-proteinL-proteinPrecursor Protein Amino Acids 1,057 165 408 501Mature Protein - Actual MW105 kDa14 kDa41 kDa50 kDa - Amino Acids971131378470Complex Subunit Structure dimer monomer monomer dimerComplex Subunit Ratio 4 27 9 2Gene Copies per Genome 2 1 1 1 or 2MRNA Size3.4 kb0.7 kb1.4 kb1.8 kb b. Reaction mechanism  c. Major substrate in leaf mitochondria in light - can out compete the TCA cycle and is about 5 times the dark respiration rate. d. Is NADH from glycine oxidation reoxidized by the mitochondrial electron transport chain? Probably exported and used for hydroxypyruvate reduction. 6. Serine hydroxymethyltransferase a. Pyridoxal 5-phosphate-dependent b. Homotetramer of 50 kDa subunits c. Localized in mitochondria, chloroplast, cytosol d. The mitochondrial form is required for photorespiration (mutant) e. 2 glycine : 1 serine stoichiometry Glycine Decarboxylase Reaction Glycine + NAD+ + THF ( methylene-THF + CO2 + NH3 + NADH Serine Hydroxymethyltransferase Reaction Glycine + methylene-THF + H2O ( Serine + THF Overall Reaction 2 Glycine + NAD+ ( Serine + CO2 + NH3 7. Transaminase 8. Hydroxypyruvate reductase - peroxisomal 9. Glycerate kinase - chloroplast D. The Photorespiratory Nitrogen cycle 1. The rate of photorespiratory NH3 release is 10 to 20 times the rate of primary N fixation. The N must be effectively recycled. 2. The NH3 is produced in the mitochondria but mitochondrial glutamate dehydrogenase does not have sufficient activity or substrate affinity to refix. 3. Originally inhibitor studies and later Arabidopsis mutants showed that the chloroplast Fd-GOGAT system is important. a. Glutamine synthetase glutamate + NH3 + ATP ( glutamine + ADP + Pi b. Glutamine:oxoglutarate aminotransferase glutamine + (-ketoglutarate + Fd(ox) ( 2 glutamate + Fe(red) c. Chloroplast envelope transporters needed E. Function of C2 cycle 1. Protect from photooxidation 2. Inevitable consequence of Rubisco chemistry F. Metabolic Regulation: It is generally assumed that the C2 cycle is not controlled. Once carbon enters the cycle, it must be efficiently returned to the C3 cycle or photosynthesis is inhibited. There is some regulation possible. 2-phosphoglycolate inhibits triose-P isomerase and glycerate inhibits sedoheptulose bisphosphatase and fructose bisphosphatase. Conditions that slow the C2 cycle should result in the accumulation of these intermediates and a suppression of the C3 cycle. Inhibition of the C3 cycle would decrease substrate availability for the C2 cycle. G. Developmental expression 1. The C2 cycle is a subset of the reactions of the C3 cycle. It is not, therefore, surprising that it is controlled by light in a similar manner. 2. Hydroxypyruvate reductase - in germinating seeds the microbodies are glyoxysomes are mainly dedicated to the metabolism of lipids. Shortly after germination, the microbodies of the cotyledons are converted into peroxisomes, where the major function is photorespiration. Beckers group has studied hydroxypyruvate reductase and has studied the light-dependent conversion of glyoxysomes to peroxisomes. The initial photoreceptor is phytochrome and two period of light responsiveness have been identified. The first is a light-dependent establishment of competence and the second involves transcriptional activation. 3. The glycine decarboxylase complex has received the most study. a. All four nuclear encoded genes are light-activated. The increase is less with the L-protein due to its role in other mitochondrial multienzyme complexes. b. Phytochrome is the primary light receptor although a secondary signal from the mature chloroplasts is also essential. c. Control is at the transcriptional level. d. Promoter analysis has shown cis-acting elements in the promoter are essential for light-dependent and tissue-specific gene activation. e. All four proteins are synthesized with N-terminal presequences that are responsible to mitochondrial targeting and are removed after import. f. Assembly of the complex is spontaneous in vitro and presumably in vivo. Transcriptional control of glycine decarboxylase. An predictable story with a twist. The expression of the H-protein of glycine decarboxylase is light-dependent and the enzyme is found at its highest level in leaves. Protein level is controlled at the transcriptional level and the transcription of the gene closely follows that for the small subunit of Rubisco. Promoter deletion analysis with transgenic plants has identified a region within the promoter between 370 and 117 bp that is essential for light-dependent and tissue-specific gene expression. Footprinting experiments have identified two sequences within this region that bind nuclear proteins from Arabidopsis. These binding proteins were characterized by electrophoretic mobility retardation experiments and were cloned using Southwestern screening. One protein was a unique myb-type transcription factor and the other was a zinc finger protein. Transcription of the mRNA for the H-protein Expression of GUS activity, light-dark ratio, of glycine decarboxylase (gdcH) and the small and leaf/root ratio by transgenic plants subunit of Rubisco (rbcS) by etiolated containing portions of the promoter of the Arabidopsis plants following their transfer gdcH gene fused to GUS. from dark to light.  References: H.R. Abbaraju and D. J. Oliver. Identification of an Unusual Myb-type Transcription Factor that Controls the Light-Dependent Expression of the H-Protein of Glycine Decarboxylase. Plant Molecular Biology (in press - 1999) Diane W. Husic, H. David Husic, and N. Edward Tolbert (1987) The oxidative photosynthetic carbon cycle or C2 cycle. CRC Critical Reviews in Plant Science 5: 45-100 David J. Oliver (1994) The glycine decarboxylase complex from plant mitochondria. Annu. Rev. Plant Physiol. 45: 323-337 D.J. Oliver and R. Raman. Glycine Decarboxylase: Protein Chemistry and Molecular Biology of the Major Protein in Leaf Mitochondria. Journal of Bioenergetics and Biomembranes 27: 407-414 (1996) R. Srinivasan and D.J. Oliver. Light-Dependent and Tissue-Specific Expression of the H-Protein of the Glycine Decarboxylase Complex. Plant Physiology 109: 161-168 (1995) Vauclare P et al. The gene encoding T protein of the glycine decarboxylase complex involved in the mitochondrial step of the photorespiratory pathway in plants exhibits features of light-induced genes. Plant Mol Biol 37:309-18 (1998) There is a new general book on photosynthesis that might be of interest: A.S. Raghavendra Photosynthesis: A Comprehensive Treatise Cambridge University Press, Cambridge, 1998 (ISBN 0 521 57000). 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Oliver.C:\My Documents\Presentations\DOE-Biochem2.docDavid J. Oliver-C:\TEMP\AutoRecovery save of DOE-Biochem2.asdDavid J. Oliver-C:\TEMP\AutoRecovery save of DOE-Biochem2.asdDavid J. Oliver-C:\TEMP\AutoRecovery save of DOE-Biochem2.asdDavid J. Oliver-C:\TEMP\AutoRecovery save of DOE-Biochem2.asdDavid J. Oliver-C:\TEMP\AutoRecovery save of DOE-Biochem2.asdDavid J. Oliver-C:\TEMP\AutoRecovery save of DOE-Biochem2.asdDavid M. KramerB:\sum99\DOE-Bioc.doc@Brother HL-720 seriesLPT1:brohl96aBrother HL-720 seriesBrother HL-720 series#XXSBrother HL-720 seriesBrother HL-720 series#XXSBrother HL-720 series0MP@GTimes New Roman5Symbol3& ArialIWP Greek CenturyY CG TimesTimes New Roman;Wingdings"A h6f6f 6F= @ # 0NK&Plant Biochemistry - C3 Photosynthesis David OliverDavid M. Kramer Oh+'0   8D ` l x 'Plant Biochemistry - C3 Photosynthesis lan David Oliveristaviavi Normal.dotrDavid M. 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