Regulation of Photosynthetic Carbon Metabolism Prof. Louise E. Anderson
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1 Regulation of Photosynthetic Carbon Metabolism Louise E. Anderson University of Illinois-Chicago 1 The black dots are gold particles; The smaller particles mark the thylakoid-bound ATP synthase; The larger particles mark the Calvin cycle enzyme The thylakoid stroma consists P-glycerate membranes kinase, are separate the first from of the the soluble two enzyme envelope phase in membranes the cycle to use ATP that in the surround chloroplast; the chloroplast; They It contains make the up a enzymes membrane involved network within in photosynthetic the chloroplast; C 2 fixation Chlorophyll and in a number and the other pigments involved of other metabolic in light trapping processes are contained in the thylakoid membrane The enzymes of the Calvin cycle are located in the stroma 2 The Calvin cycle; The abbreviations are:, ribulose bisphosphate carboxylase; PGK, phosphoglycerate kinase; GAPD, glyceraldehyde-3-p dehydrogenase; ALD, aldolase; TPI, triose-p isomerase; FBP, fructose bisphosphatase; BP, sedoheptulose bisphosphatase; TK, transketolase; EPIM, ribulose-5-p 3-epimerase; PRI, phosphoriboisomerase; PRK, phosphoribulokinase; P used in place of phosphate on structures 3 The screen versions of these slides have full details of copyright and acknowledgements 1
2 C 2 C C C 2P CP C C 2P C C C 2P C 2 C C 2P C 2P C C C C 2P P 2C C 2P makes up a large part of the soluble stromal protein; Levels as high as 70% of the soluble stromal protein have been reported P2C P 2C C 2P C 2 P 2 C C C C 2 C C 2P C C C P 2 C C 2P C 2 C C C C 2 C 2P C 2 C C C C 2P 4 NADP ATP ATP and NADP are generated as a result of the electron transport that takes place in the thylakoid membranes in the light 5 C C C 2P A T P CP C NADP C 2P C C C 2P Glyceraldehyde-3-P P-glycerate dehydrogenase kinase C 2 C C 2P C 2P C C ATP C C 2P Phosphoribulokinase C 2 C C C C 2P C 2 P 2C P 2C C C C C 2P 2 C C 2P C C C C 2P P 2 C P 2 C C 2 P C 2 C 2 C C C C 2P P 2 C 6 The screen versions of these slides have full details of copyright and acknowledgements 2
3 C 2P C C C C 2P To starch C C C 2P CP C To cytosol and sucrose C 2P C C C 2P C 2 C C 2P P 2C C 2P P 2 C The triose phosphates, glyceraldehyde-3-p and dihydroxyacetone-p, exit the cycle and leave the chloroplast via a translocator; Fructose-6-P exits the cycle and is used for the formation of starch within the chloroplast P 2C C 2 P C 2 P 2C C C C C 2 P 2 C C 2P C C C C 2P C 2 C 2 C C C C 2P C 2 C C C C 2P 7 The activity of each of the enzymes of the Calvin cycle is controlled by the level of the available substrates and cofactors; In addition there are changes in p, Mg ++ concentration, and levels of reductants that occur in the light; These have profound affects on the activity of certain Calvin cycle enzymes 8 Light activation Fd, ferredoxin FTR, ferredoxin thioredoxin reductase Trx, Thioredoxin 9 The screen versions of these slides have full details of copyright and acknowledgements 3
4 activase C 2P C C C C 2P C 2 C C C C 2P CP C C 2P C C C 2P C 2 C C 2P C C C 2P C 2 P 2C P 2C C C C C 2P 2 C C 2P C C C C 2P P2C P 2C C 2P C 2 C 2 C C C C 2P P 2 C C 2P C C C C 2P Mg ++ Mg ++ Mg ++ C CP C C C 2P C 2P C C C 2P C 2 C C 2P P 2C C 2P P2C Mg ++ P 2C Mg ++ is a required for activity by, the Changes two kinases, Mg ++ P-glycerate levels in the kinase stroma and will phosphoribulokinase, affect the activity of these two enzymes phosphatases, fructose bisphosphatase and sedoheptulose bisphosphatase, and by transketolase Mg ++ P 2C Mg ++ C 2P C 2 C 2 C C C C 2P C C C C 2P Mg ++ P 2 C C 2 C 2 C C C C 2P C 2 C C C C 2P 12 The screen versions of these slides have full details of copyright and acknowledgements 4
5 Ca ++ K + ther The effect cations, of these including cations Ca ++ on and stromal K +, metabolism are has released not been from thoroughly the thylakoid investigated membranes into the stroma as protons are moved into the thylakoid lumen The p in the stroma is around 7.2 in the dark and between 7.8 and 8 in the light 15 The screen versions of these slides have full details of copyright and acknowledgements 5
6 16 4 Relative activity BPase p 200 nm 17 activase C 2P C C C C 2P C C C 2P CP C C 2P C C C 2P C 2 C C 2P P 2C C 2P P 2 C activase, like BPase, has a narrow p optimum P 2C C 2 P C 2 P 2 C C 2 C C C C 2P C C C C 2P P2C C 2 C 2 C C C C 2P C 2 C C C C 2P 18 The screen versions of these slides have full details of copyright and acknowledgements 6
7 Increase Mg ++ FBPase a c t i v i t y p 19 Light activ ation FBPase a c t i v i t y p 20 Light activation, the increase in stromal Mg ++ concentration, and the increase in stromal p, will all affect FBPase FBPase a c t i v i t y p 21 The screen versions of these slides have full details of copyright and acknowledgements 7
8 Most of the other enzymes of the Calvin cycle have broad p dependency curves; Most are slightly more active at p 7.8 than at p 7.2 a c t i v i t y p 22 Light activation Fd, ferredoxi n FTR, ferredoxi n thioredoxin reductase Trx, Thioredoxi n 23 activase C 2P C C C C 2P Phosphoribulokinase C C C 2P CP C C C C 2P C 2P Glyceraldehyde-3-P dehydrogenase C 2 C C 2P C 2 C C C C 2P C 2 P 2C P 2C C C FBPase C 2P C 2 C C 2P C C C C 2P P 2 C P 2 C C 2 P C 2 C BPase 2 C C C C 2P P 2 C 24 The screen versions of these slides have full details of copyright and acknowledgements 8
9 Thioredoxin Thioredoxin The four Calvin cycle enzymes and activase contain Activation cystine disulfide can affect bonds both that the are maximum reduced rate by thioredoxin of in the enzyme light; There reaction are additional and the apparent enzymes affinity involved for in other substrate; pathways Inactivation that are of reductivel the Calvin y activated; cycle enzymes prevents wasteful ome enzymes use of ATP that are involved in pathways and NADP in the dark that operate in the dark in the plastid are reductively inactivated 25 Thioredoxins are small (about 12 kda) proteins with two protruding cysteine residues (in the reduced form) at the apex of a β turn; The cysteines are separated by a glycine and a proline residue; The cysteine sulfhydr yls are easily oxidized to form a disulfide bond 26 Thioredoxin There are thioredoxins outside of the Thioredoxin chloroplast; There is no evidence for light-dependent reduction of these thioredoxins; There Activation major are two cytosolic major of thioredoxins, the thioredoxin chloroplast f and enzymes is m, thioredoxin in the chloroplast; can affect h Thioredoxi n f is involved in the activati on both the rate of the enzyme reaction of the four Calvin cycle enzymes; Thioredoxi and n the m apparent is involved affinity the activati for on substrate of NADP-linked malate dehydr ogenase and the inactivation of glucose-6-p dehydrog enase 27 The screen versions of these slides have full details of copyright and acknowledgements 9
10 Activation can affect both the rate of the enzyme reaction and the apparent affinity for substrate Vmax v o [ubstrate] 28 Activation can affect both the rate of the enzyme reaction and the apparent affinity for substrate K m v o [ubstrate] 29 Thioredoxin Thioredoxin Thioredoxin Dark inactivation probably of the acts Calvin as the cycle electron enzymes acceptor in prevents dark inactivation; wasteful use of ATP and NADP, Dark in the inactivation absence of results light in turning off the Calvin cycle and turning on the oxidative pentose phosphate pathway 30 The screen versions of these slides have full details of copyright and acknowledgements 10
11 FBPase M D A A The In at redox-sensiti least one case ve (malate cysteine dehydr residues og enase) on fructose the active site bisphosphatase blocked by the are C-terminal located in tail a of loop the that enzyme protrudes that obstructs from the surface active site of the when enzyme; the redox-sensiti When the ve cysteines are residues oxidized form there a disulfide a change bond; Reduction in confor mation by thioredoxi in the n loop apparentl (helix y formation) results that in a change results in in changes conformati on the that active allows site access (A) located on of substrate the other to side the of active the subunit; site When the disulfide bond is reduced by thioredoxi n the change in conformati on near the cysteine residues is felt across the enzyme molecule at the active site; The enzyme is activated and the p optima drops Activity p 31 We do not yet know exactl y how the activity of the other light activated (and light inactivated) enzymes is changed; The redox-sensitive cysteines in glyceraldehyde-3- P dehydrog enase are located in a C-terminal extension; In sedoheptulose bisphosphatase they are located in an insertion into the peptide chain further from the terminus; In ribulose-5-p kinase one of the redox-sensitive cysteine residues is located in the ATP-binding site; It seems that redox-sensiti vity evolved separatel y in each of these enzymes 32 Thioredoxin Thioredoxin There are a number of non-reductive pentose phosphate pathway enzymes in the chloroplast that are redox-regulated 33 The screen versions of these slides have full details of copyright and acknowledgements 11
12 ADP ATP CF 1, the chloroplast ATP synthase, is light activated 34 M D The chloroplast NADP-linked malate dehydrogenase that utilizes photosynthetically-generated NADP to reduce oxalacetate to malate is light activated; NADP cannot be transported out of the chloroplast; The malate is exported from the chloroplast to the cytosol, thus accomplishing the export of reducing equivalents out of the chloroplast 35 3 CC~CoA + C 2 CC 2 C~CoA The chloroplast acetyl CoA carboxylase, the enzyme that catalyzes the first, committing step in the synthesis of lipids, is light activated 36 The screen versions of these slides have full details of copyright and acknowledgements 12
13 ADP-glucose pyrophosphorylase P + ATP ADP-Glu + PPi ADP-glucose pyrophosphorylase, the committing enzyme in starch synthesis, is light activated; The activity of the enzyme is also stimulated by P-glycerate 37 Glucose-6-P + NADP + 6-P-gluconolactone + NADP The first enzyme in the oxidative pentose phosphate pathway, glucose-6-p dehydrogenase, is reductively light inactivated, and oxidatively dark activated; The enzyme is involved in the formation of NADP at night in the chloroplast 38 A second oxidative pentose phosphate pathway enzyme, transaldolase, which catalyzes one of the carbon rearrangements in that pathway, is reductively light inactivated, and oxidatively dark activated 39 The screen versions of these slides have full details of copyright and acknowledgements 13
14 Thioredoxin Thioredoxin At least 53 stromal enzymes have been shown to bind to thioredoxin f or m in proteomics experiments; It can be expected that some of the enzymes will be found to be light activated or light inactivated by the thioredoxin system 40 activase C 2 P C C C C 2 P C C C 2 P 41 C P 2 C C C C P 2 C 2 P CC C C C 2 RuBP CA1P is inhibited by carboxyar abi ni tol- 1-P (CA1P) which is formed in the dark; CA1P resembles the substrate ribulose bisphosphate (RuBP) and the transition state intermediate that breaks down into two molecules of P-glycerate; CA1P binds tightly to 42 The screen versions of these slides have full details of copyright and acknowledgements 14
15 activase ase C CP C P C P 2 2 C 1 CC C C C C P C 2 2 C P-glycolate C 2 C C C 2 P 3-P-glycerate When 2 is substituted for C 2 as substrate, Although There P-glycolate a activase has lysine activase another in removes formed; activase is a grievous removes chaperonin-type P-glycolate the very inhibitory problem; active important can site protein; bound be that converted binds RuBP, C 2 ; If allowing Experiments It RuBP the has to the initial 3-P-glycerate, difficulty binds bound C 2 induction to to with CA1P bind distinguishing transgenic but restoring phase the 2 before molecules active of plants between s photosynthetic that site with C are lysine C 2 activity low required 2 and levels C 22 fixation, ; experiments (which of Both for are the NT linear formation activase with substrate molecules transgenic of indicate 1 C molecule 2 ) plants that it of indicate protects 3-P-glycerate is inhibited the enzyme that from it the has effects little effect of high on the temperature rate of steady in vivo state C 2 fixation 43 The P-glycolate has to be dephosphor ylated and the resultant glycolate transported out of the chloroplast into the peroxisome, where is conver ted into glycine, transported into the mitochondrion, ultimately forms serine and is transported back into peroxisome, where the serine is converted to glycerate, which is transported back to the chloroplast and phosphor ylated 44 C CP 2 1 C C C 2 P This process involves the expenditur e of ATP; It is not clear why during the course of evoluti on some mechanism that allows to select more efficientl y against 2 has not appeared; ome workers believe that there must be some benefit to the plant from the production of P-glycolate 45 The screen versions of these slides have full details of copyright and acknowledgements 15
16 2 Bundle sheath cell Mesophyll cell C 2 The problem has been solved in C4 plants, plants like maize, sorghum and sugar cane, where the chloroplasts that are invol ved in C 2 fixation and the operation of the Calvin cycle are located in bundle sheath cells distant from the leaf surface and air; C 2 is initially fixed into a four carbon acid in the mesophyll cells, then transported into the bundle sheath cells, C 2 is released and refixed into P-glycerate; ince there is no 2 to compete with the C 2 there is no formation of P-glycolate 46 Although can make up as much as 70% of the soluble protein in the chloroplast stroma the enzyme is very inefficient; and experiments with transgenic plants suggest that it limits photosynthetic C 2 fixation 47 C 2 C C C 2P PGK PGK Carbonic anhydrase CP C C 2P GAPD C C C 2P TPI C 2 C C 2P C 2P C C C C 2P Transketolase ALD P 2C C 2P P2C PRK BPase The enzymes that appear to interact There are There phosphoriboisomerase, are are also experiments unpublished that phosphoribulokinase, experiments TK suggest that some that Association Experiments, indicate may only occur of the enzymes carbonic that with there anhydrase, transgenic are some of the Calvin P-glycerate plants kinases, also cycle interact kinase, suggest P2C including between that glyceraldehyde-3-p the enzymes that follow one another and sedoheptul P-glycerate that substrate ose dehydrogenase, bisphosphatase kinase and phosphori might be channel aldolase, bul ed triose-p oki nase, associate in isomerase, the pathway, with sedoheptulose ATP or within synthase, clusters bisphosphatase, the enzyme of those that enzymes forms ATP, on and the transketolase, from transketolase thylakoid one enzyme are membrane and xylulose-5-p to rate the next limiting 3-epimerase ALD P 2C C 2P TK C 2 P 2 C C C C C 2 C 2P C C C C 2P EPIM C2 C C C 2 C C 2P C 2 C C C C 2P EPIM PRI 48 The screen versions of these slides have full details of copyright and acknowledgements 16
17 ATP This would allow direct transfer of ATP to these kinases, and protect it from other ATP-utilizing enzymes 49 C 2 C 2P C C C C 2P C C C 2P CP C GAPD C 2P C C C 2P C 2 C C 2P P 2 C There are also unpublished experiments that indicate that glyceraldehyde-3-p dehydrogenase associates with ferredoxin-nadp reductase, the enzyme that provides its substrate, NADP P 2C C 2P P 2C C 2 P C 2 P 2 C C C C C 2 C 2P C C C C 2P P 2 C C 2 C C C 2 C C 2P C 2 C C C C 2P 50 C 2 C C C 2P PGK Carbonic anhydrase CP C C 2P GAPD C C C 2P TPI ALD C 2 ALD P 2 C Interaction might allow substrate channeling, which would reduce the levels of intermediates required in order for C2 fixation to occur and shorten the lag period in C2 fixation C C 2P C 2P C C C C 2P P 2C C 2P P 2C C 2 P PRK C 2 P 2 C C C C C 2 C 2P C C C C 2P P 2 C C 2 C C C 2 C C 2P C 2 C C C C 2P PRI 51 The screen versions of these slides have full details of copyright and acknowledgements 17
18 To sum up: There are a number of factors that affect photosynthetic C2 fixation; Most important, light controls the p, Mg ++ concentration, redox-state of some key enzymes and activase; is inhibited in the dark by a transition-state analog, and in the light by 2; ome of the enzymes of the Calvin cycle may interact with resultant channeling of intermediates from one to the next; The rate limiting enzymes appear to be transketolase, sedoheptulose bisphosphatase, and despite massive quantities of enzyme protein, 52 General Biochemistry & Molecular Biology of Plants; edited by Bob B. Buchanan, Wilhelm Gruissem, and Russell L. Jones; Published by American ociety of Plant Biologists, Rockville (2002) preitzer RJ, alvucci ME. (2002) : structure, regulatory interactions, and possibilities for a better enzyme; Annu Rev Plant Biol. 53: tarch synthesis mith AM. (2001) The biosynthesis of starch granules; Biomacromolecules, ummer 2: Triose-P translocator Weber AP.(2004) olute transporters as connecting elements between cytosol and plastid stroma; Curr pin Plant Biol. 7: p References Werdan K, eldt W, Milovancev M. (1975) The role of p in the regulation of carbon fixation in the chloroplast stroma; tudies on C2 fixation in the light and dark; Biochim Biophys Acta. 396: Mg ++ Portis AR Jr, eldt W. (1976); Light-dependent changes of the Mg2+ concentration in the stroma in relation to the Mg2+ dependency of C2 fixation in intact chloroplasts; Biochim Biophys Acta; 449: Redox regulation Buchanan BB, Balmer Y.( 2005); Redox regulation: a broadening horizon; Annu Rev Plant Biol. 56: chürmann P, Jacquot JP. (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol. 51: activase Portis AR Jr, alvucci ME. (2002); The discovery of activase - yet another story of serendipity; Photosynth Res. 73: Portis AR Jr. (2003) activase - 's catalytic chaperone. Photosynth Res. 75: Fructose bisphosphatase References Preiss J, Biggs ML, Greenberg E. (1967); The effect of magnesium ion concentration on the p optimum of the spinach leaf alkaline fructose diphosphatase; J Biol Chem. 242: The screen versions of these slides have full details of copyright and acknowledgements 18
19 Transgenic plants Lefebvre, Lawson T, Zakhleniuk V, Lloyd JC, Raines CA, Fryer M. (2005); Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development; Plant Physiol. 138: enkes, onnewald U, Badur R, Flachmann R, titt M. (2001); A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism; Plant Cell. 13: udson G, Evans JR, von Caemmerer, Arvidsson YB, Andrews TJ. (1992); Reduction of Ribulose-1,5-Bisphosphate Carboxylase/xygenase Content by Antisense RNA Reduces Photosynthesis in Transgenic Tobacco Plants; Plant Physiol. 98: Enzyme-enzyme interaction References Anderson LE, Carol AA. (2004); Enzyme co-localization with rubisco in pea leaf chloroplasts; Photosynth Res. 82 :49-58 Anderson LE, Gatla N, Carol AA. (2005); Enzyme co-localization in pea leaf chloroplasts: glyceraldehyde-3-p dehydrogenase, triose-p isomerase, aldolase and sedoheptulose bisphosphatase; Photosynth Res. 83: The screen versions of these slides have full details of copyright and acknowledgements 19
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