Diatom plastids possess a phosphoribulokinase with an altered regulation and no oxidative pentose phosphate pathway

Plant Physiology

Volumn 137, Issue 3, 2005, Pages 911-920

  Michels, Andreas K ^a,d   Wedel, Norbert ^b,e   Kroth, Peter G ^c  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

^c UNIVERSITY OF KONSTANZ   (Germany)

^d HENKEL KGAA   (Germany)

^e NONE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICROORGANISMS; PHOTOSYNTHESIS; PLANTS (BOTANY); PROTEINS; REDOX REACTIONS;

CALVIN CYCLES; DIATOM PLASTIDS;

ENZYMES;

ENZYMES; MICROORGANISMS; PHOTOSYNTHESIS; PLANTS; PROTEINS; REDOX REACTIONS;

BACILLARIOPHYTA; CHLOROPHYTA; ESCHERICHIA COLI; NITZSCHIA ALBA; ODONTELLA SINENSIS; SPINACIA OLERACEA; TRACHEOPHYTA;

PHOSPHORIBULOKINASE; PHOSPHOTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; DIATOM; ENZYME ACTIVATION; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PENTOSE PHOSPHATE CYCLE; PH; PHYSIOLOGY; PLASTID; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRANSGENIC ORGANISM;

AMINO ACID SEQUENCE; DIATOMS; ENZYME ACTIVATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; ORGANISMS, GENETICALLY MODIFIED; PENTOSE PHOSPHATE PATHWAY; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PLASTIDS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 20444479515     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.055285     Document Type: Article

References (56)

1. Anderson LE (1973) Regulation of the pea leaf ribulose-5-phosphate kinase activity. Biochim Biophys Acta 321: 484-488
2. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, et al (2004) The genome of the diatom Thalassiosira pssudonana: ecology, evolution, and metabolism. Science 306: 79-86
3. 2 concentrating mechanisms in cyanobacteria. Funct Plant Biol 29: 161-173
4. Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos Trans R Soc Lond B Biol Sci 355:1433-1446
5. Bhaya D, Grossman AR (1993) Characterization of gene clusters encoding the fucoxanthin chlorophyll proteins of the diatom Phaeodactylum tricornutum, Nucleic Acids Res 21: 4458-4466
6. Brandes HK, Hartman FC, Lu T-YS, Larimer FW (1996) 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: 6490-6496
7. Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31: 341-374
8. Büchel C (2003) Fucoxanthin-chlorophyll proteins in diatoms: 18 and 19 kDa subunits assemble into different oligomeric states. Biochemistry 42: 13027-13034
9. Cline K, Werner-Washburne M, Lubben TH, Keegstra K (1984) Thermolysin is a suitable protease for probing the surface of intact pea plastids. Plant Physiol 75: 667-675
10. Delwiche CF, Palmer JD (1997) The origin of plastids and their spread via secondary symbiosis. Plant Syst Evol 11: 53-86
11. Eicks M, Maurino V, Knappe S, Flügge UI, Fischer K (2002) The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol 128: 512-522
12. Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281: 200-205
13. Farr TJ, Huppe HC, Turpin DH (1994) Coordination of chloroplastic metabolism in N-limited Chlamydomonas reinhardtii by redox modulation: The activation of phosphoribulosekinase and glucose-6-phosphate dehydrogenase is relative to the photosynthetic supply of electrons. Plant Physiol 105: 1037-1042
14. 2 fixation: regulation of spinach ribulose-5-phosphate kinase by stromal metabolite levels. Biochim Biophys Acta 722: 51-60
15. Geck MK, Hartman FC (2000) Kinetic and mutational analyses of the regulation of phosphoribulokinase by thioredoxins. J Biol Chem 275: 18034-18039
16. Hariharan T, Johnson PJ, Cattolico RA (1998) Purification and characterization of phosphoribulokinase from the marine chromophytic alga Heterosigma carterae. Plant Physiol 117: 321-329
17. Heldt HW, Sauer F (1971) The inner membrane of the chloroplast as the site of specific metabolite transport. Biochim Biophys Acta 234: 83-91
18. Hertig CM, Wolosiuk RA (1983) Studies on the hysteretic properties of chloroplast fructose-1,6-bisphosphatase. J Biol Chem 258: 984-989
19. Hirasawa M, Brandes HK, Hartman FC, Knaff DB (1998) Oxidation-reduction properties of the regulatory site of spinach phosphoribulokinase. Arch Biochem Biophys 350: 127-131
20. Hirasawa M, Schürmann P, Jacquot JP, Manieri W, Jacquot P, Keryer E, Hartman FC, Knaff DB (1999) Oxidation-reduction properties of chloroplast thioredoxins, ferredoxin:thioredoxin reductase, and thioredoxin f-regulated enzymes. Biochemistry 38: 5200-5205
21. Hutchison RS, Ort DR (1995) Measurement of equilibrium midpoint potentials of thiol/disulfide regulatory groups in thioredoxin activated chloroplast enzymes. Methods Enzymol 252: 220-228
22. Hwang S-R, Tabita FR (1991) Cotranscription, deduced primary structure, and expression of the chloroplast-encoded rbcL and rbcS genes of the marine diatom Cylindrotheca sp. strain N1. J Biol Chem 266: 6271-6279
23. Jacquot J-P, Lancelin J-M, Meyer Y (1997) Thioredoxins: structure and function in plant cells. New Phytol 136: 543-570
24. 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz (BPP) 167: 191-194
25. Jensen RA (1985) The shikimate/arogenate pathway: link between carbohydrate metabolism and secondary metabolism. Physiol Plant 66: 164-168
26. Kilian O, Kroth PG (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41: 175-183
27. Kobayashi D, Tamoi M, Iwaki T, Shigeoka S, Wadano A (2003) Molecular characterization and redox regulation of phosphoribulokinase from the cyanobacterium Synechococcus sp. PCC 7942. Plant Cell Physiol 44: 269-276
28. Kroth PG (2002) Protein transport into secondary plastids and the evolution of primary and secondary plastids. Int Rev Cytol 221: 191-255
29. Lavaud J, van Gorkom HJ, Etienne AL (2002) Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynth Res 74: 49-57
30. Lebreton S, Graciet E, Gontero B (2003) Modulation, via protein-protein interactions, of glyceraldehyde-3-phosphate dehydrogenase activity through redox phosphoribulokinase regulation. J Biol Chem 278: 12078-12084
31. Lees WJ, Whitesides GM (1993) Equilibrium constants for thiol-disulfide interchange reactions: a coherent, corrected set. J Org Chem 58: 642-647
32. Liaud MF, Lichtle C, Apt K, Martin W, Cerff R (2000) Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol Biol Evol 17: 213-223
33. Lundström J, Holmgren A (1993) Determination of the reduction-oxidation potential of the thioredoxin-like domains of protein disulfide isomerase from the equilibrium with glutathion and thioredoxin. Biochemistry 32: 6649-6655
34. Martin W, Schnarrenberger C (1997) The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet 32: 1-18
35. Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393: 162-165
36. Milanez S, Mural RJ (1988) Cloning and sequencing of cDNA encoding the mature form of phosphoribulokinase from spinach. Gene 66: 55-63
37. Milanez S, Mural RJ, Hartman FC (1991) Roles of cysteinyl residues of phosphoribulokinase as examined by site-directed mutagenesis. J Biol Chem 266: 10694-10699
38. Moreira D, Le Guyader H, Philippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405: 69-72
39. Mouche F, Gontero B, Callebaut I, Mornon JP, Boisset N (2002) Striking conformational change suspected within the phosphoribulokinase dimer induced by interaction with GAPDH. J Biol Chem 277: 6743-6749
40. Ocheretina O, Haferkamp I, Tellioglu H, Scheibe R (2000) Light-modulated NADP-malate dehydrogenases from mossfern and green algae: insights into evolution of the enzyme's regulation. Gene 258: 147-154
41. 1 from the diatom Odontella sinensis. Bot Acta 103: 274-280
42. 1 of the diatom Odontella sinensis including its presequence. FEBS Lett 320: 61-66
43. Porter MA, Hartman FC (1990) Exploration of the function of a regulatory sulfhydryl of phosphoribulokinase from spinach. Arch Biochem Biophys 281: 330-334
44. Porter MA, Milanez S, Stringer CD, Hartman FC (1986) Purification and characterization of ribulose-5-phosphate kinase from spinach. Arch Biochem Biophys 245: 14-23
45. Porter MA, Stringer CD, Hartman FC (1988) Characterization of the regulatory thioredoxin site of phosphoribulokinase. J Biol Chem 263: 123-129
46. Racker E (1957) The reductive pentose phosphate cycle. I. Phosphoribulokinase and ribulose diphosphate carboxylase. Arch Biochem Biophys 69: 300-310
47. Riddles WP, Blakeley RL, Zerner B (1979) Ellmann's reagent: 5,5′-Dithiobis (nitrobenzoic acid): a reexamination. Anal Biochem 94: 75-81
48. Ruelland E, Miginiac-Maslow M (1999) Regulation of chloroplast enzyme activities by thioredoxin: activation or relief from inhibition? Trends Plant Sci 4: 136-141
49. Schnarrenberger C, Flechner A, Martin W (1995) Enzymatic evidence for a complete oxidative pentose phosphate pathway in chloroplasts and an incomplete pathway in the cytosol of spinach leaves. Plant Physiol 108: 609-614
50. Schnarrenberger C, Oeser A, Tolbert NE (1973) Two isoenzymes each of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase in spinach leaves. Arch Biochem Biophys 154: 438-448
51. Stumpp MT, Motohashi K, Hisabori T (1999) Chloroplast thioredoxin mutants without active-site cysteines facilitate the reduction of the regulatory disulphide bridge on the γ-subunit of chloroplast ATP synthase. Biochem J 341: 157-163
52. Wedel N, Soll J (1998) Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/ glyceraldehyde-3-phosphate dehydrogenase complex dissociation. Proc Natl Acad Sci USA 95: 9699-9704
53. Wedel N, Soll J, Paap BK (1997) CP12 provides a new mode of light regulation of Calvin cycle activity in higher plants. Proc Natl Acad Sci USA 94: 10479-10484
54. Wenderoth I, Scheibe R, von Schaewen A (1997) Identification of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. J Biol Chem 272: 26985-26990
55. Wittpoth C, Kroth PG, Weyrauch K, Kowallik KV, Strotmann H (1998) Functional characterization of isolated plastids from two marine diatoms. Planta 206: 79-85
56. Wolosiuk RA, Buchanan BB (1978) Regulation of chloroplast phosphoribulokinase by the ferredoxin/thioredoxin system. Arch Biochem Biophys 189: 97-101