Regulation of phosphoenolpyruvate carboxylase phosphorylation by metabolites and abscisic acid during the development and germination of barley seeds

Plant Physiology

Volumn 148, Issue 2, 2008, Pages 761-774

  Feria, Ana Belén ^a   Alvarez, Rosario ^a   Cochereau, Ludivine ^a   Vidal, Jean ^b   García Mauriño, Sofía ^a   Echevarría, Cristina ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); HORDEUM; HORDEUM VULGARE; RICINUS COMMUNIS;

EID: 57749107450     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.124982     Document Type: Article

References (68)

1. 4 photosynthesis. Plant Cell Physiol 46: 389-398
2. 4 plants. Biochem Biophys Res Commun 286: 1158-1162
3. 4 phosphoenolpyruvate carboxylase catalytic activity and phosphorylation state. Photosynth Res 58: 153-162
4. Blonde JD, Plaxton WC (2003) Structural and kinetic properties of high and low molecular mass phosphoenolpyruvate carboxylase isoforms from the endosperm of developing castor oil seeds. J Biol Chem 278: 11867-11873
5. 2 fixation in Crassulacean acid metabolism. Plant Physiol 121: 889-896
6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
7. Chollet R, Vidal J, O'Leary MH (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 273-298
8. 4Cl-treated protoplasts from Digitaria sanguinalis. Plant J 23: 497-506
9. Drozdowicz YM, Jones RL (1995) Hormonal regulation of organic and phosphoric acid release by barley aleurone layers and scutela. Plant Physiol 108: 769-776
10. 4 phosphoenolpyruvate carboxylase kinase signal transduction chain. Planta 199: 467-474
11. 4 phosphoenolpryruvate carboxylase from Sorghum leaf. Arch Biochem Biophys 315: 425-430
12. Echevarría C, Vidal J (2003) The unique phosphoenolpyruvate carboxylase kinase. Plant Physiol Biochem 41: 541-547
13. Echevarría C, Vidal J, Jiao JA, Chollet R (1990) Reversible light activation of the phosphoenolpyruvate carboxylase protein-serine kinase in maize leaves. FEBS Lett 275: 25-28
14. 2+-calmodulin dependent process. Biochem Biophys Res Commun 155: 835-840
15. Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedling. Plant Cell (Suppl) 14: S15-S45
16. Fontaine V, Hartwel G, Jenkins HG, Nimmo HG (2002) Arabidopsis thaliana contains two phosphoenolpyruvate carboxylase kinase genes with different expression pattern. Plant Cell Environ 25: 115-122
17. Gennidakis S, Rao S, Greenham K, Glen Uhrig R, O'Leary B, Snedden WA, Lu C, Plaxton WC (2007) Bacterial- and plant-type phosphoenolpyruvate carboxylase polypeptides interact in the hetero-oligomeric class-2 PEPC complex of developing castor oil seeds. Plant J 52: 839-849
18. 4 phosphoenolpyruvate carboxylase in protoplasts from Digitaria sanguinalis. Plant Cell 8: 573-586
19. Golombek S, Heim U, Horstmann C, Wobus U, Weber H (1999) Phosphoenolpyruvate carboxylase in developing seeds of Vicia faba L.: gene expression and metabolic regulation. Planta 208: 66-72
20. González MC, Echevarría C, Vidal J, Cejudo FJ (2002) Isolation and characterisation of a wheat phosphoenolpyruvate carboxylase gene: modelling of the encoded protein. Plant Sci 162: 233-238
21. González MC, Osuna L, Echevarría C, Vidal J, Cejudo FJ (1998) Expression and localization of phosphoenolpyruvate carboxylase in developing and germinating wheat grains. Plant Physiol 116: 1249-1258
22. Hamabata A, García-Maya M, Romero T, Bernal-Lugo I (1988) Kinetics of the acidification capacity of aleurone layer and its effect upon solubilization of reserve substances from starchy endosperm of wheat. Plant Physiol 86: 643-644
23. Hartwell J, Gill A, Nimmo GA, Wilkins MB, Jenkins GL, Nimmo HG (1999) Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression. Plant J 20: 333-342
24. 3 on extracellular and intracellular pH and malate in barley aleurone. Plant Physiol 106: 359-365
25. Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Physiol Plant Mol Biol 45: 577-607
26. Izui K, Matsumura H, Furumoto T, Kai Y (2004) Phosphoenolpyruvate carboxylase: a new era of structural biology. Annu Rev Plant Biol 55: 69-84
27. 4 plants. Proc Natl Acad Sci USA 88: 2712-2715
28. Kai Y, Matsumura H, Inoue T, Terada K, Nagara Y, Yoshinaga T, Kihara A, Tsumura A, Izui K (1999) Three-dimensional structure of phosphoenolpyruvate carboxylase: a proposed mechanism for allosteric inhibition. Proc Natl Acad Sci USA 96: 823-828
29. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277: 680-685
30. Law RD, Plaxton WC (1997) Regulatory phosphorylation of banana fruit phosphoenolpyruvate carboxylase by a copurifying phosphoenolpyruvate carboxylase-kinase. Eur J Biochem 247: 642-651
31. Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 19: 199-222
32. Lowry OH, Passoneau JV (1972) A Flexible System of Enzymatic Analysis. Academic Press, New York
33. Macnicol PK, Jacobsen JV (1992) Endosperm acidification and related metabolic changes in the developing barley grain. Plant Physiol 98: 1098-1104
34. Macnicol PK, Raymond P (1998) Role of phosphoenolpyruvate carboxylase in malate production by the developing barley aleurone layer. Physiol Plant 103: 132-138
35. Mamedov TG, Moellering ER, Chollet R (2005) Identification and expression analysis of two inorganic C- and N-responsive genes encoding novel and distinct molecular forms of eukaryotic phosphoenolpyruvate carboxylase in the green microalga Chlamydomonas reinhardtii. Plant J 42: 832-843
36. 4 from maize and quaternary complex of E. coli phosphoenolpyruvate carboxylases. Structure 10: 1721-1730
37. Meimoun P, Ambard-Bretteville F, Colas des Francs-Small C, Valot B, Vidal J (2007) Analysis of plant phosphoproteins. Anal Biochem 371: 238-246
38. Moellering ER, Ouyang Y, Mamedov TG, Chollet R (2007) The two divergent PEP-carboxylase catalytic subunits in the green microalga Chlamydomonas reinhardtii respond reversibly to inorganic-N-supply and co-exist in the high-molecular-mass, hetero-oligomeric class-2-PEPC complex. FEBS Lett 581: 4871-4876
39. Monreal JA, Feria AB, Vinardell JM, Vidal J, Echevarría C, García-Mauriño S (2007) ABA modulates the degradation of phosphoenolpyruvate carboxylase kinase in sorghum leaves. FEBS Lett 581: 3468-3472
40. Murmu J, Plaxton WC (2007) Phosphoenolpyruvate carboxylase protein kinase from developing castor oil seeds: partial purification, characterization, and reversible control by photosynthate supply. Planta 226: 1299-1310
41. Nhiri M, Bakrim N, Bakrim N, El Hachimi-Messouak Z, Echevarría C, Vidal J (2000) Posttranslational regulation of phosphoenolpyruvate carboxylase during germination of Sorghum seeds: influence of NaCl and L-malate. Plant Sci 151: 29-37
42. 4 phosphoenolpyruvate carboxylase. Plant Cell Physiol 39: 241-246
43. Nimmo GA, McNaughton GA, Fewson CA, Wilkins MB, Nimmo HG (1987) Changes in the kinetic properties and phosphorylation state of phosphoenolpyruvate carboxylase in Zea mays leaves in response to light and dark. FEBS Lett 213: 18-22
44. Nimmo GA, Wilkins MB, Nimmo HG (2001) Partial purification and characterization of a protein inhibitor of phosphoenolpyruvate carboxylase kinase. Planta 213: 250-257
45. Nimmo HG (2003) Control of the phosphorylation of phosphoenolpyruvate carboxylase in higher plants. Arch Biochem Biophys 414: 189-196
46. (2+)-dependent protein kinase phosphorylating phosphoenolpyruvate carboxylase. Plant Cell Physiol 39: 1010-1019
47. Osuna L, González MC, Cejudo FJ, Vidal J, Echevarría C (1996) In vivo and in vitro phosphorylation of the phosphoenolpyruvate carboxylase from wheat seed during germination. Plant Physiol 111: 551-558
48. 2+-independent phosphoenolpyruvate carboxylase kinase in the aleurone endosperm tissue of germinating barley seeds. Plant Physiol 119: 511-520
49. Pacquit V, Giglioli N, Crétin C, Pierre JN, Vidal J, Echevarría C (1995) Regulatory phosphorylation of C4 phosphoenolpyruvate carboxylase from sorghum: an immunological study using specific anti-phosphorylation site-antibodies. Photosynth Res 43: 283-288
50. Rivoal J, Dunford R, Plaxton WC, Turpin DH (1996) Purification and properties of four phosphoenolpyruvate carboxylase isoforms from the green alga Selenastrum minutum: evidence that association of the 102-kDa catalytic subunit with unrelated polypeptides may modify the physical and kinetic properties of the enzyme. Arch Biochem Biophys 332: 47-57
51. Rivoal J, Plaxton WC, Turpin DH (1998) Purification and characterization of high- and low-molecular-mass isoforms of phosphoenolpyruvate carboxylase from Chlamydomonas reinhardtii: kinetic, structural and immunological evidence that the green algal enzyme is distinct from the prokaryotic and higher plant enzyme. Biochem J 331: 201-209
52. Rivoal J, Smith CR, Moraes TF, Turpin DH, Plaxton WC (2002) A method for activity attaining after native polyacrylamide gel electrophoresis using a coupled enzyme assay and fluorescence detection: application to the analysis of several glycolytic enzymes. Anal Biochem 300: 94-99
53. Rock CD, Quatrano RS (1995) The role of hormones during seed development. In PJ Davies, ed, Plant Hormones: Physiology, Biochemistry and Molecular Biology. Kluwer Academic Publisher, Dordrecht, The Netherlands, pp 671-697
54. Ruuska SA, Girke T, Benning C, Ohlrogge JB (2002) Contrapuntal networks of gene expression during the Arabidopsis seed filling. Plant Cell 14: 1191-1206
55. Sánchez R, Cejudo FJ (2003) Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiol 132: 949-957
56. Sangwan RS, Singh N, Plaxton WC (1992) Phosphoenolpyruvate carboxylase activity and concentration in the endosperm of developing and germinating castor oil seeds. Plant Physiol 99: 445-449
57. Schwender J, Ohlrogge JB, Shachar-Hill Y (2004) Understanding flux in plant metabolic networks. Curr Opin Plant Biol 7: 309-317
58. Sullivan S, Jenkins GI, Nimmo HG (2004) Roots, cycles and leaves: expression of the phosphoenolpyruvate carboxylase gene family in soybean. Plant Physiol 135: 2078-2087
59. Tripodi KE, Turner WL, Gennidakis S, Plaxton WC (2005) In vivo regulatory phosphorylation of novel phosphoenolpyruvate carboxylase isoforms in endosperm of developing castor oil seed. Plant Physiol 139: 969-978
60. Tsuchida Y, Furumoto T, Hisabori T, Izui K (2004) Mechanism of redox regulation of a C4-phosphoenolpyruvate carboxylase (PEPC) via thioredoxin (Trx). Plant Cell Physiol 45: S154
61. Turner WL, Knowles VL, Plaxton WC (2005) Cytosolic pyruvate kinase: subunit composition, activity, and amount in developing castor and soybean seeds, and biochemical characterization of the purified castor seed enzyme. Planta 6: 1051-1062
62. Uhrig RG, O'Leary B, Spang HE, MacDonald JA, She YM, Plaxton WC (2008) Co-immunopurification of phosphorylated bacterial- and plant-type phosphoenolpyruvate carboxylase with the plastidial pyruvate dehydrogenase complex from developing castor oil seeds. Plant Physiol 146: 1346-1357
63. 4 phosphoenolpyruvate carboxylase. Trends Plant Sci 2: 230-237
64. Vidal J, Godbillon P, Gadal P (1981) Recovery of active highly purified phosphoenolpyruvate carboxylase from specific immunoabsorbent column. FEBS Lett 118: 31-34
65. Wadham C, Winter H, Schuller KA (1996) Regulation of soybean nodule phosphoenolpyruvate carboxylase in vivo. Physiol Plant 97: 531-535
66. Wang YH, Chollet R (1993) Partial purification and characterization of phosphoenolpyruvate carboxylase protein-serine kinase from illuminated maize leaves. Arch Biochem Biophys 304: 496-502
67. Zhang XQ, Chollet R (1997) Phosphoenolpyruvate carboxylase protein kinase from soybean root nodules: partial purification, characterization, and up/down regulation by photosynthate supply from the shoots. Arch Biochem Biophys 343: 260-269
68. Zhang XQ, Li B, Chollet R (1995) In vivo regulatory phosphorylation of soybean nodule phosphoenolpyruvate carboxylase. Plant Physiol 108: 1561-1568