Redox regulation of a novel plastid-targeted β-amylase of arabidopsis

Plant Physiology

Volumn 141, Issue 3, 2006, Pages 840-850

  Sparla, Francesca ^a   Costa, Alex ^b   Lo Schiavo, Fiorella ^a   Pupillo, Paolo ^a   Trost, Paolo ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; METABOLISM; MONOMERS; PROTEINS; SEED;

ARABIDOPSIS THALIANA; STARCH METABOLISM;

GENETIC ENGINEERING;

ENZYMES; GENES; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 33745961686     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.106.079186     Document Type: Article

References (63)

1. Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54: 207-233
2. Ballicora MA, Frueauf JB, Fu Y, Schurmann P, Preiss J (2000) Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. J Biol Chem 275: 1315-1320
3. Balmer Y, Vensel WH, Cai N, Manieri W, Schurmann P, Hurkman WJ, Buchanan BB (2006) A complete ferredoxin/thioredoxin system regulates fundamental processes in amyloplasts. Proc Natl Acad Sci USA 103: 2988-2993
4. Baunsgaard L, Lutken H, Mikkelsen R, Glaring MA, Pham TT, Blennow A (2005) A novel isoform of glucan, water dikinase phosphorylates prephosphorylated alpha-glucans and is involved in starch degradation in Arabidopsis. Plant J 41: 595-605
5. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56: 187-220
6. Caspar T, Lin TP, Kakefuda G, Benbow L, Preiss J, Somerville C (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol 95: 1181-1188
7. Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin J-M, Knaff DB, Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278: 23747-23752
8. Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M, Knaff DB, Dietz KJ, Issakidis-Bourguet E (2004) Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol 136: 4088-4095
9. Critchley JH, Zeeman SC, Takaha T, Smith AM, Smith SM (2001) A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutant in Arabidopsis. Plant J 26: 89-100
10. Datta R, Selvi MT, Seetharama N, Sharma R (1999) Stress-mediated enhancement of beta-amylase activity in pearl millet and maize leaves is dependent on light. J Plant Physiol 154: 657-664
11. Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139: 847-856
12. Dreier W, Schnarrenberger C, Börner T (1995) Light- and stress-dependent enhancement of amylolytic activities in white and green barley leaves: beta-amylases are stress-induced proteins. J Plant Physiol 145: 342-348
13. Duby G, Oufattole M, Boutry M (2001) Hydrophobic residues within the predicted N-terminal amphiphilic alpha-helix of a plant mitochondrial targeting presequence play a major role in in vivo import. Plant J 27: 539-549
14. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978-984
15. Fobert PR, Despres C (2005) Redox control of systemic acquired resistance. Curr Opin Plant Biol 8: 378-382
16. 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
17. Hirata A, Adachi M, Sekine A, Kang YN, Utsumi S, Mikami B (2004) Structural and enzymatic analysis of soybean β-amylase mutants with increased pH optimum. J Biol Chem 279: 7287-7295
18. Hutchinson RS, Groom Q, Ort DR (2000) Differential effects of chilling-induced photooxidation on the redox regulation of photosynthetic enzymes. Biochemistry 39: 6679-6688
19. Hutchinson RS, Ort DR (1995) Measurement of equilibrium midpoint potentials of thiol/disulfide regulatory groups on thioredoxin-activated chloroplast enzymes. Methods Enzymol 252: 220-228
20. Jacquot JP, Lopez-Jaramillo J, Miginiac-Maslow M, Lemaire S, Cherfils J, Chueca A, Lopez-Gorge J (1997) Cysteine-153 is required for redox regulation of pea chloroplast fructose-1,6-bisphosphatase. FEBS Lett 401: 143-147
21. Kaplan F, Guy CL (2004) β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135: 1674-1684
22. Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44: 730-743
23. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102: 11118-11123
24. Kötting O, Pusch K, Tiessen A, Geigenberger P, Steup M, Ritte G (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves: the phosphoglucan, water dikinase. Plant Physiol 137: 242-252
25. Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynth Res 60: 151-163
26. Laby RJ, Kim D, Gibson SI (2001) The ram1 mutant of Arabidopsis exhibits severely decreased β-amylase activity. Plant Physiol 127: 1798-1807
27. Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kavanagh TA (1999) An Arabidopsis gene encoding a chloroplast targeted β-amylase. Plant J 20: 519-527
28. Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Ann Bot (Lond) 89: 871-885
29. Lloyd JR, Lossmann J, Ritte G (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci 10: 130-137
30. Locatelli F, Vannini C, Magnani E, Coraggio I, Bracale M (2003) Efficiency of transient transformation in tobacco protoplasts is independent of plasmid amount. Plant Cell Rep 21: 865-871
31. Lu Y, Sharkey T (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218: 466-473
32. Marri L, Sparla F, Pupillo P, Trost P (2005a) Coordinated gene expression of photosynthetic glyceraldehyde-3-phosphate dehydrogenase, phosphoribulokinase and CP12 in Arabidopsis thaliana. J Exp Bot 56: 73-80
33. Marri L, Trost P, Pupillo P, Sparla F (2005b) Reconstitution and properties of the recombinant GAPDH/CP12/PRK supramolecular complex of Arabidopsis thaliana. Plant Physiol 139: 1433-1443
34. Mikami B, Hehre EJ, Sato M, Katsube Y, Hirose M, Morita Y, Sacchettini JC (1993) The 2.0-A resolution structure of soybean beta-amylase complexed with alpha-cyclodextrin. Biochemistry 32: 6836-6845
35. Mikkelsen R, Mutenda KE, Mant A, Schurmann P, Blennow A (2005) Alpha-glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci USA 102: 1785-1790
36. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays in tobacco tissue cultures. Physiol Plant 15: 473-497
37. Nagy JI, Maliga P (1976) Callus induction and plant regeneration from mesophyll protoplasts of Nicotiana sylvestrys. Z Pflanzenphysiol 78: 453-544
38. Nakai K, Horton P (1999) PSORT: a program for detecting the sorting signals of proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-35
39. Nielsen TH, Wischmann B, Enevoldsen K, Moller BL (1994) Starch phosphorylation in potato tubers proceeds concurrently with de novo biosynthesis of starch. Plant Physiol 105: 111-117
40. Nielsen TM, Deiting U, Stitt M (1997) A beta-amylase in potato tubers is induced by storage at low temperature. Plant Physiol 113: 503-510
41. Nnttylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87-89
42. Rey P, Cuine S, Eymery F, Garin J, Court M, Jacquot JP, Rouhier N, Broin M (2005) Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J 41: 31-42
43. Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, Steup M (2002) The starch-related protein R1 is an α-glucan, water dikinase. Proc Natl Acad Sci USA 99: 7166-7171
44. Ritte G, Scharf A, Eckermann N, Haebel S, Steup M (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiol 135: 2068-2077
45. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide: the response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134: 1683-1696
46. Rodriguez-Suarez RJ, Mora-Garcia S, Wolosiuk RA (1997) Characterization of cysteine residues involvement in the reductive activation and the structural stability of rapeseed (Brassica napus) chloroplast fructose-1,6-bisphosphatase. Biochem Biophys Res Commun 232: 388-393
47. Scheidig A, Fröhlich A, Schulze S, Lloyd JR, Kossmann J (2002) Down-regulation of chloroplast-targeted β-amylase leads to a starch excess phenotype in leaves. Plant J 30: 581-591
48. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann J (2005) A gene expression map of Arabidopsis development. Nat Genet 37: 501-506
49. Schürmann P, Jacquot J-P (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51: 371-400
50. Serrato AJ, Perez-Ruiz JM, Spinola MC, Cejudo FJ (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 15: 43821-43827
51. Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56: 73-97
52. Sparla F, Pupillo P, Trost P (2002) The C-terminal extension of glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide. J Biol Chem 277: 44946-44952
53. Sparla F, Tedeschi G, Pupillo P, Trost P (1999) Cloning and heterologous expression of NAD(P)H:quinone reductase of Arabidopsis thaliana, a functional homologue of animal DT-diaphorase. FEBS Lett 463: 382-386
54. Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch Synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14: 2191-2213
55. Walters RG, Ibrahim DG, Horton P, Kruger NJ (2004) A mutant of Arabidopsis lacking the triose-phosphate/phosphate translocator reveals metabolic regulation of starch breakdown in the light. Plant Physiol 135: 891-906
56. Wang Q, Monroe J, Sjölund RD (1995) Identification and characterization of a phloem-specific β-amylase, Plant Physiol 109: 743-750
57. Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Groner F, Hebbeker U, Flugge UI (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12: 787-802
58. Yu TS, Kofler H, Hausler RE, Hille D, Flugge UI, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, et al (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in e chloroplast hexose transporter. Plant Cell 13: 1907-1918
59. Yu T-S, Zeeman SC Thorneycroft D, Fulton DC, Dunstan H, Lue W-L, Hegemann B, Tung S-Y, Umemoto T, Chapple A, et al (2005) α-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280: 9773-9779
60. Zeeman SC, Smith SM, Smith AM (2004) The breakdown of starch in leaves. New Phytol 163: 247-261
61. Zeeman SC, Tiessen A, Pilling E, Kato KL, Donald AM, Smith AM (2002) Starch synthesis in Arabidopsis: granule synthesis, composition, and structure. Plant Physiol 129: 516-529
62. +-ATPase pma4 transcription promoter from Nicotiana plumbaginifolia activated by the CaMV 35S promoter enhancer. Plant Sci 149: 157-165
63. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632