Spatio-temporal profiling and degradation of α-amylase isozymes during barley seed germination

FEBS Journal

Volumn 274, Issue 10, 2007, Pages 2552-2565

  Bak Jensen, Kristian S ^b   Laugesen, Sabrina ^a,c   Østergaard, Ole ^b   Finnie, Christine ^b,c   Roepstorff, Peter ^a   Svensson, Birte ^b,c  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b CARLSBERG LABORATORY   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

amylase isozymes; 2D western blot and mass spectrometry; Barley seed germination; Gibberellic acid; Proteolytic processing

Indexed keywords

AMYLASE; AMYLASE 1; AMYLASE 2; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ALEURONE; ALPHA HELIX; ARTICLE; BARLEY; BETA SHEET; CARBOXY TERMINAL SEQUENCE; ENDOSPERM; GENE IDENTIFICATION; GENETIC CODE; GERMINATION; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PLANT TISSUE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

ALPHA-AMYLASE; AMINO ACID SEQUENCE; BLOTTING, WESTERN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GERMINATION; GIBBERELLINS; HORDEUM; HYDROGEN-ION CONCENTRATION; ISOENZYMES; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; SEEDS; SEQUENCE ALIGNMENT; TANDEM MASS SPECTROMETRY; TISSUE DISTRIBUTION;

HORDEUM;

EID: 34247601653     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05790.x     Document Type: Article

References (71)

1. Fincher GB Stone B (1993) Physiology and Biochemistry of Germination in Barley. In Barley, Chemistry and Technology (MacGregor, AW Bhatty, RS, eds), pp. 247 295. American Association of Cereal Chemists, St. Paul, MN.
2. Briggs DE (2002) Malts and Malting, 1st edn. Aspen Publishers, London, UK.
3. Huang N, Stebbins GL Rodriguez RL (1992) Classification and evolution of α-amylase genes in plants. Proc Natl Acad Sci USA 89, 7526 7530.
4. Henrissat B Bairoch A (1996) Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316, 695 696.
5. Søgaard M, Olsen FL Svensson B (1991) C-terminal processing of barley α-amylase 1 in malt, aleurone protoplasts, and yeast. Proc Natl Acad Sci USA 88, 8140 8144.
6. Mundy J, Svendsen I Hejgaard J (1983) Barley α-amylase/subtilisin inhibitor. I. Isolation and characterization. Carlsberg Res Commun 48, 81 90.
7. Bush DS, Sticher L, van Huystee R, Wagner D Jones RL (1989) The calcium requirement for stability and enzymatic activity of two isoforms of barley aleurone α-amylase. J Biol Chem 264, 19392 19398.
8. Søgaard M Svensson B (1990) Expression of cDNAs encoding barley α-amylase 1 and 2 in yeast and characterization of the secreted proteins. Gene 94, 173 179.
9. Ajandouz EH, Abe J, Svensson B Marchis-Mouren G (1992) Barley malt α-amylase: purification, action pattern, and subsite mapping of isozyme 1 and two members of the isozyme 2 subfamily using p-nitrophenylated maltooligosaccharide substrates. Biochim Biophys Acta 1159, 193 202.
10. Valleé F, Kadziola A, Bourne Y, Juy M, Rodenburg KW, Svensson B Haser R (1998) Barley α-amylase bound to its endogenous protein inhibitor BASI: crystal structure of the complex at 1.9 Å resolution. Structure 6, 649 659.
11. Jensen MT, Gottschalk TE Svensson B (2003) Differences in conformational stability of barley α-amylase isozymes 1 and 2. Role of charged groups and isozyme 2 specific salt-bridges. J Cereal Sci 38, 289 300.
12. Kadziola A, Abe J, Svensson B Haser R (1994) Crystal and molecular structure of barley alpha-amylase. J Mol Biol 239, 104 121.
13. Kadziola A, Søgaard M, Svensson B Haser R (1998) Molecular structure of a barley α-amylase-inhibitor complex: implications for starch binding and catalysis. J Mol Biol 278, 205 217.
14. Rodenburg KW, Valleé F, Juge N, Aghajari N, Guo X, Haser R Svensson B (2000) Specific inhibition of barley α-amylase 2 by barley α-amylase/subtilisin inhibitor depends on charge interactions and can be conferred to isozyme 1 by mutation. Eur J Biochem 267, 1019 1029.
15. Khursheed B Rogers JC (1988) Barley alpha-amylase genes: quantitative comparison of steady-state mRNA levels from individual members of the two different families expressed in aleurone cells. J Biol Chem 263, 18953 18960.
16. Perata P, Matsukura C, Vernieri P Yamaguchi J (1997) Sugar repression of a gibberellin-dependent signaling pathway in barley embryos. Plant Cell 9, 2197 2208.
17. Fincher GB (1989) Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu Rev Plant Physiol Plant Biol 40, 305 346.
18. Jones RL Jacobsen JV (1991) Regulation of synthesis and transport of secreted proteins in cereal aleurone. Int Rev Cytol 126, 49 88.
19. Ritchie S, McCubbin A, Ambrose G, Kao T Gilroy S (1999) The sensitivity of barley aleurone tissue to gibberellin is heterogeneous and may be spatially determined. Plant Physiol 120, 361 370.
20. Ritchie S Gilroy S (1998) Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase d activity. Proc Natl Acad Sci USA 95, 2697 2702.
21. Rogers JC (1985) Two barley alpha-amylase gene families are regulated differently in aleurone cells. J Biol Chem 260, 3731 3738.
22. Caspers MP, Lok F, Sinjorgo KM, van Zeijl MJ, Nielsen KA Cameron-Mills V (2001) Synthesis, processing and export of cytoplasmic endo-beta-1,4-xylanase from barley aleurone during germination. Plant J 26, 191 204.
23. Jones BL, Marinac LA Fontanini D (2000) Quantitative study of the formation of endoproteolytic activities during malting and their stabilities to kilning. J Agric Food Chem 48, 3898 3905.
24. Phillips HA Wallace W (1989) A cysteine endopeptidase from barley malt which degrades hordein. Phytochemistry 28, 3285 3290.
25. Enari TM Sopanen T (1986) Mobilisation of endospermal reserves during the germination of barley. J Inst Brew 92, 25 31.
26. Breddam K, Sørensen SB Ottesen M (1983) Isolation of a carboxypeptidase from malted barley by affinity chromatography. Carlsberg Res Commun 48, 217 223.
27. Breddam K (1985) Enzymatic properties of malt carboxypeptidase II in hydrolysis and aminolysis reactions. Carlsberg Res Commun 50, 309 323.
28. Kreiss M Shewry PR (1992) Control of protein synthesis in developing barley seeds. In Barley: Genetics, Biochemistry, Molecular Biology and Biotechnology (Shewry, PR, ed.), pp. 3 19 333. CAB International, Oxford, UK.
29. Østergaard O, Finnie C, Laugesen S, Roepstorff P Svensson B (2004) Proteome analysis of barley seeds and malt: Identification of major proteins from two-dimensional gels (pI 4-7). Proteomics 4, 2437 2447.
30. Weiss W, Postel W Görg A (1992) Application of sequential extraction procedures and glycoprotein blotting for the characterization of the 2-D polypeptide patterns of barley seed proteins. Electrophoresis 13, 770 773.
31. Weiss W, Postel W Görg A (1991) Barley cultivar discrimination. II. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and isoelectric focusing with immobilized pH gradients. Electrophoresis 12, 330 337.
32. Weiss W, Postel W Görg A (1991) Barley cultivar discrimination. I. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and glycoprotein blotting. Electrophoresis 12, 323 330.
33. Görg A, Postel W, Baumer M Weiss W (1992) Two-dimensional polyacrylamide gel electrophoresis, with immobilized pH gradients in the first dimension, of barley seed proteins: discrimination of cultivars with different malting grades. Electrophoresis 13, 192 203.
34. Görg A, Postel W, Domscheit A Gunther S (1988) Two-dimensional electrophoresis with immobilized pH gradients of leaf proteins from barley (Hordeum vulgare): method, reproducibility and genetic aspects. Electrophoresis 9, 681 692.
35. Görg A, Postel W Weiss W (1992) Detection of polypeptides and amylase isoenzyme modifications related to malting quality during malting process of barley by two-dimensional electrophoresis and isoelectric focusing with immobilized pH gradients. Electrophoresis 13, 759 770.
36. Østergaard O, Melchior S, Roepstorff P Svensson B (2002) Initial proteome analysis of mature barley seeds and malt. Proteomics 2, 733 739.
37. Finnie C, Melchior S, Roepstorff P Svensson B (2002) Proteome analysis of grain filling and seed maturation in barley. Plant Physiol 129, 1308 1319.
38. Finnie C, Steenholdt T, Roda Noguera O, Knudsen S, Larsen J, Brinch-Pedersen H, Bach Holm P, Olsen O Svensson B (2004) Environmental and transgene expression effects on the barley seed proteome. Phytochemistry 65, 1619 1627.
39. Finnie C, Maeda K, Østergaard O, Bak-Jensen KS, Larsen J Svensson B (2004) Aspects of the barley seed proteome during development and germination. Biochem Soc Trans 32, 517 519.
40. Bak-Jensen KS, Laugesen S, Roepstorff P Svensson B (2004) Two-dimensional electrophoresis pattern (pH 6-11) and identification of water-soluble barley seed and malt proteins by mass spectrometry. Proteomics 4, 728 742.
41. Maeda K, Finnie C Svensson B (2004) Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms. Biochem J 378, 497 507.
42. Koller A, Washburn MP, Lange BM, Andon NL, Deciu C, Haynes PA, Hays L, Schieltz D, Ulaszek R, Wei J et al. (2002) Proteomic survey of metabolic pathways in rice. Proc Natl Acad Sci USA 99, 11969 11974.
43. Kersten B, Burkle L, Kuhn EJ, Giavalisco P, Konthur Z, Lueking A, Walter G, Eickhoff H Schneider U (2002) Large-scale plant proteomics. Plant Mol Biol 48, 133 141.
44. Nanjo Y, Asatsuma S, Itoh K, Hori H Mitsui T (2004) Proteomic identification of α-amylase isoforms encoded by RAmy3B/3C from germinating rice seeds. Biosci Biotechnol Biochem 68, 112 118.
45. Kim JK Wu R (1992) Nucleotide sequence of a high-pI rice (Oryza sativa) α-amylase gene. Plant Mol Biol 18, 399 402.
46. Yu SM, Lee YC, Fang SC, Chan MT, Hwa SF Liu LF (1996) Sugars act as signal molecules and osmotica to regulate the expression of alpha-amylase genes and metabolic activities in germinating cereal grains. Plant Mol Biol 30, 1277 1289.
47. Finnie C Svensson B (2002) Proteolysis during the isoelectric focusing step of two-dimensional gel electrophoresis may be a common problem. Anal Biochem 311, 182 186.
48. Zhang N Jones BL (1995) Characterization of germinated barley endoproteolytic enzymes by two-dimensional gel electrophoresis. J Cereal Sci 21, 145 153.
49. Davy A, Svendsen I, Sørensen SO, Blom SM, Rouster J, Meldal M, Simpson DJ Cameron-Mills V (1998) Substrate specificity of barley cysteine endoproteases EP-A and EP-B. Plant Physiol 117, 255 261.
50. Davy A, Sørensen MB, Svendsen I, Cameron-Mills V Simpson DJ (2000) Prediction of protein cleavage sites by the barley cysteine endoproteases EP-A and EP-B based on the kinetics of synthetic peptide hydrolysis. Plant Physiol 122, 137 146.
51. Maya-Ampudia V Bernal-Lugo I (2006) Redox-sensitive target detection in gibberellic acid-induced barley aleurone layer. Free Radic Biol Med 40, 1362 1368.
52. Berven FS, Karlsen OA, Murrell JC Jensen HB (2003) Multiple polypeptide forms observed in two-dimensional gels of Methylococcus capsulatus (Bath) polypeptides are generated during the separation procedure. Electrophoresis 24, 757 761.
53. Veith PD, Talbo GH, Slakeski N Reynolds EC (2001) Identification of a novel heterodimeric outer membrane protein of Porphyromonas gingivalis by two-dimensional gel electrophoresis and peptide mass fingerprinting. Eur J Biochem 268, 4748 4757.
54. Lutter P, Meyer HE, Langer M, Witthohn K, Dormeyer W, Sickmann A Bluggel M (2001) Investigation of charge variants of rViscumin by two-dimensional gel electrophoresis and mass spectrometry. Electrophoresis 22, 2888 2897.
55. Sticher L Jones RL (1992) α-amylase isoforms are posttranslationally modified in the endomembrane system of the barley aleurone layer. Plant Physiol 98, 1080 1086.
56. Akazawa T Hara-Nishimura I (1985) Topographic aspects of biosynthesis, extracellular secretion, and intracellular storage of proteins in plant cells. Ann Rev Plant Physiol 36, 441 472.
57. Rodenburg KW, Juge N, Guo X-J, Sogaard M, Chaix J-C Svensson B (1994) Domain B protruding at the third β strand of the α/β barrel in barley α-amylase confers distinct isozyme-specific properties. Eur J Biochem 221, 277 284.
58. Juge N, Rodenburg KW, Guo X-J, Chaix J-C Svensson B (1995) Isozyme hybrids within the protruding third loop domain of the barley α-amylase (β/α)8-barrel implication for BASI sensitivity and substrate affinity. FEBS Lett 263, 299 303.
59. Chen K An Y-QC (2006) Transcriptional responses to gibberellin and absiscic acid in barley aleurone. J Integrated Plant Biol 48, 591 612.
60. McCallum CM, Comai L, Greene EA Henikoff S (2000) Targeting induced local lesions IN genomes (TILLING) for plant functional genomics. Plant Physiol 123, 439 442.
61. Finnie C Svensson B (2003) Feasibility study of a tissue-specific approach to barley proteome analysis: aleurone layer, endosperm, embryo and single seeds. J Cereal Sci 38, 217 227.
62. 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.
63. Heukeshoven J Dernick R (1988) Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gels. Electrophoresis 9, 28 32.
64. Yan JX, Wait R, Berkelman T, Harry RA, Westbrook JA, Wheeler CH Dunn MJ (2000) A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 21, 3666 3672.
65. Rabilloud T Charmont S (2000) Detection of proteins on two-dimensional electrophoresis gels. In Proteome Research: Two-Dimensional Gel Electrophoresis and Identification Methods (Rabilloud, T, ed.), pp. 107 126. Springer Verlag, Heidelberg.
66. Towbin H Gordon J (1984) Immunoblotting and dot immunobinding - current status and outlook. J Immunol Methods 72, 313 340.
67. Svensson B, Mundy J, Gibson RM Svendsen I (1985) Partial amino acid sequences of α-amylase isozymes from barley malt. Carlsberg Res Commun 50, 15 22.
68. Shevchenko A, Wilm M, Vorm O Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68, 850 858.
69. Gobom J, Nordhoff E, Mirgorodskaya E, Ekman R Roepstorff P (1999) Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J Mass Spectrom 34, 105 116.
70. Beavis RC Chait BT (1990) High-accuracy molecular mass determination of proteins using matrix-assisted laser desorption mass spectrometry. Anal Chem 62, 1836 1840.
71. Jensen ON, Larsen MR Roepstorff P (1998) Mass spectrometric identification and microcharacterization of proteins from electrophoretic gels: strategies and applications. Proteinssupplement 2, 74 89.