Proteomes of the barley aleurone layer: A model system for plant signalling and protein secretion

Proteomics

Volumn 11, Issue 9, 2011, Pages 1595-1605

  Finnie, Christine ^a   Andersen, Birgit ^a   Shahpiri, Azar ^a,b   Svensson, Birte ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b ISFAHAN UNIVERSITY OF TECHNOLOGY   (Iran)

Author keywords

Hydrolases; Membrane proteins; Phytohormones; Plant proteomics; Protein secretion; Seed germination

Indexed keywords

AMYLASE; BETA AMYLASE; GIBBERELLIC ACID; HYDROLASE; MEMBRANE PROTEIN; PROTEOME; REACTIVE OXYGEN METABOLITE;

ALEURONE; AMINO TERMINAL SEQUENCE; APOPTOSIS; BARLEY; CELL MEMBRANE; CHEMICAL BOND; ENDOSPERM; FERMENTATION; GERMINATION; HORMONE RESPONSE; MASS SPECTROMETRY; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ABSCISIC ACID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GIBBERELLINS; HORDEUM; MODELS, BIOLOGICAL; PLANT GROWTH REGULATORS; PLANT PROTEINS; PROTEOME; SEEDS; SIGNAL TRANSDUCTION;

HORDEUM;

EID: 79954988984     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000656     Document Type: Review

References (78)

1. Olsen, O. A., Endosperm development: cellularization and cell fate specification. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52, 233-267.
2. Skriver, K., Mundy, J., Gene expression in response to abscisic acid and osmotic stress. Plant Cell 1990, 2, 503-512.
3. Ritchie, S., Swanson, S. J., Gilory, S., Physiology of the aleurone layer and starchy endosperm during grain development and early seedling growth: new insights from cell and molecular biology. Seed Sci. Res. 2000, 10, 193-212.
4. Bewley, J. D., Seed germination and dormancy. Plant Cell 1997, 9, 1055-1066.
5. Zentella, R., Yamauchi, D., Ho, T. D., Molecular dissection of the gibberellin/abscisic acid signaling pathways by transiently expressed RNA interference in barley aleurone cells. Plant Cell 2002, 14, 2289-2301.
6. Fincher, G. B., Molecular and cellular biology associated with endosperm mobilization in geminating cereal grain. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1989, 40, 305-346.
7. Jones, R. L., Jacobsen, J. V., Regulation of synthesis and transport of secreted proteins in cereal aleurone. Int. Rev. Cytol. 1991, 126, 49-88.
8. Ho, T. H. D., Gomez-Cadenas, A., Zentella, R., Casaretto, J., Crosstalk between gibberellin and abscisic acid in cereal aleurone layer. Plant Growth Regul. 2003, 22, 185-194.
9. Sun, Z. T., Henson, C. A., A quantitative assessment of the importance of barley seed α-amylase, β-amylase, debranching enzyme, and α-glucosidase in starch degradation. Arch. Biochem. Biophys. 1991, 284, 298-305.
10. Frandsen, T. P., Svensson, B., Plant alpha-glucosidases of the glycoside hydrolase family 31. Molecular properties, substrate specificity, reaction mechanism, and comparison with family members of different origin. Plant Mol. Biol. 1998, 37, 1-13.
11. Hara-Nishimura, L., Nishimura, M., Daussant, J., Conversion of free β-amylase to bound β-amylase on starch granules in the barley endosperm during desiccation phase of seed development. Protoplasma 1986, 134, 149-153.
12. Lundgard, R., Svensson, B., The four major forms of barley β-amylase. Purification, characterization and structural relationship. Carlsberg Res. Commun. 1987, 52, 313-326.
13. Nielsen, M. M., Seo, E. S., Dilokpimol, A., Andersen, J. et al., Roles of multiple surface sites, long substrate binding clefts, and carbohydrate binding modules in the action of amylolytic enzymes on polysaccharide substrates. Biocatal. Biotransform. 2008, 26, 59-67.
14. Rodenburg, K. W., Valleé, F., Juge, N., Aghajari, N. et al., Specific inhibition of barley a-amylase 2 by barley α-amylase/subtilisin inhibitor depends on charge interactions and can be conferred to isozyme 1 by mutation. Eur. J. Biochem. 2000, 267, 1019-1029.
15. MacGregor, E. A., The proteinaceous inhibitor of limit dextrinase in barley and malt. Biochim. Biophys. Acta 2004, 1696, 165-170.
16. Stahl, Y., Coates, S., Bryce, J. H., Morris, P. C., Antisense downregulation of the barley limit dextrinase inhibitor modulates starch granule size distribution, starch composition and amylopectin structure. Plant J. 2004, 39, 599-611.
17. Næsted, H., Kramhøft, B., Lok, F., Bojsen, K. et al., Production of enzymatically active recombinant full-length barley high pI α-glucosidase of glycoside family 31 by high cell-density fermentation of Pichia pastoris and affinity purification. Protein Exp. Purif. 2006, 46, 56-63.
18. Vester-Christensen, M., Abou Hachem, M., Næsted, H., Svensson, B., Secretory expression of functional barley limit dextrinase by Pichia pastoris using high cell-density fermentation. Prot. Exp. Purif. 2010, 69, 112-119.
19. Vester-Christensen, M., Abou Hachem, M., Svensson, B., Henriksen, A., Crystal structure of an essential enzyme in seed starch degradation-barley limit dextrinase in complex with cyclodextrins. J. Mol. Biol. 2010, 403, 739-750.
20. Lovegrove, A., Hooley, R., Gibberellin and abscisic acid signaling in aleurone. Trends Plant Sci. 2000, 5, 102-110.
21. Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., Itoh, H. et al., GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellins. Nature 2005, 437, 693-698.
22. Hirano, K., Ueguchi-Tanaka, M., Matsuoka, M., GID1-mediated gibberellin signalling in plant cells. Trends Plant Sci. 2008, 13, 192-199.
23. Fath, A., Bethke, P., Beligni, V., Jones, R., Active oxygen and cell death in cereal aleurone cells. J. Exp. Bot. 2002, 53, 1273-1282.
24. Bethke, P. C., Lonsdale, J. E., Fath, A., Jones, R. L., Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell 1999, 11, 1033-1045.
25. Xie, Z., Zhang, Z. L., Zou, X. L., Yang, G. X. et al., Interactions of two abscisic-acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. Plant J. 2006, 46, 231-242.
26. Klingler, J. P., Batelli, G., Zhu, J. K., ABA receptors: the START of a new paradigm in phytohormone signalling. J. Exp. Bot. 2010, 61, 3199-3210.
27. Jones, J. A., Grain-based foods and health. Cereal Foods World 2006, 51, 108-113.
28. Hemery, Y., Rouau, X., Lullien-Pellerin, V., Barron, C., Abecassis, J., Dry processes to develop wheat fractions and products with enhanced nutritional quality. J. Cereal Sci. 2007, 46, 327-347.
29. Peterson, D. M., Barley tocols. Effects of milling, malting and mashing. Cereal Chem. 1994, 71, 42-44.
30. Fenech, M., Noakes, M., Clifton, P., Topping, D., Aleurone flour is a rich source of bioavailable folate in humans. J. Nutr. 1999, 129, 1114-1119.
31. Tang, J. W., Zou, C. Q., He, Z. H., Shi, R. L. et al., Mineral element distributions in milling fractions of Chinese wheats. J. Cereal Sci. 2008, 48, 821-828.
32. White, D. A., Fisk, I. D., Gray, D. A., Characterisation of oat (Avena sativa L.) oil bodies and intrinsically associated E-vitamers. J. Cereal Sci. 2006, 43, 244-249.
33. Jestin, L., Ravel, C., Auroy, S., Laubin, B. et al., Inheritance of the number and thickness of cell layers in barley aleurone tissue (Hordeum vulgare L.): an approach using F2-F3 progeny. Theor. Appl. Genet. 2008, 116, 991-1002.
34. Finnie, C., Svensson, B., Barley seed proteomics from spots to structures. J. Proteomics 2009, 72, 315-324.
35. Finnie, C., Svensson, B., Feasibility study of a tissue-specific approach to barley proteome analysis: aleurone layer, endosperm, embryo and single seeds. J. Cereal Sci. 2003, 38, 217-226.
36. Bønsager, B. C., Finnie, C., Roepstorff, P., Svensson, B., Germination and radicle elongation in barley tracked using proteome analysis of dissected embryo, aleurone layer and endosperm tissues. Proteomics 2007, 7, 4538-4540.
37. Laubin, B., Lullien-Pellerin, V., Gaillard-Martinie, B., Chambon, C., Branlard, G., Isolation of the wheat aleurone layer for 2D electrophoresis and proteomics analysis. J. Cereal Sci. 2008, 48, 709-714.
38. Jerkovic, A., Kriegel, A. M., Bradner, J. R., Atwell, B. J. et al., Strategic distribution of protective proteins within bran layers of wheat (Triticum aestivum L.) protects the nutrient-rich endosperm. Plant Physiol. 2010, 152, 1459-1470.
39. Chrispeels, M. J., Varner, J. E., Gibberellic acid-enhanced synthesis and release of α-amylase and ribonuclease by isolated aleurone layers. Plant Physiol. 1967, 42, 398-406.
40. Bethke, P., Fath, A., Spiegel, Y. N., Hwang, Y., Jones, R. L., Abscisic acid, gibberellin and cell viability in cereal aluerone. Euphytica 2002, 126, 3-11.
41. Fath, A., Bethke, P., Lonsdale, J., Meza-Romero, R., Jones, R., Programmed cell death in cereal aleurone. Plant Mol. Biol. 2000, 44, 255-266.
42. Fath, A., Bethke, P. C., Jones, R. L., Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol. 2001, 126, 156-166.
43. Gubler, F., Ashford, A. E., Jacobsen, J. V., The release of α-amylase through gibberellin-treated barley aleurone cell walls. Planta 1987, 172, 155-161.
44. Rose, J. K., Lee, S.-J., Straying off the highway: trafficking of secreted plant proteins and complexity in the plant cell wall proteome. Plant Physiol. 2010, 153, 433-436.
45. Østergaard, O., Finnie, C., Laugesen, S., Roepstorff, P., Svensson, B., Proteome analysis of barley seeds: identification of major proteins from two-dimensional gels (pI4-7). Proteomics 2004, 4, 2437-2447.
46. Bak-Jensen, K. S., Laugesen, S., Østergaard, O., Finnie, C. et al., Spatio-temporal profiling and degradation of α-amylase isozymes during barley seed germination. FEBS J. 2007, 274, 2552-2565.
47. Frandsen, T. P., Lok, F., Mirgorodskaya, E., Roepstorff, P., Svensson, B., Purification, enzymatic characterisation and nucleotide sequence of a high isolectric-point alpha-glucosidase from barley malt. Plant Physiol. 2000, 123, 275-286.
48. Dionisio, G., Holm, P. B., Brinch-Pedersen, H., Wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) multiple inositol polyphosphate phosphatases (MINPPs) are phytases expressed during grain filling and germination. Plant Biotech. J. 2007, 5, 325-338.
49. Tran, H. T., Hurley, B. H., Plaxton, W. C., Feeding hungry plants: the role of purple acid phosphatases in phosphate nutrition. Plant Sci. 2010, 179, 14-27.
50. Jacobsen, J. V., Knox, R. B., Cytochemical localization and antigenicity of α-amylase in barley aleurone tissue. Planta 1973, 112, 213-224.
51. Ritchie, S., McCubbin, A., Ambrose, G., Kao, T., Gilroy, S., The sensitivity of barley aleurone tissue to gibberellins is heterogeneous and may be spatially determined. Plant Physiol. 1999, 120, 361-370.
52. Erlendsson, L. S., Muench, M. O., Hellman, U., Hrafnkelsdottir, S. M. et al., Barley as a green factory for the production of functional Flt3 ligand. Biotechnol. J. 2010, 5, 163-171.
53. Burton, R. A., Zhang, X. Q., Hrmova, M., Fincher, G. B., A single limit dextrinase gene is expressed both in the developing endosperm and in germinated grains of barley. Plant Physiol. 1999, 119, 859-871.
54. Schroeder, S. W., MacGregor, A., Synthesis of limit dextrinase in germinated barley kernels and aleurone tissues. J. Am. Soc. Brew. Chem. 1998, 56, 32-37.
55. Bailly, C., Active oxygen species and antioxidants in seed biology. Seed Sci. Res. 2004, 14, 93-107.
56. Potters, G., De Gara, L., Asard, H., Horemans, N., Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol. Biochem. 2002, 40, 537-548.
57. Montrichard, F., Alkhalfioui, F., Yano, H., Vensel, W. H. et al., Thioredoxin targets in plants: the first 30 years. J. Proteomics 2009, 72, 452-474.
58. Hägglund, P., Kirkensgaard, K., Maeda, K., Finnie, C. et al., Molecular recognition in NADPH-dependent plant thioredoxin systems-catalytic mechanisms, structural snapshots and target identifications. Adv. Bot. Res. 2009, 52, 461-495.
59. De Tullio, M. C., Arrigoni, O., The ascorbic acid system in seeds: to protect and to serve. Seed Sci. Res. 2003, 13, 249-260.
60. Laloi, C., Mestres-Ortega, D., Marco, Y., Meyer, Y., Reichard, J.-P., The arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiol. 2004, 134, 1006-1016.
61. Bønsager, B. C., Shahpiri, A., Finnie, C., Svensson, B., Proteomic and activity profiles of ascorbate-glutathione cycle enzymes in germinating barley embryo. Phytochemistry 2010, 71, 1650-1656.
62. Hägglund, P., Bunkenborg, J., Maeda, K., Svensson, B., Identification of thioredoxin disulfide targets using a quantitative proteomics approach based on isotope-coded affinity tags. J. Proteome Res. 2008, 7, 5270-5276.
63. Hägglund, P., Bunkenborg, J., Yang, F., Harder, L. M. et al., Identification of thioredoxin target disulfides in proteins released from barley aleurone layers. J. Proteomics 2010, 73, 1133-1136.
64. Sørensen, S. B., Bech, L. M., Muldbjerg, M., Beenfeldt, T., Breddam, K., Barley lipid transfer protein 1 is involved in beer foam formation. Master Brew. Assoc. Am. Tech. Q. 1993, 30, 136-145.
65. Breiteneder, H., Mills, C., Nonspecific lipid-transfer proteins in plant foods and pollens: an important allergen class. Curr. Opin. Allerg. Clin. Immun. 2005, 5, 275-279.
66. Cheng, C. S., Samuel, D., Liu, Y. J., Shyu, J. C. et al., Binding mechanism of nonspecific lipid transfer proteins and their role in plant defense. Biochemistry 2004, 43, 13628-13636.
67. Shahpiri, A., Svensson, B., Finnie, C., From proteomics to structural studies of cytosolic/mitochondrial type thioredoxin systems in barley seeds. Mol. Plant 2009, 2, 390-406.
68. Maeda, K., Finnie, C., Østergaard, O., Svensson, B., Identification, cloning and characterisation of two thioredoxin h isoforms, HvTrxh1 and HvTrxh2, from the barley seed proteome. Eur J. Biochem. 2003, 270, 2633-2643.
69. Shahpiri, A., Svensson, B., Finnie, C., The NADPH-dependent thioredoxin reductase/thioredoxin system in germinating barley seeds: gene expression, protein profiles and interactions between isoforms of thioredoxin h and thioredoxin reductase. Plant Physiol. 2008, 146, 789-799.
70. Maeda, K., Hägglund, P., Finnie, C., Svensson, B., Henriksen, A., Structural basis for target protein recognition by the protein disulfide reductase thioredoxin. Structure 2006, 14, 1701-1710.
71. Maeda, K., Hägglund, P., Finnie, C., Svensson, B., Henriksen, A., Crystal structures of barley thioredoxin h isoforms HvTrxh1 and HvTrxh2 reveal features involved in protein recognition and possibly in discriminating the isoform specificity. Protein Sci. 2008, 17, 1015-1024.
72. Kirkensgaard, K. G., Hägglund, P., Finnie, C., Svensson, B., Henriksen, A., Crystal structure of Hordeum vulgare NADPH-dependent thioredoxin reductase 2. Unwinding the reaction mechanism. Acta Crystallogr. D 2009, 65, 932-941.
73. Wallin, E., von Heijne, G., Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 1998, 7, 1029-1038.
74. Ephritikhine, G., Ferro, M., Rolland, N., Plant membrane proteomics. Plant Physiol. Biochem. 2004, 42, 943-962.
75. Hynek, R., Svensson, B., Jensen, O. N., Barkholt, V., Finnie, C., Enrichment and identification of integral membrane proteins from barley aleurone layers by reversed-phase chromatography, SDS-PAGE and LC-MS/MS. J. Proteome Res. 2006, 5, 3105-3113.
76. Hynek, R., Svensson, B., Jensen, O. N., Barkholt, V., Finnie, C., The plasma membrane proteome of germinating barley embryos. Proteomics 2009, 9, 3787-3794.
77. Agrawal, G. K., Jwa, N.-S., Lebrun, M.-H., Job, D., Rakwal, R., Plant secretome: unlocking secrets of the secreted proteins. Proteomics 2010, 10, 799-827.
78. Candiano, G., Bruschi, M., Musante, L., Santucci, L. et al., Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004, 25, 1327-1333.