Tissue and cellular localization of individual β-glycosidases using a substrate-specific sugar reducing assay

Plant Journal

Volumn 60, Issue 5, 2009, Pages 894-906

  Sánchez Pérez, Raquel ^a,b   Jørgensen, Kirsten ^a   Motawia, Mohammed S ^a   Dicenta, Federico ^b   Møller, Birger L ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b RESEARCH GROUP ON QUALITY   (Spain)

Author keywords

glycosidases; 2,3,5 triphenyltetrazolium chloride (TTC); Almonds; Amygdalin hydrolase; Prunasin hydrolase; Sodium borohydride

Indexed keywords

BETA GLUCOSIDASE; DIAZONIUM COMPOUND; FAST BLUE BB; GLUCOSE; PRUNASIN HYDROLASE; TETRAZOLIUM;

ARTICLE; CHEMISTRY; CYTOCHEMISTRY; ENZYME SPECIFICITY; METHODOLOGY; OXIDATION REDUCTION REACTION; PRUNUS;

BETA-GLUCOSIDASE; DIAZONIUM COMPOUNDS; GLUCOSE; HISTOCYTOCHEMISTRY; OXIDATION-REDUCTION; PRUNUS; SUBSTRATE SPECIFICITY; TETRAZOLIUM SALTS;

PRUNUS DULCIS;

EID: 71949101264     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03997.x     Document Type: Article

References (62)

1. Ashford, A.E. (1970) Histochemical localization of beta-glycosidases in roots of Zea mays. I. A simultaneous coupling azo-dye technique for the localization of beta-glucosidase and beta-galactosidase. Protoplasma, 71, 281 293.
2. Bak, S., Kahn, R.A., Nielsen, H.L., Møller, B.L. Halkier, B.A. (1998) Cloning of three A-type cytochromes P450, CYP71E1, CYP98, and CYP99 from Sorghum bicolor (L.) Moench by a PCR approach, and identification by expression in Escherichia coli of CYP71E1 as the oxime-metabolizing cytochrome P450 in the biosynthesis of the cyanogenic glucoside dhurrin. Plant Mol. Biol. 36, 393 405.
3. Bak, S., Paquette, S.M., Morant, M. et al. (2006) Cyanogenic glycosides; a case study for evolution and application of cytochromes P450. Phytochem. Rev. 5, 309 329.
4. Baruah, P. Swain, T. (1957) β-Glycosidase of potato. Biochem. J. 66, 321 323.
5. Burmeister, W.P., Cottaz, S., Driguez, H., Iori, R., Palmieri, S. Henrissat, B. (1997) The crystal structures of Sinapis alba myrosinase and a covalent glycosyl-enzyme intermediate provide insights into the substrate recognition and active-site machinery of an S-glycosidase. Structure, 5, 663 675.
6. Cairns, J.R.K., Champattanachai, V., Srisomsap, C., Wittman-Liebold, B., Thiede, B. Svasti, J. (2000) Sequence and expression of Thai rosewood beta-glucosidase /beta-fucosidase, a family 1 glycosyl hydrolase glycoprotein. J. Biochem. 128, 999 1008.
7. Chen, C.W., Yang, Y.W., Lur, H.S., Tsai, Y.G. Chang, M.C. (2006) A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. Plant Cell Physiol. 47, 1 13.
8. Chen, F., Suzuki, Y., Nagai, N., Jin, L., Yu, J., Wang, H., Marchal, G. Ni, Y. (2007) Rodent stroke induced by photochemical occlusion of proximal middle cerebral artery: evolution monitored with MR imaging and histopathology. Eur. J. Radiol. 63, 68 75.
9. Chuenchor, W., Pengthaisong, S., Robinson, R.C. et al. (2008) Structural Insights into Rice BGlu1 β-Glucosidase Oligosaccharide Hydrolysis and Transglycosylation. J. Mol. Biol. 377, 1200 1215.
10. Cohen, R.B., Rutenburg, S.M., Tsou, K.C., Woodbury, M.A. Seligman, A.M. (1952) The colorimetric estimation of β-d-glucosidase. J. Biol. Chem. 195, 607 614.
11. Conn, E.E. (1980) Cyanogenic compounds. Annu. Rev. Plant Physiol. 31, 433 451.
12. Dharmawardhana, D.P., Ellis, B.E. Carlson, J.E. (1995) A beta-glucosidase from lodgepole pine xylem specific for the lignin precursor coniferin. Plant Physiol. 107, 331 339.
13. Escamilla-Trevino, L.L., Chen, W., Card, M.L., Shih, M.C., Cheng, C.L. Poulton, J.E. (2006) Arabidopsis thaliana beta-glucosidases BGLU45 and BGLU46 hydrolyse monolignol glucosides. Phytochemistry, 67, 1651 1660.
14. Esen, A. Stetler, D.A. (1993) Subcellular localization of maize β-glucosidase. Maize Genet. Coop. Newsletter, 67, 19 20.
15. Fia, G., Giovani, G. Rosi, I. (2005) Study of beta-glucosidase production by wine related yeasts during alcoholic fermentation. A new rapid fluorimetric method to determine enzymatic activity. J. Appl. Microbiol. 99, 509 517.
16. Gabriel, O. Gersten, D.M. (1992) Staining for enzymatic activity after gel electrophoresis, I. Anal. Biochem. 203, 1 21.
17. Gabriel, O. Wang, S.F. (1969) Determination of enzymatic activity in polyacrylamide gels. Anal. Biochem. 27, 545 554.
18. Hansen, E.H., Møller, B.L., Kock, G.R., Bünner, C.M., Kristensen, C., Jensen, O.R., Okkels, F.T., Olsen, C.E., Motawia, M.S. Hansen, J. (2009) De novo biosynthesis of vanillin in fission and baker's yeast. Appl. Environ. Microbiol. 75, 2765 2774.
19. Hösel, W. Nahrstedt, A. (1975) Glucosidases specific for the cyanogenic glucoside triglochinin. Purification and characterization of beta-glucosidases from Alocasia macrorrhiza Schott. Hoppe-Seyler's Z. Physiol. Chem. 356, 1265 1275.
20. Hösel, W., Tober, I., Eklund, S.H. Conn, E.E. (1987) Characterization of beta-glucosidases with high specificity for the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench seedlings. Arch. Biochem. Biophys. 252, 152 162.
21. Hughes, M.A., Brown, K., Pancoro, A., Murray, B.S., Oxtoby, E. Hughes, J. (1992) A molecular and biochemical analysis of the structure of the cyanogenic β-glucosidase (Linamarase) from cassava (Manihot esculenta Cranz). Arch. Biochem. Biophys. 295, 273 279.
22. Jenrich, R., Trompetter, I., Bak, S., Olsen, C.E., Møller, B.L. Piotrowski, M. (2007) Evolution of heteromeric nitrilase complexes in Poaceae with new functions in nitrile metabolism. Proc. Natl Acad. Sci. USA, 104, 18848 18853.
23. Jones, P.R., Møller, B.L. Hoj, P.B. (1999) The UDP-glucose: p-hydroxymandelonitrile-O-glucosyltransferase that catalyses the last step in synthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor. Isolation, cloning, heterologous expression, and substrate specificity. J. Biol. Chem. 274, 35483 35491.
24. Kasai, T., Kisimoto, M. Sin'itiro, K. (1981) On the free sugar and cyanogenic glycoside in the seed of Vicia angustifolia var. Segetalis. Kagawa Daigaku Nogakubu Gakujutsu Hokoku, 32, 111 119.
25. Kiran, N.S., Polanska, L., Fohlerová, R. et al. (2006) Ectopic over-expression of the maize [beta]-glucosidase Zm-p60.1 perturbs cytokinin homeostasis in transgenic tobacco. J. Exp. Bot. 57, 985 996.
26. Kojima, M., Poulton, J.E., Thayer, S.S. Conn, E.E. (1979) Tissue distributions of dhurrin and of enzymes involved in its metabolism in leaves of Sorghum bicolor. Plant Physiol. 63, 1022 1028.
27. Kristensen, C., Morant, M., Olsen, C.E., Ekstrøm, C.T., Galbraith, D.W., Møller, B.L. Bak, S. (2005) Metabolic engineering of dhurrin in transgenic Arabidopsis plants with marginal inadvertent effects on the metabolome and transcriptome. Proc. Natl Acad. Sci. USA, 102, 1779 1784.
28. Kristoffersen, P., Brzobohaty, B., Hohfeld, I., Bako, L., Melkonian, M. Palme, K. (2000) Developmental regulation of the maize Zm-g60.1 gene encoding a beta-glucosidase located to plastids. Planta, 210, 407 415.
29. Kuhn, R. Jerchel, D. (1941) Reduction from tetrazolium salts through bacterial, fermenting yeast and germinating seeds. D. Ber. Deutsch. Chem. Ges. 74, 949 952.
30. Kuroki, G.W. Poulton, J.E. (1986) Comparison of kinetic and molecular properties of two forms of amygdalin hydrolase from black cherry (Prunus serotina Ehrh.) seeds. Arch. Biochem. Biophys. 247, 433 439.
31. Kuroki, G.W. Poulton, J.E. (1987) Isolation and characterization of multiple forms of prunasin hydrolase from black cherry (Prunus serotina Ehrh.) seeds. Arch. Biochem. Biophys. 255, 19 26.
32. Leah, R., Kigel, J., Svendsen, I. Mundy, J. (1995) Biochemical and molecular characterization of a barley seed beta-glucosidase. J. Biol. Chem. 270, 15789 15797.
33. Lee, K.H., Piao, H.L., Kim, H.Y., Choi, S.M., Jiang, F., Hartung, W., Hwang, I., Kwak, J.M., Lee, I.J. Hwang, I. (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell, 126, 1109 1120.
34. Li, C.P., Swain, E. Poulton, J.E. (1992) Prunus serotina amygdalin hydrolase and prunasin hydrolase - purification, N-terminal sequencing, and antibody production. Plant Physiol. 100, 282 290.
35. Lizotte, P.A. Poulton, J.E. (1988) Catabolism of cyanogenic glycosides by purified vicianin hydrolase from squirrel's foot fern (Davallia trichomanoides Blume). Plant Physiol. 86, 322 324.
36. Maicas, S. Mateo, J.J. (2005) Hydrolysis of terpenyl glycosides in grape juice and other fruit juices: a review. Appl. Microbiol. Biotechnol. 67, 322 335.
37. Mizutani, M., Nakanishi, H., Ema, J., Ma, S.J., Noguchi, E., Inohara-Ochiai, M., Fukuchi-Mizutani, M., Nakao, M. Sakata, K. (2002) Cloning of betaprimeverosidase from tea leaves, a key enzyme in tea aroma formation. Plant Physiol. 130, 2164 2176.
38. Møller, B.L. Conn, E.E. (1979) The biosynthesis of cyanogenic glucosides in higher plants. N-Hydroxytyrosine as an intermediate in the biosynthesis of dhurrin by Sorghum bicolor (Linn) Moench. J. Biol. Chem. 254, 8575 8583.
39. Møller, B.L. Seigler, D.S. (1999) Biosynthesis of cyanogenic glucosides, cyanolipids and related compounds. In Plant Amino Acids, Biochemistry and Biotechnology (Singh, B.J., ed). New York : Marcel Dekker Inc, pp. 563 609.
40. Morant, M., Bak, S., Møller, B.L. Werck-Reichhart, D. (2003) Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr. Opin. Biotechnol. 14, 151 162.
41. Morant, A.V., Bjarnholt, N., Kragh, M.E. et al. (2008a) The β-glucosidases responsible for bioactivation of hydroxynitrile glucosides in Lotus japonicus. Plant Physiol. 147, 1072 1091.
42. Morant, A.V., Jørgensen, K., Jørgensen, C., Paquette, S.M., Sánchez-Pérez, R., Møller, B.L. Bak, S. (2008b) β-Glucosidases as detonators of plant chemical defense. Phytochemistry, 69, 1795 1813.
43. Nahrstedt, A., Hosel, W. Walther, A. (1979) Characterization of cyanogenic glucosides and β-glucosidases in Triglochin maritima seedlings. Phytochemistry, 18, 1137 1141.
44. Nelson, L. (2006) Acute cyanide toxicity: mechanisms and manifestations. J. Emerg. Nurs. 32, S8 S11.
45. Nielsen, K.A., Hrmova, M., Nielsen, J.N., Forslund, K., Ebert, S., Olsen, C.E., Fincher, G.B. Møller, B.L. (2006) Reconstitution of cyanogenesis in barley (Hordeum vulgare L.) and its implications for resistance against the barley powdery mildew fungus. Planta, 223, 1010 1023.
46. Nisius, A. (1988) The stromacenter in avena plastids-an aggregation of beta-glucosidase responsible for the activation of oat leaf saponins. Planta, 173, 474 481.
47. Odoux, E., Escoute, J., Verdeil, J.-L. Brillouet, J.-M. (2003) Localization of beta-d-glucosidase activity and glucovanillin in vanilla bean (Vanilla planifolia Andrews). Ann. Bot., 92, 437 444.
48. Ogata, J., Kikura-Hanajiri, R., Yoshimatsu, K., Kiuchi, F. Goda, Y. (2008) Detection method for the ability of hemp (Cannabis sativa L.) seed germination by the use of 2,3,4-triphenyl-2H-tetrazolium chloride (TTC). Yakugaku Zasshi, 128, 1707 1711.
49. Poulton, J.E. (1990) Cyanogenesis in plants. Plant Physiol. 94, 401 405.
50. Poulton, J.E. Li, C.P. (1994) Tissue level compartmentation of (R)-amygdalin and amygdalin hydrolase prevents large scale cyanogenesis in undamaged prunus seeds. Plant Physiol. 104, 29 35.
51. Rutenburg, A.M., Goldbarg, J.A., Rutenburg, S.H. Lang, R.T. (1960) The histochemical demonstration of α-d-glucosidase in mammalian tissues. J. Histochem. Cytochem. 8, 268 272.
52. Sánchez-Pérez, R., Jørgensen, K., Olsen, C.E., Dicenta, F. Møller, B.L. (2008) Bitterness in almonds. Plant Physiol. 46, 1040 1052.
53. Sibbesen, O., Koch, B., Halkier, B.A. Møller, B.L. (1995) Cytochrome P-450TYR is a multifunctional heme-thiolate enzyme catalyzing the conversion of L-tyrosine to p-hydroxyphenylacetaldehyde oxime in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. J. Biol. Chem. 270, 3506 3511.
54. Spielman, L.L. Mowshowitz, D.B. (1982) A specific stain for α-glucosidase in isoelectric focusing gels. Anal. Biochem. 120, 66 70.
55. Steponkus, P.L. Lanphear, F.O. (1967) Refinement of the triphenyl tetrazolium chloride method of determining cold injury. Plant Physiol. 42, 1423 1426.
56. Stoward, P.J. Mester, L. (1964) Formazan reaction as a confirmatory test for aldehyde groups in histochemistry. Nature, 204, 488 489.
57. Suda, C.N.K. Giorgini, J.F. (2003) Multiple forms of endo-1,4-β- glucanases in the endosperm of Euphorbia heterophylla L. J. Exp. Bot. 54, 2045 2052.
58. Thayer, S.S. Conn, E.E. (1981) Subcellular localization of dhurrin beta-glucosidase and hydroxynitrile lyase in the mesophyll cells of sorghum leaf blades. Plant Physiol. 67, 617 622.
59. Wöhler, F. Liebig, J. (1837) "Ueber die Bildung des Bittermandelöls". Annalen der Pharmacie, 22, 1 24.
60. Zamudio-Maya, M., Narváez-Zapata, J. Rojas-Herrera, R. (2008) Isolation and identification of lactic acid bacteria from sediments of a coastal marsh using a differential selective medium. Lett. Appl. Microbiol. 46, 402 407.
61. Zhou, J.M., Hartmann, S., Shepherd, B.K. Poulton, J.E. (2002) Investigation of the microheterogeneity and aglycone specificity-conferring residues of black cherry prunasin hydrolases. Plant Physiol. 129, 1252 1264.
62. Zouhar, J., Vévodová, J., Marek, J., Damborský, J., Su, X.D. Brzobohatý, B. (2001) Insights into the functional architecture of the catalytic center of a maize beta-glucosidase Zm-p60.1. Plant Physiol. 127, 973 985.