β-Glucosidases: Multitasking, moonlighting or simply misunderstood?

Plant Science

Volumn 241, Issue , 2015, Pages 246-259

  Ketudat Cairns, James R ^a,b   Mahong, Bancha ^c   Baiya, Supaporn ^a   Jeon, Jong Seong ^c  

^a SURANAREE UNIVERSITY OF TECHNOLOGY   (Thailand)

^b Krung Thep Maha Nakhon   (Thailand)

^c Kyung Hee University   (South Korea)

Author keywords

Functional analysis; Glycoconjugates; Phytohormones; Stress response; Transglucosidase; Glycosidase

Indexed keywords

BETA GLUCOSIDASE; PLANT PROTEIN;

ARABIDOPSIS; GENETICS; METABOLISM; ORYZA;

ARABIDOPSIS; BETA-GLUCOSIDASE; ORYZA; PLANT PROTEINS;

EID: 84946402483     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2015.10.014     Document Type: Review

References (107)

1. Ketudat Cairns J.R., Esen A. β-Glucosidases. Cell. Mol. Life Sci. 2010, 67:3389-3405.
2. Opassiri R., et al. β-Glucosidase, exo-β-glucanase and pyridoxine transglucosylase activities of rice BGlu1. Biochem. J. 2004, 379:125-131.
3. Frankova L., Fry S.C. Biochemistry and physiological roles of enzymes that 'cut and paste' plant cell-wall polysaccharides. J. Exp. Bot. 2013, 64:3519-3550.
4. Matsuba Y., et al. A novel glucosylation reaction on anthocyanins catalyzed by acyl-glucose-dependent glucosyltransferase in the petals of carnation and delphinium. Plant Cell 2010, 22:3374-3389.
5. Nishizaki Y., et al. p-Hydroxybenzoyl-glucose is a zwitter donor for the biosynthesis of 7-polyacylated anthocyanin in Delphinium. Plant Cell 2013, 25:4150-4165.
6. Lombard V., et al. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014, 42:D490-495.
7. Xu Z., et al. Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1. Plant Mol. Biol. 2004, 55:343-367.
8. Opassiri R., et al. Analysis of rice glycosyl hydrolase family 1 and expression of Os4bglu12 β-glucosidase. BMC Plant Biol. 2006, 6:33.
9. Gómez-Anduro G., et al. Genome-wide analysis of the beta-glucosidase gene family in maize (Zea mays L. var B73). Plant Mol. Biol. 2011, 77:159-183.
10. Ahn Y.O., et al. Scopolin-hydrolyzing β-glucosidases in roots of Arabidopsis. Plant Cell Physiol. 2010, 51:132-143.
11. Hosel W., Tober I., Eklund S.H., Conn E.E. Characterization of beta-glucosidases with high specificity for the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) moench seedlings. Arch. Biochem. Biophys. 1987, 252:152-162.
12. Morant A.V., et al. β-Glucosidases as detonators of plant chemical defense. Phytochemistry 2008, 69:1795-1813.
13. Sánchez-Pérez R., et al. Prunasin hydrolases during fruit development in sweet and bitter almonds. Plant Physiol. 2012, 158:1916-1932.
14. Hua Y., et al. Identification of rice Os4BGlu13 as a β-glucosidase which hydrolyzes gibberellin A4 1-O-β-d-glucosyl ester, in addition to tuberonic acid glucoside and salicylic acid derivative glucosides. Arch. Biochem. Biophys. 2015, 583:36-46.
15. Hrmova M., et al. Barley β-d-glucan exohydrolases with β-d-glucosidase activity. Purificationcharacterization, and determination of primary structure from a cDNA clone. J. Biol. Chem. 1996, 271:5277-5286.
16. Hrmova M., Burton R.A., Biely P., Lahnstein J., Fincher G.B. Hydrolysis of (1, 4)-β-d-mannans in barley (Hordeum vulgare L.) is mediated by the concerted action of (1,4)-β-d-mannan endohydrolase and beta-d-mannosidase. Biochem. J. 2006, 399:77-90.
17. Kuntothom T., et al. Rice family GH1 glycoside hydrolases with β-d-glucosidase and β-d-mannosidase activities. Arch. Biochem. Biophys. 2009, 491:85-95.
18. Opassiri R., et al. Characterization of a rice β-glucosidase highly expressed in flower and germinating shoot. Plant Sci. 2003, 165:627-638.
19. Zhao L., Yuan L., Gu R. A 40-bp A/T-rich repressor element involved in organ-dependent transcriptional regulation of ZmGLU1. Plant Cell Tissue Organ Cult. 2011, 105:291-298.
20. Rojas M., Tiessen A., Ascencio F., Angulo C., Gómez-Anduro G. Two promoters of beta-glucosidase paralogs (ZmBGlu2 and ZmBGlu5) highly active in tropical young maize hybrid seedlings. Plant Mol. Biol. Rep. 2015, 1-9.
21. Escamilla-Trevino L.L., et al. Arabidopsis thaliana β-glucosidases BGLU45 and BGLU46 hydrolyse monolignol glucosides. Phytochemistry 2006, 67:1651-1660.
22. Miyahara T., Sakiyama R., Ozeki Y., Sasaki N. Acyl-glucose-dependent glucosyltransferase catalyzes the final step of anthocyanin formation in Arabidopsis. J. Plant Physiol. 2013, 170:619-624.
23. Keresztessy Z., Hughes J., Kiss L., Hughes M.A. Co-purification from E. coli of a plant β-glucosidase-glutathione S-transferase fusion protein and the bacterial chaperonin GroEL. Biochem. J. 1996, 314:41-47.
24. Framm J.J., et al. Cloning and functional expression in E. coli of a cDNA encoding cardenolide 16'-O-glucohydrolase from Digitalis lanata Ehrh. Plant Cell Physiol. 2000, 41:1293-1298.
25. Geerlings A., Ibanez M.M., Memelink J., van Der Heijden R., Verpoorte R. Molecular cloning and analysis of strictosidine β-d-glucosidase, an enzyme in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. J. Biol. Chem. 2000, 275:3051-3056.
26. Warzecha H., Gerasimenko I., Kutchan T.M., Stockigt J. Molecular cloning and functional bacterial expression of a plant glucosidase specifically involved in alkaloid biosynthesis. Phytochemistry 2000, 54:657-666.
27. Cicek M., Esen A. Expression of soluble and catalytically active plant (monocot) β-glucosidases in E. coli. Biotechnol. Bioeng. 1999, 63:392-400.
28. Zouhar J., Nanak E., Brzobohatý B. Expressionsingle-step purification, and matrix-assisted refolding of a maize cytokinin glucoside-specific β-glucosidase. Protein Expr. Purif. 1999, 17:153-162.
29. Sue M., et al. Purification, crystallization and preliminary X-ray analysis of a hexameric β-glucosidase from wheat. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2005, 61:864-866.
30. Kuntothom T., et al. Rice family GH1 glycoside hydrolases with β-d-glucosidase and β-d-mannosidase activities. Arch. Biochem. Biophys. 2009, 491:85-95.
31. Suzuki H., et al. An isoflavone conjugate-hydrolyzing β-glucosidase from the roots of soybean (Glycine max) seedlings: purification, gene cloning, phylogenetics, and cellular localization. J. Biol. Chem. 2006, 281:30251-30259.
32. Roepke J., Bozzo G.G. Arabidopsis thaliana β-glucosidase BGLU15 attacks flavonol 3-O-β-glucoside-7-O-α-rhamnosides. Phytochemistry 2015, 109:14-24.
33. Seshadri S., Akiyama T., Opassiri R., Kuaprasert B., Ketudat Cairns J. Structural and enzymatic characterization of Os3BGlu6, a rice β-glucosidase hydrolyzing hydrophobic glycosides and (1→3)- and (1→2)-linked disaccharides. Plant Physiol. 2009, 151:47-58.
34. Luang S., et al. Rice Os9BGlu31 is a transglucosidase with the capacity to equilibrate phenylpropanoidflavonoid, and phytohormone glycoconjugates. J. Biol. Chem. 2013, 288:10111-10123.
35. Baiya S., Hua Y., Ekkhara W., Ketudat Cairns J.R. Expression and enzymatic properties of rice (Oryza sativa L.) monolignol β-glucosidases. Plant Sci. 2014, 227:101-109.
36. Ketudat Cairns J.R., et al. Sequence and expression of Thai rosewood β-glucosidase/β-fucosidase, a family 1 glycosyl hydrolase glycoprotein. J. Biochem. 2000, 128:999-1008.
37. Zhou J., Hartmann S., Shepherd B.K., Poulton J.E. Investigation of the microheterogeneity and aglycone specificity-conferring residues of black cherry prunasin hydrolases. Plant Physiol. 2002, 129:1252-1264.
38. Himeno N., et al. Identification of rice β-glucosidase with high hydrolytic activity towards salicylic acid β-d-glucoside. Biosci. Biotech. Biochem. 2013, 77:934-939.
39. Chuankhayan P., et al. Functional and structural differences between isoflavonoid β-glycosidases from Dalbergia sp. Arch. Biochem. Biophys. 2007, 468:205-216.
40. Wang M., et al. Characterization of a root-specific β-thioglucoside glucohydrolase gene in Carica papaya and its recombinant protein expressed in Pichia pastoris. Plant Sci. 2009, 177:716-723.
41. Andersson D., et al. Myrosinases from root and leaves of Arabidopsis thaliana have different catalytic properties. Phytochemistry 2009, 70:1345-1354.
42. Nong H., et al. Characterization of a novel β-thioglucosidase CpTGG1 in Carica papaya and its substrate-dependent and ascorbic acid-independent O-beta-glucosidase activity. J. Integr. Plant Biol. 2010, 52:879-890.
43. Toonkool P., et al. Expression and purification of dalcochinasea β-glucosidase from Dalbergia cochinchinensis Pierre, in yeast and bacterial hosts. Protein Expr. Purif. 2006, 48:195-204.
44. Beltrao P., Bork P., Krogan N.J., van Noort V. Evolution and functional cross-talk of protein post-translational modifications. Mol. Sys. Biol. 2013, 9:714.
45. Xu Z., Shih M.C., Poulton J.E. An extracellular exo-beta-(1,3)-glucanase from Pichia pastoris: purification, characterization, molecular cloning, and functional expression. Protein Expr. Purif. 2006, 47:118-127.
46. Zangoui P., Vashishtha K., Mahadevan S. Evolution of aromatic β-glucoside utilization by successive mutational steps in E. coli. J. Bacteriol. 2015, 197:710-716.
47. Thorlby G., Fourrier N., Warren G. The SENSITIVE TO FREEZING2 gene required for freezing tolerance in Arabidopsis thaliana, encodes a β-glucosidase. Plant Cell 2004, 16:2192-2203.
48. Moellering E.R., Muthan B., Benning C. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 2010, 330:226-228.
49. Morant A.V., et al. The β-glucosidases responsible for bioactivation of hydroxynitrile glucosides in Lotus japonicus. Plant Physiol. 2008, 147:1072-1091.
50. Kiran N.S., et al. Ectopic over-expression of the maize beta-glucosidase Zm-p60.1 perturbs cytokinin homeostasis in transgenic tobacco. J. Exp. Bot. 2006, 57:985-996.
51. Del Cueto J., Dicenta F., Jørgensen K., Møller B.L., Sánchez-Pérez R. Identification and characterization of prunasin hydrolases in sweet and bitter almonds and their expression in Nicotiana benthamiana plants. Acta Hortic. 2014, 1028:83-90.
52. Nakano R.T., Yamada K., Bednarek P., Nishimura M., Hara-Nishimura I. ER bodies in plants of the Brassicales order: biogenesis and association with innate immunity. Front. Plant Sci. 2014, 5:73.
53. Dharmawardhana D.P., Ellis B.E., Carlson J.E. cDNA cloning and heterologous expression of coniferin -glucosidase. Plant Mol. Biol. 1999, 40:365-372.
54. Mazzuca S., Spadafora A., Innocenti A.M. Cell and tissue localization of β-glucosidase during the ripening of olive fruit (Olea europaea) by in situ activity assay. Plant Sci. 2006, 171:726-733.
55. Sanchez-Perez R., Jorgensen K., Olsen C.E., Dicenta F., Møller B.L. Bitterness in almonds. Plant Physiol. 2008, 146:1040-1052.
56. Swain E., Li C.P., Poulton J.E. Tissue and subcellular localization of enzymes catabolizing (R)-amygdalin in mature Prunus serotina seeds. Plant Physiol. 1992, 100:291-300.
57. Matsushima R., Kondo M., Nishimura M., Hara-Nishimura I. A novel ER-derived compartmentthe ER body, selectively accumulates a β-glucosidase with an ER-retention signal in Arabidopsis. Plant J. 2003, 33:493-502.
58. Rouyi C., et al. Recombinant expression and characterization of the cytoplasmic rice β-glucosidase Os1BGlu4. PLoS One 2014, 9:e96712.
59. Lipka V., et al. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 2005, 310:1180-1183.
60. Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007, 2:953-971.
61. Horton P., et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007, 35:W585-587.
62. Miki D., Itoh R., Shimamoto K. RNA silencing of single and multiple members in a gene family of rice. Plant Physiol. 2005, 138:1903-1913.
63. Jiang Y., et al. Rice functional genomics research: progress and implications for crop genetic improvement. Biotechnol. Adv. 2012, 30:1059-1070.
64. Xing H.L., et al. CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 2014, 14:327.
65. Xie K., Minkenberg B., Yang Y. Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:3570-3575.
66. Till B.J., et al. Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biol. 2007, 7:19.
67. Schaeffer S.M., Nakata P.A. CRISPR/Cas9-mediated genome editing and gene replacement in plants: Transitioning from lab to field. Plant Sci. 2015, 240:130-142.
68. Palmer R.G., Rodriguez de Cianzio S. Conditional lethality involving nuclear and cytoplasmic chlorophyll mutants in soybeans. Theor. Appl. Genet. 1985, 70:349-354.
69. Lee K.H., et al. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 2006, 126:1109-1120.
70. Xu Z.Y., et al. A vacuolar β-Glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 2012, 24:2184-2199.
71. Chapelle A., et al. Impact of the absence of stem-specific β-glucosidases on lignin and monolignols. Plant Physiol. 2012, 160:1204-1217.
72. Jin S., Kanagaraj A., Verma D., Lange T., Daniell H. Release of hormones from conjugates: chloroplast expression of β-glucosidase results in elevated phytohormone levels associated with significant increase in biomass and protection from aphids or whiteflies conferred by sucrose esters. Plant Physiol. 2011, 155:222-235.
73. Kiran N.S., et al. Retargeting a maize β-glucosidase to the vacuole-Evidence from intact plants that zeatin-O-glucoside is stored in the vacuole. Phytochemistry 2012, 79:67-77.
74. Yoo D., et al. Transcription analyses of GmICHG, a gene coding for a β-glucosidase that catalyzes the specific hydrolysis of isoflavone conjugates in Glycine max (L.) Merr. Plant Sci. 2013, 208:10-19.
75. Sue M., Nakamura C., Miyamoto T., Yajima S. Active-site architecture of benzoxazinone-glucoside β-d-glucosidases in Triticeae. Plant Sci. 2011, 180:268-275.
76. Xia L., et al. Structures of alkaloid biosynthetic glucosidases decode substrate specificity. ACS Chem. Biol. 2012, 7:226-234.
77. Nomura T., Quesada A.L., Kutchan T.M. The new β-d-glucosidase in terpenoid-isoquinoline alkaloid biosynthesis in Psychotria ipecacuanha. J. Biol. Chem. 2008, 283:34650-34659.
78. Singh N.D., Kumar S., Daniell H. Expression of beta-glucosidase increases trichome density and artemisinin content in transgenic Artemisia annua plants. Plant Biotechnol. J. 2015, 10.1111/pbi.12476.
79. Wang P., Liu H., Hua H., Wang L., Song C.P. A vacuole localized β-glucosidase contributes to drought tolerance in Arabidopsis. Chin. Sci. Bull. 2011, 56:3538-3546.
80. Bednarek P., et al. Glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 2009, 323:101-106.
81. Sherameti I., et al. PYK10, a β-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J. 2008, 54:428-439.
82. Wakuta S., et al. Identification of a β-glucosidase hydrolyzing tuberonic acid glucoside in rice (Oryza sativa L.). Phytochemistry 2010, 71:1280-1288.
83. Hua Y., Sansenya S., Saetang C., Wakuta S., Cairns J.R.K. Enzymatic and structural characterization of hydrolysis of gibberellin A4 glucosyl ester by a rice β-d-glucosidase. Arch. Biochem. Biophys. 2013, 537:39-48.
84. Opassiri R., et al. Rice Os4BGlu12 is a wound-induced β-glucosidase that hydrolyzes cell wall-β-glucan-derived oligosaccharides and glycosides. Plant Sci. 2010, 179:273-280.
85. Barleben L., Panjikar S., Ruppert M., Koepke J., Stockigt J. Molecular architecture of strictosidine glucosidase: the gateway to the biosynthesis of the monoterpenoid indole alkaloid family. Plant Cell 2007, 19:2886-2897.
86. Czjzek M., et al. The mechanism of substrate (aglycone) specificity in β-glucosidases is revealed by crystal structures of mutant maize β-glucosidase-DIMBOA-DIMBOAGlc, and -dhurrin complexes. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13555-13560.
87. Verdoucq L., Czjzek M., Moriniere J., Bevan D.R., Esen A. Mutational and structural analysis of aglycone specificity in maize and sorghum β-glucosidases. J. Biol. Chem. 2003, 278:25055-25062.
88. Zouhar J., et al. Insights into the functional architecture of the catalytic center of a maize β-glucosidase Zm-p60.1. Plant Physiol. 2001, 127:973-985.
89. Saino H., et al. Crystal structures of β-primeverosidase in complex with disaccharide amidine inhibitors. J. Biol. Chem. 2014, 289:16826-16834.
90. Chuenchor W., et al. The structural basis of oligosaccharide binding by rice BGlu1 beta-glucosidase. J. Struct. Biol. 2011, 173:169-179.
91. Sansenya S., Maneesan J., Ketudat Cairns J.R. Exchanging a single amino acid residue generates or weakens a +2 cellooligosaccharide binding subsite in rice β-glucosidases. Carbohydr. Res. 2012, 351:130-133.
92. Pengthaisong S., Withers S.G., Kuaprasert B., Svasti J., Ketudat Cairns J.R. The role of the oligosaccharide binding cleft of rice BGlu1 in hydrolysis of cellooligosaccharides and in their synthesis by rice BGlu1 glycosynthase. Protein Sci. 2012, 21:362-372.
93. Pengthaisong S., Ketudat Cairns J.R. Effects of active site cleft residues on oligosaccharide binding, hydrolysis, and glycosynthase activities of rice BGlu1 and its mutants. Protein Sci. 2014, 23:1738-1752.
94. Ratananikom K., et al. Mutational analysis in the glycone binding pocket of Dalbergia cochinchinensis β-glucosidase to increase catalytic efficiency toward mannosides. Carbohydr. Res. 2013, 373:35-41.
95. Barrett T., Suresh C.G., Tolley S.P., Dodson E.J., Hughes M.A. The crystal structure of a cyanogenic β-glucosidase from white clover, a family 1 glycosyl hydrolase. Structure 1995, 3:951-960.
96. Brzobohatý B., et al. Release of active cytokinin by a β-glucosidase localized to the maize root meristem. Science 1993, 262:1051-1054.
97. Babcock G.D., Esen A. Substrate specificity of maize β-glucosidase. Plant Sci. 1994, 101:31-39.
98. Cicek M., Blanchard D., Bevan D.R., Esen A. The aglycone specificity-determining sites are different in 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA)-glucosidase (maize β-glucosidase) and dhurrinase (sorghum β-glucosidase). J. Biol. Chem. 2000, 275:20002-20011.
99. Polanska L., et al. Altered cytokinin metabolism affects cytokininauxin, and abscisic acid contents in leaves and chloroplasts, and chloroplast ultrastructure in transgenic tobacco. J. Exp. Bot. 2007, 58:637-649.
100. Xie Q., Michaeli S., Peled-Zehavi H., Galili G. Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci. 2015, 20:264-265.
101. Wang Y., et al. Autophagy contributes to leaf starch degradation. Plant Cell 2013, 25:1383-1399.
102. Wakuta S., et al. Comparison of enzymatic properties and gene expression profiles of two tuberonic acid glucoside β-glucosidases from Oryza sativa L. J. Appl. Glycosci. 2011, 58:67-70.
103. Zamioudis C., Hanson J., Pieterse C.M. β-Glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. New Phytol. 2014, 204:368-379.
104. Tsuyama T., et al. Proton-dependent coniferin transport, a common major transport event in differentiating xylem tissue of woody plants. Plant Physiol. 2013, 162:918-926.
105. Strabala T.J., MacMillan C.P. The Arabidopsis wood model-the case for the inflorescence stem. Plant Sci. 2013, 210:193-205.
106. Møller B.L. Functional diversifications of cyanogenic glucosides. Curr. Opin. Plant Biol. 2010, 13:338-347.
107. Hrmova M., et al. Structural basis for broad substrate specificity in higher plant β-d-glucan glucohydrolases. Plant Cell 2002, 14:1033-1052.