Characterization and expression profile of two UDP-glucosyltransferases, UGT85K4 and UGT85K5, catalyzing the last step in cyanogenic glucoside biosynthesis in cassava

Plant Journal

Volumn 68, Issue 2, 2011, Pages 287-301

  Kannangara, Rubini ^a   Motawia, Mohammed S ^a   Hansen, Natascha K K ^a   Paquette, Suzanne M ^b   Olsen, Carl E ^a   Møller, Birger L ^a   Jørgensen, Kirsten ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

cassava; cyanogenic glucosides; cyanohydrin UDP glucosyltransferases; linamarin; lotaustralin; nitrogen assimilation

Indexed keywords

CASSAVA; CYANOGENIC GLUCOSIDES; CYANOHYDRIN UDP-GLUCOSYLTRANSFERASES; LINAMARIN; LOTAUSTRALIN; NITROGEN ASSIMILATION;

ACETONE; AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; CATALYSTS; ENZYMES; ESCHERICHIA COLI;

CARBOHYDRATES;

ANTIBODY; COMPLEMENTARY DNA; GLUCOSIDE; GLUCOSYLTRANSFERASE; LINAMARIN; LOTAUSTRALIN; NITRILE; RECOMBINANT PROTEIN; UGT85K4 PROTEIN, MANIHOT ESCULENTA; UGT85K5 PROTEIN, MANIHOT ESCULENTA; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOCATALYSIS; CHEMISTRY; DNA SEQUENCE; ENZYME SPECIFICITY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; KINETICS; MANIHOT; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT LEAF; RABBIT; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; BIOCATALYSIS; DNA, COMPLEMENTARY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GLUCOSIDES; GLUCOSYLTRANSFERASES; KINETICS; MANIHOT; MOLECULAR SEQUENCE DATA; NITRILES; PHYLOGENY; PLANT LEAVES; PLANT PROTEINS; RABBITS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI; MANIHOT ESCULENTA; PRUNUS DULCIS; SORGHUM BICOLOR;

EID: 80054055421     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04695.x     Document Type: Article

References (52)

1. Alves, A.A.C., (2002) Cassava botany and physiology. In Cassava: Biology, Production and Utilization (Hillocks, R.J., Thresh, J.M., and, Bellotti, A.C., eds). New York: CAB International publishing, pp. 67-89.
2. Andersen, M.D., Busk, P.K., Svendsen, I., and, Møller, B.L., (2000) Cytochromes P-450 from cassava (Manihot esculenta Crantz) catalyzing the first steps in the biosynthesis of the cyanogenic glucosides linamarin and lotaustralin-Cloning, functional expression in Pichia pastoris, and substrate specificity of the isolated recombinant enzymes. J. Biol. Chem. 275, 1966-1975. (Pubitemid 30060823)
3. Awoyinka, A.F., Abegunde, V.O., and, Adewusi, S.R.A., (1995) Nutrient content of young cassava leaves and assessment of their acceptance as a green vegetable in Nigeria. Plant Foods Hum. Nutr. 47, 21-28.
4. 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. (Pubitemid 44900351)
5. Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., and, Wheeler, D.L., (2005) GenBank. Nucleic Acids Res. 33, D34-D38. (Pubitemid 40207827)
6. Bjarnholt, N., Rook, F., Motawia, M.S., Cornett, C., Jørgensen, C., Olsen, C.E., Jaroszewski, J.W., Bak, S., and, Møller, B.L., (2008) Diversification of an ancient theme: hydroxynitrile glucosides. Phytochemistry, 69, 1507-1516.
7. Chavez, A.L., Bedoya, J.M., Sánchez, T., Iglesias, H., Ceballos, H., and, Roca, W., (2000) Iron, carotene, and ascorbic acid in cassava roots and leaves. Food Nutr. Bull. 21, 410-413. (Pubitemid 32206048)
8. Conn, E.E., (1980) Cyanogenic compounds. Annu. Rev. Plant Physiol. 31, 433-451.
9. Du, L.C., Bokanga, M., Møller, B.L., and, Halkier, B.A., (1995) The biosynthesis of cyanogenic glucosides in roots of cassava. Phytochemistry, 39, 323-326.
10. FAO (2010) FAOSTAT. Accessed on August 18, 2010.
11. Forslund, K., Morant, M., Jørgensen, B., Olsen, C.E., Asamizu, E., Sato, S., Tabata, S., and, Bak, S., (2004) Biosynthesis of the nitrile glucosides rhodiocyanoside A and D and the cyanogenic glucosides lotaustralin and linamarin in Lotus japonicus. Plant Physiol. 135, 71-84. (Pubitemid 38653654)
12. Franks, T.K., Yadollahi, A., Wirthensohn, M.G., Guerin, J.R., Kaiser, B.N., Sedgley, M., and, Ford, C.M., (2008) A seed coat cyanohydrin glucosyltransferase is associated with bitterness in almond (Prunus dulcis) kernels. Funct. Plant Biol. 35, 236-246. (Pubitemid 351574135)
13. Gachon, C.M., Langlois-Meurinne, M., and, Saindrenan, P., (2005) Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends Plant Sci. 10, 542-549. (Pubitemid 41566277)
14. Gleadow, R.M., and, Woodrow, I.E., (2000) Temporal and spatial variation in cyanogenic glycosides in Eucalyptus cladocalyx. Tree Physiol. 20, 591-598. (Pubitemid 30410974)
15. Halkier, B.A., Olsen, C.E., and, Møller, B.L., (1989) The biosynthesis of cyanogenic glucosides in higher plants. The (E)- and (Z)-isomers of p-hydroxyphenylacetaldehyde oxime as intermediates in the biosynthesis of dhurrin in Sorghum bicolor (L.) Moench. J. Biol. Chem. 264, 19487-19494. (Pubitemid 20008049)
16. Hansen, K.S., Kristensen, C., Tattersall, D.B., Jones, P.R., Olsen, C.E., Bak, S., and, Møller, B.L., (2003) The in vitro substrate regiospecificity of recombinant UGT85B1, the cyanohydrin glucosyltransferase from Sorghum bicolor. Phytochemistry, 64, 143-151. (Pubitemid 37101800)
17. He, X.Z., Wang, X., and, Dixon, R.A., (2006) Mutational analysis of the Medicago glycosyltransferase UGT71G1 reveals residues that control regioselectivity for (iso)flavonoid glycosylation. J. Biol. Chem. 281, 34441-34447. (Pubitemid 46036651)
18. Hughes, J., and, Hughes, M.A., (1994) Multiple secondary plant product UDP-glucose glucosyltransferase genes expressed in cassava (Manihot esculenta Crantz) cotyledons. DNA Seq. 5, 41-49.
19. Jenrich, R., Trompetter, I., Bak, S., Olsen, C.E., Møller, B.L., and, Piotrowski, M., (2007) Evolution of heteromeric nitrilase complexes in Poaceae with new functions in nitrile metabolism. Proc. Natl Acad. Sci. USA, 104, 18848-18853. (Pubitemid 350210785)
20. Jones, P.R., Møller, B.L., and, Høj, P.B., (1999) The UDP-glucose:p-hydroxymandelonitrile-O-glucosyltransferase that catalyzes 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. (Pubitemid 129512841)
21. Jørgensen, K., Rasmussen, A.V., Morant, M., Nielsen, A.H., Bjarnholt, N., Zagrobelny, M., Bak, S., and, Møller, B.L., (2005a) Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant Biol. 8, 280-291. (Pubitemid 40607404)
22. Jørgensen, K., Bak, S., Busk, P.K., Sorensen, C., Olsen, C.E., Puonti-Kaerlas, J., and, Møller, B.L., (2005b) Cassava plants with a depleted cyanogenic glucoside content in leaves and tubers. Distribution of cyanogenic glucosides, their site of synthesis and transport, and blockage of the biosynthesis by RNA interference technology. Plant Physiol. 139, 363-374. (Pubitemid 43951619)
23. Jørgensen, K., Morant, A.V., Morant, M., Jensen, N.B., Olsen, C.E., Kannangara, R., Motawia, M.S., Møller, B.L., and, Bak, S., (2011) Biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in cassava: isolation, biochemical characterization, and expression pattern of CYP71E7, the oxime-metabolizing cytochrome P450 enzyme. Plant Physiol. 155, 282-292.
24. Kahn, R.A., Bak, S., Svendsen, I., Halkier, B.A., and, Møller, B.L., (1997) Isolation and reconstitution of cytochrome P450ox and in vitro reconstitution of the entire biosynthetic pathway of the cyanogenic glucoside dhurrin from sorghum. Plant Physiol. 115, 1661-1670. (Pubitemid 28395270)
25. Kongsawadworakul, P., Viboonjun, U., Romruensukharom, P., Chantuma, P., Ruderman, S., and, Chrestin, H., (2009) The leaf, inner bark and latex cyanide potential of Hevea brasiliensis: evidence for involvement of cyanogenic glucosides in rubber yield. Phytochemistry, 70, 730-739.
26. Larkin, M.A., Blackshields, G., Brown, N.P., et al. (2007) Clustal W and clustal X version 2.0. Bioinformatics, 23, 2947-2948. (Pubitemid 350162903)
27. Li, J.Y., Fu, Y.L., Pike, S.M., et al. (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell, 22, 1633-1646.
28. Lieberei, R., Selmar, D., and, Biehl, B., (1985) Metabolization of cyanogenic glucosides in Hevea brasiliensis. Plant Syst. Evol. 150, 49-63.
29. Lim, E.K., Baldauf, S., Li, Y., Elias, L., Worrall, D., Spencer, S.P., Jackson, R.G., Taguchi, G., Ross, J., and, Bowles, D.J., (2003) Evolution of substrate recognition across a multigene family of glycosyltransferases in Arabidopsis. Glycobiology, 13, 139-145. (Pubitemid 36511749)
30. Mackenzie, P.I., Owens, I.S., Burchell, B., et al. (1997) The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics, 7, 255-269. (Pubitemid 27358064)
31. Mederacke, H., Selmar, D., and, Biehl, B., (1995) Glucosyltransferases of the cyanogenic plant cassava (Manihot esculenta, Crantz). J. Appl. Bot-Angew. Bot. 69, 119-124.
32. Mederacke, H., Biehl, B., and, Selmar, D., (1996) Characterization of two cyano glucosyltransferases from cassava leaves. Phytochemistry, 42, 1517-1522. (Pubitemid 27065638)
33. Mgling, N., Poulter, N.H., and, Rosling, H., (1992) An outbreak of acute intoxications from consumption of insuffeciently processed cassava in Tanzania. Nutr. Res. 12, 677-687.
34. Modolo, L.V., Blount, J.W., Achnine, L., Naoumkina, M.A., Wang, X.Q., and, Dixon, R.A., (2007) A functional genomics approach to (iso)flavonoid glycosylation in the model legume Medicago truncatula. Plant Mol. Biol. 64, 499-518. (Pubitemid 46897331)
35. Møller, B.L., (2010) Plant science. Dynamic metabolons. Science, 330, 1328-1329.
36. Møller, B.L., and, Conn, E.E., (1980) The biosynthesis of cyanogenic glucosides in higher plants. Channeling of intermediates in dhurrin biosynthesis by a microsomal system from Sorghum bicolor (Linn) Moench. J. Biol. Chem. 255, 3049-3056.
37. Morant, A.V., Jørgensen, K., Jørgensen, C., Paquette, S.M., Sanchez-Perez, R., Møller, B.L., and, Bak, S., (2008) β-glucosidases as detonators of plant chemical defense. Phytochemistry, 69, 1795-1813.
38. Nielsen, K.A., Tattersall, D.B., Jones, P.R., and, Møller, B.L., (2008) Metabolon formation in dhurrin biosynthesis. Phytochemistry, 69, 88-98. (Pubitemid 350256789)
39. Okumoto, S., Schmidt, R., Tegeder, M., Fischer, W.N., Rentsch, D., Frommer, W.B., and, Koch, W., (2002) High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J. Biol. Chem. 277, 45338-45346. (Pubitemid 36159141)
40. Osmani, S.A., Bak, S., Imberty, A., Olsen, C.E., and, Møller, B.L., (2008) Catalytic key amino acids and UDP-sugar donor specificity of a plant glucuronosyltransferase, UGT94B1: molecular modeling substantiated by site-specific mutagenesis and biochemical analyses. Plant Physiol. 148, 1295-1308. (Pubitemid 352847492)
41. Osmani, S.A., Bak, S., and, Møller, B.L., (2009) Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modeling. Phytochemistry, 70, 325-347.
42. Richman, A., Swanson, A., Humphrey, T., Chapman, R., McGarvey, B., Pocs, R., and, Brandle, J., (2005) Functional genomics uncovers three glucosyltransferases involved in the synthesis of the major sweet glucosides of Stevia rebaudiana. Plant J. 41, 56-67.
43. Sanchez-Perez, R., Jørgensen, K., Olsen, C.E., Dicenta, F., and, Møller, B.L., (2008) Bitterness in almonds. Plant Physiol. 146, 1040-1052. (Pubitemid 352844121)
44. Sánchez-Pérez, R., Jørgensen, K., Motawia, M.S., Dicenta, F., and, Møller, B.L., (2009) Tissue and cellular localization of individual β-glycosidases using a substrate-specific sugar reducing assay. Plant J. 60, 894-906.
45. Sefton, M.A., Francis, I.L., and, Williams, P.J., (1994) Free and bound volatile secondary metabolites of Vitis vinifera grape cv. Sauvognon blanc. J. Food Sci. 59, 142-147.
46. Selmar, D., Lieberei, R., and, Biehl, B., (1988) Mobilization and utilization of cyanogenic glycosides-The linustatin pathway. Plant Physiol. 86, 711-716.
47. Shao, H., He, X., Achnine, L., Blount, J.W., Dixon, R.A., and, Wang, X., (2005) Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell, 17, 3141-3154.
48. TYR, which catalyzes the committed step in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L) Moench. Proc. Natl Acad. Sci. USA, 91, 9740-9744.
49. Takos, A.M., Knudsen, C., Lai, D., Kannangara, R., Mikkelsen, L., Motawia, M.S., Olsen, C.E., Sato, S., Tabata, S., Jørgensen, K., Møller, B.L., and, Rook, F., (2011) Genomic clustering of cyanogenic glucoside biosynthetic genes aids their identification in Lotus japonicus and suggests the repeated evolution of this chemical defence pathway. Plant J. doi:.
50. Tamura, K., Dudley, J., Nei, M., and, Kumar, S., (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599. (Pubitemid 47236692)
51. Thorsøe, K.S., Bak, S., Olsen, C.E., Imberty, A., Breton, C., and, Møller, B.L., (2005) Determination of catalytic key amino acids and UDP sugar donor specificity of the cyanohydrin glycosyltransferase UGT85B1 from Sorghum bicolor. Molecular modeling substantiated by site-specific mutagenesis and biochemical analyses. Plant Physiol. 139, 664-673. (Pubitemid 43907097)
52. Vogt, T., and, Jones, P., (2000) Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci. 5, 380-386.