Manipulation of sinapine, choline and betaine accumulation in Arabidopsis seed: Towards improving the nutritional value of the meal and enhancing the seedling performance under environmental stresses in oilseed crops

Plant Physiology and Biochemistry

Volumn 46, Issue 7, 2008, Pages 647-654

  Huang, Jun ^a   Rozwadowski, Kevin ^a   Bhinu, V S ^a   Schäfer, Ulrike ^a   Hannoufa, Abdelali ^a  

^a SASKATOON RESEARCH CENTRE   (Canada)

Author keywords

Arabidopsis; Betaine; Choline; Choline oxidase; Sinapine; Transgenic

Indexed keywords

ACYLTRANSFERASE; ALCOHOL DEHYDROGENASE; BACTERIAL PROTEIN; BETAINE; CHOLINE; CHOLINE OXIDASE; DRUG DERIVATIVE; SINAPINE; SINAPOYLGLUCOSE CHOLINE O SINAPOYLTRANSFERASE; SINAPOYLGLUCOSE-CHOLINE O-SINAPOYLTRANSFERASE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTHROBACTER; ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NORTHERN BLOTTING; PLANT SEED; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEEDLING; TRANSGENIC PLANT;

ACYLTRANSFERASES; ALCOHOL OXIDOREDUCTASES; ARABIDOPSIS; ARTHROBACTER; BACTERIAL PROTEINS; BETAINE; BLOTTING, NORTHERN; CHOLINE; MUTAGENESIS, INSERTIONAL; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDLING; SEEDS;

ARABIDOPSIS; ARTHROBACTER; ARTHROBACTER PASCENS;

EID: 46749126913     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2008.04.014     Document Type: Article

References (53)

1. Strack D. Phenolic metabolism. In: Dey P.B., and Harborne J.B. (Eds). Plant Biochemistry (1997), Academic Press, Toronto 387-416
2. Dixon R.A., Lamb C.J., Masoud S., Sewalt V.J.H., and Paiva N.L. Metabolic engineering: prospects for crop improvement through the genetic manipulation of phenylpropanoid biosynthesis and defence responses: a review. Gene 179 (1996) 61-71
3. Campbell M.M., and Sederoff R.R. Variation in lignin content and composition: mechanisms of control and implications for the genetic improvement of plants. Plant Physiol. 110 (1996) 3-13
4. Regenbrecht J., and Strack D. Distribution of 1-sinapoyl-glucose:choline sinapoyltransferase activity in the Brassicaeae. Phytochemistry 24 (1985) 407-410
5. Bouchereau A., Hamelin J., Lamour I., Renard M., and Larher F. Distribution of sinapine and related compounds in seeds of Brassica and allied generas. Phytochemistry 30 (1991) 1873-1881
6. Chapple C.C.S., Vogt T., Ellis B.E., and Somerville C.R. an Arabidopsis mutant defective in general phenylpropanoid pathway. Plant Cell 4 (1992) 1413-1424
7. Milkowski C., Baumert A., Schmidt D., Nehlin L., and Strack D. Molecular regulation of sinapate ester metabolism in Brassica napus: expression of genes, properties of the encoded proteins and correlation of enzyme activities with metabolite accumulation. Plant J. 38 (2004) 80-92
8. Pearson A.W., Butler E.J., and Fenwick R.G. Rapeseed meal and egg taint: the role of sinapine. J. Sci. Food. Agric. 31 (1980) 898-904
9. Ismail F., Vaisey-Genser M., and Fyfe B. Bitterness and astringency of sinapine and its components. J. Food Sci. 46 (1981) 1241-1244
10. Bell J.M. Factors affecting the nutritional value of canola meal: a review. Can. J. Anim. Sci. 73 (1993) 679-697
11. Hüsken A., Baumert A., Strack D., Becker H.C., Möllers C., and Milkowski C. Reduction of sinapate ester content in transgenic oilseed rape (Brassica napus) by dsRNAi-based suppression of BnSGT1 gene expression. Mol. Breed. 16 (2005) 127-138
12. Nair R.B., Joy IV R.W., Kurylo E., Shi X.H., Schnaider J., Datla R.S.S., Keller W.A., and Selvaraj G. Identification of a CY84 family of cytochrome P450-dependent mono-oxygenase genes in Brassica napus and perturbation of their expression for engineering sinapine reduction in the seeds. Plant Physiol. 123 (2000) 1623-1634
13. Rhodes D., and Hanson A.D. Quaternary ammonium and tertiary sulphonium compounds in higher plants. Annu. Rev. Plant Physiol. and Plant Mol. Biol. 44 (1993) 357-384
14. Kent C. Eukaryotic phospholipid biosynthesis. Annu. Rev. Biochem. 64 (1995) 315-343
15. Sakamoto A., and Murata N. Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J. Exp. Bot. 51 (2000) 81-88
16. Emmert J.L., and Baker D.H. A chick bioassay approach for determining the bioavailability choline, concentration in normal and overheated soybean meal, canola meal and peanut meal. J. Nutrit. 127 (1997) 745-752
17. Menten J.M.F., Pesti G.M., and Bakalli R.L. A new method for determining the availability of choline in soybean meal. Poul. Sci. 76 (1997) 1292-1297
18. Blusztajn J.K. A vital amine Choline. Science 281 (1998) 794-795
19. Zeisel S.H. Choline: an essential nutrient for humans. Nutrition 16 (2000) 669-671
20. Holm P.I., Ueland P.M., Kvalheim G., and Lien E.A. Determination of choline, betaine, and dimethylglycine in plasma by a high-throughput method based on normal-phase chromatography-tandem mass spectrometry. Clin. Chem. 49 (2003) 286-294
21. Zeisel S.H. The fetal origins of memory: the role of dietary choline in optimal brain development. J. Pediatr. 149 (2006) S131-S136
22. Zeisel S.H., and Blusztajn J.K. Choline and human nutrition. Annu. Rev. Nutri. 14 (1994) 269-296
23. Sakamoto A., and Murata N. The use of bacterial choline oxidase, a glycinebetaine-synthesizing enzyme, to create stress-resistant transgenic plants. Plant Physiol. 125 (2001) 180-188
24. Nuccio M.L., Russell B.L., Nolte K.D., Rathinasabapathi B., Gage D.A., and Hanson A.D. The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J. 16 (1998) 487-496
25. Nuccio M.L., Rhodes D., McNeil S.D., and Hanson A.D. Metabolic engineering of plants for osmotic stress resistance. Curr. Opin. Plant Biol. 2 (1999) 128-134
26. Huang J., Hirji R., Adam L., Rozwadowski K.L., Hammerlindl J.K., Keller W.A., and Selvaraj G. Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol. 122 (2000) 747-756
27. McNeil S.D., Nuccio M.L., Ziemak M.J., and Hanson A.D. Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase. Proc. Natl. Acad. Sci. USA 98 (2001) 10001-10005
28. Murashige T., and Skoog F. A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol. Plant. 15 (1962) 473-497
29. Yu B., Lydiate D.J., Schäfer U.A., and Hannoufa A. Characterization of a beta-carotene hydroxylase of Adonis aestivalis and its expression in Arabidopsis thaliana. Planta 226 (2007) 181-192
30. Rozwadowski K.L., Khachatourians G.G., and Selvaraj G. Choline oxidase, a catabolic enzyme in Arthrobacter pascens, facilitates adaptation to osmotic stress in Escherichia coli. J. Bacteriol. 173 (1991) 472-478
31. Josefsson L.G., Lenman M., Ericson M.L., and Rask L. Structure of a gene encoding the 1.7 S storage protein, napin, from Brassica napus. J. Biol. Chem. 262 (1987) 12196-12201
32. Clough S.J. Floral dip: agrobacterium-mediated germ line transformation. Methods Mol. Biol. 286 (2005) 91-102
33. Shirley A.M., McMichael C.M., and Chapple C. The sng2 mutant of Arabidopsis is defective in the gene encoding the serine carboxypeptidase-like protein sinapoylglucose:choline sinapoyltransferase. Plant J. 28 (2001) 83-94
34. Takayama M., Itoh S., Nagasaki T., and Tanimizu I. A new enzymatic method for determination of serum choline-containing phospholipids. Clin. Chim. Acta 79 (1977) 93-98
35. Selvaraj G., Jain R.K., Olson D.J., Hirji R., Jana S., and Hogge L.R. Glycinebetaine in oilseed canola and flax leaves: detection by liquid chromatography-continuous flow secondary ion mass spectrometry (LC-CFSIMS). Phytochemistry 38 (1995) 1143-1146
36. Su J., Hirji R., Zhang L., He C.K., Selvaraj G., and Wu R. Evaluation of the stress-inducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycine betaine. J. Exp. Bot. 57 (2006) 1129-1135
37. Bessieres M.A., Gibon Y., Lefeuvre J.C., and Larher F. A single-step purification for glycine betaine determination in plant extracts by isocratic HPLC. J. Agric. Food Chem. 47 (1999) 3718-3722
38. Fraser C.F., Thompson M.G., Shirley A.M., Ralph J., Schoenher J.A., Sinlapadech T., Hall M.C., and Chapple C. Related Arabidopsis serine carboxypeptidase-like sinapoylglucose acyltransferases display distinct but overlapping substrate specificities. Plant Physiol. 144 (2007) 1986-1999
39. Lehfeldt C., Shirley A.M., Meyer K., Ruegger M.O., Cusumano J.C., Viitanen P.V., Strack D., and Chapple C. Cloning of the SNG1 gene of Arabidopsis reveals a role for a serine carboxypeptidase-like protein as an acyltransferase in secondary metabolism. Plant Cell 12 (2000) 1295-1306
40. Li A.X., and Steffens J.C. An acyltransferase catalyzing the formation of diacylglucose is a serine carboxypeptidase-like protein. Proc. Natl. Acad. Sci. USA 97 (2000) 6902-6907
41. Wajant H., Mundry K.W., and Pfizenmaier K. Molecular cloning of hydroxynitrile lyase from Sorghum bicolor(L.). Homologies to serine carboxypeptidases. Plant Mol. Biol. 26 (1994) 735-746
42. Stehle F., Brandt W., Milkowski C., and Strack D. Structure determinants and substrate recognition of serine carboxypeptides-like acyltransferases from plant secondary metabolism. FEBS Lett. 580 (2006) 6366-6374
43. Pearson A.W., Butler E.J., Curtis R.F., Fenwick G.R., Hobson- Frohock A., Land D.G., and Hall S.A. Effects of rapeseed meal on laying hens (Gallus domesticus) in relation to fatty liver-haemorrhagic syndrome and egg taint. Res. Vet. Sci. 25 (1978) 307-313
44. Cruz-Ramirez A., Lopez-Bucio J., Ramirez-Pimentel G., Zurita-Silva A., Sanchez-Calderon L., Ramirez-Chavez E., Gonzalez-Ortega E., and Herrera-Estrella L. The xipotl mutant of Arabidopsis reveals a critical role for phospholipid metabolism in root system development and epidermal cell integrity. Plant Cell 16 (2004) 2020-2034
45. Dänicke S., Ueberschär K.H., Reese K., and Weigend S. Investigations on the effects of rape oil quality, choline and methionine concentrations in diets for laying hens on the trimethylamine content of the eggs, on trimethylamine metabolism and on laying performance. Arch. Anim. Nutr. 60 (2006) 57-79
46. Nyyssola A., Kerovuo J., Kaukinen P., von Weymarn N., and Reinikainen T. Extreme halophiles synthesize betaine from glycine by methylation. J. Biol. Chem. 275 (2000) 22196-22201
47. Waditee R., Tanaka Y., Aoki K., Hibino T., Jikuya H., Takano J., Takabe T., and Takabe T. Isolation and functional characterization of N-methyltransferases that catalyze betaine synthesis from glycine in a halotolerant photosynthetic organism Aphanothece halophytica. J. Biol. Chem. 278 (2003) 4932-4942
48. Waditee R., Bhuiyan M.N., Rai V., Aoki K., Tanaka Y., Hibino T., Suzuki S., Takano J., Jagendorf A.T., Takabe T., and Takabe T. Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proc. Natl. Acad. Sci. USA 102 (2005) 1318-1323
49. Raman S.B., and Rathinasabapathi B. β-alanine N-methyltransferase of Limonium latifolium. cDNA cloning and functional expression of a novel N-methyltransferase implicated in the synthesis of the osmoprotectant beta-alanine betaine. Plant Physiol. 132 (2003) 1642-1651
50. Mou Z., Wang X., Fu Z., Dai Y., Han C., Ouyang J., Bao F., Hu Y., and Li J. Silencing of phosphoethanolamine N-methyltransferase results in temperature-sensitive male sterility and salt hypersensitivity in Arabidopsis. Plant Cell 14 (2002) 2031-2043
51. Parkin I.A., Lydiate D.J., and Trick M. Assessing the level of collinearity between Arabidopsis thaliana and Brassica napus for A. thaliana chromosome 5. Genome 45 (2002) 356-366
52. Lagercrantz U., Putterill J., Coupland G., and Lydiate D. Comparative mapping in Arabidopsis and Brassica, fine scale genome collinearity and congruence of genes controlling flowering time. Plant J. 9 (1996) 13-20
53. Yu B., Lydiate D.J., Young L.W., Schäfer U.A., and Hannoufa A. Enhancing the carotenoid content of Brassica napus seeds by downregulating lycopene epsilon cyclase. Transgenic Res. 16 (2007) 10.1007/11248-007-9131-x