Generation of Se-fortified broccoli as functional food: Impact of Se fertilization on S metabolism

Plant, Cell and Environment

Volumn 34, Issue 2, 2011, Pages 192-207

  Hsu, Fu Chen ^a   Wirtz, Markus ^a   Heppel, Simon C ^a   Bogs, Jochen ^a,b   Krämer, Ute ^a,c   Khan, Muhammad Sayyar ^a   Bub, Achim ^d   Hell, Rudiger ^a   Rausch, Thomas ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Breitenweg 71 ^*  (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

Author keywords

Broccoli; Cancer prevention; Cysteine (Cys); Glucosinolate (GSL); Glutathione (GSH); MYB transcription factor; Selenium (Se); Sulfate transporter (SULTR)

Indexed keywords

ANTINEOPLASTIC AGENT; FERTILIZER; GLUCORAPHANIN; GLUCOSINOLATE; IMIDOESTER; SELENIC ACID; SELENIUM; SELENIUM DERIVATIVE; SULFATE; SULFUR; VEGETABLE PROTEIN;

CANCER; METABOLISM; PROTEIN; SELENIUM; SULFATE; SULFUR; VEGETABLE;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; BRASSICA; CHEMISTRY; DRUG EFFECT; FUNCTIONAL FOOD; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PLANT LEAF; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACID SEQUENCE; ANTICARCINOGENIC AGENTS; BIOLOGICAL TRANSPORT; BRASSICA; FERTILIZERS; FUNCTIONAL FOOD; GLUCOSINOLATES; IMIDOESTERS; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; SELENIUM; SELENIUM COMPOUNDS; SULFATES; SULFUR;

BRASSICA OLERACEA VAR. CAPITATA; BRASSICA OLERACEA VAR. ITALICA;

EID: 78651340004     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2010.02235.x     Document Type: Article

References (70)

1. Bednarek P., Pislewska-Bednarek M., Svatos A., et al. (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323, 101-106.
2. Bogs J., Jaffé F.W., Takos A.M., Walker A.R. & Robinson S.P. (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiology 143, 1347-1361.
3. Brader G., Tas E. & Palva E.T. (2001) Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora. Plant Physiology 126, 849-860.
4. Charron C.S., Kopsell D.A., Randle W.M. & Sams C.E. (2001) Sodium selenate fertilisation increases selenium accumulation and decreases glucosinolate concentration in rapid-cycling Brassica oleracea. Journal of the Science of Food and Agriculture 81, 962-966.
5. Chiao J.W., Chung F.L., Kancherla R., Ahmed T., Mittelman A. & Conaway C.C. (2002) Sulforaphane and its metabolite mediate growth arrest and apoptosis in human prostate cancer cells. International Journal of Oncology 20, 631-636.
6. Clark L.C., Combs G.F., Jr, Turnbull B.W., et al. (1996) Effects of selenium supplementation for cancer prevention in patients with carcinoma of the skin. A randomized controlled trial. Nutritional prevention of cancer study group. The Journal of the American Medical Association 276, 1957-1963.
7. Clay N.K., Adio A.M., Denoux C., Jander G. & Ausubel F.M. (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323, 95-101.
8. Combs G.F. (2001) Selenium in global food systems. British Journal of Nutrition 85, 517-547.
9. Cornblatt B.S., Ye L., Dinkova-Kostova A.T., et al. (2007) Preclinical and clinical evaluation of sulforaphane for chemoprevention in the breast. Carcinogenesis 28, 1485-1490.
10. Czemmel S., Stracke R., Weisshaar B., Cordon N., Harris N.N., Walker A.R., Robinson S.P. & Bogs J. (2009) The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiology 151, 1513-1530.
11. Dinkova-Kostova A.T., Jenkins S.N., Fahey J.W., Ye L., Wehage S.L., Liby K.T., Stephenson K.K., Wade K.L. & Talalay P. (2006) Protection against UV-light-induced skin carcinogenesis in skh-1 high-risk mice by sulforaphane-containing broccoli sprout extracts. Cancer Letters 240, 243-252.
12. El Kassis E., Cathala N., Rouached H., Fourcroy P., Berthomieu P., Terry N. & Davidian J.C. (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiology 143, 1231-1241.
13. Fahey J.W., Zhang Y. & Talalay P. (1997) Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proceedings of the National Academy of Sciences of the United States of America 94, 10367-10372.
14. Fahey J.W., Haristoy X., Dolan P.M., Kensler T.W., Scholtus I., Stephenson K.K., Talalay P. & Lozniewski A. (2002) Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proceedings of the National Academy of Sciences of the United States of America 99, 7610-7615.
15. Finley J.W. (2005) Proposed criteria for assessing the efficacy of cancer reduction by plant foods enriched in carotenoids, glucosinolates, polyphenols and selenocompounds. Annals of Botany (Lond) 95, 1075-1096.
16. Finley J.W., Sigrid-Keck A., Robbins R.J. & Hintze K.J. (2005) Selenium enrichment of broccoli: interactions between selenium and secondary plant compounds. The Journal of Nutrition 135, 1236-1238.
17. Ganther H.E. (1999) Selenium metabolism, selenoproteins and mechanisms of cancer prevention: complexities with thioredoxin reductase. Carcinogenesis 20, 1657-1666.
18. Geu-Flores F., Nielsen M.T., Nafisi M., Moldrup M.E., Olsen C.E., Motawia M.S. & Halkier B.A. (2009) Glucosinolate engineering identifies a γ-glutamyl peptidase. Nature Chemical Biology 5, 575-577.
19. Gigolashvili T., Yatusevich R., Berger B., Müller C. & Flügge U.I. (2007) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. The Plant Journal 51, 247-261.
20. Gigolashvili T., Engqvist M., Yatusevich R., Muller C. & Flugge U.I. (2008) Hag2/MYB76 and hag3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytologist 177, 627-642.
21. Gleave A.P. (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology 20, 1203-1207.
22. Gonzalez A., Zhao M., Leavitt J.M. & Lloyd A.M. (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. The Plant Journal 53, 814-827.
23. Grubb C.D. & Abel S. (2006) Glucosinolate metabolism and its control. Trends in Plant Science 11, 89-100.
24. Halkier B.A. & Gershenzon J. (2006) Biology and biochemistry of glucosinolates. The Annual Review of Plant Biology 57, 303-333.
25. Hell R. (1997) Molecular physiology of plant sulfur metabolism. Planta 202, 138-148.
26. Hirai M.Y., Sugiyama K., Sawada Y., et al. (2007) Omics-based identification of Arabidopsis MYB transcription factors regulating aliphatic glucosinolate biosynthesis. Proceedings of the National Academy of Sciences of the United States of America 104, 6478-6483.
27. Horstmann V., Huether C.M., Jost W., Reski R. & Decker E.L. (2004) Quantitative promoter analysis in Physcomitrella patens: a set of plant vectors activating gene expression within three orders of magnitude. BMC Biotechnology 4, 1-13.
28. Ip C. & Ganther H.E. (1992) Comparison of selenium and sulfur analogs in cancer prevention. Carcinogenesis 13, 1167-1170.
29. Kataoka T., Hayashi N., Yamaya T. & Takahashi H. (2004) Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiology 136, 4198-4204.
30. Keck A.S. & Finley J.W. (2004) Cruciferous vegetables: cancer protective mechanisms of glucosinolate hydrolysis products and selenium. Integrative Cancer Therapies 3, 5-12.
31. Kristal A.R. & Lampe J.W. (2002) Brassica vegetables and prostate cancer risk: a review of the epidemiological evidence. Nutrition and Cancer 42, 1-9.
32. Li H.F., McGrath S.P. & Zhao F.J. (2008) Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytologist 178, 92-102.
33. Lyi S.M., Heller L.I., Rutzke M., Welch R.M., Kochian L.V. & Li L. (2005) Molecular and biochemical characterization of the selenocysteine se-methyltransferase gene and se-methylselenocysteine synthesis in broccoli. Plant Physiology 138, 409-420.
34. Mewis I., Tokuhisa J.G., Schultz J.C., Appel H.M., Ulrichs C. & Gershenzon J. (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67, 2450-2462.
35. Mikkelsen M.D., Petersen B.L., Glawischnig E., Jensen A.B., Andreasson E. & Halkier B.A. (2003) Modulation of cyp79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiology 131, 298-308.
36. Mullineaux P.M. & Rausch T. (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthesis Research 86, 459-474.
37. Munday R. & Munday C.M. (2004) Induction of phase ii detoxification enzymes in rats by plant-derived isothiocyanates: comparison of allyl isothiocyanate with sulforaphane and related compounds. Journal of Agriculture and Food Chemistry 52, 1867-1871.
38. Munday R., Mhawech-Fauceglia P., Munday C.M., et al. (2008) Inhibition of urinary bladder carcinogenesis by broccoli sprouts. Cancer Research 68, 1593-1600.
39. Nestle M. (1997) Broccoli sprouts as inducers of carcinogen-detoxifying enzyme systems: clinical, dietary, and policy implications. Proceedings of the National Academy of Sciences of the United States of America 94, 11149-11151.
40. Nestle M. (1998) Broccoli sprouts in cancer prevention. Nutrition Reviews 56, 127-130.
41. Paolini M., Perocco P., Canistro D., Valgimigli L., Pedulli G.F., Iori R., Croce C.D., Cantelli-Forti G., Legator M.S. & Abdel-Rahman S.Z. (2004) Induction of cytochrome p450, generation of oxidative stress and in vitro cell-transforming and DNA-damaging activities by glucoraphanin, the bioprecursor of the chemopreventive agent sulforaphane found in broccoli. Carcinogenesis 25, 61-67.
42. Pilon-Smits E.A., Garifullina G.F., Abdel-Ghany S., Kato S., Mihara H., Hale K.L., Burkhead J.L., Esaki N., Kurihara T. & Pilon M. (2002) Characterization of a nifs-like chloroplast protein from Arabidopsis. Implications for its role in sulfur and selenium metabolism. Plant Physiology 130, 1309-1318.
43. Rangkadilok N., Nicolas M.E., Bennett R.N., Eagling D.R., Premier R.R. & Taylor P.W. (2004) The effect of sulfur fertilizer on glucoraphanin levels in broccoli (B. oleracea l. var. Italica) at different growth stages. Journal of Agriculture and Food Chemistry 52, 2632-2639.
44. Rausch T. & Wachter A. (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends in Plant Science 10, 503-509.
45. Robbins R.J., Keck A.S., Banuelos G. & Finley J.W. (2005) Cultivation conditions and selenium fertilization alter the phenolic profile, glucosinolate, and sulforaphane content of broccoli. Journal of Medicinal Food 8, 204-214.
46. Rochfort S., Caridi D., Stinton M., Trenerry V.C. & Jones R. (2006) The isolation and purification of glucoraphanin from broccoli seeds by solid phase extraction and preparative high performance liquid chromatography. Journal of Chromatography A 1120, 205-210.
47. Shibagaki N., Rose A., McDermott J.P., Fujiwara T., Hayashi H., Yoneyama T. & Davies J.P. (2002) Selenate-resistant mutants of Arabidopsis thaliana identify SULTR1;2, a sulfate transporter required for efficient transport of sulfate into roots. The Plant Journal 29, 475-486.
48. Shroff R., Vergara F., Muck A., Svatos A. & Gershenzon J. (2008) Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proceedings of the National Academy of Sciences of the United States of America 105, 6196-6201.
49. Smith C.A. & Dacombe C. (1987) Rapid method for determining total glucosinolates in rapeseed by measurement of enzymatically released glucose. Journal of the Science of Food and Agriculture 38, 141-150.
50. Sønderby I.E., Burow M., Rowe H.C., Kliebenstein D.J. & Halkier B.A. (2010) A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiology 153, 348-363.
51. Sors T.G., Ellis D.R., Na G.N., Lahner B., Lee S., Leustek T., Pickering I.J. & Salt D.E. (2005) Analysis of sulfur and selenium assimilation in astragalus plants with varying capacities to accumulate selenium. The Plant Journal 42, 785-797.
52. Sors T.G., Ellis D.R. & Salt D.E. (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynthesis Research 86, 373-389.
53. Sors T.G., Martin C.P. & Salt D.E. (2009) Characterization of selenocysteine methyltransferases from Astralagus species with contrasting selenium accumulation capacity. The Plant Journal 59, 110-122.
54. Takahashi H., Watanabe-Takahashi A., Smith F.W., Blake-Kalff M., Hawkesford M.J. & Saito K. (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. The Plant Journal 23, 171-182.
55. Toler H.D., Charron C.S. & Sams C.E. (2007) Selenium increases sulfur uptake and regulates glucosinolate metabolism in rapid-cycling Brassica oleracea. Journal of the American Society for Horticultural Science 132, 14-19.
56. Traka M., Gasper A.V., Melchini A., et al. (2008) Broccoli consumption interacts with gstm1 to perturb oncogenic signalling pathways in the prostate. PLoS ONE 3, e2568.
57. U.S. Department of Agriculture, Agricultural Research Service. (2003) USDA National Nutrient Database for Standard Reference, Release 16. Nutrient Data Laboratory Home page.
58. Van Hoewyk D., Takahashi H., Inoue E., Hess A., Tamaoki M. & Pilon-Smits E.A. (2008) Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiologia Plantarum 132, 236-253.
59. Verkerk R., Schreiner M., Krumbein A., et al. (2009) Glucosinolates in Brassica vegetables: the influence of the food supply chain on intake, bioavailability and human health. Molecular Nutrition & Food Research 53, S219-S265.
60. Whanger P.D. (2004) Selenium and its relationship to cancer: an update. British Journal of Nutrition 91, 11-28.
61. White P.J., Bowen H.C., Parmaguru P., et al. (2004) Interactions between selenium and sulphur nutrition in Arabidopsis thaliana. Journal of Experimental Botany 55, 1927-1937.
62. Wirtz M. & Hell R. (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. The Plant Cell 19, 625-639.
63. Wirtz M., Droux M. & Hell R. (2004) O-acetylserine (thiol) lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. Journal of Experimental Botany 55, 1785-1798.
64. Wittstock U. & Burow M. (2007) Tipping the scales - specifier proteins in glucosinolate biosynthesis. IUBMB Life 59, 744-751.
65. Wittstock U., Agerbirk N., Stauber E.J., Olsen C.E., Hippler M., Mitchell-Olds T., Gershenzon J. & Vogel H. (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proceedings of the National Academy of Sciences of the United States of America 101, 4859-4864.
66. Wu F., Shen S., Lee L., Lee S., Chan M. & Lin C. (2009) Tape-Arabidopsis Sandwich - a simpler Arabidopsis protoplast isolation method. Plant Methods 5, 16.
67. Yoshimoto N., Takahashi H., Smith F.W., Yamaya T. & Saito K. (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. The Plant Journal 29, 465-473.
68. Yoshimoto N., Inoue E., Watanabe-Takahashi A., Saito K. & Takahashi H. (2007) Posttranscriptional regulation of high-affinity sulfate transporters in Arabidopsis by sulfur nutrition. Plant Physiology 145, 378-388.
69. Zhang L., Ackley A.R. & Pilon-Smits E.A.H. (2007) Variation in selenium tolerance and accumulation among 19 Arabidopsis thaliana accessions. Journal of Plant Physiology 164, 327-336.
70. Zhang Y., Talalay P., Cho C.G. & Posner G.H. (1992) A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proceedings of the National Academy of Sciences of the United States of America 89, 2399-2403.