Glucosinolates Detoxification by Solid State Fermentation as Fungi "Biological" and Copper Sulfate Solution "Chemical" Methods
The seeds of Brassicaceae or Cruciferae family contain secondary plant products with various biological effects, including beneficial and harmful ones. These products contain glucosinolates (Gls). They have many types, but the bitter taste type and the anti-nutritive effect are thioglucosides, which contain a sulfate group on the aromatic ring. The seeds of the watercress plant, which were used in the current study in order to try to get rid of the impact of those substances, by cracking by the enzyme myrosinase and is able to crack and decompose Glycoside bond, a water enzyme, and Using six fungal strains: Sclerotinia sclerotiorum, Macrophomina phaseolina, Trichoderma longibrachiatum, Penicillium digitatum, and Fusarium oxysporum in addition to one chemical treatment using hydrothermal copper sulphate (CuSO4), and comparing the previous seven fungal and chemical biological parameters with a control treatment in which the parasite was treated The seeds of watercress are the same as the pre-treatment in the preparation of the solid fermentation environment but without fertilization of the environment in any fungal chain and the control treatment was incubated in the same conditions as the six fungal treatments. Because the seeds of watercress seeds are rich in antioxidants and anti-cancer, These materials are in all experimental and knowledgeable transactions The following tests were performed: Total polyphenols, Total flavonoids, Reducing power, ABTS+ action radical, DPPH radical, and Hydrogen peroxide scavenging activity, in addition to analysis The results of the various chemical treatments from the normal chemical analysis of protein, fiber, ash, fat and carbohydrates as well as the major mineral elements, to determine the effect of each treatment on the seedling of watercress seeds (Eruca sativa meal). The biological treatment included natural thermal treatment by sterilization of the plant material and biological fungal treatment by pollination and incubation and then the secretion of the water enzyme Capable of cracking glucosinolate for other substances. The results of this study showed that there are three biological factors which are T2 (Macrophomina phaseolina), T4 (Trichoderma longibrachiatum), and T6 (Penicillium digitatum) achieved the highest ratios that exceed the control treatment (Non-biologically and chemically treated), in the measurements of total polyphenols and total flavonoids content, Reducing power, (ABTS+) action radical, (DPPH) radical, and Hydrogen peroxide (H2O2) scavenging activity of rocket meal seed (RMS) in different treatments.
Solid Fermentation, Glucosinolates Detoxification, Copper Sulfate Solution, Antifungal Activity, Isothiocyanates, Antioxidant Activity, Chemical Composition, Watercress Plant (Rocket Seed Meal "RSM")
[1]
Taylor, F. I. (2013). Control of soil-borne potato pathogens using Brassica spp. mediated biofumigation. PhD thesis, University of Glasgow, UK.
[2]
Smolinska, U.; Morra, M. J.; Knudsen, G. R.; James, R. L. (2003). Isothiocyanates produced by Brassicaceae species as inhibitors of Fusarium oxysporum. Plant Disease 87: 407-412.
[3]
Inyang, E. N.; Butt, T. M.; Doughty, K. J.; Todd, A. D.; Archer, S. (1999). The effects of isothiocyanates on the growth of the entomopathogenic fungus Metahizium anisopliae and its infection of the mustard beetle. Mycology Res. 103: 974-980.
[4]
Sellam, A.; Lacomi-Vasilescu, B.; Hudhomme, P.; Simoneau, P. (2006). In vitro antifungal activity of brassinin, camalexin and two isothiocyanates against the crucifer pathogens Alternaria brassicicola and Alternaria brassicae. Plant Pathology 56: 296-301.
[5]
Sellam, A.; Poupard, P.; Simoneau, P. (2006). Molecular cloning of AbGst1 encoding a glutathione transferase differentially expressed during exposure of Alternaria brassicicola to isothiocyanates. FEMS Microbiology Letters 258, 241-9.
[6]
Kliebenstein, D. J. (2004). Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana tinged glasses. Plant Cell Environ. 27: 675-684.
[7]
Bednarek, P.; Osbourn, A. (2009). Plant-microbe interactions: chemical diversity in plant defense. Sci., 324: 746-748.
[8]
Pedras, M. S.; Jha, M.; Minic, Z.; Okeola, O. G. (2007). Isosteric probes provide structural requirements essential for detoxification of the phytoalexin brassinin by the fungal pathogen Leptosphaeria maculans. Bioorg. Med. Chem. 15: 6054-6061.
[9]
Schuhegger, R.; Nafisi, M.; Mansourova, M.; Petersen, B. L.; Olsen, C. E.; Svatos, A.; Halkier, B. A.; Glawischnig, E. (2006). CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiol. 141: 1248-1254.
[10]
Ferrari, S.; Plotnikova, J. M.; De Lorenzo, G.; Ausubel, F. M. (2003). Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 35: 193-205.
[11]
Kliebenstein, D. J.; Rowe, H. C.; Denby, K. J. (2005). Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. Plant J. 44: 25-36.
[12]
Rowe, H. C.; Kliebenstein, D. J. (2008). Complex genetics control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea. Genetics, 180: 2237-2250.
[13]
Halkier, B. A.; Gershenzon, J. (2006). Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303-333.
[14]
Lambrix, V.; Reichelt, M.; Mitchell-Olds, T.; Kliebenstein, D. J.; Gershenzon, J. (2001). The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia in herbivory. Plant Cell, 13: 2793-2807.
[15]
Tierens K.; Thomma, B. P. H.; Brouwer, M.; Schmidt, J.; Kistner, K. (2001). Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of arabidopsis to microbial pathogens. Plant Physiol, 125: 1688-1699.
[16]
Tripathi, M. K. and Mishra, A. S. (2007). Glucosinolates in animal nutrition: A review. Animal Feed Sci. Technol., 132: 1-27.
[17]
Stotz, H. U.; Sawada, Y.; Shimada, Y.; Hirai, M. Y.; Sasaki, E.; Krischke, M.; Brown, P. D.; Saito, K.; Kamiya, Y. (2011). Role of camalexin, indole glucosinolates, and side chain modification of glucosinolate-derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum. Plant J., 67 (1): 81-93.
[18]
Rahmanpour, S.; Backhouse, D.; Nonhebel, H. M. (2009). Induced tolerance of Sclerotinia sclerotiorum to isothiocyanates and toxic volatiles from Brassica Species. Plant Pathology, 58: 479-486.
[19]
Pedras, C. M. S.; Montaut, S. (2003). Probing crucial metabolic pathways in fungal pathogens of crucifers: biotransformation of indole-3-acetaldoxime, 4-hydroxyphenyl acetaldoxime, and their metabolites. Bioorg. Med. Chem., 11 (14): 3115-3120.
[20]
Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43: 205-227.
[21]
Bolton, M. D., Thomma, B. P. H. J.; Nelson, B. D. (2006). Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol. Plant Pathol. 7: 1-16.
[22]
Kim, K. S.; Min, J. Y.; Dickman, M. B. (2008). Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol. Plant Microbe Interact. 21: 605-612.
[23]
Guo, X.; Stotz, H. U. (2010). ABA signaling inhibits oxalate-induced production of reactive oxygen species and protects against Sclerotinia sclerotiorum. Eur. J. Plant Pathol. 128: 7-19.
[24]
Burow, M.; Losansky, A.; Muller, R.; Plock, A.; Kliebenstein, D. J.; Wittstock, U. (2009). The genetic basis of constitutive and herbivore-induced ESP independent nitrile formation in Arabidopsis. Plant Physiol. 149: 561-574.
[25]
Kissen, R.; Bones, A. M. (2009). Nitrile-specifier proteins involved in glucosinolate hydrolysis in Arabidopsis thaliana. J. Biol. Chem. 284: 12057-12070.
[26]
Dickman, M. B. and Mitra, A. (1992). Arabidopsis thaliana as a model for studying Sclerotinia sclerotiorum pathogenesis. Physiol. Mol. Plant Pathol. 41, 255-263.
[27]
Guo, X.; Stotz, H. U. (2007). Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Mol. Plant Microbe Interact. 20: 1384-1395.
[28]
Perchepied, L.; Balague, C.; Riou, C.; Claudel-Renard, C.; Riviere, N.; Grezes-Besset, B.; Roby, D. (2010). Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol. Plant Microbe Interact. 23: 846-860.
[29]
Glawischnig, E.; Hansen, B. G.; Olsen, C. E.; Halkier, B. A. (2004). Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. Proc. Natl Acad. Sci. USA, 101: 8245-8250.
[30]
Hirai, M. Y.; Sugiyama, K.; Sawada, Y. (2007). Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl Acad. Sci. USA, 104: 6478-6483.
[31]
Sonderby, I. E.; Hansen, B. G.; Bjarnholt, N.; Ticconi, C.; Halkier, B. A.; Kliebenstein, D. J. (2007). A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE, 2 (12): e1322.
[32]
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 Phytol. 177: 627-642.
[33]
Raymer, P. L. (2002). Canola: an emerging oilseed crop. In: Janick J, Whipkey A, eds. Trends in New Crops and New Uses. Alexandria, VA, USA: ASHS Press, 122-6.
[34]
Lamey, H. A. (1995). Survey of blackleg and Sclerotinia stem rot of canola in North Dakota in 1991 and 1993. Plant Disease 79: 322-4.
[35]
Hind, T. L.; Ash, G. J.; Murray, G. M. (2003). Prevalence of sclerotinia stem rot of canola in New South Wales. Aust. J. of Exp. Agric., 43: 163-8.
[36]
Boland, G. J.; Hall, R. (1994). Index of plant hosts of Sclerotinia sclerotiorum. Can. J. Plant Pathol. 16: 93-108.
[37]
Osbourn, A. E. (1996). Preformed antimicrobial compounds and plant defense against fungal attack. The Plant Cell, 8: 1821-31.
[38]
Brown J.; Morra M. J. (2005). Glucosinolate-containing seed meal as a soil amendment to control plant pests. Subcontract Report NREL/SR-510-35254.
[39]
Manici, L. M.; Lazzeri, L.; Palmieri, S. (1997). In vitro fungitoxic activity of some glucosinolates and their enzyme-derived products toward plant pathogenic fungi. J. Agric. Food Chem., 45: 2768-2773.
[40]
Smith, B. J., Kirkegaard, J. A. (2002). In vitro inhibition of soil microorganisms by 2-phenylethyl isothiocyanate. Plant Pathology 51, 585-593.
[41]
Brader, G.; Mikkelsen, M. D.; Halkier, B. A.; Palva, E. T. (2006). Altering glucosinolate profiles modulates disease resistance in plants. The Plant Journal 46: 758-767.
[42]
Sexton, A. C.; Kirkgaard, J. A.; Howlett, B. J. (1999). Glucosinolates in Brassica juncea and resistance to Australian isolates of Leptosphaeria maculans, the blackleg fungus. Australasian Plant Pathology 28: 95-102.
[43]
Li, Y.; Kiddle, G.; Bennett, R. N.; Wallsgrove, R. M. (1999) Local and systemic changes in glucosinolates in Chinese and European cultivars of oilseed rape (Brassica napus L.) after inoculation with Sclerotinia sclerotiorum (stem rot). Ann. Appl. Biol. 134, 45-58.
[44]
Pedras, M. S. C.; Ahiarhonu, P. W. K.; Hossain, M. (2004). Detoxification of the cruciferous phytoalexin brassinin in Sclerotinia sclerotiorum requires an inducible glucosyltransferase. Phytochemistry 65, 2685-94.
[45]
Cramer, R. A.; Lawrence, C. B. (2004). Identification of Alternaria brassicicola genes expressed in planta during pathogenesis of Arabidopsis thaliana. Fungal Genetics and Biology 41, 115-28.
[46]
Sellam, A.; Dongo, A.; Guillemette, T.; Hudhomme, P.; Simoneau, P. (2007). Transcriptional responses to exposure to the brassicaceous defence metabolites camalexin and allyl-isothiocyanate in the necrotrophic fungus Alternaria brassicicola. Molecular Plant Pathology 8, 195-208.
[47]
Ndiaye, M.; Termorshuizen, A. J.; van Bruggen, A. H. C. (2010). Effects of compost amendment and the biocontrol agent Clonostachys rosea on the development of charcoal rot (Macrophomina phaseolina) on cowpea. J. Plant Pathol., 92: 173-180.
[48]
Wrather J. A.; Anderson, T. R.; Arsyad, D. M.; Tan, Y.; Ploper, L. D.; Porta-Puglia, A.; Ram, H. H.; Yorinori, J. T. (2001). Soybean disease loss estimates for the top 10 soybean producing countries in 1998. Can. J. Plant Pathol., 23: 115-221.
[49]
Wrather, J. A.; Anderson, T. R.; Arsyad, D. M.; Gai, J.; Ploper, L. D.; Porta-Puglia, A.; Ram, H. H.; Yorinori, J. T. (1997). Soybean disease loss estimates for the top 10 soybean producing countries in 1994. Plant Disease 81: 107-110.
[50]
Buttery, R. G. (1993). Quantitative and sensory aspects of flavor of tomato and other vegetable and fruits. In T. E. Acree and R. Teranishi, eds., Flavor Science: Sensible Principles and Techniques, pp. 259-286. ACS, Washington, DC.
[51]
Buttery, R. G.; Ling, L. C. (1993). Volatiles of tomato fruit and plant parts: relationship and biogenesis. In R. Teranishi, R. Buttery, and H. Sugisawa, eds., Bioactive Volatile Compounds from Plants, Am. Chem. Soc. Symposium Series no. 525: 23-34. ACS Books, Washington, DC.
[52]
Báez Flores, M. E.; Troncoso-Rojas, R.; Tiznado Hernández, M. E. (2011). Genetic Responses Induced by Isothiocyanates Treatment on the Fungal Genus Alternaria. Revista Mexicana de Fitopatología, 29: 61-68.
[53]
Troncoso-Rojas, R.; Sánchez-Estrada, A.; Ruelas, C.; García, H. S.; Tiznado-Hernández, M. (2005). Effect of benzyl isothiocyanate on tomato fruit infection development by Alternaria alternata. J. Sci. Food Agric. 85: 1427-1434.
[54]
Sigareva, M. A.; Earle, E. D. (1999). Camalexin induction in intertribal somatic hybrids between Camelina sativa and rapid-cycling Brassica oleracea. Theoret. Appl. Genetics 98: 164-170.
[55]
Troncoso, R.; Espinoza, C.; Sanchez-Estrada, A.; Tiznado, M. E.; Hugo, S.; Garcia, H. S. (2005). Analysis of the isothiocyanates present in cabbage leaves extract and their potential application to control Alternaria rot in bell peppers. Food Res. Int., 38: 701-708.
[56]
Benitez, T.; Rincon, A. M.; Limon, M. C.; Codon, A. C. (2004). Biocontrol mechanisms of Trichoderma strains. Int. Microbiol., 7: 249-260.
[57]
Harman, G. E.; Howell, C. R.; Viterbo, A.; Chet, I.; Lorito, M. (2004). Trichoderma species: opportunistic, a virulent plant symbionts. Nat. Rev. Microbiology 2: 43-56.
[58]
Winther M.; Nielsen PV. (2006). Active packaging of cheese with allyl isothiocyanate, an alternative to modified atmosphere packaging. J. Food Prod. 69 (10): 2430-2435.
[59]
Mari M.; Leoni O.; Lori O.; Cembali T. (2002). Antifungal vapour-phase activity of allyl- isothiocyanate Against Penicillium expansum on pears. Plant Pathol. 51: 231-236.
[60]
Tunc S. E.; Chollet P.; Chalier L.; Preziosi-Belloy; Gontard N. (2007). Combined effect of volatile antimicrobial agents on the growth of Penicillium notatum. Int. J. Food Microbiol. 113 (3): 263-270.
[61]
Vaughn S. F.; Berhow M. A. (2005). Glucosinolate Hydrolysis Products from Various Plant Sources: Ph Effects, Isolation, and Purification. Ind. Crops Prod. 21: 193-202.
[62]
Mennicke W. H.; Gorler K.; Krumbiegel G.; Lorenz D. and Rittmann N. (1988). Studies on the Metabolism and Excretion of Benzyl Isothiocyanate in Man. Xenobiotica 18: 441-447.
[63]
Bednarek, P.; Pislewska-Bednarek, M.; Svatos, A. (2009). A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Sci., 323: 101-106.
[64]
Clay, N. K.; Adio, A. M.; Denoux, C.; Jander, G.; Ausubel, F. M. (2009). Glucosinolate metabolites required for an Arabidopsis innate immune response. Sci., 323: 95-101.
[65]
Smolinska, U.; Horbowicz, M. (1999). Fungicidal activity of volatiles from selected cruciferous plants against resting propagules of soil-borne fungal pathogens. J. Phytopathol., 147: 119-124.
[66]
Searle, L. M.; Chamberlain, K.; Butcher, D. N. (1984). Preliminary studies on the effects of copper, iron and manganese ions on the degradation of 3-indolylmethylglucosinolate (a constitute of Brassica spp.) by myrosinase. J. Sci. Food Agric. 35: 745-748.
[67]
Rouzaud, G.; Rabot, S.; Ratcliffe, B.; Duncan, A. J. (2003). Influence of plant and bacterial myrosinase activity on the metabolic fate of glucosinolates in gnotobiotic rats. Brit. J. Nutr. 90: 395-405.
[68]
Vig, A. P.; Walia, A. (2001). Beneficial effects of Rhizopus oligosporus fermentation on reduction of glucosinolates, fiber and phytic acid in rapeseed (Brassica napus) meal. Bioresource Technol. 78: 309-312.
[69]
Rakariyatham, N.; Sakorn, P. (2002). Biodegradation of glucosinolates in brown mustard meal (Brassica juncea) by Aspergillus sp. NR-4201 in liquid and solid culture. Biodegradation 3: 395-409.
[70]
Das, M. M.; Singhal, K. K. (2001). Influence of chemical treatment of mustard oil cake on its glucosinolate content and myrosinase activity. Indian J. Anim. Sci. 71: 793-796.
[71]
Das, M. M.; Singhal, K. K. (2005). Effect of feeding chemically treated mustard cake on growth, thyroid and liver function and carcass characteristics in kids. Small Rumin. Res. 56: 31-38.
[72]
El-Fadaly, H. A.; El-Kadi, S. M.; El-Moghazy, M. M.; Soliman, A. A.; El-Haysha, M. S. M. (2017a). Correlation Between Active Components of Rocket (Eruca sativa) as Cytotoxicity (Brine Shrimp Lethality Assay). American Journal of Biomedical Science and Engineering. Vol. 3, No. 2, pp. 20-24.
[73]
El-Fadaly, H. A.; El-Kadi, S. M.; El-Moghazy, M. M.; Soliman, A. A. M.; El-Haysha, M. S. (2017b). Antioxidant activity studies on extracts of Eruca sativa seed meal and oil, detoxification, the role of antioxidants in the resistant microbes. IJSRM Human J., 6 (3): 31-51.
[74]
Lin, J.-Y.; Tang, C.-Y. (2007). Determination of total phenolic and flavonoid contents in selected fruits and vegetables, as well as their stimulatory effects on mouse splenocyte proliferation. Food Chem., 101: 140-147.
[75]
Chang, C. C.; Yang, M. H.; Wen, H. M.; Chern, J. C. (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J. Food Drug Anal., 10: 178-182.
[76]
Oyaizu, M. (1986). Studies on products of browning reaction: antioxidative activities of products of browning reaction prepared from glucosamine, Jpn. J. Nutr., 44: 307-315.
[77]
Re, R.; Pellegrini N.; Proteggente A.; Pannala A.; Yang M.; Rice-Evans C. (1999). Antioxidant activity applying an improved ABTS radical. cation decolorization assay. Free Rad. Biol. Med., 26: 1231-1237.
[78]
Pratap, C. R.; Vysakhi, M. V.; Manju, S.; Kannan, M.; Abdul, K. S.; Sreekumaran, N. A. (2013). In vitro free radical scavenging activity of Aqueous and Methanolic leaf extracts of Aegle tamilnadensis (Rutaceae). Int. J. Pharm Sci., 819-823.
[79]
Keser, S.; Celik, S.; Turkoglu, S.; Yilmaz, O.; Turkoglu, I. (2012). Hydrogen Peroxide radical scavenging and total antioxidant activity of hawthorn. Chem. J. 02: 9-12.
[80]
Mithen, R. F.; Lewis, B. C.; Fenwick, G. R. (1986). In vitro activity of glucosinolates and their products against Leptosphaeria maculans. Trans Br Mycol. Soc. 87: 433-440.
[81]
Mithen, R. F.; Lewis, B. C.; Heaney, R. K.; Fenwick, G. R. (1987). Resistance of leaves of Brassica species to Leptosphaeria maculans. Trans Br Mycol. Soc. 88: 525-531.
[82]
Doughty, K. J.; Porter, A. J. R.; Morton, A. M.; Kiddie, G.; Bock, C. H.; Wallsgrove, R. (1991). Variation in the glucosinolate content of oilseed rape (Brassica napus L.) leaves. II. Response to infection by Alternaria brassicae (Berk.) Sacc. Ann Appl. Biol., 118: 469-477.
[83]
Doughty, K. J.; Blight, M. M.; Bock, C. H.; Fieldsend, J. K.; Pickett, J. A. (1996). Release of alkenyl isothiocyanates and other volatiles from Brassica rapa seedlings during infection by Alternaria brassicae. Phytochemistry 43: 371-374.
[84]
Fekete, S.; Gippert, T. (1986). Digestibility and nutritive value of nineteen feedstuffs. J. Appl. Rabbit Res., 9: 103-108.
[85]
Chung, F.-L.; Jiao, D.; Getahun, S. M.; Yu, M. C. (1998). A urinary biomarker for uptake of dietary isothiocyanates in humans. Cancer Epidemiol., Biomarkers & Prev. 7: 103-108.
[86]
Meskin, M. S.; Bidlack, W. R.; Davies, A. J.; Omaye, S. T. (2002). Phytochemicals in Nutrition and Health. CRC Press LLC. Printed in the United States of America, ISBN 1-58716-083-8; pp 96-97.
[87]
Bravo, L. (1998). Polyphenols: chemistry, dietary sources, metabolism and nutritional significance. Nutr. Rev. 56: 317-333.
[88]
Shahidi, E.; Wanasundara, P. K. J. E. D. (1992). Phenolic antioxidants. Crit. Rev. Food Sci. Nutr. 32: 67-103.
[89]
Ruegger, M.; Chapple, C. (2001). Mutations that reduce inapoylmalate accumulation in Arabidopsis thaliana define loci with diverse roles in phenylpropanoid metabolism, Genetics 159: 1741-1749.
[90]
Jahangir, M.; Abdel-Farid, I. B.; Kim, H. K.; Choi, Y. e.; Verpoorte, R. (2009). Healthy and unhealthy plants: The effect of stress on the metabolism of Brassicaceae. Environ. Exp. Bot., 67 (1): 23-33.
[91]
Rice-Evans, C. A.; Miller, N. J.; Bolwell, P. G.; Bramley, P. M.; Pridham, J. B. (1995). The relative antioxidant activities of plant-derived polyphenolic flavonoids, Free Rad. Res., 22 (4): 375-383.
[92]
Buchwaldt, L.; Nielsen, J. K.; Sorensen, H. (1984). Preliminary investigations of the effect of sinigrin on in vitro growth of three fungal pathogens of oilseed rape. Advances in the production and utilization of cruciferous crops. Proceedings of a Seminar CEC Programme Research Plant Protein Improvement, Copenhagen, pp 260-267.
[93]
Wettasinghe, M.; Shahidi, F. (1999). Antioxidant and free radical-scavenging properties of ethanolic extracts of defatted borage (Borago officinalis L.) seeds, Food Chem., 67: 399-414.
[94]
Wettasinghe, M.; Shahidi, F. (1999). Evening primrose meal: A source of national antioxidants and scavengers of hydrogen peroxide at oxygen-derived free radicals, J. Agric. Food Chem., 47: 1801-1812.
[95]
Shahidi, F. (2000). Antioxidant factors in plant foods and selected oilseeds, BioFactors, 13: 179-185.
[96]
Hatano, T.; Yasuhara, T.; Matsuda, M.; Yazaki, K.; Yoshida, T.; Okuda, T. (1990). Oenothein B, a dimeric, hydrolysable tannin with macrocyclic structure, and accompanying tannins from Oenothera erythrose pala. Journal of the Chemical Society, Perkin Transactions 1, (10), 2735-2743.
[97]
Miyamoto, K.-I.; Nomura, M.; Sasakura, M.; Matsui, E.; Koshiura, R.; Murayama, T.; Furukawa, T.; Hatano, T.; Yoshida, T.; Okuda, T. (1993). Anti–tumor activity of or nothin B, a unique macrocyclic ellagitannin, Jpn. J. Cancer Res., 84: 99-203.
[98]
Shahidi, F.; Wettasinghe, M.; Amarowicz, R.; Khan, M. A. (2000). Antioxidants of evening primrose, in Phytochemicals and Phytopharmaceuticals, Shahidi, F. and Ho, C.-T., eds., AOCS Press, Champaign, IL., pp. 278-295.
[99]
Balasinska, B. (1998). Hypocholesterolemic effect of dietary evening primrose (Oenothera paradoxa) cake extract in rat, Food Chem., 63: 453-459.
[100]
Arizza, R. R.; Pueyo, C. (1991). The involvement of reactive oxygen species in the direct acting mutagenicity of wine, Mutat. Res., 251: 115-121.
[101]
Stadler, R. H.; Markovic, J.; Turesky, R. J. (1995). In vitro anti- and pro-oxidative effects of natural polyphenols, Biol. Trace Element Res., 47: 299-305.
[102]
Halliwell, B. (1991). Reactive oxygen species in living systems, Am. J. Med. 91: 14S.
