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RESEARCH ARTICLE

High nitrogen during growth reduced glucoraphanin and flavonol content in broccoli (Brassica oleracea var. italica) heads

R. B. Jones A B , M. Imsic A , P. Franz A , G. Hale A and R. B. Tomkins A
+ Author Affiliations
- Author Affiliations

A Knoxfield Centre, Primary Industries Research Victoria, Private Bag 15, Ferntree Gully DC, Vic. 3156, Australia.

B Corresponding author. Email: rod.jones@dpi.vic.gov.au

Australian Journal of Experimental Agriculture 47(12) 1498-1505 https://doi.org/10.1071/EA06205
Submitted: 4 July 2006  Accepted: 24 May 2007   Published: 16 November 2007

Abstract

Broccoli (Brassica oleracea var. italica) heads are commonly consumed in the Western diet and frequent consumption is thought to help protect against certain cancers and cardiovascular disease. Broccoli heads contain relatively high levels of glucosinolates and flavonols, thought to be the key phytochemicals that contribute to the health benefits gained upon consumption. In this study, we investigated the effect of applied nitrogen (N) at either 0, 15, 30 or 60 kg/ha, or 30, 60, 90 or 150 kg/ha with applied sulfur (S) at 50 or 100 kg/ha on the glucosinolates glucoraphanin, glucobrassicin and progoitrin, and the flavonols quercetin and kaempferol in broccoli cv. Marathon florets. Trials were conducted in two sites in either heavy clay or sandy loam to also assess the effect of soil type on phytochemical content. Application rates were based around recommended N and S applications for this crop in south-east Australia. N applications over 30 kg/ha caused a decrease in the content of glucoraphanin (18–34%) and both flavonols (20–38%). Progoitrin content was not affected while glucobrassicin increased by up to 44% with N applications >30 kg/ha. S applications of 50 or 100 kg/ha had no significant effect on either glucosinolates or flavonols. Crop yield (fresh weight), however, was significantly depressed (up to 40%) by N applications below 60 kg/ha. Fresh weight was also significantly depressed in plants grown in heavy clay compared with plants grown in a sandy loam, and phytochemical content increased, possibly due to a concentration effect. Therefore, low N applications to optimise phytochemicals may be only commercially useful if growers are producing mini-broccoli heads, as levels required to optimise phytochemical content (<30 kg/ha) also caused a significant decline in yield.


Acknowledgements

The authors wish to thank Sonja Winkler, Christine Frisina and Bret Henderson for their valuable technical assistance. This paper is a publication from Vital Vegetables, a Trans-Tasman research project jointly funded and supported by Horticulture Australia Ltd, New Zealand Institute for Crop and Food Research Ltd, the New Zealand Foundation for Research, Science and Technology, the Australian Vegetable and Potato Growers Federation Inc., New Zealand Vegetable and Potato Growers Federation Inc. and the Victorian Department of Primary Industries.


References


Ackland L, van de Waarsenburg S, Jones RB (2005) Synergistic antiproliferative effect of the flavonols quercetin and kaempferol in cultured human cancer cell lines. International Journal of Experimental and Clinical Pathophysiology and Drug Research 19, 69–76. open url image1

Bongue-Bartelsman M, Phillips DA (1995) Nitrogen stress regulates gene expression of enzymes in the flavonoid biosynthetic pathway of tomato. Plant Physiology and Biochemistry 33, 539–546. open url image1

Brown AF, Yousef GG, Jeffrey EH, Klein BP, Wallig MA, Kushad MM, Juvik JA (2002) Glucosinolate profiles in broccoli: variation in levels and implications in breeding for cancer chemoprotection. Journal of the American Society for Horticultural Science 127, 807–813. open url image1

Bryant JP, Chapin FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357–368.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ciska E, Martyniak-Przybyszewska B, Kozlowska H (2000) Content of glucosinolates in cruciferous vegetables grown at the same site for two years under different climatic conditions. Journal of Agricultural and Food Chemistry 48, 2862–2867.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dick-Hennes E, Büning-Pfaue H (1992) Influence of sulphur and nitrogen supply on flavour and health-affecting compounds in Brassicaceae. In ‘Progress in flavour precursor studies’. (Eds P Schreier, P Winterhalter) pp. 185–188. (Allured Publishing Corp.: Carol Stream, IL)

Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. The Plant Cell 7, 1085–1097.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Elangovan V, Sekar S, Govindasamy S (1994) Chemopreventative potential of dietary bioflavonoids against 20-methylcholanthrene-induced tumourgenesis. Cancer Letters 87, 107–113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fahey JW, 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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56, 5–51.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fahey JW, Haristoy X, Dolan PM, Kensler TW, Scholtus I, Stephenson KK, 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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fischer J (1992) The influence of different nitrogen and potassium fertilisation on the chemical flavour composition of kohlrabi (Brassica oleracea var gongylodes L). Journal of the Science of Food and Agriculture 60, 465–470.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fismes J, Vong PC, Guckert A, Frossard E (2000) Influence of sulfur on apparent N-use efficiency, yield and quality of oilseed rape (Brassica napus L.) grown on a calcereous soil. European Journal of Agronomy 12, 127–141.
Crossref | GoogleScholarGoogle Scholar | open url image1

Guidi L, Lorefice G, Pardossi A, Malorgio F, Tognini F, Soldatini GF (1997) Growth and photosynthesis of Lycopersicon esculentum (L.) plants as affected by nitrogen deficiency. Biologia Plantarum 40, 235–244.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hertog MGL, Hollman PCH, Katan MJ (1992) Content of potentially anticarcinogenic flavonoids of 28 vegetables and 9 fruits commonly consumed in the Netherlands. Journal of Agricultural and Food Chemistry 40, 2379–2383.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hilbert G, Soyer JP, Molot J, Giraudon J, Milin S, Gaudillere JP (2003) Effects of nitrogen supply on must quality and anthocyanin accumulation in berries of cv. Merlot. Vitis 42, 69–76. open url image1

Hollman PCH (2001) Evidence for health benefits of plant phenols: local or systemic effects. Journal of the Science of Food and Agriculture 81, 842–852.
Crossref | GoogleScholarGoogle Scholar | open url image1

Huang C, Ma WY, Li J, Hecht SS, Don Z (1998) Essential role of p53 in phenethyl isothiocyanate induced apoptosis. Cancer Research 58, 4102–4106.
PubMed |
open url image1

Johnson IT (2000) Brassica vegetables and human health: glucosinolates in the food chain. Acta Horticulturae 539, 39–44. open url image1

Krumbein A, Schonhof I, Ruhlmann J, Widell S (2001) Influence of sulphur and nitrogen supply on flavour and health-affecting compounds in Brassicaceae. In ‘Plant nutrition – food security and sustainability of agro-ecosystems’. (Ed. WJ Horst) pp. 294–295. (Kluwer Academic Publishers: Dordrecht)

Kushad MM, Brown AF, Kurilich AC, Juvik JA, Klein BP, Wallig MA, Jeffery EH (1999) Variation of glucosinolates in vegetable crops of Brassica oleracea. Journal of Agricultural and Food Chemistry 47, 1541–1548.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Leser C, Treutter D (2005) Effects of nitrogen supply on growth, contents of phenolic compounds and pathogen (scab) resistance of apple trees. Physiologia Plantarum 123, 49–56.
Crossref | GoogleScholarGoogle Scholar | open url image1

Margna U (1977) Control at the level of substrate supply – an alternative in the regulation of phenylpropanoid accumulation in plant cells. Phytochemistry 16, 419–426.
Crossref | GoogleScholarGoogle Scholar | open url image1

Munday R, Munday CM (2004) Induction of Phase II detoxification enzymes in rats by plant-derived isothiocyanates: comparison of allyl isothiocyanate with sulforaphane and related compounds. Journal of Agricultural and Food Chemistry 52, 1867–1871.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Musk SR, Smith TK, Johnson IT (1995) On the cytotoxicity and genotoxicity of allyl and phenethyl isothiocyanates and their parent glucosinolates sinigrin and gluconasturtiin. Mutation Research 34, 19–23. open url image1

Price KR, Casuscelli F, Colquhoun IJ, Rhodes MJC (1998) Composition and content of flavonol glycosides in broccoli florets (Brassica oleracea) and their fate during cooking. Journal of the Science of Food and Agriculture 77, 468–472.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rangkadilok N, Nicolas ME, Bennett RN, Eagling DE, Premier RR, Taylor PW (2004) The effect of sulphur fertilizer on glucoraphanin levels in broccoli (Brassica oleracea L. var. italica) at different growth stages. Journal of Agricultural and Food Chemistry 52, 2632–2639.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rosa EAS, Heany RK, Fenwick GR, Portas CAM (1997) Glucosinolates in crop plants. Horticultural Reviews 19, 99–215. open url image1

Rosen CJ, Fritz VA, Gardner GM, Hecht SS, Carmella SG, Keney PM (2005) Cabbage yield and glucosinolate concentrations as affected by nitrogen and sulfur fertility. HortScience 40, 1493–1498. open url image1

Sato K, Nakayama M, Shigeta J (1996) Culturing conditions affecting the production of anthocyanin in suspended cell cultures of strawberry. Plant Science 113, 91–98.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schnug E, Haneklaus S (2000) Significance of interactions between sulfur and nitrogen supply for growth and quality of crop plants. In ‘Sulfur nutrition and sulfur assimilation in higher plants: molecular, biochemical and physiological aspects’. (Eds C Brunold, H Rennenberg, LJ De Kok, I Stulen, J-C Davidian) pp. 345–7. (Paul Haupt: Bern)

Schonhof I, Krumbein A, Bruckner B (2004) Genotypic effects on glucosinolates and sensory properties of broccoli and cauliflower. Die Nahrung 48, 25–33.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sesso HD, Gaziano JM, Liu S, Buring JE (2003) Flavonoid intake and the risk of cardiovascular disease in women. The American Journal of Clinical Nutrition 77, 1400–1408.
PubMed |
open url image1

Shelp BJ, Liu L, McLellan D (1993) Glucosinolate composition of broccoli (Brassica oleracea var. italica) grown under various boron treatments at three Ontario sites. Canadian Journal of Plant Science 73, 885–888. open url image1

Smith TK, Lund EK, Musk SRR, Johnson IT (1998) Inhibition of DMH-induced aberrant crypt foci, and induction of apoptosis in rat colon, following oral administration of a naturally occurring glucosinolate. Carcinogenesis 19, 267–273.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stewart AJ, Chapman W, Jenkins GI, Graham I, Martin T, Crozier A (2001) The effect of nitrogen and phosphorous deficiency on flavonol accumulation in plant tissues. Plant, Cell & Environment 24, 1189–1197.
Crossref | GoogleScholarGoogle Scholar | open url image1

Talalay P, Fahey JW, Holtzclaw WD, Prestera T, Zhang Y (1995) Chemoprotection against cancer by Phase II enzyme induction. Toxicology Letters 82, 173–179.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vallejo F, Garcia-Viguera C, Tomas-Berberan FA (2003) Changes in broccoli (Brassica olearacea L. var. italica) health-promoting compounds with inflorescence development. Journal of Agricultural and Food Chemistry 51, 3776–3782.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

van Poppel G, Verhoeven DT, Verhagen H, Goldbohm RA (1999) Brassica vegetables and cancer prevention. Epidemiology and mechanisms. Advances in Experimental Medicine and Biology 472, 159–168.
PubMed |
open url image1

Verma AK, Johnson JA, Gould MN, Tanner MA (1988) Inhibition of 7,12-dimethylbenz[a]anthracene and N-nitro-somethylurea induced rat mammary cancer by the dietary flavonol quercetin. Cancer Research 48, 5754–5788.
PubMed |
open url image1

Wallsgrove RM, Bennett RN (1995) The biosynthesis of glucosinolates in Brassicas. In ‘Amino acids and their derivatives in higher plants’. (Ed. RM Wallsgrove) pp. 243–260. (Cambridge University Press: Cambridge)

West L, Tsui I, Haas G (2002) Single column approach for the liquid chromatographic separation of polar and non-polar glucosinolates from broccoli sprouts and seeds. Journal of Chromatography. A. 966, 227–232.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Withers PJA, O’Donnell FM (1994) The response of double-low winter oilseed rape to fertiliser sulphur. Journal of the Science of Food and Agriculture 66, 93–101.
Crossref | GoogleScholarGoogle Scholar | open url image1

Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218–223.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wu L, Noyan Ashraf MH, Facci M, Wang R, Paterson PG, Ferrie A, Juurlink BH (2004) Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system. Proceedings of the National Academy of Sciences of the United States of America 101, 7094–7099.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhang Y, Talalay P, Cho CG, Posner GH (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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhao F, Evans EJ, Bilsborrow PE, Syers JK (1993) Influence of sulphur and nitrogen on seed yield and quality of low glucosinolate oilseed rape (Brassica napus L). Journal of the Science of Food and Agriculture 63, 29–37.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zhao F, Evans EJ, Bilsborrow PE, Syers JK (1994) Influence of nitrogen and sulphur on the glucosinolate profile of rapeseed (Brassica napus L). Journal of the Science of Food and Agriculture 64, 295–304.
Crossref | GoogleScholarGoogle Scholar | open url image1