Reduced nitrogen availability during growth improves quality in red oak lettuce leaves by minimizing nitrate content, and increasing antioxidant capacity and leaf mineral content

Dario Stefanelli, Sonja Winkler, Rod Jones

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DOI: 10.4236/as.2011.24061                

Abstract

Overuse of N in lettuce production can lead to environmental problems caused by leaching and the accumulation of harmful nitrates in edible tissues. This study investigated the effect of applied nitrogen (N) concentrations between 40 and 2400 mg·L^–1 on growth, nitrate accumulation, mineral leaf content, and antioxidant capacity in Oak Leaf lettuce cv. “Shiraz” grown under hydroponic conditions in Australia. Yield (g FW) increased with nitrogen (N) application rate up to 1200 mg·L^–1, as did leaf N content, while C:N declined. Nitrogen Utilization Efficiency (NUtE) increased rapidly from 40 to 75 mg·L^–1 applied N, leveling at 150 mg·L^–1 with no subsequent effect of N concentrations between 400 and 2400 mg·L^–1. Nitrate content rose significantly with increased N, particularly at 1200 and 2400 mg·L^–1. Leaf total plant phenolic content (TPP) and antioxidant capacity (measured by ferric reducing antioxidant power—FRAP) were both maximal at 75 and 400 mg·L^–1 applied N, while highest oxygen radical absorption capacity (ORAC) values were found in leaves supplied with low N (40 to 400 mg·L^–1). Applied N as calcium nitrate also significantly affected leaf mineral content as B, Mg, Mn, and Zn significantly decreased with increasing N. These results indicate that N applications of 1200 mg·L^–1 or higher can result in reduced antioxidant capacity and mineral content in lettuce leaves.

Keywords

Lactuca sativa L.; Hydroponic; Phenolic Content; Zinc; Manganese; Magnesium

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Burt, R., Chataway, J., Cotter, J., Darcy-Vrillon, B., Debailleul, G., Grundy, A., Hinga, K., Johnson, B., Kahiluoto, H., Lutman, P., Madden, U. and Navrátilová, M. (2009a) Changes in agriculture and food production in North Amercia and Europe. In: McIntyre, B.D., Herren, H.R, Wakhungu, J. and Watson, R.T., Eds., Agriculture at a Crossroads. International Assessment of Agricultural Knowledge, Science and Technology for Development. Island Press, Washington, 20-78.
[2]	Burt, R., Chataway, J., Cotter, J., Darcy-Vrillon, B., Debailleul, G., Grundy, A., Hendrickson, M., Hinga, K., Johnson, B., Kahiluoto, H., Madden, Miele, M., Navrátilová, M. and Schuler, T. (2009b) Environmental, economic and social impacts of north america and europe agriculture and agricultural knowledge, science and technology. In: McIntyre, B.D., Herren, H.R, Wakhungu, J. and Watson, R.T., Eds., Agriculture at a Crossroads. International Assessment of Agricultural Knowledge, Science and Technology for D
[3]	Demsar, J., Osvald, J. and Vodnik, D. (2004). The effect of light-dependent application of nitrate on the growth of aeroponically grown lettuce (Lactuca sativa L.). Journal of the American Society for Horticultural Science, 129, 570-575.
[4]	Maynard, D.N. and Barker, A.V. (1979) Regulation of nitrate accumulation in vegetables. Acta Horticulturae, 93, 153-162.
[5]	Broadley, M.R., Seginer, I., Burns, A., Escobar-Gutiérrez, A.J., Burns, I.G. and Wite, P.J. (2003) The nitrogen and nitrate economy of butterhead lettuce (Lactuca saviva var. capitata L.). Journal of Experimental Botany, 390, 2081-2090. doi:10.1093/jxb/erg222
[6]	Zhu, W., Li, X.L., Christie, P. and Li, J.L. (2005) Environmental implications of low nitrogen use efficiency in excessively fertilized hot pepper (Capsicum frutescens L.) cropping systems. Agriculture, Ecosystems & Environment, 111, 70-80. doi:10.1016/j.agee.2005.04.025
[7]	Stefanelli, D., Goodwin, I. and Jones, R. (2010) Minimal nitrogen and water use in horticulture: Effects on quality and content of selected nutrients. Food Research International, 43, 1833-1843. doi:10.1016/j.foodres.2010.04.022
[8]	Maranville, J.W. and Madhavan, S. (2002) Physiological adaptation for nitrogen use efficiency in sorghum. Plant and Soil, 245, 25-34. doi:10.1023/A:1020660504596
[9]	Chiesa, A., Mayorga, I. and Leon, A. (2009) Quality of fresh cut lettuce (Lactuca sativa L.) as affected by lettuce genotype, nitrogen fertilisation and crop season. Advances in Horticultural Science, 23, 143-149.
[10]	Nicolle, C., Cardinault, N., Gueux, E., Jaffrelo, L., Rock, E., Mazur, A., Amouroux, P. and Remesy, C. (2004) Health effect of vegetable-based diet: lettuce consumption improves cholesterol metabolism and antioxidant status in the rat. Clinical Nutrition, 23, 605-614. doi:10.1016/j.clnu.2003.10.009
[11]	Birt, D.F., Hendrich, S. and Wang, W. (2001) Dietary agents in cancer prevention: Flavonoids and isoflavonoids. Pharmacology & Therapeutics, 90, 157-177. doi:10.1016/S0163-7258(01)00137-1
[12]	Hu, F.B. (2003) Plant-based foods and prevention of cardiovascular disease: An overview. Americal Journal of Clinical Nutrition, 78, 544S-551S.
[13]	Hollman, P.C.H. and Katan, M.B. (1999) Dietary flavonoids: Intake, health effects and bioavailability. Food Chemistry and Toxicology, 37, 937-942. doi:10.1016/S0278-6915(99)00079-4
[14]	Larson, A.J., Symons, J.D. and Jalili, T. (2010) Quercetin: A treatment for hypertension? A review of efficacy and mechanisms. Pharmaceuticals (Basel), 3, 237-250.
[15]	Vargas, A.J. and Burd, R. (2010) Hormesis and synergy: Pathways and mechanisms of quercetin in cancer prevention and management. Nutrition Reviews, 68, 418-428. doi:10.1111/j.1753-4887.2010.00301.x
[16]	Kim, J.-D., Liu, L., Guo, W. and Meydani, M. (2006) Chemical structure of flavonols in relation to modulation of angiogenesis and immune-endothelial cell adhesion. The Journal of Nutritional Biochemistry, 17, 165-176. doi:10.1016/j.jnutbio.2005.06.006
[17]	Ackland, L., Van de Waarsenburg, S. and Jones, R.B. (2005) Synergistic antiproliferative effect of the flavonols quercetin and kaempferol in cultured human cancer cell lines. In Vivo, 19, 69-76.
[18]	Poulsen, N., Johansen, A.S. and Sorensen, J.N. (1995) Influence of growth conditions on the value of crisphead lettuce. 4. Quality changes during storage. Plant Foods for Human Nutrition, 47, 157-162. doi:10.1007/BF01089265
[19]	D’Antuono, L.F. and Neri, R. (2001) The evaluation of nitrogen effect on lettuce quality by means of descriptive sensory profiling. Acta Horticulturae, 563, 217-223.
[20]	Seginer, I. (2003) A dynamic model for nitrogen-stressed lettuce. Annals of Botany, 91, 623-635. doi:10.1093/aob/mcg069
[21]	Stewart, A.J., Chapman, W., Jenkins, G.I., Graham, I., Martin, T. and Crozier, A. (2001) The effect of nitrogen and phosphorous deficiency on flavonol accumulation in plant tissues. Plant, Cell & Environment, 24, 1189-1197. doi:10.1046/j.1365-3040.2001.00768.x
[22]	Jones, R.B., Imsic, M., Franz, P., Hale, G. and Tomkins, R.B. (2007) High nitrogen during growth reduced glucoraphanin and flavonol content in broccoli (Brassica oleracea var. italica) heads. Australian Journal of Experimental Agriculture, 47, 1498-1505. doi:10.1071/EA06205
[23]	Bongue-Bartelsman, M. and Phillips, D.A. (1995) Nitrogen stress regulates gene expression of enzymes in the flavonoid biosynthetic pathway of tomato. Plant Physiology and Biochemistry, 33, 539-546.
[24]	Mogren, L.M., Olsson, M.E. and Gertsson, U.E. (2007) Quercetin content in stored onions (Allium cepa L.): Effects of storage conditions, cultivar, lifting time and nitrogen fertiliser level. Journal of the Science of Food and Agriculture, 87, 1595-1602. doi:10.1002/jsfa.2904
[25]	Nguyen, P.M. and Niemeyer, E.D. (2008) Effects of nitrogen fertilization on the phenolic composition and antioxidant properties of Basil (Ocimum basilicum L.). Journal of Agricultural and Food Chemistry, 56, 8685- 8691. doi:10.1021/jf801485u
[26]	Mareczek, A. and Leja, M. (2005) Effect of urea foliar application on antioxidant properties of lettuce and broccoli. Lithuanian Institute of Hortictulture Archives, 24, 235-241.
[27]	White, P.J. and Broadley, M.R. (2009) Biofortification of crops with seven mineral elements often lacking in human diets—iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytologist, 182, 49-84. doi:10.1111/j.1469-8137.2008.02738.x
[28]	White, P.J. and Brown, P.H. (2010) Plant nutrition for sustainable development and global health. Annals of Botany, 105, 1073-1080. doi:10.1093/aob/mcq085
[29]	Salt, DE. (2004) Update on ionomics. Plant Physiology, 136, 2451-2456. doi:10.1104/pp.104.047753
[30]	Baxter, I. (2009) Ionomics: Studying the social network of mineral nutrients. Current Opinion in Cell Biology, 3, 381-386.
[31]	Watanabe, T., Broadley, M.R., Jansen, S., White, P.J., Takada, J., Satake, K., Takamatsu, T., Tuah, S.J. and Osaki, M. (2007) Evolutionary control of leaf element composition in plants. New Phytologist, 174, 516-523. doi:10.1111/j.1469-8137.2007.02078.x
[32]	Broadley M.R., Hammond, J.P., White, P.J. and Salt, D.E. (2010) An efficient procedure for normalizing ionomics data for Arabidopsis thaliana. New Phytologist, 186, 270-274. doi:10.1111/j.1469-8137.2009.03145.x
[33]	Neeser, C., Savidov, N. and Driedger, D. (2007) Production of hydroponically grown calcium fortified lettuce. Acta Horticulturae, 744, 317-321.
[34]	Seginer, I., Shina, G., Albright, L.D. and Marsh, L.S. (1991) Optimal temperature setpoints for greenhouse lettuce. Journal of Agricultural Engineering Research, 49, 209-226. doi:10.1016/0021-8634(91)80040-L
[35]	Yilmaz, H. and Dasgan, H.Y. (2009) Comparison of different nitrogen forms for growing lettuce. Acta Horticulturae, 807,327-332.
[36]	Gent, M.P.N. (2003) Solution electrical conductivity and ratio of nitrate to other nutrients affect accumulation of nitrate in hydroponic lettuce. HortScience, 38, 222-227.
[37]	Ryan, A. (1998) Rapid measurement of major, minor and trace elements in plant and food material using the Varian 730-ES. ICP-OES Application Note Number, 33, 1-6. http://www.varianinc.com/image/vimage/docs/applications/apps/io-033.pdf
[38]	Leco Corporation (2010) Carbon, nitrogen, and sulfur in plant tissue. Organic Application Note, 203-821-172. http://www.leco.com/resources/application_notes/pdf/CNS2000_PLANT_TISSUE_203-821-172.pdf
[39]	Eaton, A.D., Clesceri, L.S., Rice, E.W. and Greenberg, A.E. (2005) Standard methods for the examination of water and wastewater. 21st Edition, American Public Health Association (APHA) Press, Washington, DC.
[40]	Singleton, V.L., Orthofer, R. and Lamuela-Raventós, R.M. (1999) Analysis of total phenolics and other oxidation substrates and antioxidants by means of Folin-Cio- calteu reagent. In Lester Packer, Ed. Methods in Enzymology. Oxidants and Antioxidants, Part A, Elsevier, San Diego, 299, 152-178. doi:10.1016/S0076-6879(99)99017-1
[41]	Ou, B., Huang, D., Hampsch-Woodill, M., Flanagan, J.A. and Deemer, E.K. (2002) Analysis of antioxidant activities of common vegetables employing oxyen radical absorbance capacity (ORAC) and ferric reducing antioxidant power (FRAP) assays: A comparative study. Journal of Agricultural and Food Chemistry, 50, 3122-3128. doi:10.1021/jf0116606
[42]	Huang, D., Ou, B., Hampsch-Woodill, M., Flanagan, J.A. and Prio, R.L. (2002) High-throughput assay of oxygen radical absorbance capacity (ORAC) using a multichannel liquid handling system coupled with a microplate fluorescence reader in 96-well format. Journal of Agricultural and Food Chemistry, 50, 4437-4444. doi:10.1021/jf0201529
[43]	Benzie, I.F. and Strain, J.J. (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry, 239, 70-76. doi:10.1006/abio.1996.0292
[44]	Hirel, B., Le Gouis, J., Ney, B. and Gallais, A. (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. Journal of Experimental Botany, 58, 2369- 2387. doi:10.1093/jxb/erm097
[45]	Balint, T. and Rengel, Z. (2008) Nitrogen efficiency of canola genotypes varies between vegetative stage and grain maturity. Euphytica, 164, 421-423. doi:10.1007/s10681-008-9693-6
[46]	Mengel, K. and Kirby, E.A. (2001) Principles of plant nutrition. 5th Edition, Kluwer Academic Publisher, Dor- drecht.
[47]	Collins N.C., Tardieu, F. and Tuberosa, R. (2008) Quantitative trait loci and crop performance under abiotic stress: Where do we stand? Plant Physiology, 147, 469-486. doi:10.1104/pp.108.118117
[48]	European Union. Commission Regulation (EU) No. 420/2011 of 29 April (2011) Amending Regulation (EC) No 1881/2006. Setting maximum levels for certain contaminats in foodstuffs. Official Journal of the European Union L111, 30 April 2011. http://faolex.fao.org/docs/pdf/eur102437.pdf
[49]	Santamaria, P. (2006) Nitrate in vegetables: Toxicity, content, intake and EC regulation. Journal of the Science of Food and Agriculture, 86, 10-17. doi:10.1002/jsfa.2351
[50]	Coria-Cayupan, Y.S., Sanchez de Pinto, M.I. and Nazareno, N.A. (2009) Variations in bioactive substance contents and crop yields of lettuce (Lactuca sativa L.) cultivated in soils with different fertilization treatments. Journal of Agricultural and Food Chemistry, 57, 10122- 10129. doi:10.1021/jf903019d
[51]	Zhu, W., Lin, X., Zhang, Y. and Fang, P. (2009) Effects of nitrogen application rates on antioxidant contents and antioxidative activities in Chinese cabbage (Brassica chinensis L.). Journal of the Zhejiang University (Agriculture and Life Sciences), 35, 299-306.
[52]	Kang, H.M. and Saltveit, M.E. (2002) Antioxidant capacity of lettuce leaf tissue increases after wounding. Journal of Agricultural and Food Chemistry, 50, 7536- 7541. doi:10.1021/jf020721c
[53]	Oh, M.-M., Carey, E.E. and Rajashekar, C.B. (2009) Environmental stresses induce health-promoting phytochemicals in lettuce. Plant Physiology and Biochemistry, 47, 578-583. doi:10.1016/j.plaphy.2009.02.008
[54]	Olsen, K.M., Slimestad, R., Lea, U.S., Brede, C., Lovdal, T., Ruoff, P., Verheul, M.J. and Lillo, C. (2009) Temperature and nitrogen effects on regulators and products of the flavonoid pathway: experimental and kinetic model studies. Plant, Cell & Environment, 32, 286-299. doi:10.1111/j.1365-3040.2008.01920.x
[55]	Dumas, Y., Dadomo, M., Di Lucca, G. and Grolier, P. (2003) Effects of environmental factors and agricultural techniques on antioxidant content of tomatoes. Journal of the Science of Food and Agriculture, 83, 369-382. doi:10.1002/jsfa.1370
[56]	Kovacik, J. and Backor, M. (2007) Changes of phenolic metabolism and oxidative status in nitrogen-deficient Matricaria chamomilla plants. Plant and Soil, 297, 255- 265. doi:10.1007/s11104-007-9346-x
[57]	Giorgi, A., Mingozzi, M., Madeo, M., Speranza, G. and Cocucci, M. (2009) Effect of nitrogen starvation on the phenolic metabolism and antioxidant properties of yarrow (Achillea collina Becker ex Rchb.). Food Chemistry, 114, 204-211. doi:10.1016/j.foodchem.2008.09.039
[58]	Rochfort, S.J., Imsic, M., Jones, R.B., Tomkins, R.B. and Trenerry, C.V. (2006) Characterisation of flavonol conjugates in immature leaves of Pak Choi (Brassica rapa L. ssp. chinensis L. (Hanelt.) by HPLC-DAD and LC- MS/MS. Journal of Agricultural and Food Chemistry, 54, 4855-4860. doi:10.1021/jf060154j
[59]	Heimler, D., Isolani, L., Vignolini, P., Tombelli, S. and Romani, A. (2007) Polyphenol content and antioxidant activity in some species of freshly consumed salads. Journal of Agricultural and Food Chemistry, 55, 1724- 1729. doi:10.1021/jf0628983
[60]	Mozafar, A. (1996) Decreasing the NO3 and increasing the vitamin C contents in spinach by a nitrogen deprivation method. Plant Foods for Human Nutrition, 49, 155- 162. doi:10.1007/BF01091973
[61]	Bryant, J.P., Chapin, F.S. and Klein, D.R. (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos, 40, 357-368. doi:10.2307/3544308
[62]	Abou-Hadid A.F., Abd-Elmoniem, E.M., El-Shinawy, M.Z. and Abou-Elsoud, M. (1996) Electrical conductivity effect on growth and mineral composition of lettuce plants in hydroponic system. Acta Horticolturae, 343, 59-66.