Effects of soil and foliar applications of iron with or without nitrogen on production and nutritional quality of broccoli (Brassica oleracea var. italica)
Maria J. Poblaciones
A , Carlos García-Latorre A * , Manuel Martinez A and Rocio Velazquez A
A
Abstract
Iron (Fe) is an essential nutrient; however, it is deficient in the diets of millions of people globally, resulting in anaemia. Agronomic biofortification has been shown to be effective in alleviating Fe deficiency.
We evaluated the efficacy of soil and foliar applications of Fe with or without nitrogen (N) on floret and plant yield, and nutritional properties of broccoli (cv. Parthenon), in order to assess biofortification potential.
A greenhouse experiment comprised seven treatments: (1) control, no Fe or N application; (2) soil application of Fe (10 mg FeSO4.7H2O/kg before transplanting); (3) soil application of Fe + foliar application of N (0.4% (w/v) calcium ammonium nitrate at floret emergence); (4) foliar application of Fe (0.5% (w/v) FeSO4.7H2O at floret emergence); (5) foliar applications of Fe and N; (6) soil + foliar applications of Fe; (7) soil application of Fe + foliar applications of Fe and N.
Foliar Fe application with N and/or with soil Fe significantly increased commercial floret weight relative to the control (>62.5 vs 46 g), whereas treatments without foliar Fe (i.e. soil Fe alone or with N) did not differ from the control. Similarly, treatments with foliar Fe generally significantly increased floret diameter, whereas those without foliar Fe did not. Treatments with foliar Fe significantly increased floret Fe concentration (>10-fold), resulting in highly available Fe, with phytic acid:Fe molar ratios <0.2, and higher antioxidant activity and polyphenol content.
Foliar application of Fe, especially in combination with N, is the most efficient and effective application method, not only for biofortification purposes but also for productivity and for enhancing bioactive compounds in broccoli.
This study opens the door to implementation of effective and economically viable Fe biofortification programs with broccoli and other crops.
Keywords: bioavailability, biofortification, Brassicas, fertiliser, iron, nitrogen, phytate, phytic acid.
References
Abdalla ZF, El-Bassiony AE-M, El-Ramady H, El-Sawy SM, Shedeed SI, Mahmoud SH (2023) Broccoli biofortification using biological nano- and mineral fertilizers of selenium: a comparative study under soil nutrient deficiency stress. Egyptian Journal of Soil Science 63, 57-66.
| Crossref | Google Scholar |
Cakmak I (2009) Enrichment of fertilizers with zinc: an excellent investment for humanity and crop production in India. Journal of Trace Elements in Medicine and Biology 23, 281-289.
| Crossref | Google Scholar | PubMed |
Cano A, Acosta M, Arnao MB (2000) A method to measure antioxidant activity in organic media: application to lipophilic vitamins. Redox Report 5, 365-370.
| Crossref | Google Scholar | PubMed |
Casquete R, Castro SM, Martín A, Ruiz-Moyano S, Saraiva JA, Córdoba MG, Teixeira P (2015) Evaluation of the effect of high pressure on total phenolic content, antioxidant and antimicrobial activity of citrus peels. Innovative Food Science & Emerging Technologies 31, 37-44.
| Crossref | Google Scholar |
Colombo C, Palumbo G, He J-Z, Pinton R, Cesco S (2014) Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. Journal of Soils and Sediments 14, 538-548.
| Crossref | Google Scholar |
Colwell JD (1965) An automatic procedure for the determination of phosphorus in sodium hydrogen carbonate extract of soil. Chemistry & Industry 1965, 893-895.
| Google Scholar |
Connorton JM, Balk J (2019) Iron biofortification of staple crops: lessons and challenges in plant genetics. Plant and Cell Physiology 60, 1447-1456.
| Crossref | Google Scholar | PubMed |
Connorton JM, Balk J, Rodríguez-Celma J (2017) Iron homeostasis in plants – a brief overview. Metallomics 9, 813-823.
| Crossref | Google Scholar | PubMed |
Conte SS, Walker EL (2011) Transporters contributing to iron trafficking in plants. Molecular Plant 4, 464-476.
| Crossref | Google Scholar | PubMed |
Daru J, Zamora J, Fernández-Félix BM, Vogel J, Oladapo OT, Morisaki N, Tunçalp Ö, Torloni MR, Mittal S, Jayaratne K, Lumbiganon P, Togoobaatar G, Thangaratinam S, Khan KS (2018) Risk of maternal mortality in women with severe anaemia during pregnancy and post partum: a multilevel analysis. The Lancet Global Health 6, 548-554.
| Crossref | Google Scholar | PubMed |
De N, Singh R (2010) Effect of biofertilizer on nodulation of pea in an alluvial soil. Journal of Food Legumes 23, 50-53.
| Google Scholar |
del Amor FM, Marcelis LFM (2006) Differential effect of transpiration and Ca supply on growth and Ca concentration of tomato plants. Scientia Horticulturae 111, 17-23.
| Crossref | Google Scholar |
Di Gioia F, Petropoulos SA, Ozores-hampton M, Morgan K, Rosskopf EN (2019) Zinc and iron agronomic biofortification of Brassicaceae microgreens. Agronomy 9, 677.
| Crossref | Google Scholar |
EFSA (2015) Scientific opinion on dietary reference values for iron. EFSA Journal 13, 4254.
| Crossref | Google Scholar |
Erenoglu EB, Kutman UB, Ceylan Y, Yildiz B, Cakmak I (2011) Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (65Zn) in wheat. New Phytologist 189, 438-448.
| Crossref | Google Scholar | PubMed |
Evans WJ, Martin CJ (1988) Interactions of Mg(II), Co(II), Ni(II), and Zn(II) with phytic acid. VIII. A calorimetric study. Journal of Inorganic Biochemistry 32, 259-268.
| Crossref | Google Scholar |
Farnham MW, Stephenson KK, Fahey JW (2000) Capacity of broccoli to induce a mammalian chemoprotective enzyme varies among inbred lines. Journal of the American Society for Horticultural Science Jashs 125, 482-488.
| Crossref | Google Scholar |
Finkelstein JL, Haas JD, Mehta S (2017) Iron-biofortified staple food crops for improving iron status: a review of the current evidence. Current Opinion in Biotechnology 44, 138-145.
| Crossref | Google Scholar | PubMed |
Finkelstein JL, Fothergill A, Hackl LS, Haas JD, Mehta S (2019) Iron biofortification interventions to improve iron status and functional outcomes. Proceedings of the Nutrition Society 78, 197-207.
| Crossref | Google Scholar | PubMed |
Gibson RS (2007) The role of diet- and host-related factors in nutrient bioavailability and thus in nutrient-based dietary requirement estimates. Food and Nutrition Bulletin 28, S77-S100.
| Crossref | Google Scholar | PubMed |
Glahn RP, Noh H (2021) Redefining bean iron biofortification: a review of the evidence for moving to a high Fe bioavailability approach. Frontiers in Sustainable Food Systems 5, 682130.
| Crossref | Google Scholar |
Gomez-Coronado F, Poblaciones MJ, Almeida AS, Cakmak I (2017) Combined zinc and nitrogen fertilization in different bread wheat genotypes grown under mediterranean conditions. Cereal Research Communications 45, 154-165.
| Crossref | Google Scholar |
Hallberg L, Brune M, Rossander L (1989) Iron absorption in man: ascorbic acid and dose-dependent inhibition by phytate. The American Journal of Clinical Nutrition 49, 140-144.
| Crossref | Google Scholar | PubMed |
House WA (1999) Trace element bioavailability as exemplified by iron and zinc. Field Crops Research 60, 115-141.
| Crossref | Google Scholar |
Ishfaq M, Wang Y, Yan M, Wang Z, Wu L, Li C, Li X (2022) Physiological essence of magnesium in plants and its widespread deficiency in the farming system of China. Frontiers in Plant Science 13, 802274.
| Crossref | Google Scholar |
Kaur A, Singh G (2022) Zinc and iron application in conjunction with nitrogen for agronomic biofortification of field crops – a review. Crop & Pasture Science 73(8), 769-780.
| Crossref | Google Scholar |
Kałużewicz A, Bosiacki M, Frąszczak B (2016) Mineral composition and the content of phenolic compounds of ten broccoli cultivars. Journal of Elementology 21, 53-65.
| Crossref | Google Scholar |
Khoja KK, Buckley A, Aslam MF, Sharp PA, Latunde-dada GO (2020) In vitro bioaccessibility and bioavailability of iron from mature and microgreen fenugreek, rocket and broccoli. Nutrients 12(4), 1057.
| Crossref | Google Scholar | PubMed |
Kobayashi T, Nozoye T, Nishizawa NK (2019) Iron transport and its regulation in plants. Free Radical Biology and Medicine 133, 11-20.
| Crossref | Google Scholar | PubMed |
Kutman UB, Yildiz B, Ozturk L, Cakmak I (2010) Biofortification of durum wheat with zinc through soil and foliar applications of nitrogen. Cereal Chemistry 87, 1-9.
| Crossref | Google Scholar |
Lata-Tenesaca LF, de Mello Prado R, Ajila-Celi GE, da Silva DL, Junior JSP, Mattiuz B-H (2023) Iron biofortification in quinoa: effect of iron application methods on nutritional quality, anti-nutrient composition, and grain productivity. Food Chemistry 404, 134573.
| Crossref | Google Scholar |
Li Z, Zheng S, Liu Y, Fang Z, Yang L, Zhuang M, Zhang Y, Lv H, Wang Y, Xu D (2021) Characterization of glucosinolates in 80 broccoli genotypes and different organs using UHPLC-Triple-TOF-MS method. Food Chemistry 334, 127519.
| Crossref | Google Scholar | PubMed |
Liu M, Zhang L, Ser SL, Cumming JR, Ku K-M (2018) Comparative phytonutrient analysis of broccoli by-products: the potentials for broccoli by-product utilization. Molecules 23, 900.
| Crossref | Google Scholar |
López-Hernández AA, Ortega-Villarreal AS, Vázquez Rodríguez JA, López-Cabanillas Lomelí M, González-Martínez BE (2022) Application of different cooking methods to improve nutritional quality of broccoli (Brassica oleracea var. italica) regarding its compounds content with antioxidant activity. International Journal of Gastronomy and Food Science 28, 100510.
| Crossref | Google Scholar |
Morris ER, Ellis R (1989) Usefulness of the dietary phytic acid/zinc molar ratio as an index of zinc bioavailability to rats and humans. Biological Trace Element Research 19, 107-117.
| Crossref | Google Scholar | PubMed |
Mukherjee V, Mishra PK (2012) Broccoli-an underexploited neutraceutical. Science Research Reporter 2, 291-294.
| Google Scholar |
NIH (2022) Iron. Fact Sheet for Health Professionals. National Institutes of Health, Bethesda, MD, USA. Available at https://ods.od.nih.gov/factsheets/Iron-HealthProfessional/ [accessed 17 May 2023]
Pal V, Singh G, Dhaliwal SS (2021) A new approach in agronomic biofortification for improving zinc and iron content in chickpea (Cicer arietinum L.) grain with simultaneous foliar application of zinc sulphate, ferrous sulphate and urea. Journal of Soil Science and Plant Nutrition 21, 883-896.
| Crossref | Google Scholar |
Pasricha S-R, Tye-Din J, Muckenthaler MU, Swinkels DW (2021) Iron deficiency. The Lancet 397, 233-248.
| Crossref | Google Scholar |
Perera CA, Biggers RP, Robertson A (2019) Deceitful red-flag: angina secondary to iron deficiency anaemia as a presenting complaint for underlying malignancy. BMJ Case Reports 12, e229942.
| Crossref | Google Scholar |
Pivina L, Semenova Y, Doşa MD, Dauletyarova M, Bjørklund G (2019) Iron deficiency, cognitive functions, and neurobehavioral disorders in children. Journal of Molecular Neuroscience 68, 1-10.
| Crossref | Google Scholar | PubMed |
Platzer M, Kiese S, Herfellner T, Schweiggert-Weisz U, Miesbauer O, Eisner P (2021) Common trends and differences in antioxidant activity analysis of phenolic substances using single electron transfer based assays. Molecules 26, 1244.
| Crossref | Google Scholar |
Rivera-Martin A, Broadley MR, Poblaciones MJ (2020) Soil and foliar zinc application to biofortify broccoli (Brassica oleracea var. italica L.): effects on the zinc concentration and bioavailability. Plant, Soil and Environment 66, 113-118.
| Crossref | Google Scholar |
Rivera-Martin A, Reynolds-Marzal D, Martin A, Velazquez R, Poblaciones MJ (2021) Combined foliar zinc and nitrogen application in broccoli (Brassica oleracea var. italica L.): effects on growth, nutrient bioaccumulation, and bioactive compounds. Agronomy 11(3), 548.
| Crossref | Google Scholar |
Rout GR, Sahoo S (2015) Role of iron in plant growth and metabolism. Reviews in Agricultural Science 3, 1-24.
| Crossref | Google Scholar |
Samaniego-Vaesken MDL, Partearroyo T, Olza J, Aranceta-Bartrina J, Gil Á, González-Gross M, Ortega RM, Serra-Majem L, Varela-Moreiras G (2017) Iron intake and dietary sources in the Spanish population: findings from the ANIBES Study. Nutrients 9, 203.
| Crossref | Google Scholar |
Sosulski FW, Imafidon GI (1990) Amino acid composition and nitrogen-to-protein conversion factors for animal and plant foods. Journal of Agricultural and Food Chemistry 38, 1351-1356.
| Crossref | Google Scholar |
Sultana S, Naser HM, Quddus MA, Shill NC, Hossain MA (2018) Effect of foliar application of iron and zinc on nutrient uptake and grain yield of wheat under different irrigation regimes. Bangladesh Journal of Agricultural Research 43, 395-406.
| Crossref | Google Scholar |
Taskin MB, Gunes A (2022) Iron biofortification of wheat grains by foliar application of nano zero-valent iron (nZVI) and other iron sources with urea. Journal of Soil Science and Plant Nutrition 22, 4642-4652.
| Crossref | Google Scholar |
Teixeira DM, Canelas VC, do Canto AM, Teixeira JMG, Dias CB (2009) HPLC-DAD quantification of phenolic compounds contributing to the antioxidant activity of Maclura pomifera, Ficus carica and Ficus elastica extracts. Analytical Letters 42, 2986-3003.
| Crossref | Google Scholar |
Trod BS, Buttarelli MS, Stoffel MM, Céccoli G, Olivella L, Barengo PB, Llugany M, Guevara MG, Muñoz FF, Daurelio LD (2023) Postharvest commercial quality improvement of broccoli (Brassica oleracea L.) after foliar biofortification with selenium. Crop Science 63, 784-800.
| Crossref | Google Scholar |
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37, 29-38.
| Crossref | Google Scholar |
Wallace A, Mueller RT (1980) Calcium uptake and distribution in plants. Journal of Plant Nutrition 2, 247-256.
| Crossref | Google Scholar |
Wang J, Mao S, Liang M, Zhang W, Chen F, Huang K, Wu Q (2022) Preharvest methyl jasmonate treatment increased glucosinolate biosynthesis, sulforaphane accumulation, and antioxidant activity of broccoli. Antioxidants 11, 1298.
| Crossref | Google Scholar |
Wani SH, Gaikwad K, Razzaq A, Samantara K, Kumar M, Govindan V (2022) Improving zinc and iron biofortification in wheat through genomics approaches. Molecular Biology Reports 49, 8007-8023.
| Crossref | Google Scholar | PubMed |
Witte C-P, Tiller SA, Taylor MA, Davies HV (2002) Leaf urea metabolism in potato. Urease activity profile and patterns of recovery and distribution of 15N after foliar urea application in wild-type and urease-antisense transgenics. Plant Physiology 128, 1129-1136.
| Crossref | Google Scholar | PubMed |
Xiao J, Park YG, Guo G, Jeong BR (2021) Effect of iron source and medium pH on growth and development of Sorbus commixta in vitro. International Journal of Molecular Sciences 22, 133.
| Crossref | Google Scholar |
Zhao F, McGrath SP (1994) Extractable sulphate and organic sulphur in soils and their availability to plants. Plant and Soil 164, 243-250.
| Crossref | Google Scholar |
Zuo Y, Zhang F (2011) Soil and crop management strategies to prevent iron deficiency in crops. Plant and Soil 339, 83-95.
| Crossref | Google Scholar |
