http://orcid.org/0000-0002-2356-6440
Figures
Abstract
In modern agriculture, besides providing high and stable yields, it is imperative to produce products with a high nutritive quality. The goal of this study was to determine the effect of different fertilization regimes on the macro- and micronutrients in beetroot. A 3-year field trial was set up according to a Latin square method with four types of fertilization (unfertilized control, 50 t stable manure ha−1, and 500 and 1,000 kg NPK 5-20-30 ha−1). The mineral content was determined as follows (mg 100 g−1 in fresh weight of beetroot): 14–29 P, 189–354 K, 18–34 Ca, 17–44 Mg, 0.67–1.83 Fe, 0.41–0.65 Mn and 0.28–0.44 Zn. The highest beetroot P content was determined for the treatment with stable manure, especially in a year with dry climatic conditions. The highest beetroot K content was determined for the treatment with 1,000 kg NPK 5-20-30 ha−1, but at the same time for the same treatment, a general decreasing trend of micronutrient content was determined, due to the possible antagonistic effect of added potassium. For better mineral status of beetroot, application of combined mineral and organic fertilizers supplemented with additional foliar application of micronutrients can be suggested.
Citation: Petek M, Toth N, Pecina M, Karažija T, Lazarević B, Palčić I, et al. (2019) Beetroot mineral composition affected by mineral and organic fertilization. PLoS ONE 14(9): e0221767. https://doi.org/10.1371/journal.pone.0221767
Editor: Nicoletta Righini, Universidad Nacional Autonoma de Mexico Instituto de Investigaciones en Ecosistemas y Sustentabilidad, MEXICO
Received: January 25, 2019; Accepted: August 14, 2019; Published: September 6, 2019
Copyright: © 2019 Petek et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper.
Funding: This work was supported only by the Ministry of Science and Education of the Republic of Croatia under Grant 0178017. Publication was supported by the OpenAccess Publication Fund of the University of Zagreb Faculty of Agriculture.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Today, the challenge is no longer the production of agricultural products that are high-yielding only, but also those that have high quality, especially nutritional. Efficient vegetable production is based on large investments, including in fertilizers, and optimizing plant nutrition is essential in achieving high yields and product quality. Imbalances of all nutrients can increase the risk of environmental damage [1] as well as reduce plant growth. Only a well-nourished plant can provide enough minerals for human nutrition, which can be achieved by optimal fertilization following the rules of good agricultural practices.
The adoption of suitable fertilizer management strategies often results in large economic benefits to producers [2] and choosing the appropriate strategy is not an easy process due to different soil type and pH [3,4]. Agriculture, as an economic sector, has to carry out its activity with a profit with respect to the basic principles of sustainable agricultural production, with minimal impact on the environment [5] and rational use of fertilizers, pesticides and irrigation systems. The content and quantity of minerals is affected by plant cultivar [6,7], soil conditions [8], weather conditions during the growing season, fertilizer use [9] and harvest maturity state [10], and can be changed by fertilizer application to balance the content of microelements with macroelements [11,12]. In vegetable production, the yield, as well as the commercial and nutritional quality, is affected by NPK fertilizer application [13].
In plants, as well as humans, minerals play an important role in metabolism and affect health. Humans require carbohydrates, lipids and proteins (amino acids), as well as 13 vitamins and 17 minerals. The nutritive value of vegetables is not based on energy or protein content [14,15] only but also on the content of minerals [16,17] which are necessary for maintaining a healthy and well-nourished body.
Due to its nutritional composition, beetroot (red beet) consumption contributes to the improvement and maintenance of human health and helps in the prevention and treatment of various malignancies, leukaemia and the consequences of radiation exposure as well as the regulation of blood pressure, cholesterol and triglycerides. As beetroot contains high levels of iron, it can be useful during pregnancy and menstruation [18,19].
According to all above, the aim of this investigation was to determine the impact of organic and mineral fertilization on the nutrient content of beetroot.
Materials and methods
Field work
A field fertilization trial with beetroot (Beta vulgaris var. conditiva Alef.), cultivar ‘Bikor’, was carried out in Brašljevica (E N: 411107.5 5060488.5; 45°40’42.99” N 15°21’32.17” E) and Hrvatsko Polje (E N: 395207.625 4973293.5; 44°53’30.64” N 15°10’23.90” E) (Croatia) from 2003 to 2005 (Brašljevica in 2003, B-2003; Hrvatsko Polje in 2004, HP-2004, and in 2005, HP-2005) using the Latin square method with four treatments (unfertilized control, 50 t stable manure ha−1, 500 and 1,000 kg NPK 5-20-30 ha−1). Untreated beetroot seed was sown (22nd May 2003, 21st May 2004 and 29th June 2005) directly into soil with a plant spacing of 0.07 m × 0.40 m and a main plot area of 12 m2. Beetroot were harvested after ~90 days (21st Aug 2003, 24th Aug 2004 and 28th Sep 2005).
The field study was carried out on private land and owners of the land on both locations gave permission to conduct the study on their land properties. During the field study none of endangered or protected species were involved. No specific permissions were required for conducting the field study because it was not carried out in protected area.
Chemical plant analysis
The edible parts of six plants from each plot at harvest were randomly selected for analysis. Samples of plant material (dried at 105°C) were analysed in triplicate and the results presented as mean values. Prior to digestion the samples were re-dried in order to remove possible moisture gained before the analyses. After digestion of plant material with concentrated HNO3 (MILESTONE 1200 Mega Microwave Digester), the phosphorus content was determined using a spectrophotometer, and potassium using a flame photometer, while calcium, magnesium, iron, zinc and manganese were analysed using an atomic absorption spectrophotometer (AAS) [20].
Chemical soil analysis
Air-dried, ground and homogenized soil was analysed according to the following methods: soil pH was determined electrometrically using a combined electrode (pH-meter MA5730) for a soil : water suspension (1 : 2.5, w/v) (active acidity) [21]; humus by the Tjurin method [22]; potassium and phosphorus by the Egner–Riehm–Domingo method [23]; and nitrogen by the Kjeldahl method [20].
Climate conditions
Climate data consist of total daily precipitation (mm) and mean daily temperature (°C) and were collected and delivered by the Croatian Meteorological and Hydrological Service for the closest meteorological stations: Jastrebarsko for Brašljevica, and Otočac for Hrvatsko Polje. Multiannual (1961–1991) climate data are organized as total monthly precipitation (mm) and average monthly temperature (°C). Climate data for the years investigated are organized as total decade precipitation (mm) and mean decade temperature (°C), represented in the form of Walter climate diagrams.
Statistical data analysis
Statistical data analyses were performed using the SAS 8.2 System (2002–2003). Analysis of variance (ANOVA) was performed following a Latin square experimental design. A Tukey’s multiple comparison test (Tukey’s HSD) was applied applied to identify differences among treatments (e.g., fertilization, environment, and their interactions). Normality of the collected data was tested by checking the residual plots and homogeneity of variance (homoscedasticity) by plotting of residuals against fitted values.
Results
Chemical soil analysis
Field investigations were carried out on silty loam soil with a soil reaction (pHH2O) of 6.1–6.6, with low to moderate humus and nitrogen content, poor in phosphorus and low to rich in potassium (Table 1).
Climate conditions
The closest meteorological station to Brašljevica is Jastrebarsko and to Hrvatsko Polje is Otočac.
The total precipitation throughout 2003 (Fig 1A) was 766 mm, which is less than the multiannual average (935 mm; Table 2). Precipitation during the vegetation months of red beet growth was 247 mm. In the third decade of May, precipitation was 34 mm, in June 96 mm, in July 56 mm and in the first two decades of August 61 mm. Mean daily air temperature during the period of beetroot growth was 19–23°C. There was an arid period from the beginning of February, so plants were not able to use the water reserves from the soil.
(a, b and c). Walter Climate Diagrams for Jastrebarsko (Brašljevica Location) and Otočac (Hrvatsko Polje Location) Meteorological Stations.
In 2004 (Fig 1B), weather conditions during the growing season were favourable for beetroot growing thanks to the reserves of soil water before the growing period as well as to the rain during the first half of the growing period. Total precipitation during the year was 1238 mm, which is 133 mm more than the multiannual average (1105 mm, Table 2). During the growing period, precipitation was unevenly distributed. In the last decade of May, precipitation was 46 mm, in June 96 mm, in July 34 mm and in the first two decades of August 0.4 mm. Air temperature during the growing period gradually increased, from 12°C in May to 21°C in August. Generally, temperatures were lower than in 2003, and the ratio between temperature and precipitation was good and had a favourable effect on the growth and development of beetroot.
The total precipitation in 2005 was 1339 mm, 234 mm more than the multiannual average (1105 mm, Table 2). Also, during the vegetation period (July–September), the total precipitation was 423 mm (a lot at the end of vegetation period: in August 231 mm and in September 95 mm) (Fig 1C). Temperatures were favourable for the growth of beetroot. From the beginning to the end of the vegetation period, daily mean temperature decreased from 20°C in July and 17°C in August to 15°C in September. During the whole growing period, the precipitation/temperature ratio was favourable, except in August, when precipitation was significantly higher than required.
Beetroot macro- and microelement content
In the present study the effect of different fertilization in different environments was evaluated. Table 3 shows the content of dry weight (DW) and content of macroelements (P, K, Ca and Mg) of beetroot in fresh weight, while Table 4 shows the content of microelements (Fe, Mn and Zn) of beetroot in fresh weight according to different fertilization treatments. The results of analysis of variance (ANOVA) of fertilization treatments according to environments are shown in Table 5, while in Table 6 results of combined analysis of variance of experiment in three environments are shown.
According to results, beetroot obtained the highest (p = 0.0006) dry weight content at Hrvatsko Polje in 2004 (14.8% DW) when the climate conditions were favourable, compared to other two environments. Results showed that at Brašljevica in 2003 and Hrvatsko Polje in 2004, the highest average beetroot phosphorus content (24 mg P 100 g−1 fresh weight) was determined for the treatment with stable manure compared to other fertilization treatments. Also, the environment had a significant impact on the beetroot phosphorus content, which was higher (p = 0.0335) at Hrvatsko Polje in 2004 and 2005 (average 29 and 26 mg P 100 g−1 fresh weight, respectively). The highest average beetroot potassium content (300 mg K 100 g−1 fresh weight) was obtained for fertilization with 1,000 kg NPK ha−1. The same trend was noticed at Hrvatsko Polje in 2004 and 2005. Regardless of fertilization the highest potassium content (p = 0.0001) was found at Hrvatsko Polje in 2004 (354 mg K 100 g−1 fresh weight). No kind of fertilization in this study showed a positive effect on calcium and magnesium uptake by beetroot, so the highest average content was determined for the control treatment (28 mg Ca 100 g−1 fresh weight and 33 mg Mg 100 g−1 fresh weight). On the other hand, the environment showed a significant effect on uptake of calcium and magnesium. The highest annual average calcium content (31 mg Ca 100 g−1 fresh weight) was found for Hrvatsko Polje in 2004 (p = 0.0027) although it was not significantly different to that at Brašljevica in 2003 (29 mg Ca 100 g−1 fresh weight). The highest magnesium content (44 mg Mg 100 g−1 fresh weight) was found for Brašljevica in 2003 (p<0.0001).
The results show that, similar to Ca and Mg content, the highest content of microelements was determined for the control treatment (1.51 mg Fe 100 g−1 fresh weight, 0.63 mg Mn 100 g−1 fresh weight and 0.39 mg Zn 100 g−1 fresh weight), and fertilization had no significant effect. The highest microelement content (Fe, Mn and Zn) was found either at Brašljevica in 2003 and/or at Hrvatsko Polje in 2004 (p = 0.0032, p = 0.0056 and p = 0.0011, respectively).
Discussion
Beetroot is an important vegetable in the human diet, not just because of its mineral content, but also because of its bioactive compounds such as amino acids, flavonoids and phenols, as well as carotenoids and betalains which, among others, have great anti-oxidative activity [6,24,25]. Minerals affect the synthesis of secondary metabolites directly (as part of their structure) or indirectly (as parts or co-factors or activators of enzymes). Therefore, it is very important to optimize nutrient supply [26] for all plants, which can be done by choosing appropriate and sustainable fertilization design.
Many authors have reported the positive effect of fertilization with mineral and/or organic fertilizers on the nutritive value and yield of vegetables: cabbage and spinach [27,28], eggplant [29], common bean [30], carrot [31] and red head chicory [32].
In the literature, different recommendations for beetroot fertilization can be found: 150 kg N ha−1, 50 kg P ha−1, 220 kg K ha−1 and 40 kg Mg ha−1 [19]; 60 kg N ha−1, 80 kg P2O5 ha−1 and 150 kg K2O ha−1 [16]; or 85–110 kg N ha−1, 50–170 kg P2O5 ha−1 and 50–170 kg K2O ha-1 [33]; in this present research as mineral fertilization treatments we used 25 kg N ha−1, 100 kg P2O5 ha−1 and 150 kg K2O ha−1 (as 500 kg NPK 5-20-30 ha−1) and 50 kg N ha−1, 200 kg P2O5 ha−1 and 300 kg K2O ha−1 (as 1,000 kg NPK 5-20-30 ha-1). However, it is worth highlighting that any fertilization recommendation for serious agriculture production should be based on both the chemical composition of the soil and plant species nutrient need for the desired yield, taking into account cultivar characteristics.
Statistical analyses showed variations in the quantity of certain minerals with respect to the research environments, which were dependent upon the initial soil nutrient content and subject to weather conditions (total precipitation and mean daily temperature) as well as differences in the nutrient-holding capacity of the soil on which the study was conducted.
The nutrient status of soils and crops can be affected by different fertilization. Results showed that organic fertilization had a positive effect on beetroot P content. Organic fertilization increases the availability of phosphorus in soil [34] as during the mineralization process a certain amount of P is released from organic compounds [35]. The highest beetroot P content was determined for the treatment with stable manure, and was more pronounced in the year with less precipitation (2003). Therefore, increased soil organic matter content has a positive effect in extreme climate conditions due to its favourable effect on soil water-air properties [4,36].
In this study, organic fertilization had no significant effect on microelement uptake, a result that was reported by some other authors too [37,38], although it would have been expected that the application of stable manure would increase the uptake of the microelement through the formation of chelators, and following the chelates, during the mineralization process. On the contrary, some other studies reported significantly increased availability of Zn, Fe and Mn [39] and overall soil fertility [40] by organic fertilization. Also, the DTPA-extractable soil Zn, Fe and Mn concentrations were increased from 0.41 to 1.08 mg kg−1, from 10.3 to 17.7 mg kg−1, and from 9.7 to 11.8 mg kg−1, respectively, with increasing soil organic matter content, thus showing the importance of soil organic matter in micronutrient availability for crops [41]. Finally, despite there being no effect of organic fertilization, the microelement values obtained for beetroot are higher than almost all the literature data shown in Table 7.
Furthermore, not just the total content of nutrients in the soil, but the interaction of soil macronutrients and micronutrients affect micronutrients uptake [46]. In our study, the soil potassium content had a big role (most probably due to the high added potassium quantity) in decreasing uptake of the macroelements Ca and Mg, as potassium has an antagonistic relationship with those elements [47–49], although there are some findings that claim the opposite [50]. So, in mineral fertilizer treatments, a negative effect on uptake of those cations was observed, due to the tendency of plants to maintain a constant amount of total cations [50] and the amount of potassium ion in the soil being much higher than that of other cations.
Nevertheless, the genetic traits of a beetroot cultivar have a great effect on its mineral composition without any differences in fertilization treatments [6]. As in our study only one cultivar (‘Bikor’) was used, we could assume that some other cultivar may have a better response to fertilization treatments.
Comparing climatological conditions in all three investigation years during the growing period, it is evident that the most favourable conditions for normal growth and development of beetroot prevailed in 2004; 2003 was relatively unfavourable because of low precipitation and a poor ratio of temperature and precipitation, as was 2005 with an increased precipitation rate. The results show that weather conditions have a significant effect on the mineral composition of beetroot, and also on the yield. A previous paper [51] showed that in dry conditions (in 2003), application of 50 t stable manure ha−1 increased yield up to three times compared to the control treatment. On the contrary, mineral fertilization showed better results in years with optimal precipitation. However, in rainy 2005, the nutrient uptake determined was at a lower level due to possible leaching of nutrients [52]. All this suggests that the best results could be expected with the combined application of organic and mineral fertilizers [53,54], as well as microelements, especially by foliar fertilizers [55] in climatic extreme conditions.
As previously mentioned, not only plants need an optimal dose of nutrients for normal growth and development, but also humans. Table 8 shows the recommended daily intake of macro- and micronutrients for humans by age and sex. Regardless of the various data obtained, beetroot from this research is an extremely valuable food because it is a very good source of minerals. This thesis supports the fact that daily consumption of 100 g of beetroot (from our current study) can assure 2–4% of the daily requirement of phosphorus, 9–18% of potassium, 2–4% of calcium, 5–12% of magnesium, 5–13% of iron, 21–33% of manganese and 3–4% of zinc according to Regulation (EU) No 1169/2011 [56].
With all that is presented and discussed, one question will always be asked: what amount of any macro- or micronutrient has to be available to plants in the soil or has to be added to the soil, at what time and in what form to achieve high, stable yields of the desired quality without crossing economic, environmental or energy limits? All that must be considered in order to maintain and improve soil fertility without an adverse impact on the environment, plants, animals and/or humans [46].
So, in agricultural production, it is not possible to expect that fertilization will have a strong effect on plant mineral composition in all conditions, because as it can be seen, numerous different factors affect the open-field food factory.
Conclusions
Data indicated that the macro- and micronutrient content of beetroot can be affected by the environment in which they are grown to a greater extent than by fertilization. The highest phosphorus, potassium and calcium content was found in beetroot grown at Hrvatsko Polje in 2004 under favourable climatic conditions. The highest phosphorus content was achieved by treatment with 50 t stable manure ha−1 (especially in dry climatic conditions), and the highest potassium content with 1,000 kg NPK 5-20-30 ha−1. The highest content of the microelements calcium and magnesium in beetroot was determined for the unfertilized treatment, probably due to antagonism with potassium. Therefore, beetroot nutrient status would surely be considerably higher if common fertilization with mineral fertilizers were to be both combined with organic fertilizers and supplemented with additional foliar application of micronutrient fertilizers in order to increase the content of all nutrients to produce a high-value food.
Supporting information
S1 File. All data collected for minerals in beetroot.
https://doi.org/10.1371/journal.pone.0221767.s001
(PDF)
References
- 1. Zhang K, Greenwood DJ, White PJ, Burns IG. A dynamic model for the combined effects of N, P, and K fertilizers on yield and mineral composition; description and experimental test. Plant Soil. 2007;298:81–98.
- 2. Escalante HJ, Rodríguez-Sánchez S, Jiménez-Lizárraga M, Morales-Reyes A, De La Calleja J, Vazquez R. Barley yield and fertilization analysis from UAV imagery: a deep learning approach. Int J Remote Sens. 2019;40(7):2493–2516.
- 3. Popović B, Lončarić Z, Rastija D, Karalić K, Iljkić D. Ameliorative PK-fertilization and liming impacts on soil status. Növénytermelés. 2010;59(Supplement 2):9–12.
- 4.
Lončarić Z, Parađiković N, Popović B, Lončarić R, Kanisek J. Gnojidba povrća, organska gnojiva i kompostiranje. Osijek: Poljoprivredni fakultet u Osijeku, Sveučilište Josipa Jurja Strossmayera u Osijeku; 2015.
- 5. Vanden Auweele W, Vandendriessche H. A decision support system for field vegetable crops: focus on fertilization. Acta Hortic. 2002;571(571):149–152.
- 6. Wruss J, Waldenberger G, Huemer S, Uygun P, Lanzerstorfer P, Müller U, et al. Compositional characteristics of commercial beetroot products and beetroot juice prepared from seven beetroot varieties grown in Upper Austria. J Food Compos Anal. 2015;42:46–55.
- 7. Palčić I, Karažija T, Petek M, Lazarević B, Herak Ćustić M, Gunjača J, et al. Relationship between origin and nutrient content of Croatian common bean landraces. J Cent Eur Agric. 2018;19(3):490–502.
- 8. Gluhić D, Petek M, Peršurić D, Slunjski S. Relationship between plant and soil potassium on calcareous vineyard soils. Cereal Res Commun. 2008;36(S6/Part1):451–454.
- 9. Karažija T, Ćosić T, Lazarević B, Horvat T, Petek M, Palčić I, et al. Effect of organic fertilizers on soil chemical properties on vineyard calcareous soil. Agric Conspec Sci. 2015;80(2):79–84.
- 10. Ekholm P, Reinivuo H, Mattila P, Pakkala H, Koponen J, Happonen A, et al. Changes in the mineral and trace element contents of cereals, fruits and vegetables in Finland. J Food Compos Anal. 2007;20:487–495.
- 11. Reddy NS, Bhatt G. Contents of minerals in green leafy vegetables cultivated in soil fortified with different chemical fertilizers. Plant Food Hum Nutr. 2001;56:1–6.
- 12. Schenk MK. Nutrient efficiency of vegetable crops. Acta Hortic. 2006;700:21–33.
- 13. Wang ZH, Li SX, Malhi S. Effects of fertilization and other agronomic measures on nutritional quality of crops. J Sci Food Agr. 2008;88(1):7–23.
- 14. Herak Ćustić M, Horvatić M, Pecina M. Nitrogen fertilization influences protein nutritional quality in red head chicory. J Plant Nutr. 2009;32(4):598–609.
- 15. Petek M, Herak Ćustić M, Toth N, Slunjski S, Čoga L, Pavlović I, et al. Nitrogen and crude proteins in beetroot (Beta vulgaris var. conditiva) under different fertilization treatments. Not Bot Horti Agrobo. 2012;40(2):215–219.
- 16. Lisiewska Z, Kmiecik W, Gebczynnski P. Effects on mineral content of different methods of preparing frozen root vegetables. Food Sci Technol Int. 2006;12:497–503.
- 17. Ekholm P, Reinivuo H, Mattila P, Pakkala H, Koponen J, Happonen A, et al. Changes in the mineral and trace element contents of cereals, fruits and vegetables in Finland. J Food Compos Anal. 2007;20:487–495.
- 18. Bobek P, Galbavy S, Mariassyova M. The effect of red beet (Beta vulgaris var. rubra) fiber on alimentary hypercholesterolemia and chemically induced colon carcinogenesis in rats. Nahrung. 2000;44(3):184–187. pmid:10907240
- 19.
Lešić R, Borošić J, Buturac I, Ćustić M, Poljak M, Romić D. Povrćarstvo. Čakovec: Zrinski; 2016.
- 20.
AOAC. Official methods of analysis of AOAC International, vol. I. 16th ed. AOAC: Arlington, USA; 1995.
- 21.
Škorić A. Priručnik za pedološka istraživanja. Zagreb: Fakultet Poljoprivrednih Znanosti; 1982.
- 22.
JDPZ. Priručnik za ispitivanje zemljišta. Knjiga I. Beograd: Kemijske Metode Ispitivanja Zemljišta; 1966.
- 23. Egner H, Riehm H, Domingo WR. Untersuchung über die chemische Bodenanalyse als Grundlage für die Beurteilung des Nahrstoffzustanden der Boden. II, Chemische Extraktionsmethoden zur Phosphor und Kaliumbestimmung. K Lantbr Hogsk Annir. 1960;26:199–215.
- 24. Chhikara N, Kushwaha K, Sharma P, Gat Y, Panghal A. Bioactive compounds of beetroot and utilization in food processing industry: a critical review. Food Chem. 2018;272:192–200. pmid:30309532
- 25. Yashwant K. Beetroot: a super food. IJESTA. 2015;1:20–26.
- 26. Crotty FV, Fychan R, Theobald VJ, Sanderson R, Chadwick DR, Marley CL. The impact of using alternative forages on the nutrient value within slurry and its implications for forage productivity in agricultural systems. PLoS ONE. 2014;9(5):e97516. pmid:24830777
- 27. Jakse M, Mihelic R. The influence of organic and mineral fertilisation on vegetable growth and N availability in soil: preliminary results. Acta Hortic. 1999;506:69–75.
- 28. Reddy NS, Bhatt G. Contents of minerals in green leafy vegetables cultivated in soil fortified with different chemical fertilizers. Plant Food Hum Nutr. 2001;56:1–6.
- 29. Russo VM. Cultural methods and mineral content of eggplant (Solanum melongena) fruit. J Sci Food Agric. 1996;71:119–123.
- 30. Liu ZH, Jiang LH, Li XL, Hardter R, Zhang WJ, Zhang YL, et al. Effect of N and K fertilizers on yield and quality of greenhouse vegetable crops. Pedosphere. 2008;18(4):496–502.
- 31. Chen Q, Li X, Horlacher D, Liebig HP. Effects of different nitrogen rates on open-filled vegetable growth and nitrogen utilization in the North China Plain. Commun Soil Sci Plan. 2004;35(11–12):1725–1740.
- 32. Herak Ćustić M, Poljak M, Čoga L, Ljubičić M, Ćosić T, Pavlovic I, et al. Use of nutrients from organic and inorganic fertilizers for red head chicory production. Acta Hortic. 2006;700:111–114.
- 33.
Maynard DN, Hochmuth GJ. Knott’s handbook for vegetable growers. New York: John Wiley & Sons, Inc.; 1997.
- 34. Shahabifar J, Panahpour E, Moshiri F, Gholami A, Mostashari M. The quantity/intensity relation is affected by chemical and organic P fertilization in calcareous soils. Ecotox Environ Safe. 2019;172:144–151.
- 35. Andry A, Tiphaine C, Dominique M, Herintsitohaina R, Tantely R. Land management modifies the temperature sensitivity of soil organic carbon, nitrogen and phosphorus dynamics in a Ferralsol. Appl Soil Ecol. 2019;138:112–122.
- 36. Wagner S, Cattle SR, Scholten T. Soil–aggregate formation as influenced by clay content and organic–matter amendment. J Plant Nutr Soil Sci. 2007;170(1):173–180.
- 37. Herencia JF, Ruiz JC, Morillo E, Melero S, Villaverde J, Maqueda C. The effect of organic and mineral fertilization on micronutrient availability in soil. Soil Sci. 2008;173(1):69–80.
- 38. Tamoutsidis E, Papadopoulos I, Tokatlidis I, Zotis S, Mavropoulos T. Wet sewage sludge application effect on soil properties and element content of leaf and root vegetables. J Plant Nutr. 2002;25(9):1941–1955.
- 39. Zhang SX, Wang XB, Jin K. Effect of different N and P levels on availability of zinc, copper, manganese and iron under arid conditions. Plant Nutr Fert Sci. 2001;7:391–396.
- 40. Cai A, Xu M, Wang B, Zhang W, Liang G, Hou E, et al. Manure acts as a better fertilizer for increasing crop yields than synthetic fertilizer does by improving soil fertility. Soil Till Res. 2019;189:168–175.
- 41. Li BY, Zhou DM, Cang L, Zhang HL, Fan XH, Qin SW. Soil micronutrient availability to crops as affected by long-term inorganic and organic fertilizer applications. Soil Tillage Res. 2007;96(1–2):166–173.
- 42. Grembecka M, Szeefer P, Dybek K, Gurzynska A. Ocena zawartości wybranych biopierwiastków w wartywach. Roczn Pzh. 2008;59(2):179–186.
- 43.
Kołota E, Adamczevska-Sowińska K. Burak ćwikłowy, liściowy. Warszawa: Hortpress; 2006.
- 44. Lindow CW, Peterson WH. The manganese content of plant and animal materials. J Biol Chem. 1927;169–176.
- 45. Siener R, Hönow R, Seidler A, Voss S, Hesse A. Oxalate contents of species of the Polygonaceae, Amaranthaceae and Chenopodiaceae families. Food Chem. 2006;98:220–224.
- 46. Aulakh MS, Malhi SS. Interactions of nitrogen with other nutrients and water: effect on crop yield and quality, nutrient use efficiency, carbon sequestration, and environmental pollution. Adv Agron. 2005;86:342–409.
- 47.
Bergmann W. Nutritional disorders of plants. Jena, Stuttgart, New York: Gustav Fischer Verlag; 1992.
- 48. Madhava Rao KV, Raghavendra AS, Janardhan Reddy K. Physiology and molecular biology of stress tolerance in plants. Dordrecht: Springer; 2006. pp. 187–217.
- 49. Kadar I, Fekete S, Radics L. Effect of mineral fertilisation on the yield and quality of pea (Pisum sativum L.). Novenytermeles. 2003;52(2):229–242.
- 50. Ranade-Malvi U. Interaction of micronutrients with major nutrients with special reference to potassium. Karnataka J Agric Sci. 2011;24(1):106–109.
- 51. Herak Ćustić M, Petek M, Toth N, Poljak M, Ćosić T. Effects of organic and mineral fertilization on NPK status in soil and plant, and yield of beetroot (Beta vulgaris var. conditiva). Cereal Res Commun. 2007;35(2):449–452.
- 52. Yamaguchi T, Sato T, Katoh M. Post-depositional changes in elemental leaching from recovered soils separated from disaster waste and tsunami deposits generated by the Great East Japan Earthquake and tsunami. J Environ Manage. 2019;233:89–96. pmid:30572267
- 53. Pavlov A, Georgiev V, Ilieva M. Betalain biosynthesis by red beet (Beta vulgaris L.) hairy root culture. Process Biochem. 2005;40:1531–1533.
- 54. Diacono M, Montemurro F. Long-term effects of organic amendments on soil fertility. A review. Agron Sustain Dev. 2010;30:401–422.
- 55. Gluhić D, Herak Ćustić M, Petek M, Čoga L, Slunjski S, Sinčić M. The content of Mg, K and Ca ions in vine leaf under foliar application of magnesium on calcareous soils. Agric Conspec Sci. 2009;74(2):81–84.
- 56.
Regulation (EU) No 1169/2011 of the European Parliament and of the Council of 25 October 2011 on the provision of food information to consumers, amending Regulations (EC) No 1924/2006 and (EC) No 1925/2006 of the European Parliament and of the Council, and repealing Commission Directive 87/250/EEC, Council Directive 90/496/EEC, Commission Directive 1999/10/EC, Directive 2000/13/EC of the European Parliament and of the Council, Commission Directives 2002/67/EC and 2008/5/EC and Commission Regulation (EC) No 608/2004.
- 57. Flynn A, Moreiras O, Stehle P, Fletcher RJ, Müller DJG, Rolland V. Vitamins and minerals: a model for safe addition to foods. Eur J Nutr. 2003;42:118–130. pmid:12638033
- 58.
Institute of Medicine. Dietary reference intakes for calcium, phosphorus and magnesium. Washington: National Academy Press; 1997.
- 59.
Institute of Medicine. Dietary reference intakes for copper, iron, manganese and zinc. 2001.
- 60.
Institute of Medicine. Dietary reference intakes for potassium. Washington: National Academy Press; 2004.
- 61.
WHO/FAO. Vitamin and mineral requirements in human nutrition. Geneva/Rome: World Health Organization/Food and Agriculture Organization of the United Nations; 2004. pp. 338–339.