Next Article in Journal
An Ongoing Blended Long-Term Vegetation Health Product for Monitoring Global Food Security
Previous Article in Journal
15N-Fertilizer Recovery in Maize as an Additional Strategy for Understanding Nitrogen Fertilization Management with Blends of Controlled-Release and Conventional Urea
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Biofertilizers Enhance Quality of Onion

1
Department of Vegetable Sciences and Floriculture, Mendel University in Brno, Valticka 337, 69144 Lednice, Czech Republic
2
Department of Horticulture, University of Agriculture in Krakow, 31-425 Kraków, Poland
*
Author to whom correspondence should be addressed.
Agronomy 2020, 10(12), 1937; https://doi.org/10.3390/agronomy10121937
Submission received: 13 November 2020 / Revised: 4 December 2020 / Accepted: 7 December 2020 / Published: 9 December 2020

Abstract

:
This investigation was conducted to determine the effect of organic fertilizers on the content of chlorophyll a, chlorophyll b, antioxidant activity, crude fibre, and zinc in two onion cultivars, Stuttgarter Riesen and Rote Laaer, during 2016, 2017, and 2018. In this research, the following treatments were used: B-Stimul (contains Azospirillum Tarrand et al., Azotobacter Beij., Bacillus Cohn, Chlorella vulgaris Beij., and Herbaspirillum Baldani et al.), EkoBooster 2 (contains biostimulators and mineral salts of nitrogen, phosphorus, and potassium) and Vermifit A (extract of compost of Californian earthworm). The results showed that the application of biofertilizers to onion resulted in the highest chlorophyll b content in 2017 in Stuttgarter Riesen. EkoBooster 2 positively affected crude fibre content in both cultivars, but only in 2016. Antioxidant activity was not significantly affected by the interaction of experimental factors. The application of the biostimulating fertilizers can have a positive impact on the quality parameters of onion, but the kind of fertilizer must be suited to seasonal conditions and the cultivar.

1. Introduction

Onion (Allium cepa L.) is considered to be an economically important vegetable grown worldwide and used year-round, fresh, and processed. Onion contains carbohydrates, vitamins, minerals, antioxidants, and essential oils [1,2] and can be successfully grown in an organic production system. Organic fertilizers improve the chemical and physical properties of onion, namely the content of minerals and total soluble solids [3]. Organic fertilizers contain nutrients necessary for the balanced growth and development of plants, moreover, they also improve the physical (absorption, soil friability, granulometric composition), biological (microorganism biodiversity and abundance), and chemical properties of the soil (pH, Corg, organic matter, available forms of micro and macroelements, soil enzyme activity) [4,5]. This can be attributed to the increase in availability which allows onion plants, forming weak and shallow root systems, to absorb more N and effectively synthesize more chlorophylls and carotenoids [6]. Chlorophylls are one of the strong antioxidant substances in a Plant Kingdom. Thus, chlorophyll adding to human food ratio leads to a significant decrease in oxidative effects induced by carcinogens [7]. Crude fibre covers the quantity of indigestible cellulose, lignin, and other carbohydrates indigestible for human digestive enzymes. In plants, crude fibre is a main component of cell walls, useful for the human diet because of antidiabetic potential as well as a source of nutrients for the gut microflora [8]. The content of crude fibre in onion depends on origin and genotype, for example, Bhattacharjee et al. [9] determined that fibre was higher in the Bangladeshi onion (26.5 g kg−1) compared to those of Indian origin (16.5 g kg−1). However, Modu et al. [10], studying the content of crude fibre in local white, yellow, and red onions, did not find any significant difference in crude fibre content between cultivars. According to Krishnamurthy et al. [11], vegetables with a higher amount of crude fibre improve protection against constipation. They also protect humans against cardiovascular diseases because soluble fibre lowers levels of artery-clogging cholesterol in the bloodstream. Manas [12] determined that onion is a species with a high content of flavonoid compounds (mainly quercetin and its conjugates) and sulphur compounds (i.e., thiosulphinates), both of which have a high antioxidant activity. The content of antioxidants in onion is genotype-dependent [13]. A study evaluating antioxidant activity in red and white onion cultivars emphasized that the extract of red-husk genotypes possessed higher antioxidant activity (63.8% to 77.6%) compared to the extract of white-husk cultivars (58.1% to 66.4%) [14]. Feiyue et al. [15] found that antioxidant activity was higher in organic onion, and the flavonols were up to 20% higher in organic onion bulbs compared to the conventionally grown ones. The excessive application of nitrogen and other inorganic fertilizers and organic manures to vegetables can lead to the modification of crops’ mineral composition with respect to macro and microelements and heavy metals, although zinc toxicity was not reported. Zinc takes part in the formation of metalloenzymes, RNA conformation, membrane stabilization, and protein metabolism, and its dietary recommended parenteral nutrition dose is 2.5–4.0 mg per day, although higher amounts may be needed as the enteral recommended dietary allowance is 8–11 mg per day [16]. Zinc has an important role in photosynthesis due to the direct effect on chlorophyll biosynthesis [17]. Therefore, the monitoring of Zn content in onion was considered to be an important factor in the evaluation of chlorophyll synthesis in onion. Although the production of biofertilizers has become increasingly popular and economically significant nowadays, the reports on the effectiveness of biofertilizers are inconclusive because of many factors affecting plant-soil interactions in agricultural ecosystems. Onion has a good response to biofertilizers due to root system morphology, so the novelty of this study is a comparison of onion reaction to different biofertilizers and expanding knowledge on the relationship between biofertilizer and quality of onion in subsequent growing seasons.
The main objective of this investigation was to study the effect of organic fertilizers on the content of chlorophyll a, chlorophyll b, crude fibre, antioxidant activity, and zinc in two onion cultivars.

2. Materials and Methods

The trials were conducted according to the Latin square system in four repetitions at the certified organic experimental field of the Faculty of Horticulture in Lednice, Mendel University in Brno, Czech Republic, (48°47′36″ N, 16°47′48″ E) during 2016, 2017, and 2018. Two onion cultivars, Stuttgarter Riesen and Rote Laaer, provided by Permaland Company (Czech Republic), were used in this trial. Stuttgarter Riesen is medium-early, the yellow-skinned bulbs grow up to 60–90 g in weight, and they are suitable for fresh use and winter storage. Rote Laaer is valued for the attractive violet-red colour of its husks and its delicate taste. The bulbs were round and well-stored.
The experimental treatments involved the foliar application of three organic fertilizers: B-Stimul, EkoBooster 2, and VermiFit A. B-Stimul (Rawat Ltd., Brno, Czech Republic) contains a mixture of the following bacterial and algal cultures with a concentration of cfu g−1: Azospirillum (min. 3.6 × 107), Azotobacter (min. 8.9 × 107), Bacillus (min. 9.4 × 108), Chlorella vulgaris (min. 2.5 × 107), and Herbaspirillum (min. 2.7 × 107). Ekobooster 2 (Ekopatent company, Vrbas, Serbia) contains 7.8% of organic matter: N 9%, P 1%, K 4%. Vermifit A (Biocont Laboratory, Ltd., Modřice, Czech Republic) is an extract of compost from Californian earthworms (Eisenia foetida), peat, nutrients in available forms, plant hormones, enzymes, amino acids, and sugars. The composition is as follows: pH/H2O—8.2, total nitrogen N—1.9%, total potassium as K2O—35.6%, total phosphorus as P2O5—2.8%, dry matter 0.95%. According to the fertilizer company’s instructions, VermiFit A was applied four times during the vegetation period while B-Stimul and EkoBooster 2 were applied three times in a form of foliar spraying with a dose per 1 m2: VermiFit A 0.4 mL in 39.6 mL of water, B-Stimul 3.38 mg in 36.2 mL of water, EkoBooster 2 0.125 mL in 25 mL of water.
The experimental plot had a size of 4 m2 and plant spacing was 0.3 × 0.035 m. Each treatment was repeated four times. Sowing into plugs was done on 15 to 16 March in all experimental years. The plants were sown in greenhouse containers at a depth of 20 mm into sowing substrate ProfiMix (Agro CS, Ltd., Říkov, Czech Republic). The containers were kept in the greenhouse under a temperature of 20/16 °C for 7 weeks. Transplanting to the field was performed on 4 May 2016, 10 May 2017, and 9 May 2018. Every year, harvesting was done manually, on 6 August 2016, 12 August 2017, and 13 August 2018. Every year, weed control was done mechanically three times and sprinkle irrigation was applied according to weather conditions.

2.1. Laboratory Analyses

Ten plants were randomly selected for chemical analyses. The parameters which were considered for the determination were chlorophyll a, chlorophyll b in leaves, antioxidant activity in bulbs, crude fibre, and zinc in bulbs at the laboratory of the Faculty of Horticulture in Lednice, Mendel University in Brno, Czech Republic. The determination of chlorophyll a and chlorophyll b was done according to Holm [18] methodology by using a microwave extraction system (Start E, Milestone, Germany). The absorbance was analysed at 644 nm for chlorophyll a and 662 nm for chlorophyll b by spectrophotometer Specord 50 PLUS (Analytik Jena, Jena, Germany). The photosynthetic pigments were calculated using the equations proposed by Holm [18] and expressed as mg g−1 of dry weight (DW). The total antioxidant capacity was determined by the FRAP method [19]. The reaction was analysed at 593 nm. Trolox (6-hydroxy-2.5.7.8-tetramethylchroman-2-carboxylic acid) was used as a standard. The results were expressed in g of Trolox equivalents per 100 g of DW (g TE 100 g−1 DW). Crude fibre was determined by using the FibreBag system (Gerhard, Königswinter, Germany). A determination was performed according to the AOCS [20] methodology. The cups with samples were dried at 105 °C for 12 h. The weight of the cups with dried samples was recorded as χ in the protocol. To determine the content of zinc, 0.2 g of dry samples with 6 mL HNO3+ 2 mL H2O2 were used. The determination was performed by colorimetric analysis on an Eca-Flow instrument (Istran, Bratislava, Slovakia). The results of the zinc content are expressed as μg kg−1 fresh weight (FW).

2.2. Weather Conditions in Onion Growing Season

During the vegetation period (May–August) in 2016, 2017, and 2018, the amount of rainfall and sunshine duration (defined as the number of sunny hours), as well as mean monthly temperature, was measured (Figure 1). The highest amount of rainfall was in 2016, especially in July (114 mm), in comparison to this month in 2017 (71.7 mm) and 2018 (62.9 mm). The mean monthly temperature (May–August) was 18.9 °C in 2016, 20.2 °C in 2017, and 21 °C in 2018, respectively. The 2016 year was represented by a lower sunshine duration from May–August (mean: 249.6 h) compared to 2017 (284 h), and 2018 (301 h).

2.3. Soil Analyses

Before transplanting, soil samples were taken for the determination of N levels in the soil from the depth of 0.3 m. The determination of N-NO2, N-NO3, N-NH4, and pH was performed according to [21] at the laboratory of the Faculty of Horticulture in Lednice, Mendel University in Brno, Czech Republic. Onion requires 60–70 N ha−1 for integrated production. According to agrochemical analyses in 2016, the N was lower than what is usually required by onion plants (21.8 kg N ha−1). Due to that 50 g N per 1 m2, Universal Organic Fertilizer 8-3-8 (Rašelina Ltd., Soběslav, Czech Republic) was applied per 1 m2 after transplanting. Agrochemical analyses in 2017 showed that the content of N in the soil was higher than what is usually required for growing onions (101.6 kg N ha−1), while in 2018, the content of N in the soil was at the optimal level required by onions (65.9 kg N ha−1) and no fertilizer was applied. The level of pH (H2O) was 7.18 in 2016, 7.16 in 2017, and 6.81 in 2018.

2.4. Statistical Analyses

Data were evaluated by a two-way analysis of variance (ANOVA) using PC software Statistica CZ v. 12 (StatSoft CZ, Prague, Czech Republic). The vertical bars denoted standard error. The differences between the cultivars and treatments were estimated through Fisher’s LSD test at p ≤ 0.05. The cluster analysis (CA) and principal component analysis (PCA) were performed to obtain precise analysis of the data, using Statistica 13.3 software (TIBCO Software Inc., Tulsa, OK, USA).

3. Results

3.1. Chlorophyll a and Chlorophyll b Content

In general, the distribution of chlorophyll a was similar to chlorophyll b, and it showed significant differences especially between cultivars and the years of research, but the interaction of three experimental factors was significant only for chlorophyll b (Table 1).
The effect of treatments on chlorophyll a and chlorophyll b content in the leaf blades of both cultivars is shown in Figure 2. Analysis of the main effects showed that plants contained higher amounts of chlorophylls in 2017, and the most effective treatment in this respect was EkoBooster 2. Stuttgarter Riesen exceeded Rote Laaer concerning the level of photosynthetically active pigments. For the Stuttgarter Riesen in 2018, a higher content of chlorophyll a and chlorophyll b was found in the plants treated with biostimulating fertilizers compared to the control. Rote Laaer contained the highest levels of both chlorophylls in the control and the EkoBooster 2 treatment in 2017.

3.2. Crude Fibre

The highest content of crude fibre in both cultivars was found in 2016 (Figure 3). For Stuttgarter Riesen there was no significant difference between treatments in 2017, while in 2018 there were no significant differences between the control, B-Stimul, and VermiFit A. The application of EkoBooster 2 in Stuttgarter Riesen resulted in the highest content of crude fibre (48.82 g kg−1 DW), while the lowest was found in the treatment B-Stimul (27.81 g kg−1 DW) in 2016. In the Rote Laaer cultivar, the highest content of crude fibre was found in the treatment EkoBooster 2 (50.79 g kg−1 DW) in 2016.

3.3. Antioxidant Activity

The interaction of experimental treatments was not significant concerning the total antioxidant activity of onion bulbs. Analysis of the main effects showed that the highest level of antioxidant activity was found in 2017, followed by 2016 and 2018. The B-Stimul and VermiFit A treatments caused significantly higher antioxidant activity in the onion bulbs compared to the control and EkoBooster 2 (Figure 4). The bulbs of Stuttgarter Riesen were characterized by lower antioxidant activity compared to Rote Laaer, and this was confirmed by the main effects analysis.

3.4. Zinc Content

The content of zinc was analysed in the bulb samples and, according to the results (Figure 5), it can be stated that the application of VermiFit A resulted in the lowest content of zinc in 2016: 783.52 μg kg−1 FW. The highest content of zinc was found in the control as well as the Rote Laaer plants treated with B-Stimul in 2018. In the case of the cultivar Rote Laaer, the lowest content of zinc was found in 2017 for all treatments.

3.5. Cluster and Principal Component Analysis

The component analysis was used to determine the similarity between the objects in the study, namely the biostimulant fertilizers, and this was determined by their location in the multidimensional space. The results are presented in the form of dendrograms (Figure 6), and separately for cultivars. In the dendrograms, the x-axis shows the distances between the objects while the y-axis represents the analysed treatments. The distance was calculated using the Ward agglomeration method.
On the basis of the cluster analysis (CA) method, two clusters were distinguished for Stuttgarter Riesen, with the first formed by B-Stimul and Vermifit A and the second by the control and EkoBooster 2. The components of the one main cluster distinguished for Rote Laaer were VermiFit A and the control treatments. The fact that the mentioned objects belong to particular clusters proves their considerable similarity within the group in question, which can be identified with the amount of chlorophylls, antioxidant activity, and zinc content in the onion bulbs. The short arms of the dendrogram within the cluster corresponding to the chemical composition of onion bulbs and leaf blades represent the highest similarity between these treatments (Miller and Miller, 1999). The CA was complemented with principal component analysis (PCA) to describe the correlation between the measured parameters and reduce these data to a minimum that was necessary to describe the correlations between the parameters. From PCA, it was found that 76.1% of the variability in the results presented can be described by means of two main components of Stuttgarter Riesen, and 75.3% of Rote Laaer (Figure 7).
The size of the assigned load corresponds to the correlation coefficient of the component with the input variable. On this basis, it was concluded that the chlorophyll b showed the most significant influence on the PC1 (the first principal component) for Stuttgarter Riesen, because this parameter had the greatest loading value (0.498) in PC1 and the chlorophyll a contributed the most significantly in the PC1 of Rote Laaer (0.459). The conversely directed eigenvectors of zinc content and antioxidant activity in Figure 7b illustrate the negative correlation between these parameters for Rote Laaer, with correlation coefficient value r = −0.168, p ≤ 0.05. Both cultivars also showed a negative correlation between zinc content and chlorophyll a: chlorophyll b ratio (r = −0.232, p ≤ 0.005 for Stuttgarter Riesen and r = −0.184, p = 0.027 for Rote Laaer).

4. Discussion

The genetic variability for total chlorophyll pigments among different Allium species and cultivars has previously been reported by Stajner et al. [22]. The leaf tissues of onion cultivars contain nutritionally important carotenoid and chlorophyll pigments. The current study demonstrated high concentrations of these pigments in onion leaves, especially in 2017. These results strongly imply that organic matter and the content of N in the soil positively affected the content of chlorophyll pigments in onion bulbs, especially in 2017 where the highest N soil content was noted (151.6 kg N ha−1). Additionally, EkoBooster 2 seemed to be the most effective source of N and microelements favouring pigment synthesis. The effect of this fertilizer was more spectacular than the remaining treatments B-Stimul (based on bacterial and algal cultures) and VermiFit A (compost from Californian earthworms). Beneficial microorganisms are known to be the most effective as plant stimulants in stress conditions, and EkoBooster 2 is composed of organic matter and NPK (nitrogen, phosphorus, potassium) in available forms, which led to the optimal nutritional status of onion plants [23,24]. Hanci and Cebeci [25] noted that drought, occurring especially during the vegetative phase of the onion life cycle, significantly decreased chlorophyll a and b content and total chlorophyll content, but not the chlorophyll a/b ratio, indicating that chlorophyll a was more sensitive to drought. In the conditions of the present experiment, the rainfall distribution was rather constant in 2017 when the level of chlorophylls was the highest and the chlorophyll a:b ratio was low.
Onions, like other vegetables, are composed mainly of water with small quantities of dietary fibre. Nevertheless, onion showed a more beneficial soluble/insoluble dietary fibre ratio than other vegetables, depending on tissue. Fibre from brown skin was mainly insoluble, whereas fibre from the outer fleshy leaves showed a more balanced composition with a soluble/insoluble dietary fibre ratio of 1:3 [26]. The content of crude fibre in both cultivars was similar, as reported by Akeem et al. [27], but lower than the results of Modu et al. [10]. In both cultivars, the mean for treatments’ highest content was found in 2016. The year 2016 recorded the highest amount of precipitation during growing season (63.47 mm). According to Ombodi et al. [28], fibre and ash content were found to be the most stable nutritional characteristics of onions, affected neither by the environmental conditions nor by the irrigation. The cultivar Rote Laaer showed a higher content of crude fibre in all years in comparison to the cultivar Stuttgarter Riesen. This was due to the genetic variability between cultivars. Similar results were reported by Bhattacharjee et al. [9]. In the human diet, the recommended amounts of dietary fibre for health promotion range from 25 to 38 g per day [29]. So, both of the investigated onion cultivars are important sources of fibre in the human diet.
The red onion cultivar Rote Laaer was characterized by higher antioxidant activity compared to the yellow onion cultivar Stuttgarter Riesen. The higher antioxidant activity in red onion was reported by numerous researchers [30,31] and can be related to anthocyanin content, correlated with antioxidant activity [32]. Prakash et al. [33] and Sidhu [34] compared the outer, middle, and inner layers of onions with different husk colours for their specific phenolic contents, contributing to total antioxidant activity. Total antioxidant activity was the highest in the outmost layers of the bulbs than in their middle and inner layers. Regardless of the layers, they found that red onions had the highest quercetin and kaempherol contents. Red onions are rich in anthocyanins, while yellow onions have a high concentration of flavonols, quercetin, and kaempherol. The results of Gökçe et al. [35] confirmed that red onions, in general, have higher antioxidant activities, although some yellow cultivars might have high antioxidant activities linked to high total phenolics content. Zinc uptake and accumulation is frequently used to evaluate the nutritional quality of plants, including onion, which is highly sensitive to Zn deficiency, simultaneously showing the high responsiveness to Zn supply [36,37,38]. Many factors affect the micronutrient composition of onion bulbs, such as environmental and agronomic conditions, cultivar, and ripening stage [39]. Results obtained by Yogita and Ram (2012) [40] on the application of inorganic fertilizers with biofertilizers to onion showed the significant effect of mycorrhizal fungi and Azotobacter on phosphorus and calcium content in onion bulbs. Zn acts as a structural and catalytic component of proteins and enzymes, as well as a co-factor for chlorophyll pigment biosynthesis [16]. The present research did not confirm a general correlation between Zn and chlorophyll content, probably due to the differentiated soil biofertilizers effect, but the negative correlation between Zn and the chl. a : chl. b ratio pointed out a stronger positive relationship between Zn and chlorophyll a synthesis. Zn was reported as an element that increases the antioxidant enzyme activity in onion [41], and this research provides an explanation for the negative correlation noted for Zn content and antioxidant activity of onion bulbs in the present study. The genetic variability may be one of the possible reasons for differences between the onion cultivars’ Zn content in bulbs. Cota et al. [42] and Akinwande and Olatunde [43] reported values for microelements including zinc in the bulbs of onion cultivars, and red skinned onions had the highest content of all the minerals determined. The present study demonstrated higher zinc content in yellow-skinned Stuttgarter Riesen. In every year, the content of Zn in both cultivars was in line with the recommend daily allowance for an adult person [16]. Moreover, both onion cultivars have a promoting influence on the bioaccessibility of iron and zinc from food grains, so dietary onion improves the bioavailability of trace minerals [44].

5. Conclusions

The biofertilizers applied as a foliar spray to two onion cultivars modified the chemical composition of the onion bulbs/leaves in different manners. The environmental conditions of growing, unrepeatable in a subsequent vegetation period, resulted in the diverse response of onion plants, which was also genotype-dependent. Growers can use limited methods of fertilizing and supporting plant nutrition in the organic farming system. However, the biostimulants, which are one of the significantly supported forms of nutritional management, may not ensure an adequate effect on the internal quality of production. In general, biofertilizers can be successfully applied to onion plants under conditions which are favourable for the effective action of a particular kind of fertilizer, but the expectations of their potential should be reasonable.

Author Contributions

B.P. conducted the experimental work, collected and analysed data, wrote the paper; R.P. gave suggestions and equally contributed to manuscript writing; A.S. critically evaluated the manuscript and contributed to improving the quality of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Mendel University in Brno, Czech Republic, project IGA ZF/2020-AP004 and supported by infrastructure project CZ.02.1.01/0.0/0.0/16_017/0002334 Research Infrastructure for Young Scientists, co-financed from Operational Programme Research, Development and Education, Ministry of Education, CZ.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Roldan, E.; Sanchez-Moreno, C.; de Ancos, B.; Cano, M.P. Characterization of onion (Allium cepa L.) by-products as food ingredients with antioxidant and antibrowning properties. Food Chem. 2008, 108, 907–916. [Google Scholar] [CrossRef] [PubMed]
  2. Sękara, A.; Pokluda, R.; Del Vacchio, L.; Somma, S.; Caruso, G. Interactions among genotype, environment and agronomic practices on production and quality of storage onion (Allium cepa L.)—A review. Hort. Sci. (Prague) 2017, 44, 201–212. [Google Scholar] [CrossRef] [Green Version]
  3. Gadelrabh, H.M.; Elamin, S.M. Effect of different organic fertilizers on growth, yield and total soluble solid of the onion (Allium cepa L.) variety Baftaim-s. J. Agric. Vet. Sci. 2013, 14, 61–67. [Google Scholar]
  4. Ibrahim, A. The effect of inorganic fertilizer on onion production. Int. J. Biol. Sci. 2014, 1, 21–29. [Google Scholar]
  5. Enping, Z.; Yu, D.; Fulei, T.; Shuhong, Z. Effects of long-term nitrogen and organic fertilization on antioxidants content of tomato fruits. Hort. J. 2016, 3, 8–12. [Google Scholar]
  6. Shedeed, I.S.; Sayed-el, S.A.A.; Doaa, M.A.B. Effectiveness of bio-fertilizers with organic matter on the growth, yield and nutrient content of onion (Allium cepa L.) plants. Eur. Inter. J. Sci.Tech. 2014, 3, 115–122. [Google Scholar]
  7. Moldovan, C.; Ianculov, I.; Nicoleta, G.H.; Delia, D.; Crăiniceanuc, E.; Drugă, M.; Liana, A.; Moldovan, G.Z. Influence of chlorophyll content from onion (Allium cepa) after selenium and zinc adding. J. Agroaliment. Proc. Technol. 2009, 15, 437–440. [Google Scholar]
  8. Benítez, V.; Mollá, E.; Martín-Cabrejas, M.A.; Aguilera, Y.; Esteban, R.M. Physicochemical properties and in vitro antidiabetic potential of fibre concentrates from onion by-products. J. Funct. Foods 2017, 36, 34–42. [Google Scholar] [CrossRef]
  9. Bhattacharjee, S.; Abida, S.; Muhammad, H.S. Analysis of the proximate composition and energy values of two varieties of onion (Allium cepa L.) bulbs of different origin: A comparative study. Int. J. Food Sci. 2013, 2, 246–253. [Google Scholar] [CrossRef] [Green Version]
  10. Modu, S.; Chamba, G.; Falmata, A.; Laminu, H.; Babagana, M.; Hauwa, H. Studies on the effect of drying and varietal differences on chemical composition of some selected onion cultivars. Nutr. Res. 2015, 2, 376–385. [Google Scholar]
  11. Krishnamurthy, V.M.; Wei, G.; Baird, B.C.; Murtaugh, M.; Chonchol, M.B.; Raphael, K.L.; Greene, T.; Beddhu, S. High dietary fibre intake is associated with decreased inflammation and all-cause mortality in patients with chronic kidney disease. Kidney Inter. 2012, 81, 300–306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Manas, D. The determination of vitamin C, total phenol and antioxidant activity of some commonly cooking spices crops used in west Bengal. Int. J. Plant Physiol. Biochem. 2014, 6, 66–70. [Google Scholar] [CrossRef]
  13. Lu, X.; Jun, W.; Al-Qadiri, H.M.; Carolyn, F.R.; Joseph, R.P.; Juming, T.; Barbara, A.R. Determination of total phenolic content and antioxidant capacity of onion (Allium cepa) and shallot (Allium oschaninii) using infrared spectroscopy. Food Chem. 2011, 129, 637–644. [Google Scholar] [CrossRef] [PubMed]
  14. Kandoliya, U.K.; Bodar, N.P.; Bajaniya, V.K.; Bhadja, N.V.; Golakiya, B.A. Determination of nutritional value and antioxidant from bulbs of different onion (Allium cepa) variety. Int. J. Curr. Microbiol. Appl. Sci. 2015, 4, 635–641. [Google Scholar]
  15. Feiyue, R.; Kim, R.; Joseph, P.K.; Gaffney, M.; Hossain, M.; Rai, D.K. Higher antioxidant activity, total flavonols, and specific quercetin glucosides in two different onion (Allium cepa L.) varieties grown under organic production: Results from a 6-year field study. J. Agric. Food Chem. 2017, 65, 5122–5132. [Google Scholar]
  16. Sriram, K.; Lonchyna, V.A. Micronutrient supplementation in adult nutrition therapy: Practical considerations. J. Parenter. Enteral Nutr. 2009, 33, 548–562. [Google Scholar] [CrossRef] [Green Version]
  17. Kosesakal, T.; Unal, M. Role of Zn deficiency in photosynthetic pigments and peroxidase activity of tomato seedlings IUFS. J. Biol. 2009, 68, 113–120. [Google Scholar]
  18. Holm, G. Chlorophyll mutations in barley. Acta Agric. Scand. 1954, 4, 457–471. [Google Scholar] [CrossRef]
  19. Zloch, Z.; Čelakovský, J.; Aujezdska, A. Determination of Polyphenol Content and Total Antioxidant Capacity in Plant Food; Final Report Implementation of the DANONE 2004 Research Project; Plzeň, Czech Republic, 2004; Available online: https://docplayer.cz/14474044-Stanoveni-obsahu-polyfenolu-a-celkove-antioxidacni-kapacity-v-potravinach-rostlinneho-puvodu-z-zloch-j-celakovsky-a.html (accessed on 30 December 2004).
  20. AOCS. Crude Fibre Analysis in Feeds Filter Bag Technique. 2006. Available online: http://www.ssco.com.tw/Ankom/PDF_file/Crude%20Fiber%20Method%20A200.pdf (accessed on 21 October 2005).
  21. Zbíral, J.; Malý, S.; Váňa, M. Soil Analysis III. In Central Institute for Supervising and Testing in Agriculture; Soil analysis: Brno, Czech Republic, 2011. (In Czech) [Google Scholar]
  22. Stajner, D.; Milic, N.; Candanovic-Brunet, J.; Kapor, A.; Stajner, M.; Popovic, B.M. Exploring allium species as a source of potential medicinal agents. Phytother. Res. 2006, 20, 581–584. [Google Scholar] [CrossRef]
  23. Nassar, R.M.A.; Seleem, E.A.; Caruso, G.; Sekara, A.; Abdelhamid, M.T. The Nitrogen-fixing bacteria—Effctive enhancers of growth and chemical composition of Egyptian henbane under varied mineral N nutrition. Agronomy 2020, 10, 921. [Google Scholar] [CrossRef]
  24. Petrovic, B.; Kopta, T.; Pokluda, R. Effect of biofertilizers on yield and morphological parameters of onion cultivars. Folia Hort. 2019, 31, 51–59. [Google Scholar] [CrossRef] [Green Version]
  25. Hanci, F.; Cebeci, E. Investigation of proline, chlorophyll and carotenoids changes under drought stress in some onion (Allium cepa L.) cultivars. Türk Tarım ve Doğa Bilimleri Dergisi 2014, 2, 1499–1504. [Google Scholar]
  26. Jaime, L.; Mollá, E.; Fernández, A.; Martín-Cabrejas, M.A.; López-Andréu, F.J.; Esteban, R.M. Structural carbohydrate differences and potential source of dietary fiber of onion (Allium cepa L.) tissues. J. Agric. Food Chem. 2002, 50, 122–128. [Google Scholar] [CrossRef] [PubMed]
  27. Akeem, A.; Azeez, O.Y. Phytochemical screening and proximate analysis of newbouldia laevis and allium sativum. Nigerian J. Anim. Sci. 2016, 1, 242–256. [Google Scholar]
  28. Ombodi, A.; Lugasi, A.; Daood, H.G.; Berki, M.; Helyes, L. Water supply and temperature effects on some nutritive constituents of direct sown onion. Not. Bot. Horti Agrobot. Cluj-Napoca 2016, 44, 245–249. [Google Scholar] [CrossRef] [Green Version]
  29. Available online: https://ec.europa.eu/jrc/en/health-knowledge-gateway/promotion-prevention/nutrition/fibre (accessed on 10 November 2020).
  30. Sirag, N.; Imd, M.T.; Mohamed, A.; Alaa, M. Determination of antioxidant activity of some varieties of onion (Allium cepa L.) grown in Sudan. Gezira J. Health Sci. 2015, 2, 1–7. [Google Scholar] [CrossRef]
  31. Cheng, A.; Xiangyan, C.; Qiong, J.; Wenliang, W.; John, S.; Yaobo, L. Comparison of phenolic content and antioxidant capacity of red and yellow onions. Czech J. Food Sci. 2013, 31, 501–508. [Google Scholar] [CrossRef]
  32. Zhang, S.L.; Peng, D.E.N.G.; Xu, Y.C.; Lü, S.W.; Wang, J.J. Quantification and analysis of anthocyanin and flavonoids compositions, and antioxidant activities in onions with three different colors. J. Integr. Agric. 2016, 15, 2175–2181. [Google Scholar] [CrossRef] [Green Version]
  33. Prakash, D.; Singh, B.N.; Upadhyay, G. Antioxidant and free radical scavenging activities of phenols from onion (Allium cepa). Food Chem. 2007, 102, 1389–1393. [Google Scholar] [CrossRef]
  34. Sidhu, J.S.; Ali, M.; Al-Rashdan, A.; Ahmed, N. Onion (Allium cepa L.) is potentially a good source of important antioxidants. J. Food Sci. Technol. 2019, 56, 1811–1819. [Google Scholar] [CrossRef]
  35. Gökçe, A.F.; Kaya, C.; Serçe, S.; Özgen, M. Effect of scale color on the antioxidant capacity of onions. Sci. Hort. 2010, 123, 431–435. [Google Scholar] [CrossRef]
  36. Gamelli, H.H. The effect of some foliar fertilizers application on growth, bulb plant biomass, quality and storage ability of Giza 20 onion cultivar (Allium cepa L.). Ann. Agric. Sci. Moshtohor. 2000, 38, 1727–1737. [Google Scholar]
  37. Machado, R.M.A.; Shahidian, S.; Pivetta, C.R.; Oliveira, M.R.G. Nitrogen fertilization effects on rooting pattern and plant biomass of intermediate-day onions bulb in Alentejo region. Rev. Ciênc. Agrárias. 2009, 32, 113–122. [Google Scholar]
  38. Almendros, P.; Obrador, A.; Gonzalez, D.; Alvarez, J.M. Biofortification of zinc in onions (Allium cepa L.) and soil Zn status by the application of different organic Zn complexes. Sci. Hortic. 2015, 186, 254–265. [Google Scholar] [CrossRef]
  39. Mlcek, J.; Valsikova, M.; Druzbikova, H.; Ryant, P.; Jurikova, T.; Sochor, J.; Borkovcova, M. The antioxidant capacity and macroelement content of several onion cultivars. Turk. J. Agric. For. 2015, 39, 999–1004. [Google Scholar] [CrossRef]
  40. Yogita; Ram, R.B. Effect of chemical and bio-fertilizers on quality of onion. HortFlora Res. Spectrum. 2012, 1, 367–370. [Google Scholar]
  41. Yatsenko, V.; Ulianych, O.; Yanowskiy, Y. Effect of iron, zinc and boron on the growth, physiological state, productivity and storability of Allium sativum L. Ukr. J. Ecol. 2020, 10, 33–42. [Google Scholar] [CrossRef]
  42. Cota, J.; Gvozdanovic-Varga, J.; Hadžic, A.; Petrovic, A.; Saraic, E.; Savic, A.; Cota, J. Yield and mineral composition of two new onion varieties from Bosnia and Herzegovina. In Proceedings of the Fourth International Scientific Symposium, Agrosym, Jahorina, Bosnia and Herzegovina, 3–6 October 2013; pp. 251–256. [Google Scholar]
  43. Akinwande, B.A.; Olatunde, S.J. Comparative evaluation of the mineral profile and other selected components of onion and garlic. Int. Food Res. J. 2015, 22, 332–336. [Google Scholar]
  44. Gautam, S.; Platel, K.; Srinivasan, K. Higher bioaccessibility of iron and zinc from food grains in the presence of garlic and onion. J. Agric. Food Chem. 2010, 58, 8426–8429. [Google Scholar] [CrossRef]
Figure 1. Mean daily temperature and rainfall during the vegetation period of onion in the experimental years 2016, 2017, and 2018.
Figure 1. Mean daily temperature and rainfall during the vegetation period of onion in the experimental years 2016, 2017, and 2018.
Agronomy 10 01937 g001aAgronomy 10 01937 g001b
Figure 2. Chlorophyll a (a) and b (b) content, sum of chlorophylls (c) and chl. a:b ratio (d) depending on the cultivar, treatments, and years of investigation. The data are the mean values of four replications. Different letters denote significant differences: lowercase letters refer to the interaction and capital letters to the main effects (Fisher’s test, p ≤ 0.05). Abbreviations: C—control; BS—B-Stimul; EB—EkoBooster 2; VF—VermiFit A; SR—Stuttgarter Riesen; RL—Rote Laaer.
Figure 2. Chlorophyll a (a) and b (b) content, sum of chlorophylls (c) and chl. a:b ratio (d) depending on the cultivar, treatments, and years of investigation. The data are the mean values of four replications. Different letters denote significant differences: lowercase letters refer to the interaction and capital letters to the main effects (Fisher’s test, p ≤ 0.05). Abbreviations: C—control; BS—B-Stimul; EB—EkoBooster 2; VF—VermiFit A; SR—Stuttgarter Riesen; RL—Rote Laaer.
Agronomy 10 01937 g002aAgronomy 10 01937 g002b
Figure 3. Crude fibre content in onion bulbs of Stuttgarter Riesen (a) and Rote Laaer (b). The data are the mean values of four replications. Different letters denote significant differences (Fisher’s test, p ≤ 0.05). Vertical bars denote standard error.
Figure 3. Crude fibre content in onion bulbs of Stuttgarter Riesen (a) and Rote Laaer (b). The data are the mean values of four replications. Different letters denote significant differences (Fisher’s test, p ≤ 0.05). Vertical bars denote standard error.
Agronomy 10 01937 g003
Figure 4. Antioxidant activity in onion bulbs depending on the cultivar, treatments, and years of investigation. The data give the mean values of four replications. Different letters denote significant differences: lowercase letters refer to the interaction and capital letters to the main effects (Fisher’s test, p ≤ 0.05). Abbreviations: C—control; BS—B-Stimul; EB—EkoBooster 2; VF—VermiFit A; SR—Stuttgarter Riesen; RL—Rote Laaer.
Figure 4. Antioxidant activity in onion bulbs depending on the cultivar, treatments, and years of investigation. The data give the mean values of four replications. Different letters denote significant differences: lowercase letters refer to the interaction and capital letters to the main effects (Fisher’s test, p ≤ 0.05). Abbreviations: C—control; BS—B-Stimul; EB—EkoBooster 2; VF—VermiFit A; SR—Stuttgarter Riesen; RL—Rote Laaer.
Agronomy 10 01937 g004
Figure 5. Zinc content in onion bulbs depending on the cultivar, treatments, and years of investigation. The data give the mean values of four replications. Different letters denote significant differences: lowercase letters refer to the interaction and capital letters to the main effects (Fisher’s test, p ≤ 0.05). Abbreviations: C—control; BS—B-Stimul; EB—EkoBooster 2; VF—VermiFit A; SR—Stuttgarter Riesen; RL—Rote Laaer.
Figure 5. Zinc content in onion bulbs depending on the cultivar, treatments, and years of investigation. The data give the mean values of four replications. Different letters denote significant differences: lowercase letters refer to the interaction and capital letters to the main effects (Fisher’s test, p ≤ 0.05). Abbreviations: C—control; BS—B-Stimul; EB—EkoBooster 2; VF—VermiFit A; SR—Stuttgarter Riesen; RL—Rote Laaer.
Agronomy 10 01937 g005
Figure 6. Dendrogram presenting the similarity between the chemical compositions of Stuttgarter Riesen (a) and Rote Laaer (b) bulbs in relation to the biostimulant fertilizers (Euclidean, Ward’s algorithm).
Figure 6. Dendrogram presenting the similarity between the chemical compositions of Stuttgarter Riesen (a) and Rote Laaer (b) bulbs in relation to the biostimulant fertilizers (Euclidean, Ward’s algorithm).
Agronomy 10 01937 g006
Figure 7. Biplot presenting the correlation between the tested parameters of onion bulbs of investigated cultivars, on a basis of data collected from 3 years of investigations. Stuttgarter Riesen (a) and Rote Laaer (b).
Figure 7. Biplot presenting the correlation between the tested parameters of onion bulbs of investigated cultivars, on a basis of data collected from 3 years of investigations. Stuttgarter Riesen (a) and Rote Laaer (b).
Agronomy 10 01937 g007
Table 1. Results from analysis of variance (ANOVA) relevant to antioxidant activity and Zn content as affected by fertilizer treatment, cultivar, and year of investigation.
Table 1. Results from analysis of variance (ANOVA) relevant to antioxidant activity and Zn content as affected by fertilizer treatment, cultivar, and year of investigation.
ANOVA Source of VariationChlorophyll aChlorophyll bChl. a + bChl. a:bAntioxidant ActivityZn
Treatment (T)*************n.s.
Cultivar (C)******************
Year (Y)******************
T × C*********n.s.n.s.***
C × Y****************
T × Y******************
T × C × Yn.s.********n.s.**
* p ≤ 0.05; ** p ≤ 0.01; *** p ≤ 0.001; n.s.—not significant.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Petrovic, B.; Sękara, A.; Pokluda, R. Biofertilizers Enhance Quality of Onion. Agronomy 2020, 10, 1937. https://doi.org/10.3390/agronomy10121937

AMA Style

Petrovic B, Sękara A, Pokluda R. Biofertilizers Enhance Quality of Onion. Agronomy. 2020; 10(12):1937. https://doi.org/10.3390/agronomy10121937

Chicago/Turabian Style

Petrovic, Bojana, Agnieszka Sękara, and Robert Pokluda. 2020. "Biofertilizers Enhance Quality of Onion" Agronomy 10, no. 12: 1937. https://doi.org/10.3390/agronomy10121937

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop