Next Article in Journal
Spatial Heterogeneity Analysis of Factors on Commuting Carbon Emissions: Evidence from the Shenzhen Metropolitan Area in China
Previous Article in Journal
Andiroba Oil (Carapa guianensis Aubletet) as a Functionalizing Agent for Titica Vine (Heteropsis flexuosa) Nanofibril Films: Biodegradable Products from Species Native to the Amazon Region
Previous Article in Special Issue
Image-Based Phenotyping Study of Wheat Growth and Grain Yield Dependence on Environmental Conditions and Nitrogen Usage in a Multi-Year Field Trial
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Optimizing Nitrogen Nutrient Management for the Sustainable Enhancement of Secondary Metabolites and Yield in Onion Cultivation

Faculty of Agrobiology and Food Resources, Slovak University of Agriculture in Nitra, 2, Tr. A. Hlinku, 94901 Nitra, Slovakia
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(11), 4396; https://doi.org/10.3390/su16114396
Submission received: 17 April 2024 / Revised: 17 May 2024 / Accepted: 21 May 2024 / Published: 22 May 2024

Abstract

:
This study investigates the impact of nitrogen (N), sulfur (S), and iron (Fe) fertilization on secondary metabolites, particularly quercetin and its forms, in onion bulbs (Allium cepa L.). Field experiments over two years examined four onion varieties with red, yellow, and white colors of bulbs: Kamal, Robin, Pueblo, and Mundo. The parameters investigated included the yield, dry matter content, and average onion weight. The phenolic and flavonoid contents were also analyzed. The free quercetin, bound quercetin, and total quercetin contents were determined using the HPLC method. The results demonstrated notable increases in yield following the application of nitrogen (NH4+) and sulfur (SO42−) fertilizers. Incorporating iron (Fe2+) alongside these fertilizers did not yield a significant impact compared to N+S variant. The phenolic and flavonoid content varied with fertilization, while the quercetin content did not yield statistically significant results. Overall, the study highlights the complex relationship between fertilization practices and secondary metabolite production in onions, emphasizing the need for sustainable intensification in modern agriculture.

1. Introduction

In the dynamic landscape of modern agriculture, understanding the intricate interplay between fertilization practices, particularly nitrogen (NH4+), iron (Fe2+), and sulfur (SO42−) applications, and their impact on the nutritional profile of crops is imperative [1,2,3]. It is recognized that the selection or recommendation of an optimal fertilization system is crucial for each plant, as it contributes to achieving a high yield and ensuring the quality of plant products for food consumption [4,5]. For example, effective quality improvement technology for garlic (Allium sativum L.) involves defining the metabolic transformation of sulfur-containing compounds under exogenous regulation by mineral elements, specifically increasing alliin and organic sulfides in garlic bulbs while maintaining productivity. Applying 125 kg S ha−1 of fertilizers and treating with lipoic acid doubles the food and pharmacological value of garlic bulbs [6]. However, nitrogen (NH4+) fertilization is also important for members of the Allium genus. For instance, nitrogen in onion bulbs accounts for 65% of the nitrogen in the aboveground biomass, and nitrogen use efficiency can be improved with slow- or controlled-release fertilizers [7]. Another study demonstrated that treatments with 25% usable humidity and nitrogen fertilization of 150 and 250 kg ha−1 favored the physical, chemical, and bioactive quality of onion bulbs [8]. Additionally, the interaction effect of nitrogen and sulfur significantly increased the main growth parameters and yield of onion bulbs under the application of 200 kg N ha−1 and 45 kg S ha−1 [9]. Plant nutrition responsibility adheres to a food system and circular economy perspective [10].
Onions (Allium cepa L.) have emerged as a noteworthy focus due to their rich content of bioactive compounds, including the health-promoting quercetin and other secondary metabolites [11,12]. Inter- and intra-landrace variability in various onion (Allium cepa L.) varieties was observed in terms of volatile profiles and phenolic compounds [13], which may be influenced by environmental factors. The multifaceted influence of nitrogen and sulfur fertilization on the synthesis and accumulation of these phytochemicals in onion bulbs is a critical aspect of contemporary agricultural research.
Nitrogen and sulfur, two essential nutrients for plant growth and development, play pivotal roles in shaping the metabolic pathways responsible for secondary metabolite production [14,15]. The intricate relationship between these fertilizers and the biochemical processes within the onion plants underscores the need for targeted investigations to optimize their application for enhanced nutritional content [16,17]. The application of boron, copper, and zinc ions has been shown to favor a greater accumulation of micronutrients in onion bulbs [18]. However, studies incorporating Fe as an additional fertilization element, a crucial micronutrient for the photosynthesis process [19], are limited or lacking. Moreover, nowadays, studies align with the principles of sustainable agriculture, aiming not only to maximize yield but also to minimize the environmental impact and promote long-term soil health.
In the face of a growing global population, the significance of sustainable agricultural practices cannot be overstated in ensuring food security while preserving the nutritional quality of crops [20,21]. Sustainable agriculture plays a crucial role in mitigating the environmental impact of fertilization practices and enhancing the resilience of agroecosystems. This study aims to provide actionable insights for farmers, policymakers, and researchers by exploring the intricate relationships between fertilization, crop varieties, and the phytochemical composition. Specifically, the research focuses on unraveling the distinct effects of nitrogen, iron, and sulfur fertilization on the quercetin and secondary metabolite content in onions, with an emphasis on promoting the sustainable intensification of agriculture.

2. Materials and Methods

2.1. Characteristics of Onion Varieties

Kamal: Kamal is a red onion variety known for its premium quality and delightful taste. Its bulbs are uniform with thin necks, exhibiting good resistance to mold and ensuring excellent storage capability. Sowing typically occurs outdoors between March and April, with a maturation period of approximately 24 weeks.
Robin: Robin, a dark red variety introduced in 2005, features semi-erect to horizontal leaves of a moderate length. The bulbs are medium to large and broadly ovate with a narrow neck. They tend to sprout moderately late to late during storage.
Pueblo: Pueblo is a very early white onion variety producing round bulbs suitable for both fresh market consumption and drying purposes, yielding outstanding results. Sowing usually takes place in April, with harvesting in August and storage until October. The growing period spans approximately 115 days from sowing, with a seeding rate of 1 million seeds per hectare.
Mundo: Mundo, a late-maturing variety, is ideal for spring sowing. It features moderately long, upright leaves with a slight droop and a light green hue. The bulbs are large and round with a moderate neck thickness, boasting firm white flesh suitable for year-round storage. Mundo has been a registered variety since 1998 (Figure 1).

2.2. Field Small-Plot Nutrition Experiment Description

A two-year field small-plot nutrition experiment with four varieties of kitchen onion (Allium cepa L.) was established in the cadastral area of PD Madunice. The region of Dolné Považie, where the village of Madunice is located, belongs to a warm, moderately dry climatic zone with mild winters. The average annual air temperature (30-year average) reaches 9.2 °C. The coldest month is January, with an average temperature of −2 °C, and the warmest is July, with an average temperature of 18.9 °C. The experimental site in the Madunice locality is formed by moderately heavy fluvial soils. The onion varieties Kamal, Robin, Pueblo, and Mundo were used in the field experiment.
The nutrition experiment with onion varieties was established in the form of a small-plot trial on a site with a fluvial soil type, the agrochemical characteristics of which are provided in Table 1. The soil was a medium–heavy fluvisol containing fluvial silicate and carbonate sediments with textural diversity and varying mineral richness. It was characterized as fertile to very fertile according to the productivity potential. Before the onion seeds were sown directly in spring, germinating plants (weeds) on the soil surface were removed, and the surface layer (to a depth of 30 mm) was cultivated.
The experimental onion varieties were sown at the optimal agronomic term using a precision seeder for precise seeding into four double rows spaced 0.3 m apart and at a depth of 20 mm. The field bed width was 1.5 m. As part of the cropping sequence, maize was planted as the preceding crop in the first year, followed by annual sunflower in the second growing year.
In the experiment conducted using a block method with the arrangement of experimental variants in strips and with the regular distribution of replications within individual blocks, the influence of different nutrition and fertilization variants on the yield and content substances of the four onion varieties was investigated.
In each block, four fertilization variants were monitored for each variety:
  • 1 Variant—unfertilized control (further referred to as “0” in the text).
  • 2 Variant—fertilization at a rate of 140 kg N ha−1 (NH4+).
  • 3 Variant—fertilization at a rate of 140 kg N ha−1 + fertilization at a rate of 19 kg of available sulfur (SO42+) per hectare (N+S).
  • 4 Variant—fertilization at a rate of 140 kg N ha−1 + fertilization at a rate of 19 kg of available sulfur (SO42+) per hectare + 5 kg of iron (Fe2+) per hectare (N+S+Fe).
Each fertilization variant was replicated four times, with the size of one replication (experimental plot) being 5 m2, meaning the area of one variant amounted to 20 m2.

2.3. Fertilization Application Description

The nitrogen application aimed at reaching a soil level of 140 kg ha−1. It was calculated based on soil N content analysis. Split into two parts, the calculated doses (120 kg N ha−1 in the first year and 80 kg N ha−1 in the second year) were applied. The first part (80 kg N ha−1 in the first year and 53 kg N ha−1 in the second year) was applied one week post-sowing, while the second part (40 kg N ha−1 in the first year and 27 kg N ha−1 in the second year) was applied at the fifth true leaf stage of the onion.
To meet the specified sulfur level (19 kg ha−1), 33.88 kg S ha−1 was applied to the third and fourth fertilization variants in the first year, and 11.65 kg S ha−1 was applied in the second year using ammonium sulfate. Iron was applied with nitrogen and sulfur for the fourth variant: 2.5 kg Fe ha−1 as a soil spray post-sowing and at the fifth true leaf stage, foliarly as FeSO4·7H2O.
Phosphorus fertilization occurred in autumn via simple superphosphate application (8% P) based on soil analysis. Potassium fertilization was unnecessary due to the soil’s high potassium content.
Granulated urea, ammonium sulfate, and urea were used for the first partial nitrogen application across variants, while the second application utilized DAM-390 for all fertilized variants.

2.4. Determining Yield and Other Fundamental Parameters

In the field experiment with kitchen onion, the following key parameters were determined: the yield, dry matter content, dry matter yield, and average weight of one onion.
The quantity of fresh onions harvested per hectare (t ha−1) was measured to assess the productivity of the crop. The percentage of dry matter in the harvested onions was analyzed, providing insight into the proportion of solid material present in the crop. Based on the dry matter content and the total yield, the yield of dry matter per hectare (t ha−1) was calculated. The average weight of a single onion (in grams) was determined, helping to understand the size distribution of the harvested onions.

2.5. Determining the Content of Free Quercetin in Kitchen Onion

After harvest maturity, the content of free quercetin in the onion was determined in an extract of 80% ethanol using an HPLC/MS/MS system (AGILENT 1260, Santa Clara, CA, USA) with a DAD detector, Triple Quadrupole 6410 MS/MS detector, following the method described by Patil et al. (1995), expressed in mg kg−1 of fresh weight [22].

2.6. Sample Preparation for HPLC Analysis

Sample preparation involved obtaining 20 g of tissue from the middle section around the equator of the bulb, excluding dry skin. This tissue was blended with 80 mL of 80% ethanol for 1 min and then filtered through filter paper. The filtrate was stored in screw-capped vials at −20 °C until analysis. A 5 mL aliquot was evaporated to dryness under vacuum at 50 °C using a Buchler evaporator (Evapomix, Washington, DC, USA) and then re-suspended in 1 mL of ethanol (80%). The extracts were filtered through 0.45 µm nylon membrane filters (Sigma-Aldrich, Merck, Germany), and a 10 µL volume of this solution was injected into the HPLC system for analysis.

2.7. Determination of the Bound Quercetin Content in Onion

To determine the bound quercetin content in kitchen onion, a method of extraction in 62.5% ethanol and 6 M HCl was employed, followed by quantification using an HPLC instrument according to the method described by Hertog et al. (1992) [23]. The results were calculated in mg kg−1 of fresh weight of the onion.

2.8. Determination of the Total Phenolic Content in the Onion

The phenolic content in the kitchen onion was determined according to Ragazzi and Veronese (1973) in an extract of 2% trichloroacetic acid (TCA) using the Folin-Ciocalteu method, expressed in mg of gallic acid (GA) per 1000 g of fresh weight of the onion [24].

2.9. Determination of the Total Flavonoid Content in the Experimental Onion Varieties

The flavonoid content was determined according to Bergamini et al. (2004) in an extract of 2% trichloroacetic acid (TCA), expressed in mg of catechin per 1 kg of fresh weight of the onion [25]. Note: In subsequent text, the flavonoid content will be reported in units of mg kg−1, indicating mg of catechin per kilogram of fresh weight of the onion.

3. Results

All onion varieties exhibited the highest yields of fresh weight in the variant fertilized with nitrogen and sulfur (Variant 3 (N+S)). There was a significant increase in the yield of 15% for the Mundo cultivar, 29% for the Robin cultivar, 15% for the Kamal cultivar, and 19% for the Pueblo cultivar.
The highest yield of dry matter, on average over 2 years, was observed for the white variety Pueblo in the variant with N+S+Fe fertilization, reaching 5.11 t ha−1. Following this, the red varieties Kamal (16%) and Robin (17%) were observed, and the lowest dry matter content was determined for the yellow variety Mundo (13%) (Table 2).
The phenol content in onion varieties varied due to nitrogen fertilization in all its experimental variants. On average, over 2 years, nitrogen fertilization had the most significant impact on the phenol content in onions, especially in the Kamal variety (0.929 mg g−1) and Robin variety (0.865 mg g−1). For the white variety Pueblo and the yellow variety Mundo, N+S+Fe fertilization seemed to be the most effective (Table 3).
Fertilization had a differential impact on the flavonoid content during the 2-year experiment across various onion varieties. The highest flavonoid content in the N+S-fertilized variant was observed in the red variety Kamal (0.286 mg g−1 FW). In the N+S+Fe-fertilized variant, the highest flavonoid content was found in the red variety Robin (0.299 mg g−1 FW). However, the highest overall flavonoid content was achieved in the N-fertilized variant, with the red variety Robin reaching a level of 0.353 mg g−1 FW. The yellow variety Mundo did not show significant changes in flavonoid levels under the effect of variant fertilization (0.160 mg g−1 FW in the control variant (O)). The lowest contents of flavonoids were recorded for the white variety Pueblo in all experimental variants with fertilization (ranging from 0.104 to 0.116 mg g−1 FW). At the same time, in the N+S-fertilized variant, the white variety Pueblo showed an increased level of flavonoids by 10% compared to the control variant (without fertilization (O)).
Over the span of 2 years, we observed statistically significant variations in the determination of free, bound, and total quercetin contents among different years and onion varieties (Table 4). However, the impact of fertilization on the quercetin content and its fractions did not yield statistically significant results. The hypothesis suggesting that the foliar application of fertilizer containing iron would elevate the quercetin concentration in onions was not substantiated. Conversely, the crucial metabolic roles of nitrogen and sulfur in quercetin formation were confirmed, evident in the increased concentration of bound quercetin with the combined application of nitrate and sulfate nutrition in red onion varieties. In a 2-year experiment involving the red Kamal variety, the highest quercetin production (17.46 kg ha−1) was observed in the N+S fertilization variant.
In our experiment, a dosage of sulfur of 19 kg ha−1 was not shown to have an impact on the quercetin content. At the same time, an enhanced level of bound quercetin with the combined application of nitrate and sulfate nutrition in red onion varieties was observed.

4. Discussion

Integrated nutrient management practices, such as precision fertilization, nutrient cycling, and agroecological approaches, play a crucial role in promoting sustainable agriculture. Overall, the optimization of N, S, and Fe fertilization in the context of sustainable agriculture represents a critical frontier in agricultural science, with implications for food security, environmental sustainability, and human well-being [26]. The results of the presented research work demonstrated notable increases in the onion yield following the application of nitrogen (N) and sulfur (S) fertilizers. Incorporating iron (Fe) alongside these fertilizers did not yield a significant impact compared to N+S. Al-Fraihat (2009) [9] demonstrated that the application of 200 kg N ha−1 + 100 kg S ha−1 resulted in increased total and marketable yields of onion bulbs, specifically of the Giza 20 cultivar. Another study conducted in India revealed that the application of 150 kg N ha−1 and 90 kg S ha−1 led to significant improvements in the growth, yield attributes, and overall yield of Rabi onion under the conditions of Rajasthan, India [27]. These findings suggest that even higher dosages of nitrogen and sulfur may have a considerable impact on onion yield.
Sulfur is essential for protein synthesis, including the formation of crucial sulfur-containing amino acids like methionine and cysteine, as well as for producing vitamins and chlorophyll [28]. Once considered deficient only in specific soils during the early 1950s, sulfur deficiency has become universal. Additionally, sulfur plays a vital role in activating specific enzymes and serves as a fundamental component of ferredoxin, a molecule critical in photosynthesis. Insufficient sulfur availability compromises plants’ ability to achieve maximum yield potential and efficiently utilize applied nitrogen [29].
The application of sulfur modifies the physicochemical properties of soil, improving nutrient availability and facilitating plant growth and development. This enhances nutrient translocation to reproductive organs, boosts photosynthesis, and, consequently, significantly enhances yields and yield components [30,31].
However, excessive fertilizer application leads to the emission of harmful greenhouse gases into the atmosphere, contributing to environmental pollution. Unused fertilizers become pollutants in the air, water, and soil [32]. Moreover, excessive nitrogen fertilizer application can harm Actinobacteria, posing a threat to microorganisms in agricultural systems [33]. Hence, an optimal fertilization approach entails the application of 140 kg N ha−1 combined with 19 kg of available sulfur per hectare (N+S), as supported by the observed outcomes. These results indicate a notable increase in yield, with improvements of 15% for the Mundo cultivar, 29% for the Robin cultivar, 15% for the Kamal cultivar, and 19% for the Pueblo cultivar.
Numerous studies have examined onion skin as an abundant source of fructooligosaccharides, dietary fibers, polyphenols, and antioxidants [34,35]. Two primary subgroups of flavonoids present in onions are anthocyanins and quercetin and its derivatives. These compounds are responsible for imparting yellow to purple hues to onion skins [36]. A comparative study involving fifteen Indian onion cultivars with diverse skin colors revealed that red-colored varieties exhibit the highest levels of flavonoids and natural antioxidants [37]. It is also noteworthy that phenolic compounds in the black (or red/purple) onion variety remained stable during the digestion process, exhibiting a higher bioaccessibility index [38]. In the presented study, the red onion varieties showed an evident increase in the concentration of bound quercetin with the combined application of nitrate and sulfate.
The red onion varieties Kamal and Robin exhibited the highest flavonoid contents in the N+S-fertilized variant, with values of 0.286 mg g−1 and 0.299 mg g−1, respectively. Meanwhile, in the N+S+Fe-fertilized variant, the highest flavonoid content recorded was 0.353 mg g−1, matching that of the N-fertilized variant. Simultaneously, within the N+S-fertilized variant, the white variety Pueblo exhibited a 10% elevation in flavonoid levels compared to the control variant (without fertilization). The study from 2024 highlighted the significant potential of optimizing nitrogen fertilizer sources to enhance the nutritional quality of white short-day onions, encompassing phenolics, flavonoids, and free radical scavenging activity—specifically, the synergistic effect of pre-plant CaCN2 application (80 kg N ha−1) [39]. However, it is conceivable to suggest that the experimental combination of N+S fertilizers may increase the level of flavonoids in onion varieties, with a more pronounced enhancement observed in red onion varieties.
Fe is involved in the synthesis of chlorophyll and in other enzymatic and metabolic processes without which plants cannot carry out the plant lifecycle [40,41]. Therefore, in the one fertilization variant N+S+Fe of our experiment, we used Fe at a dose of 5 kg ha−1. At the same time, a significant increase in the growth and yield parameters compared to those of the variant N+S was not observed. Previous studies found that the shoot growth decreased and the root length increased in soybean seedlings with increasing Fe application doses [42]. However, an interactive effect of N and Fe fertilization on the growth and yield of soybean was demonstrated in soil with high bicarbonate and pH. There was a positive interaction between N and Fe at N rates up to 80 kg N ha−1 [3]. We suppose that the interaction between N and Fe fertilization may vary depending on the type of plant, soil, and dosage. For example, it was found that plants of the Poaceae family are more susceptible to nanoscale zero-valent iron than Fabaceae [43]. It is possible that in our experimental variant, the dose of N was high enough to observe some positive effects of Fe on the growth and qualitative parameters of the experimental onion varieties.
It was shown that sulfur fertilization increased the quercetin and total polyphenol contents, along with the antioxidant activity in experimental onions. The red cultivars statistically significantly exhibited the highest polyphenol and quercetin contents at a sulfur dose of 40 kg·ha−1. The yellow cultivars showed the highest polyphenol contents at a sulfur dose of 50 kg·ha−1. The white cultivars had the lowest polyphenol and quercetin contents, with the highest values observed at a sulfur dose of 40 kg·ha−1 [44]. In our experiment with a dosage of sulfur of 19 kg ha−1, no impact of such fertilization on the quercetin content was shown. At the same time, an enhanced level of bound quercetin with the combined application of nitrate and sulfate nutrition in red onion varieties was observed.
The correct balance of nutrients is particularly important for high sulfur-using crops like canola and alfalfa [45]. Balanced and judicious nutrient management practices for a specific plant object are crucial for promoting sustainable agriculture. Excessive applications of sulfur and nitrogen can lead to environmental pollution. Nitrogen can leach into groundwater, causing contamination, while sulfur can contribute to acid rain formation when released into the atmosphere as sulfur dioxide [46,47,48]. High doses of sulfur and nitrogen can negatively impact soil biodiversity by favoring certain plant species over others. This can lead to a decline in beneficial soil organisms and a loss of biodiversity in agricultural ecosystems.
This study underscores the critical importance of precise nutrient management tailored to specific plant species, particularly onions (Allium cepa L.), for sustainable agricultural practices. Our experiments focused on the effects of nitrogen (NH4+), sulfur (SO42+), and iron (Fe2+) fertilization on secondary metabolites, notably quercetin, across four onion varieties. Over two years, we observed increased onion yields with nitrogen–sulfur (N+S) fertilization, while the addition of iron did not significantly affect the yield compared to N+S fertilization. The phenolic and flavonoid contents varied with fertilization but showed no significant changes in the quercetin content. Effective nutrient management practices are essential for promoting sustainable agriculture while ensuring environmental stewardship. While excessive sulfur and nitrogen application can lead to environmental degradation, judicious fertilization, particularly the synergistic effects of nitrogen and sulfur, enhances the onion yield and nutritional quality. Our findings highlight the need for balanced fertilization strategies tailored to specific crop requirements to mitigate environmental pollution and preserve soil biodiversity. Striking a balance between optimal fertilization and environmental sustainability is paramount for advancing sustainable agriculture and securing long-term agricultural viability.

5. Conclusions

Effective nutrient management practices tailored to specific plant species are imperative for fostering sustainable agricultural systems. The overapplication of sulfur, nitrogen, and iron can result in detrimental environmental consequences, highlighting the importance of optimal dosages for onion cultivars. Our experimentation revealed that sulfur application at a dosage of 19 kg ha−1 did not significantly impact the quercetin content in onions. Conversely, a combined nitrogen and sulfur (N+S) fertilizer approach led to increased levels of bound quercetin, particularly evident in red onion varieties. Notably, the application of N+S fertilizers significantly enhanced the flavonoid levels across all onion cultivars, resulting in notable increases in the yield. However, the addition of iron alongside N+S did not yield significant growth or yield improvements compared to N+S alone. Our findings underscore the beneficial effects of sulfur in promoting onion growth and development. Furthermore, the interaction between nitrogen and iron fertilization suggested that high nitrogen doses might overshadow the potential benefits of iron for onion growth and quality parameters.
Integrated nutrient management practices are crucial for sustainable agriculture, highlighting the importance of precision fertilization and agroecological approaches. Optimal fertilization strategies are essential for food security, environmental sustainability, and human well-being. Balanced fertilization, particularly the synergistic effects of nitrogen and sulfur fertilization, enhances the onion yield and nutritional quality, contributing to long-term sustainability in onion cultivation.

Author Contributions

K.O.: investigation, conceptualization, resources, writing—review and editing. A.G.: investigation, formal analysis, methodology. O.S.: statistical analysis, writing—original draft, writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data generated or analyzed during this study are included in this published article.

Acknowledgments

The authors extend their heartfelt appreciation to Pavol Slamka for his invaluable scientific guidance, which encompassed practical recommendations pertaining to sustainable crop cultivation within the ago-ecological context of Slovakia.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

  1. Ayamba, B.E.; Abaidoo, R.C.; Opoku, A.; Ewusi-Mensah, N. Mechanisms for nutrient interactions from organic amendments and mineral fertilizer inputs under cropping systems: A review. PeerJ 2023, 11, e15135. [Google Scholar] [CrossRef]
  2. Astolfi, S.; Celletti, S.; Vigani, G.; Mimmo, T.; Cesco, S. Interaction Between Sulphur and Iron in Plants. Front. Plant Sci. 2021, 12, 670308. [Google Scholar] [CrossRef]
  3. Caliskan, S.; Ozkaya, I.; Caliskan, M.E.; Arslan, M. The effects of nitrogen and iron fertilization on growth, yield and fertilizer use efficiency of soybean in a Mediterranean-type soil. Field Crops Res. 2008, 108, 126–132. [Google Scholar] [CrossRef]
  4. Ishfaq, M.; Wang, Y.; Xu, J. Improvement of nutritional quality of food crops with fertilizer: A global meta-analysis. Agron. Sustain. Dev. 2023, 43, 74. [Google Scholar] [CrossRef]
  5. Penuelas, J.; Coello, F.; Sardans, J. A better use of fertilizers is needed for global food security and environmental sustainability. Agric. Food Secur. 2023, 12, 5. [Google Scholar] [CrossRef]
  6. Kosyan, A.; Sytar, O.; Taran, N. Quality increasing technology of garlic bulbs growing (Allium sativum L.) owing to the use of sulphuric fertilizers. Agrochémia Agrochem. 2010, XXIII, 7–11. [Google Scholar]
  7. Geisseler, D.; Ortiz, S.R.; Diaz, J. Nitrogen nutrition and fertilization of onions (Allium cepa L.)—A literature review. Sci. Hortic. 2022, 291, 110591. [Google Scholar] [CrossRef]
  8. Barrales-Heredia, S.M.; Grimaldo-Juárez, O.; Suárez-Hernández, Á.M.; González-Vega, R.I.; Díaz-Ramírez, J.; García-López, A.M.; Soto-Ortiz, R.; González-Mendoza, D.; Iturralde-García, R.D.; Dórame-Miranda, R.F. Effects of Different Irrigation Regimes and Nitrogen Fertilization on the Physicochemical and Bioactive Characteristics of onion (Allium cepa L.). Horticulturae 2023, 9, 344. [Google Scholar] [CrossRef]
  9. Al-Fraihat, A.H. Effect of Different Nitrogen and Sulphur Fertilizer Levels on Growth, Yield and Quality of Onion (Allium cepa L.). Jordan J. Agric. Sci. 2010, 5, 155. [Google Scholar]
  10. Dobermann, A.; Bruulsema, T.; Cakmak, I.; Gerard, B.; Majumdar, K.; McLaughlin, M.; Reidsma, P.; Vanlauwe, B.; Wollenberg, L.; Zhang, F.; et al. Responsible plant nutrition: A new paradigm to support food system transformation. Glob. Food Secur. 2022, 33, 100636. [Google Scholar] [CrossRef]
  11. Kumar, M.; Barbhai, M.D.; Hasan, M.; Punia, S.; Dhumal, S.; Radha; Rais, N.; Chandran, D.; Pandiselvam, R.; Kothakota, A.; et al. Onion (Allium cepa L.) peels: A review on bioactive compounds and biomedical activities. Biomed. Pharmacother. 2022, 146, 112498. [Google Scholar] [CrossRef]
  12. Ren, F.; Zhou, S. Phenolic Components and Health Beneficial Properties of Onions. Agriculture 2021, 11, 872. [Google Scholar] [CrossRef]
  13. Cozzolino, R.; Malorni, L.; Martignetti, A.; Picariello, G.; Siano, F.; Forte, G.; De Giulio, B. Comparative analysis of volatile profiles and phenolic compounds of Four Southern Italian onion (Allium cepa L.) Landraces. J. Food Compos. Anal. 2021, 101, 103990. [Google Scholar] [CrossRef]
  14. Jian, S.F.; Huang, X.J.; Yang, X.N.; Zhong, C.; Miao, J.H. Sulphur Regulates the Trade-Off Between Growth and Andrographolide Accumulation via Nitrogen Metabolism in Andrographis paniculata. Front. Plant Sci. 2021, 12, 687954. [Google Scholar] [CrossRef]
  15. Takahashi, H.; Marsolais, F.; Cuypers, A.; Kopriva, S. Sulphur metabolism: Actions for plant resilience and environmental adaptation. J. Exp. Bot. 2023, 74, 3271–3275. [Google Scholar] [CrossRef]
  16. Vojnović, Đ.; Maksimović, I.; Tepić Horecki, A.; Karadžić Banjac, M.; Kovačević, S.; Daničić, T.; Podunavac-Kuzmanović, S.; Ilin, Ž. Onion (Allium cepa L.) Yield and Quality Depending on Biostimulants and Nitrogen Fertilization—A Chemometric Perspective. Processes 2023, 11, 684. [Google Scholar] [CrossRef]
  17. Matrella, M.L.; Valletti, A.; Marra, F.; Mallamaci, C.; Cocco, T.; Muscolo, A. Phytochemicals from Red Onion, Grown with Eco-Sustainable Fertilizers, Protect Mammalian Cells from Oxidative Stress, Increasing Their Viability. Molecules 2022, 27, 6365. [Google Scholar] [CrossRef]
  18. Bertino, N.M.F.; Grangeiro, L.C.; da Costa, J.P.N.; Costa, R.M.C.; de Lacerda, R.R.A.; Gomes, V.E. Growth, nutrient accumulation and yield of onion as a function of micronutrient fertilization. Rev. Bras. Eng. Agrícola Ambient. 2022, 26, 126–134. [Google Scholar] [CrossRef]
  19. Therby-Vale, R.; Lacombe, B.; Rhee, S.Y.; Nussaume, L.; Rouached, H. Mineral nutrient signaling controls photosynthesis: Focus on iron deficiency-induced chlorosis. Trends Plant Sci. 2022, 27, 502–509. [Google Scholar] [CrossRef]
  20. Fróna, D.; Szenderák, J.; Harangi-Rákos, M. The Challenge of Feeding the World. Sustainability 2019, 11, 5816. [Google Scholar] [CrossRef]
  21. Pawlak, K.; Kołodziejczak, M. The Role of Agriculture in Ensuring Food Security in Developing Countries: Considerations in the Context of the Problem of Sustainable Food Production. Sustainability 2020, 12, 5488. [Google Scholar] [CrossRef]
  22. Patil, B.S.; Pike, L.M.; Yoo, K.S. Variation in the Quercetin Content in Different Colored Onions (Allium cepa L.). J. Am. Soc. Hortic. Sci. 1995, 120, 909–913. [Google Scholar] [CrossRef]
  23. Hertog, M.G.L.; Hollman, P.C.H.; Katan, M.B. Content of potentially anticarcinogenic flavonoids of 28 vegetables and 9 fruits commonly consumed in the Netherlands. J. Agric. Food Chem. 1992, 40, 2379–2383. [Google Scholar] [CrossRef]
  24. Ragazzi, E.; Veronese, G. Quantitative analysis of phenolic compounds after thin-layer chromatographic separation. J. Chromatogr. 1973, 77, 369–375. [Google Scholar] [CrossRef]
  25. Bergamini, C.M.; Gambetti, S.; Dondi, A.; Cervellati, C. Oxygen, Reactive Oxygen Species and Tissue Damage. Curr. Pharm. Des. 2004, 10, 1611–1626. [Google Scholar] [CrossRef]
  26. Shanmugavel, D.; Rusyn, I.; Solorza-Feria, O.; Kamaraj, S.K. Sustainable SMART fertilizers in agriculture systems: A review on fundamentals to in-field applications. Sci. Total Environ. 2023, 904, 166729. [Google Scholar] [CrossRef]
  27. Sharma, G.P.; Dhaka, R.S.; Shankar, U.T.; Meena, V.S. Effect of nitrogen and sulphur levels on growth and yield of Rabi onion (Allium cepa L.). Pharma Innov. J. 2022, 11, 5697–5701. [Google Scholar]
  28. Narayan, O.P.; Kumar, P.; Yadav, B.; Dua, M.; Kumar Johri, A. Sulphur nutrition and its role in plant growth and development. Plant Signal. Behav. 2023, 18, 2030082. [Google Scholar] [CrossRef]
  29. Sharma, R.K.; Cox, M.S.; Oglesby, C.; Dhillon, J.S. Revisiting the role of sulphur in crop production: A narrative review. J. Agric. Food Res. 2024, 15, 101013. [Google Scholar] [CrossRef]
  30. Dhaker, S.C.; Mundra, S.L.; Nepalia, V. Effect of weed management and sulphur nutrition on productivity of soybean [Glycine max (L.) Merrill]. Indian J. Weed Sci. 2010, 42, 232–234. [Google Scholar]
  31. Głowacka, A.; Jariene, E.; Flis-Olszewska, E.; Kiełtyka-Dadasiewicz, A. The Effect of Nitrogen and Sulphur Application on Soybean Productivity Traits in Temperate Climates Conditions. Agronomy 2023, 13, 780. [Google Scholar] [CrossRef]
  32. Bisht, N.; Singh Chauhan, P. Excessive and Disproportionate Use of Chemicals Cause Soil Contamination and Nutritional Stress. In Soil Contamination—Threats and Sustainable Solutions; IntechOpen: London, UK, 2021. [Google Scholar] [CrossRef]
  33. Gu, Y.; Wang, J.; Cai, W.; Li, G.; Mei, Y.; Yang, S. Different Amounts of Nitrogen Fertilizer Applications Alter the Bacterial Diversity and Community Structure in the Rhizosphere Soil of Sugarcane. Front. Microbiol. 2021, 12, 721441. [Google Scholar] [CrossRef]
  34. Stoica, F.; Rațu, R.N.; Veleșcu, I.D.; Stănciuc, N.; Râpeanu, G. A comprehensive review on bioactive compounds, health benefits, and potential food applications of onion (Allium cepa L.) skin waste. Trends Food Sci. Technol. 2023, 141, 104173. [Google Scholar] [CrossRef]
  35. Samota, M.K.; Sharma, M.; Kaur, K.; Sarita; Yadav, D.K.; Pandey, A.K.; Tak, Y.; Rawat, M.; Thakur, J.; Rani, H. Onion anthocyanins: Extraction, stability, bioavailability, dietary effect, and health implications. Front. Nutr. 2022, 9, 917617. [Google Scholar] [CrossRef]
  36. Benítez, V.; Mollá, E.; Martín-Cabrejas, M.A.; Javier López-Andréu, F.; Downes, K.; Terry, L.A.; Esteba, R.M. Study of bioactive compound content in different onion sections. Plant Food Hum. Nutr. 2011, 66, 48–57. [Google Scholar] [CrossRef]
  37. Sagar, N.A.; Pareek, S.; Gonzalez-Aguilar, G.A. Quantification of flavonoids, total phenols and antioxidant properties of onion skin: A comparative study of fifteen Indian cultivars. J. Food Sci. Technol. 2020, 57, 2423–2432. [Google Scholar] [CrossRef]
  38. Moreno-Ortega, A.; Ordóñez, J.L.; Moreno-Rojas, R.; Moreno-Rojas, J.M.; Pereira-Caro, G. Changes in the Organosulphur and Polyphenol Compound Profiles of Black and Fresh Onion during Simulated Gastrointestinal Digestion. Foods 2021, 10, 337. [Google Scholar] [CrossRef]
  39. Simelane, M.P.Z.; Soundy, P.; Maboko, M.M. Effect of Calcium Cyanamide as an Alternative Nitrogen Source on Growth, Yield, and Nitrogen Use Efficiency of Short-Day Onion. Agronomy 2023, 13, 2746. [Google Scholar] [CrossRef]
  40. Ning, X.; Lin, M.; Huang, G.; Mao, J.; Gao, Z.; Wang, X. Research progress on iron absorption, transport, and molecular regulation strategy in plants. Front. Plant Sci. 2023, 14, 1190768. [Google Scholar] [CrossRef]
  41. Li, M.; Watanabe, S.; Gao, F.; Dubos, C. Iron Nutrition in Plants: Towards a New Paradigm? Plants 2023, 12, 384. [Google Scholar] [CrossRef] [PubMed]
  42. Gülser, F.; Yavuz, H.I.; Gökkaya, T.H.; Sedef, M. Effects of iron sources and doses on plant growth criteria in soybean seedlings. Eurasian J. Soil. Sci. 2019, 8, 298–303. [Google Scholar] [CrossRef]
  43. Cui, X.; Hou, D.; Tang, Y.; Liu, M.; Qie, H.; Qian, T.; Xu, R.; Lin, A.; Xu, X. Effects of the application of nanoscale zero-valent iron on plants: Meta analysis, mechanism, and prospects. Sci. Total Environ. 2023, 900, 165873. [Google Scholar] [CrossRef] [PubMed]
  44. Tóth, T.; Bystrická, J.; Tomáš, J.; Siekel, P.; Kovarovič, J.; Lenková, M. Effect of sulphur fertilization on contents of phenolic and sulphuric compounds in onion (Allium cepa L.). J. Food Nutr. Res. 2018, 57, 170–178. [Google Scholar]
  45. Malhi, S.S.; Schoenau, J.J.; Grant, C.A. A review of sulphur fertilizer management for optimum yield and quality of canola in the Canadian Great Plains. Can. J. Plant Sci. 2005, 85, 297–307. [Google Scholar] [CrossRef]
  46. Wick, K.; Heumesser, C.; Schmid, E. Groundwater nitrate contamination: Factors and indicators. J. Environ. Manag. 2012, 111, 178–186. [Google Scholar] [CrossRef] [PubMed]
  47. Abbasi, M.R.; Sepaskhah, A.R. Nitrogen leaching and groundwater N contamination risk in saffron/wheat intercropping under different irrigation and soil fertilizers regimes. Sci. Rep. 2023, 13, 6587. [Google Scholar] [CrossRef]
  48. Hinckley, E.L.S.; Driscoll, C.T. Sulphur fertiliser use in the Midwestern US increases as atmospheric sulphur deposition declines with improved air quality. Commun. Earth Environ. 2022, 3, 324. [Google Scholar] [CrossRef]
Figure 1. Experimental onion varieties: (A) Kamal, (B) Robin, (С) Pueblo, (D) Mundo.
Figure 1. Experimental onion varieties: (A) Kamal, (B) Robin, (С) Pueblo, (D) Mundo.
Sustainability 16 04396 g001
Table 1. The results of the soil agrochemical analysis before sowing.
Table 1. The results of the soil agrochemical analysis before sowing.
YearpHHumus
(%)
Nutrient Content (mg kg−1 of Soil)
NanSFePKCaMg
1 year5.962.827.218.019.68352604200830
2 year6.904.1613.527.514.1317.5242.55600935.0
Table 2. The yield parameters of the experimental onion cultivars (2-year experiment).
Table 2. The yield parameters of the experimental onion cultivars (2-year experiment).
VariantYield (t ha−1)Dry Matter Content (%)Dry Matter Yield (t ha−1)Average Weight of One Onion (g)
Cultivar Mundo
1 (0)26.12 a12.01 a3.13 a59.66 a
2 (N)29.04 b11.93 a3.45 b68.99 b
3 (N+S)30.57 b12.32 a3.69 c65.55 ab
4 (N+S+Fe)29.92 b12.41 a3.79 bc77.05 c
LSD 0.052.350.740.307.82
Cultivar Robin
1 (0)23.72 a13.28 b3.06 a61.64 a
2 (N)31.57 b12.71 a3.99 b84.83 c
3 (N+S)33.50 b13.24 b4.40 b81.72 c
4 (N+S+Fe)32.76 b13.05 b4.22 b73.64 b
LSD 0.053.350.330.447.67
Cultivar Kamal
1 (0)23.68 a14.53 ab3.37 a39.96 a
2 (N)26.62 b14.14 a3.67 ab45.67 bc
3 (N+S)28.93 c14.61 b4.23 c48.61 c
4 (N+S+Fe)27.82 bc14.54 b3.94 bc42.94 ab
LSD 0.052.030.380.355.44
Cultivar Pueblo
1 (0)22.86 a19.05 b4.17 a62.25 a
2 (N)25.78 b18.61 b4.77 b73.51 c
3 (N+S)28.60 c17.93 a5.00 b69.42 bc
4 (N+S+Fe)28.37 c18.59 b5.11 b65.50 ab
LSD 0.052.350.530.375.47
Note: The same letters in the averages of the observed characteristics indicate a statistical difference; LSD = least significant difference, at p = 95% (α = 0.05).
Table 3. The level of phenolics and flavonoids in the experimental onion cultivars (2-year experiment).
Table 3. The level of phenolics and flavonoids in the experimental onion cultivars (2-year experiment).
VariantCultivar
KamalRobinPuebloMundo
Phenolics (mg gallic acid equivalents per g FW)
1 (0)0.808 a0.776 a0.395 a0.752 a
2 (N)0.929 b0.865 a0.458 b0.858 b
3 (N+S)0.861 ab0.842 a0.453 b0.858 b
4 (N+S+Fe)0.856 ab0.849 a0.500 c0.921 b
LSD 0.050.0890.0980.0360.093
Flavonoids (mg g−1 FW)
1 (0)0.273 b0.278 a0.104 a0.160 a
2 (N)0.282 b0.353 b0.105 a0.158 a
3 (N+S)0.286 b0.279 a0.105 a0.154 a
4 (N+S+Fe)0.238 a0.299 a0.116 a0.158 a
LSD 0.050.0330.0300.0180.013
Note: The same letters in the averages of the observed characteristics indicate a statistical difference; LSD = least significant difference, at p = 95% (α = 0.05).
Table 4. Quercetin fractions in onions and their share of the total quercetin content (mg g−1 FW), averaged over 2 years.
Table 4. Quercetin fractions in onions and their share of the total quercetin content (mg g−1 FW), averaged over 2 years.
VariantFree Quercetin% of Total QuercetinBound Quercetin% of Total QuercetinTotal QuercetinRel. %
Cultivar Mundo
1 (0)0.065 ab200.265 ab800.329 a100
2 (N)0.063 ab190.263 ab810.327 a100
3 (N+S)0.072 b220.262 a780.334 a100
4 (N+S+Fe)0.053 a150.308 b850.360 a100
LSD 0.050.013-0.044-0.048-
Cultivar Robin
1 (0)0.052 c170.255 a830.307 a100
2 (N)0.040 ab120.286 ab880.326 ab100
3 (N+S)0.048 bc140.306 b860.354 b100
4 (N+S+Fe)0.038 a120.265 a880.303 a100
LSD 0.050.007-0.003-0.028
Cultivar Kamal
1 (0)0.030 a60.434 a940.464 a100
2 (N)0.043 b80.477 b920.520 bc100
3 (N+S)0.034 ab60.514 c940.547 c100
4 (N+S+Fe)0.032 a60.471 b940.503 b100
LSD 0.050.010-0.031-0.033
Cultivar Pueblo
1 (0)0.008 b150.005 b850.006100
2 (N)0.005 a140.003 a860.004100
3 (N+S)0.004 a140.002 a860.003100
4 (N+S+Fe)0.004 a150.002 ab850.003100
LSD 0.050.0002-0.0001-0.0001
Note: The same letters in the averages of the observed characteristics indicate a statistical difference; LSD = least significant difference, at p = 95% (α = 0.05).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Olsovska, K.; Golisova, A.; Sytar, O. Optimizing Nitrogen Nutrient Management for the Sustainable Enhancement of Secondary Metabolites and Yield in Onion Cultivation. Sustainability 2024, 16, 4396. https://doi.org/10.3390/su16114396

AMA Style

Olsovska K, Golisova A, Sytar O. Optimizing Nitrogen Nutrient Management for the Sustainable Enhancement of Secondary Metabolites and Yield in Onion Cultivation. Sustainability. 2024; 16(11):4396. https://doi.org/10.3390/su16114396

Chicago/Turabian Style

Olsovska, Katarina, Andrea Golisova, and Oksana Sytar. 2024. "Optimizing Nitrogen Nutrient Management for the Sustainable Enhancement of Secondary Metabolites and Yield in Onion Cultivation" Sustainability 16, no. 11: 4396. https://doi.org/10.3390/su16114396

APA Style

Olsovska, K., Golisova, A., & Sytar, O. (2024). Optimizing Nitrogen Nutrient Management for the Sustainable Enhancement of Secondary Metabolites and Yield in Onion Cultivation. Sustainability, 16(11), 4396. https://doi.org/10.3390/su16114396

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