Next Article in Journal
Effects of Prey Switching at Different Stages on Life Parameters of Neoseiulus bicaudus
Previous Article in Journal
Collaboration to Address the Challenges Faced by Smallholders in Practicing Organic Agriculture: A Case Study of the Organic Sorghum Industry in Zunyi City, China
Previous Article in Special Issue
The Impact of Long-Term Fallowing on the Yield and Quality of Winter Rape and Winter and Spring Wheat
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 14
Issue 5
10.3390/agriculture14050727
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Communication

The Effect of Renewable Phosphorus Biofertilizers on Selected Wheat Grain Quality Parameters

by
Magdalena Jastrzębska
1,*,
Marta K. Kostrzewska
1 and
Agnieszka Saeid
2
1
Department of Agroecosystems and Horticulture, Faculty of Agriculture and Forestry, University of Warmia and Mazury in Olsztyn, Plac Łódzki 3, 10-718 Olsztyn, Poland
2
Department of Engineering and Technology of Chemical Processes, Faculty of Chemistry, Wroclaw University of Science and Technology, Wyspiańskiego 42, 50-370 Wrocław, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(5), 727; https://doi.org/10.3390/agriculture14050727
Submission received: 5 April 2024 / Revised: 30 April 2024 / Accepted: 5 May 2024 / Published: 8 May 2024
(This article belongs to the Special Issue Integrated Management and Efficient Use of Nutrients in Crop Systems)
Versions Notes

Abstract

:
Recycling and reusing phosphorus in agriculture can reduce the consumption of natural phosphorus resources, which are continuing to shrink. Phosphorus fertilizers made from renewable raw materials (sewage sludge ash, animal bones, dried animal blood) and activated with phosphorus solubilizing microorganisms (Bacillus megaterium, Acidithiobacillus ferrooxidans) offer an alternative to conventional fertilizers. These products should meet consumer and environmental safety standards. In this paper, based on field experiments conducted in northeast Poland, the effects of waste-derived biofertilizers on selected parameters of wheat yield quality are discussed. The study focuses on the technological properties of the grain (hectoliter weight, hardness index, Zeleny index, starch, wet gluten, and protein content), the content of proteogenic amino acids, macro- and micronutrients, and selected toxic elements in the grain. The quality parameters of wheat grain were not affected by the tested biofertilizers applied in P doses up to 35.2 kg ha−1, nor by conventional fertilizers.

1. Introduction

The urgent need to feed the world’s growing population, coupled with increasing concerns about nutrient pollution of the environment and climate change, have made rational nutrient management one of the major challenges of this century [1,2]. Food production begins in the field, and crop productivity is highly dependent on nutrient availability [3]. The soil pool of many nutrients is usually insufficient for achieving satisfactory yields, and additional plant nutrition from external sources is required [2]. The most commonly used nutrient carriers are synthetic mineral fertilizers [1], although alternative nutrient sources are increasingly being adopted [4].
One of the six key elements in plant nutrition is phosphorus (P) [5]. It plays a vital role in all their major metabolic activities, including photosynthesis and respiration, as well as nucleic acid, protein, starch, and membrane phospholipid synthesis [6,7]. Phosphorus cannot be replaced by any other element, and its deficiency severely limits crop productivity [8,9]. Given the critical role of P in global crop production, demand for P fertilizers is expected to increase significantly by 2050 [1,10]. Regardless of this global trend, there are huge disparities between world regions in terms of the amount of P fertilizer applied [11] and thus the soil P budget. P fertilization is most commonly achieved through the application of chemical fertilizers derived from phosphate rock (PR) [1]. PR is a finite, non-renewable and geographically restricted resource [12]. In addition, the PR economy is currently predominantly linear, with significant P wastage and loss from mine to fork (currently about 90%) [13], due to inefficient use of P fertilizers and high P losses to the environment [14]. In Europe, PR reserves are almost non-existent [12], both PR and P are critical raw materials [15], and most European countries are dependent on imported PR [16]. For the P economy in European countries, the significant increase in P prices since 2020 due to pandemic, geopolitical conflicts, trade wars and rising fuel prices, and the conflict between Russia and Ukraine, further disrupting the PR trade, is also of great importance [17]. Closing the P cycle and using P more efficiently, particularly in agricultural production, seems to be indispensable and inevitable not only in Europe but also at the global level [8,14].
Increasing the use of recycled P in the fertilizer industry, as an alternative or supplement to PR, is considered one of the key actions towards global P sustainability [18]. A goal for fertilizer products to contain a minimum of 20% recycled P by 2030 has been advocated [19]. In recent years, multiple strategies have been developed to reuse P from P-rich wastes, such as manures, abattoir residues, food processing and domestic wastes, sewage derived biosolids and wastewaters, and the ashes of incinerated residues [4]. Great potential for P recycling exists by applying P-rich organic wastes and manures to agricultural soils [20]. In some cases, however, there is a need to recover, detoxify and modify P from waste to make recycling safe and effective and to achieve higher levels of nutrient use efficiency [4]. According to Kabbe and Rinck-Pfeiffer [21], there are more than 30 different technologies available for recovering P from waste streams, and new ones are still emerging.
Numerous studies prove that recycling-derived P fertilizers match conventional P fertilizers in terms of performance [22,23,24]. However, making these products marketable requires legislative support [25,26]. National policies that optimize P recycling in some European countries (e.g., mandatory P recovery from sewage sludge and slaughterhouse waste [27]), as well as EU regulations [28] and strategies [29], can help recycled nutrient carriers become competitive in the market.
One of the approaches that could be applied to the recycled fertilizer industry is the use of microbial solubilization [30]. The mechanisms of this natural process in the P cycle are fairly well understood, and numerous microbial strains (phosphorus solubilizing microorganisms—PSMs) performing this process are known [31,32]. Studies have shown that PSMs can be activators of insoluble P compounds in soils [33] and fertilizer feedstocks from both primary and secondary sources [34,35,36]. PSMs also promote plant growth through other biological mechanisms [37], which is an additional benefit of their use as/in biofertilizers (definition according to Mącik et al. [38]).
The concept of incorporating living PSM cultures into waste-based formulations [39] has led to the development of several biofertilizers from sewage sludge ash (SSA), animal bones and blood. The substrate used was activated by Bacillus megaterium or Acidithiobacillus ferrooxidans strains. The agronomic usefulness of these biofertilizers was tested under field conditions. Promising results have already been reported on the yield and environmental performance of these products [40,41,42,43,44]. This paper deals with the influence of waste-derived biofertilizers on the selected quality parameters of wheat (test crop) yield, i.e., technological properties (hectoliter (test) weight, hardness index, Zeleny (sedimentation) index, starch, wet gluten, and protein content), proteinogenic amino acid contents, and the content of macro- and micronutrients and selected toxic elements. The listed technological characteristics of grain are among the properties that determine grain destination and suitability for processing [45,46], amino acid profile and other macro- and micronutrient compositions are elements of the nutritional value of grain [47], while the absence/presence of potentially toxic elements determines the safety of grain products for their consumers (humans or livestock) [48]. The study hypothesized that the tested bioproducts would not have a negative impact on the studied yield quality parameters when compared to conventional P fertilizers.

2. Materials and Methods

2.1. Fertilizers and Experiments

Six biofertilizers made from waste materials and activated with PSMs were evaluated agronomically based on field experiments. The raw materials used for fertilizer production were sewage sludge ash (SSA), animal (poultry) bones, and dried animal (porcine) blood. The PSMs used were Bacillus megaterium or Acidithiobacillus ferrooxidans strains. The fertilizers were formulated as suspensions or granules. Table 1 presents an overview of the biofertilizers under study, while Table S1 provides a detailed listing of their chemical composition.
The study compared biofertilizers to conventional P fertilizers, including superphosphate Fosdar™40 (SP; Grupa Azoty FOSFORY Sp. z o.o. in Gdańsk, Poland), and phosphorite Syria (PR; Luvena in Luboń, Poland). Biofertilizer analogues without PSM, such as ash-water solution (A + H2O), granular fertilizer from SSA and bones (ABg), and granular fertilizer from SSA and blood (AHg), were also included in the study. Additionally, a no-P treatment was used. The New Chemical Syntheses Institute in Puławy, Poland, produced biofertilizers and fertilizers from waste using a formula developed by the Department of Advanced Material Technologies at Wrocław University of Science and Technology, Poland.
Between 2014 and 2017, seven field experiments were conducted to test renewable fertilizers on winter or spring common wheat (Triticum aestivum ssp. vulgare Mac Key). Table 2 presents basic information on the experiments. More details on the experiment designs and other agricultural data can be found in Table S2. All agricultural practices, except for P treatments, were consistent within each experiment and followed the principles of good agricultural practice.

2.2. Experimental Site Description

The experiments were conducted at the Production and Experimental Station “Bałcyny” Sp. z o.o. in Bałcyny, located in the Warmińsko-Mazurskie province of northeastern Poland. The region has a temperate climate and glacial landforms, with the most common soil type being Luvisols [50]. Soils meeting the requirements of the test crop were used in the trials. The pHKCl values of the 0–30 cm soil layer ranged from 4.98 to 6.28. The total contents of C, N, P, K, and Mg were 6.48 to 8.90 g kg−1, 1.01 to 1.42 g kg−1, 0.43 to 0.61 g kg−1, 2.90 to 3.30 g kg−1, and 1.88 to 2.25 g kg−1, respectively (see Table S3 for detailed basic soil characteristics before the start of the individual experiments). The precipitation and thermal regimes during the experimental growing seasons differed from those typical of the region. Seasons in experiments I–III were too dry for wheat, while seasons in experiments IV–VII were rather too wet for this species (see Table S4 for detailed data).

2.3. Grain Sampling and Analyses

Samples of wheat grain weighing approximately 1 kg were taken from each plot after combine harvesting. From these samples, approximately 200 g portions of grain were weighed, cleaned of impurities and weed seeds, and forwarded for further analyses. The technological properties of the grain were analyzed, including hectoliter (test) weight, hardness index, Zeleny (sedimentation) index, starch, wet gluten, and protein content (in Experiments II–VII). Additionally, proteinogenic amino acid contents (in Experiments II and V), and contents of macronutrients, micronutrients, and selected toxic elements (in Experiments I–V) were determined.
The technological properties of wheat grain were analyzed using a near-infrared (NIR) grain analyzer (Infratec 1241, FOSS, Hillerød, Denmark) following the manufacturer’s instructions.
The analysis of amino acids in grain was performed by Eurofins Steins Laboratorium (Vejen, Denmark; accredited according to DS-EN ISO/IEC 17025 [51], the Danish Accreditation Fund DANAK Reg. No. 222) according to the standard methods [52] and regulation [53]. Three different methods were used to hydrolyze the plant material for amino acid analysis: alkaline hydrolysis for tryptophan, acid hydrolysis preceded by oxidation for cysteine and methionine, and acid hydrolysis for the remaining amino acids. The hydrolyzed amino acids were quantified via ion exchange chromatography with ultraviolet detection (IC-UV).
Elemental analysis of grain samples was performed by the Chemical Laboratory of Multielemental Analysis at Wrocław University of Science and Technology (Wrocław, Poland; accredited according to PN-EN ISO/IEC 17025, Polish Center for Accreditation Certificate No. AB 696). The Vario Macro Cube Elementar (C,H,N) analyzer (Elementar Analysensysteme, Langenselbold, Germany) was used to analyze the C and N contents of the grain samples, with D-phenylalanine as the standard solution. The contents of other elements were determined using an inductively coupled plasma-optical emission spectrometer (ICP-OES) with a pneumatic nebulizer and axial view (iCAP Duo, Thermo Scientific, Waltham, MA, USA) [54]. The levels of detection (LoD) were 1.0, 2.5, 0.5, 0.025, 1.0, 0.5, 0.04, 0.04, 0.025, 0.025, 0.002, 0.013, 0.05, 0.015, 0.001, 0.005, and 0.01 mg kg−1 for P, K, Ca, Mg, S, B, Cu, Fe, Mn, Mo, Ni, Zn, As, Al, Cd, Cr, and Pb, respectively.

2.4. Statistical Analysis

The effect of P fertilization on the studied grain quality traits was tested for significance using the analysis of variance (ANOVA) or the Kruskal-Wallis test when the assumptions of ANOVA were not met. Statistical analysis was performed for each experiment separately. The normality of variable distribution and homogeneity of variance were verified by applying the Shapiro-Wilk W test and Levene’s test, respectively. For statistical calculations, values of element content below the level of detection (LoD) were replaced by the LoD. Statistical analysis was performed with Statistica 13.3 [55]. When there were no significant differences between fertilizer treatments, only the means, medians and standard errors (SEs) of the variables from the entire experiment are shown in the tables.

3. Results

There was no significant effect of P fertilization (p > 0.05), whether in the form of conventional fertilizers, recycled fertilizers, or biofertilizers, applied at different rates, on the technological traits of wheat grain, i.e., hectoliter weight, hardness index, Zeleny index, starch, wet gluten, and protein content, in any of the experiments under study (II–VII) (Table 3).
The content of essential and non-essential amino acids in wheat grain was not affected by the tested phosphorus fertilization treatments in Experiments II and V (p > 0.05) (Table 4).
No significant changes (p > 0.05) were observed in the content of macronutrients, micronutrients and potentially toxic elements in wheat grain under the applied P fertilization treatments in the experiments studied (I–V) (Table 5 and Table 6).

4. Discussion

Wheat grain quality is influenced by genetics, environment, and management practices, including fertilization [57]. After nitrogen (N), phosphorus (P) is the second limiting element for plant growth, and is usually supplemented with fertilizers. The forms of P in the applied sources and soil characteristics influence the amount of P in the soil solution [58]. The availability of P in the soil solution can lead to improved nutrient uptake by wheat plants, especially N, which ultimately affects the levels of protein, wet gluten, starch, macronutrients and micronutrients in the wheat grain. In addition, it can have a positive impact on hectoliter (test) weight, wheat grain hardness, and Zeleny (sedimentation) index. Hectoliter weight is a measure of the bulk density and soundness of grain [59], wheat grain hardness refers to the endosperm texture and resistance to deformation that affects grinding and milling processes [60], and Zeleny (sedimentation) index is a measure of gluten strength and protein quality [61].
The present study found no significant differences in the effects of recycled and conventional fertilizers on wheat grain technological properties, amino acid and nutrient/element contents, which is a satisfactory result. This finding indicates that neither the form of P carrier nor the dose of P played a significant role in the development of these grain quality characteristics. The studies by Gaj et al. [62] and Boukhalfa-Deraoui et al. [63] found no significant difference in grain protein content as a function of P source used. Similarly, Wołoszyk et al. [64] observed no effect of different waste-derived soil amendments on test weight, protein content, and Zeleny test. In contrast, Jiao et al. [65] observed no variation in N content in durum wheat grain depending on the type of P source (different commercial fertilizers), while the type of P source differentiated P and K content in grain. Although the lower solubility of P compounds in the waste feedstock has been reported elsewhere [23], this potential drawback did not alter grain quality characteristics in the present study.
The lack of response of technological properties of the grain, particularly protein, gluten, and starch content, to an increase in P dosage may be explained by the findings of Agapie and Bostan [66], which suggest that unilaterally applied P does not significantly affect the studied qualitative parameters, but is used as a support for N. Furthermore, the results of the present study are consistent with the findings of Eppendorfer [67] that P affects the amino acid composition of wheat grain only indirectly through its effects on N concentration. Boukhalfa-Deraoui et al. [63] reported that the P application rates (30, 60, 90 and 120 kg P ha−1) were not significant for the protein content of the wheat grain when the N fertilization level was fixed. In the present study, the N rate was the same for all plots within each experiment, including those with no P treatments.
The present study found no significant differences in grain quality between the control (no P) and P-treated plots, regardless of the dose. The results indicate that plants from the control (no P) plots did not experience a P deficit that would contribute to yield quality deterioration, however, P supplementation appeared to help maintain the level of quality traits while increasing yield (Table S5). This could be attributed to the fact that P application stimulates root development, more intensive plant uptake of other nutrients as well as their translocation, assimilation and accumulation of assimilates in the grain [6,7,9], leading to the observed stability in yield quality. According to current knowledge, plants use a variety of molecular, physiological, and ecological mechanisms to maintain nutrient homeostasis [68,69].
Other authors [66,70] have also reported no response of the protein, starch, and wet gluten content in wheat grains, as well as the Zeleny and hardness indices, to P application and increased rates (0–120 kg P2O5 ha−1). No significant effect of P fertilization on protein and amino acid contents was observed by Zheng et al. [71]. Jordan-Meille et al. [72] reported non-significant effects of P treatments (no P; 25–100 kg P ha−1y−1) on the concentration of some macronutrients, micronutrients, and trace elements in wheat grain (long-term experiment). On the other hand, positive responses of protein content [63,73,74,75], hectoliter (test) weight [75,76], gluten content [75] to P application compared to no P treatments have been reported by other authors, with no differences between P rates in some cases [73,74]. In other studies conducted under different environmental conditions, the application of external P was observed to have varying effects on the amino acid [77,78,79,80] and elemental content [81,82] of wheat grain.
Panayotova et al. [83] and Stefanova-Dobreva et al. [75] observed that the over-application of P fertilizer (160 kg P2O5 ha−1) led to a decrease in test weight, protein, and gluten content, particularly when N was not supplied simultaneously [83]. A reduction in grain protein content and zinc (Zn) bioavailability in wheat due to excessive P fertilizer application was reported by Zhang et al. [84]. In the present study, no changes in grain quality were observed when the highest, already yield-ineffective dose of P was applied. With constant N and K fertilization, the excess P could be deposited in the straw, taken up by weeds, immobilized in the soil or leached into the soil profile [42].
Given the role of PSMs in increasing P availability for plant uptake [33,37], this increased P availability can be expected to increase the uptake of other nutrients, particularly N, by the wheat plant, ultimately affecting the quality of the traits studied. However, the present study did not find any evident effect of the PSM strains used in waste-based biofertilizers on grain quality. It is noteworthy that the experiments revealed also a rather weak response of wheat yield to these bioactivators, with more promising results only under poorer habitat conditions (lower soil P content, worse previous crop; Tables S2, S3 and S5). There are many reports in the literature of significant responses of certain crop/cereal quality traits to PSMs when used alone [85,86] or in combination with a P substrate [73,79,87,88]. Most reports relate to increases in seed/grain protein content under PSMs [73,79,86,87,88,89,90,91], but increases in hectoliter weight [92,93], sedimentation value [89], starch content [90], and some amino acids [90] and elements [88,92] have also been demonstrated. The results of the present study, however, are consistent with those that found no effects of PSMs on yield quality: protein content [73,92,94], gluten content [92], hectoliter weight [85,89,91,95], grain hardness [96], and some element contents [89,92]. The effects may also depend on the microbial strain used [73]. The limited effectiveness of applied PSMs as plant growth promoters may be due to their low abundance when introduced with biofertilizers, poor competitiveness with other soil microorganisms [97], and susceptibility to uncontrolled environmental factors under varying field conditions [98].
Primary and secondary raw materials for P fertilizer production often contain potentially toxic elements, and the possibility of these elements accumulating in consumable plant parts, including grain, is a concern [99]. In the present study, the predominant feedstock for recycled fertilizers and the potential source of toxic elements was SSA (Table S1). However, the application of P fertilizers, including products based on SSA, did not change the PTE content in the wheat grain and the content remained below the permitted or recommended limits for plant material intended for human and animal consumption (Table S6). This can be attributed to the low concentration of toxic elements in the fertilizers, reasonable fertilizer application rates and, consequently, negligible PTE input to soil and poor translocation to wheat grain. The PSMs are claimed to affect the levels of toxic elements in wheat grain by influencing their availability, uptake and distribution in the plant. These microbes can immobilize heavy metals and prevent their redistribution in plants through precipitation, binding affinity, and sorption [100,101,102]. Moreover, they can help reduce the translocation and accumulation of toxic elements in wheat grain by improving overall plant health and vigor, nutrient uptake and plant growth [103]. Such phenomena were not observed in the present study. In previous articles by the authors [41,43,56], the issue of PTE levels in soils and plants under the influence of certain recycled P fertilizers was discussed in more detail, and caution was recommended for their repeated application due to the chemical heterogeneity of secondary nutrient sources [104] and the complexity of toxic element fate along the source-pathway-sink/receptor chain [105].

5. Conclusions

Phosphorus biofertilizers made from renewable raw materials, i.e., sewage sludge ash, animal bones, dried animal blood and activated with Bacillus megaterium or Acidithiobacillus ferrooxidans bacteria, similarly to conventional fertilizers, did not affect the technological properties of wheat grain, the content of proteogenic amino acids, macro and micronutrients or selected toxic elements in wheat grain when applied at P doses up to 35.2 kg ha−1.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture14050727/s1, Table S1: Elemental composition of P-fertilizers used in the field experiments; Table S2: Field experiments conducted; experiment details and basic agricultural data; Table S3: Soil characteristics before the start of the experiment; Table S4: Precipitation and air temperature during the study period according to the Meteorological Station in Bałcyny, Poland; Table S5: Wheat yields (t ha−1) under the influence of P treatments in the experiments; Table S6: Reference values for potentially toxic elements (mg kg−1) in plants, according to various sources; references [106,107,108,109,110,111,112,113,114] are used in the Supplementary Materials section.

Author Contributions

Conceptualization, M.J., M.K.K. and A.S.; methodology, M.J., M.K.K. and A.S.; validation, M.J., M.K.K. and A.S.; formal analysis, M.J.; investigation, M.J., M.K.K. and A.S.; resources, M.J., M.K.K. and A.S.; writing—original draft preparation, M.J.; writing—review and editing, M.K.K. and A.S.; visualization, M.J.; funding acquisition, A.S., M.J. and M.K.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Center for Research and Development, Poland, grant number PBS 2/A1/11/2013. The APC was funded by the University of Warmia and Mazury in Olsztyn, Faculty of Agriculture and Forestry, Department of Agroecosystems and Horticulture (grant No. 30.610.015-110).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data is contained within the article and Supplementary Materials.

Acknowledgments

The Institute of New Chemical Synthesis in Puławy is highly acknowledged for providing fertilizers’ batches for field experiments. Authors kindly acknowledge the technical support of the employees from the Department of Agroecosystems and Horticulture of the University of Warmia and Mazury in Olsztyn and from the Production and Experimental Plant ‘Bałcyny’ Sp. z o.o.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Chowdhury, R.B.; Moore, G.A.; Weatherley, A.J.; Arora, M. Key sustainability challenges for the global phosphorus resource, their implications for global food security, and options for mitigation. J. Clean. Prod. 2017, 140, 945–963. [Google Scholar] [CrossRef]
  2. Zhang, X.; Davidson, E.A.; Zou, T.; Lassaletta, L.; Quan, Z.; Li, T.; Zhang, W. Quantifying nutrient budgets for sustainable nutrient management. Glob. Biogeochem. Cycles 2020, 34, e2018GB006060. [Google Scholar] [CrossRef]
  3. Salim, N.; Raza, A. Nutrient use efficiency (NUE) for sustainable wheat production: A review. J. Plant Nutr. 2020, 43, 297–315. [Google Scholar] [CrossRef]
  4. Hermann, L.; McGrath, J.W.; Kabbe, C.; Macintosh, K.A.; van Dijk, K.; Brownlie, W.J. Opportunities for recovering phosphorus from residue streams. In Our Phosphorus Future; Brownlie, W.J., Sutton, M.A., Heal, K.V., Reay, D.S., Spears, B.M., Eds.; UK Centre for Ecology and Hydrology: Edinburgh, UK, 2022; pp. 277–312. [Google Scholar]
  5. Solangi, F.; Zhu, X.; Khan, S.; Rais, N.; Majeed, A.; Sabir, M.A.; Iqbal, R.; Ali, S.; Hafeez, A.; Ali, B.; et al. The global dilemma of soil legacy phosphorus and its improvement strategies under recent changes in agro-ecosystem sustainability. ACS Omega 2023, 8, 23271–23282. [Google Scholar] [CrossRef] [PubMed]
  6. Dissanayaka, D.; Ghahremani, M.; Siebers, M.; Wasaki, J.; Plaxton, W.C. Recent insights into the metabolic adaptations of phosphorus-deprived plants. J. Exp. Bot. 2021, 72, 199–223. [Google Scholar] [CrossRef] [PubMed]
  7. Xu, L.; Yi, K. Unloading phosphate for starch synthesis in cereal grains. Mol. Plant 2021, 14, 1232–1233. [Google Scholar] [CrossRef] [PubMed]
  8. Faucon, M.-P.; Houben, D.; Reynoird, J.-P.; Mercadal-Dulaurent, A.-M.; Armand, R.; Lambers, H. Advances and perspectives to improve the phosphorus availability in cropping systems for agroecological phosphorus management. In Advances in Agronomy; Sparks, D.L., Ed.; Academic Press: Cambridge, MA, USA, 2015; Volume 134, pp. 51–79. [Google Scholar]
  9. Yi, H.; Hu, S.; Zhang, Y.; Wang, X.; Xia, Z.; Lei, Y.; Duan, M. Proper delay of phosphorus application promotes wheat growth and nutrient uptake under low phosphorus condition. Agriculture 2023, 13, 884. [Google Scholar] [CrossRef]
  10. 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]
  11. FAO. FAOSTAT Database 2021, Food and Agriculture Organization of the United Nations. Crops. Available online: http://www.fao.org/faostat/en/#data/QC (accessed on 12 January 2024).
  12. USGS. Mineral Commodity Summaries 2024. Phosphate Rock; USGS: Reston, VA, USA, 2024; pp. 134–135.
  13. Mew, M.C. Why and when do reserves estimates in mining change and innovations take place? Ecol. Econ. 2024, 217, 108085. [Google Scholar] [CrossRef]
  14. Stamm, C.; Binder, C.R.; Frossard, E.; Haygarth, P.M.; Oberson, A.; Richardson, A.E.; Schaum, C.; Schoumans, O.; Udert, K.M. Towards circular phosphorus: The need of inter- and transdisciplinary research to close the broken cycle. Ambio 2022, 51, 611–622. [Google Scholar] [CrossRef] [PubMed]
  15. EC. Study on the Critical Raw Materials for the EU 2023–Final Report; Publications Office of the European Union: Luxemburg, 2023; p. 158. [Google Scholar]
  16. Szołdrowska, D.; Smol, M. Chapter 18—Phosphorus raw materials in sustainable agriculture. In Sustainable and Circular Management of Resources and Waste towards a Green Deal; Vara Prasad, M.N., Smol, M., Eds.; Elsevier: Amsterdam, The Netherlands, 2023; pp. 247–255. [Google Scholar]
  17. Brownlie, W.J.; Sutton, M.A.; Cordell, D.; Reay, D.S.; Heal, K.V.; Withers, P.J.A.; Vanderbeck, I.; Spears, B.M. Phosphorus price spikes: A wake-up call for phosphorus resilience. Front. Sustain. Food Syst. 2023, 7, 1088776. [Google Scholar] [CrossRef]
  18. Brownlie, W.J.; Spears, B.M.; Heal, K.V.; Reay, D.S.; Sutton, M.A.; Benton, T.G.; Cordell, D.; Heathwaite, A.L.; Hermann, L.; Penny, J.J.; et al. Towards our phosphorus future. In Our Phosphorus Future; Brownlie, W.J., Sutton, M.A., Heal, K.V., Reay, D.S., Spears, B.M., Eds.; UK Centre for Ecology and Hydrology: Edinburgh, UK, 2022; pp. 339–369. [Google Scholar]
  19. Brownlie, W.J.; Sutton, M.A.; de Boer, M.A.; Camprubí, L.; Hamilton, H.A.; Heal, K.V.; Morgandi, T.; Neset, T.-S.; Spears, B.M. Phosphorus reserves, resources and uses. In Our Phosphorus Future; Brownlie, W.J., Sutton, M.A., Heal, K.V., Reay, D.S., Spears, B.M., Eds.; UK Centre for Ecology and Hydrology: Edinburgh, UK, 2022; pp. 21–71. [Google Scholar]
  20. Brownlie, W.J.; Sakrabani, R.; Metson, G.S.; Blackwell, M.S.A.; Spears, B.M. Opportunities to recycle phosphorus-rich organic materials. In Our Phosphorus Future; Brownlie, W.J., Sutton, M.A., Heal, K.V., Reay, D.S., Spears, B.M., Eds.; UK Centre for Ecology and Hydrology: Edinburgh, UK, 2022; pp. 219–270. [Google Scholar]
  21. Kabbe, C.; Rinck-Pfeiffer, S. Global Compendium on Phosphorus Recovery from Sewage/Sludge/Ash; Christian Kabbe: Berlin, Germany, 2019. [Google Scholar]
  22. Severin, M.; Breuer, J.; Rex, M.; Stemann, J.; Adam, C.; Van den Weghe, H.; Kücke, M. Phosphate fertilizer value of heat treated sewage sludge ash. Plant Soil Environ. 2014, 60, 555–561. [Google Scholar] [CrossRef]
  23. Huygens, D.; Saveyn, H.G.M. Agronomic efficiency of selected phosphorus fertilisers derived from secondary raw materials for European agriculture. A meta-analysis. Agron. Sustain. Dev. 2018, 38, 52. [Google Scholar] [CrossRef]
  24. Kratz, S.; Vogel, C.; Adam, C. Agronomic performance of P recycling fertilizers and methods to predict it: A review. Nutr. Cycl. Agroecosyst. 2019, 115, 1–39. [Google Scholar] [CrossRef]
  25. Grames, J.; Zoboli, O.; Laner, D.; Rechberger, H.; Zessner, M.; Sánchez-Romero, M.; Prskawetz, A. Understanding feedbacks between economic decisions and the phosphorus resource cycle: A general equilibrium model including material flows. Resour. Policy 2019, 61, 311–347. [Google Scholar] [CrossRef]
  26. Raniro, H.R.; Soares, T.d.M.; Adam, C.; Pavinato, P.S. Waste-derived fertilizers can increase phosphorus uptake by sugarcane and availability in a tropical soil. J. Plant Nutr. Soil Sci. 2022, 185, 391–402. [Google Scholar] [CrossRef]
  27. Günther, S.; Grunert, M.; Müller, S. Overview of recent advances in phosphorus recovery for fertilizer production. Eng. Life Sci. 2018, 18, 434–439. [Google Scholar] [CrossRef] [PubMed]
  28. EU. Regulation (EU) 2019/1009 of the European Parliament and of the Council of 5 June 2019 laying down rules on the making available on the market of EU fertilising products and amending Regulations (EC) No 1069/2009 and (EC) No 1107/2009 and repealing Regulation (EC) No 2003/2003 (Text with EEA relevance). Off. J. Eur. Union 2019, L170, 1–114. [Google Scholar]
  29. Boix-Fayos, C.; de Vente, J. Challenges and potential pathways towards sustainable agriculture within the European Green Deal. Agric. Syst. 2023, 207, 103634. [Google Scholar] [CrossRef]
  30. Saeid, A. Phosphorus microbial solubilization as a key for phosphorus recycling in agriculture. In Phosphorus-Recovery and Recycling; Zhang, T., Ed.; IntechOpen: London, UK, 2018. [Google Scholar]
  31. Alori, E.T.; Glick, B.R.; Babalola, O.O. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front. Microbiol. 2017, 8, 971. [Google Scholar] [CrossRef] [PubMed]
  32. Sarmah, R.; Sarma, A.K. Phosphate solubilizing microorganisms: A Review. Commun. Soil Sci. Plant Anal. 2023, 54, 1306–1315. [Google Scholar] [CrossRef]
  33. Zhu, J.; Li, M.; Whelan, M. Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: A review. Sci. Total Environ. 2018, 612, 522–537. [Google Scholar] [CrossRef] [PubMed]
  34. Galavi, M.; Yosefi, K.; Ramrodi, M.; Mousavi, S.R. Effect of bio-phosphate and chemical phosphorus fertilizer accompanied with foliar application of micronutrients on yield, quality and phosphorus and zinc concentration of maize. J. Agric. Sci. 2011, 3, 22. [Google Scholar] [CrossRef]
  35. Qian, T.; Yang, Q.; Jun, D.C.F.; Dong, F.; Zhou, Y. Transformation of phosphorus in sewage sludge biochar mediated by a phosphate-solubilizing microorganism. Chem. Eng. J. 2019, 359, 1573–1580. [Google Scholar] [CrossRef]
  36. Torres-Cuesta, D.; Mora-Motta, D.; Chavarro-Bermeo, J.P.; Olaya-Montes, A.; Vargas-Garcia, C.; Bonilla, R.; Estrada-Bonilla, G. Phosphate-solubilizing bacteria with low-solubility fertilizer improve soil P availability and yield of kikuyu grass. Microorganisms 2023, 11, 1748. [Google Scholar] [CrossRef] [PubMed]
  37. Wang, Y.-Y.; Li, P.-S.; Zhang, B.-X.; Wang, Y.-P.; Meng, J.; Gao, Y.-F.; He, X.-M.; Hu, X.-M. Identification of phosphate-solubilizing microorganisms and determination of their phosphate-solubilizing activity and growth-promoting capability. BioResources 2020, 15, 2560–2578. [Google Scholar] [CrossRef]
  38. Mącik, M.; Gryta, A.; Frąc, M. Chapter Two—Biofertilizers in agriculture: An overview on concepts, strategies and effects on soil microorganisms. In Advances in Agronomy; Sparks, D.L., Ed.; Academic Press: Cambridge, MA, USA, 2020; Volume 162, pp. 31–87. [Google Scholar]
  39. Saeid, A.; Wyciszkiewicz, M.; Jastrzebska, M.; Chojnacka, K.; Gorecki, H. A concept of production of new generation of phosphorus-containing biofertilizers. BioFertP project. Przem. Chem. 2015, 94, 361–365. [Google Scholar] [CrossRef]
  40. Jastrzębska, M.; Kostrzewska, M.; Treder, K.; Makowski, P.; Saeid, A.; Jastrzębski, W.; Okorski, A. Fertiliser from sewage sludge ash instead of conventional phosphorus fertilisers? Plant Soil Environ. 2018, 64, 504–511. [Google Scholar] [CrossRef]
  41. Jastrzȩbska, M.; Saeid, A.; Kostrzewska, M.K.; Basladyńska, S. New phosphorus biofertilizers from renewable raw materials in the aspect of cadmium and lead contents in soil and plants. Open Chem. 2018, 16, 35–49. [Google Scholar] [CrossRef]
  42. Jastrzębska, M.; Kostrzewska, M.K.; Saeid, A. Can phosphorus from recycled fertilisers replace conventional sources? An agronomic evaluation in field-scale experiments on temperate Luvisols. Appl. Sci. 2019, 9, 2086. [Google Scholar] [CrossRef]
  43. Jastrzębska, M.; Kostrzewska, M.K.; Saeid, A.; Jastrzębski, W.P. Do new-generation recycled phosphorus fertilizers increase the content of potentially toxic elements in soil and plants? Minerals 2021, 11, 999. [Google Scholar] [CrossRef]
  44. Jastrzębska, M.; Kostrzewska, M.K.; Saeid, A. Phosphorus fertilizers from sewage sludge ash and animal blood as an example of biobased environment-friendly agrochemicals: Findings from field experiments. Molecules 2022, 27, 2769. [Google Scholar] [CrossRef] [PubMed]
  45. Helguera, M.; Abugalieva, A.; Battenfield, S.; Békés, F.; Branlard, G.; Cuniberti, M.; Hüsken, A.; Johansson, E.; Morris, C.F.; Nurit, E.; et al. Grain Quality in Breeding. In Wheat Quality for Improving Processing and Human Health; Igrejas, G., Ikeda, T.M., Guzmán, C., Eds.; Springer International Publishing: Cham, Switzerland, 2020; pp. 273–307. [Google Scholar]
  46. Singh, A.; Gupta, O.P.; Pandey, V.; Ram, S.; Kumar, S.; Singh, G.P. Physicochemical Components of Wheat Grain Quality and Advances in Their Testing Methods. In New Horizons in Wheat and Barley Research: Global Trends, Breeding and Quality Enhancement; Kashyap, P.L., Gupta, V., Prakash Gupta, O., Sendhil, R., Gopalareddy, K., Jasrotia, P., Singh, G.P., Eds.; Springer: Singapore, 2022; pp. 741–757. [Google Scholar]
  47. Baniwal, P.; Mehra, R.; Kumar, N.; Sharma, S.; Kumar, S. Cereals: Functional constituents and its health benefits. Pharma Innov. 2021, 10, 343–349. [Google Scholar] [CrossRef]
  48. Sabiha, J.; Siddque, N.; Waheed, S.; uz Zaman, Q.; Aslam, A.; Tufail, M.; Nasir, R. Uptake of heavy metal in wheat from application of different phosphorus fertilizers. J. Food Compos. Anal. 2023, 115, 104958. [Google Scholar] [CrossRef]
  49. Wyciszkiewicz, M.; Saeid, A.; Malinowski, P.; Chojnacka, K. Valorization of phosphorus secondary raw materials by Acidithiobacillus ferrooxidans. Molecules 2017, 22, 473. [Google Scholar] [CrossRef] [PubMed]
  50. WRB. World reference base for soil resources 2014. In International Soil Classification System for Naming Soils and Creating Legends for Soil Maps; Food and Agriculture Organization of the United Nations: Rome, Italy, 2014. [Google Scholar]
  51. ISO/IEC 17025; Testing and calibration laboratories. ISO: Geneva, Switzerland, 2017.
  52. ISO 13903:2005; Animal Feeding Stuffs—Determination of Amino Acids Content. ISO: Geneva, Switzerland, 2005; p. 11.
  53. EC. Commission Regulation (EC) No. 152/2009 laying down the methods of sampling and analysis for the official control of feed. Off. J. Eur. Union 2009, L54, 1–130. [Google Scholar]
  54. Górecka, H.; Chojnacka, K.; Górecki, H. The application of ICP-MS and ICP-OES in determination of micronutrients in wood ashes used as soil conditioners. Talanta 2006, 70, 950–956. [Google Scholar] [CrossRef] [PubMed]
  55. StatSoft Inc. Statistica (Data Analysis Software System), Version 13.3; TIBCO Software Inc.: Palo Alto, CA, USA, 2017. [Google Scholar]
  56. Jastrzębska, M.; Kostrzewska, M.K.; Saeid, A. Sewage sludge ash-based biofertilizers as a circular approach to phosphorus: The issue of fe and al in soil and wheat and weed plants. Agronomy 2022, 12, 1475. [Google Scholar] [CrossRef]
  57. Nuttall, J.G.; O’Leary, G.J.; Panozzo, J.F.; Walker, C.K.; Barlow, K.M.; Fitzgerald, G.J. Models of grain quality in wheat—A review. Field Crops Res. 2017, 202, 136–145. [Google Scholar] [CrossRef]
  58. Wang, Y.; Zhang, W.; Müller, T.; Lakshmanan, P.; Liu, Y.; Liang, T.; Wang, L.; Yang, H.; Chen, X. Soil phosphorus availability and fractionation in response to different phosphorus sources in alkaline and acid soils: A short-term incubation study. Sci. Rep. 2023, 13, 5677. [Google Scholar] [CrossRef] [PubMed]
  59. Manley, M.; Engelbrecht, M.L.; Williams, P.C.; Kidd, M. Assessment of variance in the measurement of hectolitre mass of wheat, using equipment from different grain producing and exporting countries. Biosyst. Eng. 2009, 103, 176–186. [Google Scholar] [CrossRef]
  60. Kaliniewicz, Z.; Markowska-Mendik, A.; Warechowska, M. An analysis of the correlations between the hardness index and selected physicochemical properties of wheat grain. J. Cereal Sci. 2023, 110, 103643. [Google Scholar] [CrossRef]
  61. Schuster, C.; Huen, J.; Scherf, K.A. Comprehensive study on gluten composition and baking quality of winter wheat. Cereal Chem. 2023, 100, 142–155. [Google Scholar] [CrossRef]
  62. Gaj, R.; Górski, D.; Przybył, J. Effect of differentiated phosphorus and potassium fertilization on winter wheat yield and quality. J. Elem. 2013, 18, 55–67. [Google Scholar] [CrossRef]
  63. Boukhalfa-Deraoui, N.; Hanifi-Mekliche, L.; Mekliche, A.; Cheloufi, H.; Babahani, S. Influence of phosphorus fertilizers application on phosphorus use efficiency and grain protein of winter wheat in alkaline-calcareous soil, Southern Algeria. Indian J. Agric. Res. 2020, 54, 51–57. [Google Scholar] [CrossRef]
  64. Woloszyk, C.; Stankowski, S.; Izewska, A.; Swiderska-Ostapiak, M. Wpływ następczy kompostów z komunalnego osadu sciekowego z dodatkiem różnych komponentów, przy dwóch poziomach NPK, na wielkość plonu i jakość ziarna pszenicy ozimej. Zesz. Probl. Post. Nauk Rol. 2003, 494, 551–557. [Google Scholar]
  65. Jiao, W.; Chen, W.; Chang, A.C.; Page, A.L. Environmental risks of trace elements associated with long-term phosphate fertilizers applications: A review. Environ. Pollut. 2012, 168, 44–53. [Google Scholar] [CrossRef] [PubMed]
  66. Agapie, A.L.; Bostan, C. The influence of mineral fertilization on the quality of winter wheat. Life Sci. Sustain. Dev. 2021, 1, 45–50. [Google Scholar] [CrossRef]
  67. Eppendorfer, W.H. Effects of nitrogen, phosphorus and potassium on amino acid composition and on relationships between nitrogen and amino acids in wheat and oat grain. J. Sci. Food Agric. 1978, 29, 995–1001. [Google Scholar] [CrossRef]
  68. Khan, M.I.R.; Nazir, F.; Maheshwari, C.; Chopra, P.; Chhillar, H.; Sreenivasulu, N. Mineral nutrients in plants under changing environments: A road to future food and nutrition security. Plant Genome 2023, 16, e20362. [Google Scholar] [CrossRef] [PubMed]
  69. Naz, F. Plant nutrition, transport, mechanism and sensing in plants. In Sustainable Plant Nutrition; Aftab, T., Hakeem, K.R., Eds.; Academic Press: Cambridge, MA, USA, 2023; pp. 209–228. [Google Scholar]
  70. Kizilgeci, F. Physiological, agronomical and quality response of bread wheat to phosphorus application under dryland condition. Appl. Ecol. Environ. Res. 2019, 17, 1979–1987. [Google Scholar] [CrossRef]
  71. Zheng, Z.-S.; Wang, C.-Y.; Niu, J.-Y.; Zhang, M.-W.; Zhang, J.; Yao, Y.-Q. Effects of irrigation and fertilization coupling on protein and amino acids contents in grains of winter wheat. Chin. J. Eco-Agric. 2011, 19, 788–793. [Google Scholar] [CrossRef]
  72. Jordan-Meille, L.; Holland, J.E.; McGrath, S.P.; Glendining, M.J.; Thomas, C.L.; Haefele, S.M. The grain mineral composition of barley, oat and wheat on soils with pH and soil phosphorus gradients. Eur. J. Agron. 2021, 126, 126281. [Google Scholar] [CrossRef]
  73. Moradi, M.; Siadat, S.A.; Khavazi, K.; Naseri, R.; Maleki, A.; Mirzaei, A. Effect of application of biofertilizers and phosphorus fertilizers on qualitative and quantitative traits of spring wheat (Triticum aestivum L.). Crop Ecophysiol. 2011, 5, 51–66. [Google Scholar]
  74. Feng, K.K.; Zhang, Y.F.; Feng, M.C.; Wang, H.Y.; Wan, G.C.; Yang, W.D. Combined nitrogen and phosphorus application synergistically regulate grain yield and protein content in winter wheat (Triticum aestivum L.). Appl. Ecol. Environ. Res. 2022, 20, 1599–1611. [Google Scholar] [CrossRef]
  75. Stefanova-Dobreva, S.; Muhova, A.; Bonchev, B. Nitrogen and phosphorus fertilizers affecting the quality and quantity of the durum wheat. Sci. Papers Ser. A. Agron. 2022, 65, 533–539. [Google Scholar]
  76. Fana, G.; Deressa, H.; Dargie, R.; Bogale, M.; Mehadi, S.; Getachew, F. Grain hardness, hectolitre weight, nitrogen and phosphorus concentrations of durum wheat (Triticum turgidum L.var. Durum) as influenced by nitrogen and phosphorus fertilisation. World Appl. Sci. J. 2012, 20, 1322–1327. [Google Scholar]
  77. Tanács, L.; Matuz, J.; Bartók, T.; Gerö, L. Effect of NPK fertilization on the individual amino acid content of wheat grain. Cereal Res. Commun. 1995, 23, 403–409. [Google Scholar]
  78. Mishra, L.K. Effect of phosphorus and zinc fertilization on biochemical composition of wheat. Bioscan 2012, 7, 445–449. [Google Scholar]
  79. Chaikovskaya, L.; Iakusheva, N.; Ovsienko, O.; Radchenko, L.; Pashtetskiy, V.; Baranskaya, M. Influence of microbial preparations on Triticum aestivum L. grain quality. Int. J. Plant Biol. 2022, 13, 535–545. [Google Scholar] [CrossRef]
  80. Kumar, A.; Behera, U.K.; Dhar, S.; Babu, S.; Singh, R.; Upadhyay, P.K.; Saha, S.; Devadas, R.; Kumar, A.; Gupta, G.; et al. Deciphering the role of phosphorus management under conservation agriculture based wheat production system. Front. Sustain. Food Syst. 2023, 7, 1235141. [Google Scholar] [CrossRef]
  81. Gaj, R.; Górski, D. Effects of different phosphorus and potassium fertilization on contents and uptake of macronutrients (N, P, K, Ca, Mg) in winter wheat I. Content of macronutrients. J. Cent. Eur. Agric. 2014, 15, 169–187. [Google Scholar] [CrossRef]
  82. Rawal, N.; Pande, K.R.; Shrestha, R.; Vista, S.P. Nutrient concentration and its uptake in various stages of wheat (Triticum aestivum L.) as influenced by nitrogen, phosphorus, and potassium fertilization. Commun. Soil Sci. Plant Anal. 2023, 54, 1151–1166. [Google Scholar] [CrossRef]
  83. Panayotova, G.; Kostadinova, S.; Valkova, N. Grain quality of durum wheat as affected by phosphorus and combined nitrogen-phosphorus fertilization. Sci. Papers Ser. A Agron. 2017, 60, 356–363. [Google Scholar]
  84. Zhang, W.; Liu, D.; Liu, Y.; Chen, X.; Zou, C. Overuse of phosphorus fertilizer reduces the grain and flour protein contents and zinc bioavailability of winter wheat (Triticum aestivum L.). J. Agric. Food Chem. 2017, 65, 1473–1482. [Google Scholar] [CrossRef] [PubMed]
  85. Bulut, S. Evaluation of yield and quality parameters of phosphorous-solubilizing and N-fixing bacteria inoculated in wheat (Triticum aestivum L.). Turk. J. Agric. For. 2013, 37, 545–554. [Google Scholar] [CrossRef]
  86. Shabbir, I.; Ayub, M.; Tahir, M.; Ahmad, R. Effect of phosphorus solubilizing bacterial inoculation and phosphorus fertilizer application on forage yield and quality of oat (Avena sativa L.). Int. J. Mod. Agric. 2020, 2, 85–94. [Google Scholar]
  87. Zafar, M.; Rahim, N.; Shaheen, A.; Khaliq, A.; Arjamand, T.; Jamil, M.; Rehman, Z.-U.; Sultan, T. Effect of combining poultry manure, inorganic phosphorus fertilizers and phosphate solublizing bacteria on growth, yield, protein content and P uptake in maize. Adv. Agric. Bot. 2011, 3, 46–58. [Google Scholar]
  88. Majeed, A.; Farooq, M.; Naveed, M.; Hussain, M. Combined application of inorganic and organic phosphorous with inoculation of phosphorus solubilizing bacteria improved productivity, grain quality and net economic returns of pearl millet (Pennisetum glaucum [L.] R. Br.). Agronomy 2022, 12, 2412. [Google Scholar] [CrossRef]
  89. Erdemci, I.; Aktas, H.; Eren, A. Quantitative and qualitative response of wheat to Pseudomonas fluorescens rhizobacteria application. J. Anim. Plant Sci. 2019, 29, 476–482. [Google Scholar]
  90. Harish, M.N.; Choudhary, A.K.; Kumar, S.; Dass, A.; Singh, V.K.; Sharma, V.K.; Varatharajan, T.; Dhillon, M.K.; Sangwan, S.; Dua, V.K.; et al. Double zero tillage and foliar phosphorus fertilization coupled with microbial inoculants enhance maize productivity and quality in a maize–wheat rotation. Sci. Rep. 2022, 12, 3161. [Google Scholar] [CrossRef] [PubMed]
  91. Çağlar, Ö.; Bulut, S.; Öztürk, A. Determination of yield parameters of barley (Hordeum vulgare L.) inoculated with phosphorous-solubilizing and nitrogen-fixing bacteria. Pol. J. Environ. Stud. 2024, 33, 1033–1042. [Google Scholar] [CrossRef] [PubMed]
  92. Erdemci, İ. Effects of seed microbial inoculant on growth, yield, and nutrition of durum wheat (Triticum Durum L.). Commun. Soil Sci. Plant Anal. 2021, 52, 792–801. [Google Scholar] [CrossRef]
  93. Youssef, S.M.; Shaaban, A.; Abdelkhalik, A.; Abd El Tawwab, A.R.; Abd Al Halim, L.R.; Rabee, L.A.; Alwutayd, K.M.; Ahmed, R.M.M.; Alwutayd, R.; Hemida, K.A. Compost and phosphorus/potassium-solubilizing fungus effectively boosted quinoa’s physio-biochemical traits, nutrient acquisition, soil microbial community, and yield and quality in normal and calcareous soils. Plants 2023, 12, 3071. [Google Scholar] [CrossRef] [PubMed]
  94. Moradgholi, A.; Mobasser, H.; Ganjali, H.; Fanaie, H.; Mehraban, A. WUE, protein and grain yield of wheat under the interaction of biological and chemical fertilizers and different moisture regimes. Cereal Res. Commun. 2022, 50, 147–155. [Google Scholar] [CrossRef]
  95. Sonkurt, M.; Çiğ, F. The effect of plant growth-promoting bacteria on the development, yield and yield components of bread (Triticum aestivum L.) and durum (Triticum durum) wheats. Appl. Ecol. Environ. Res. 2019, 17, 3877–3896. [Google Scholar] [CrossRef]
  96. Rostamian, A.; Moaveni, P.; MehdiSadeghi, S.; Mozafari, H.; Rajabzadeh, F. Effective drought mitigation by rhizobacteria consortium in wheat field trials. Rhizosphere 2023, 25, 100653. [Google Scholar] [CrossRef]
  97. Raymond, N.S.; Jensen, L.S.; van der Bom, F.; Nicolaisen, M.H.; Müller-Stöver, D. Fertilising effect of sewage sludge ash inoculated with the phosphate-solubilising fungus Penicillium bilaiae under semi-field conditions. Biol. Fert. Soils 2019, 55, 43–51. [Google Scholar] [CrossRef]
  98. Sárdi, K. Short-Term Transformation and Dynamics of Main Nutrients in Soil. In Essential Plant Nutrients: Uptake, Use Efficiency, and Management; Naeem, M., Ansari, A.A., Gill, S.S., Eds.; Springer International Publishing: Cham, Switzerland, 2017; pp. 379–401. [Google Scholar]
  99. Iżewska, A.; Wołoszyk, C. Contents of heavy metals in plants and soil fertilization of ash from sewage sludge combustion. Ecol. Chem. Eng. A 2013, 20, 1019–1027. [Google Scholar] [CrossRef] [PubMed]
  100. Yuan, Z.; Yi, H.; Wang, T.; Zhang, Y.; Zhu, X.; Yao, J. Application of phosphate solubilizing bacteria in immobilization of Pb and Cd in soil. Environ. Sci. Pollut. Res. 2017, 24, 21877–21884. [Google Scholar] [CrossRef] [PubMed]
  101. Xu, J.-C.; Huang, L.-M.; Chen, C.; Wang, J.; Long, X.-X. Effective lead immobilization by phosphate rock solubilization mediated by phosphate rock amendment and phosphate solubilizing bacteria. Chemosphere 2019, 237, 124540. [Google Scholar] [CrossRef] [PubMed]
  102. Nawaz, A.; Nawaz, H.; Khan, K.; Haq, M.U.; Khan, H.; Manan, U.; Tariq, M. Integrated effect of heavy metal-tolerant rhizobacteria and phosphorus on maize growth and phosphorus bioavailability in contaminated soil. J. Soil Plant Environ. 2023, 2, 21–52. [Google Scholar] [CrossRef]
  103. Saeed, Q.; Xiukang, W.; Haider, F.U.; Kučerik, J.; Mumtaz, M.Z.; Holatko, J.; Naseem, M.; Kintl, A.; Ejaz, M.; Naveed, M.; et al. Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: A comprehensive review of effects and mechanisms. Int. J. Mol. Sci. 2021, 22, 529. [Google Scholar] [CrossRef] [PubMed]
  104. Smol, M.; Adam, C.; Kugler, S.A. Thermochemical treatment of Sewage Sludge Ash (SSA)-potential and perspective in Poland. Energies 2020, 13, 5461. [Google Scholar] [CrossRef]
  105. Chetyrbotskiy, V.A.; Chetyrbotskiy, A.N.; Levin, B.V. Mathematical modeling of the dynamics of plant mineral nutrition in the fertilizer–soil–plant system. Biophysics 2020, 65, 1036–1045. [Google Scholar] [CrossRef]
  106. Kabata-Pendias, A. Trace Elements in Soils and Plants, 4th ed.; CRC Press: Boca Raton, FL, USA, 2010; pp. 1–520. [Google Scholar]
  107. Kabata-Pendias, A.; Pendias, H. Biogeochemistry of Trace Elements; Polish Scientific Publishing Company: Warsaw, Poland, 1999; pp. 1–400. [Google Scholar]
  108. MH-PL. Ordinance by the Minister of Health (Poland) of 13 January 2003 on maximum concentrations of chemical and biological impurities which may be present in food, food ingredients, permitted supplementary substances and substances helpful in food processing. J. Laws 2003, 37, 326. [Google Scholar]
  109. MARD-PL. Ordinance by the Minister of Agriculture and Rural Development (Poland) of 25 August 2014 amending the ordinance on the content of undesirable substances in animal feed. J. Laws 2014, 37, 1213. [Google Scholar]
  110. MARD-PL. Ordinance by the Minister of Agriculture and Rural Development (Poland) of 29 June 2019 amending the ordinance on the content of undesirable substances in animal feed. J. Laws 2018, 2018, 1213. [Google Scholar]
  111. FAO-WHO. Codex Alimentarius. General Standard for Contaminants and Toxins in Food and Feed. CXS 193-1995; Food and Agricultural Organization of the United Nation, World Health Organization: Rome, Italy, 2023. [Google Scholar]
  112. EU. Commission Regulation (EU) 2023/915 of 25 April 2023 on maximum levels for certain contaminants in food and repealing Regulation (EC) No 1881/2006 (Text with EEA relevance). Off. J. Eur. Union 2023, L119, 103–157. [Google Scholar]
  113. USDA-FAS. China Releases the Standard for Maximum Levels of Contaminants in Foods; Foreign Agricultural Service, GAIN Report Number CH2023-0040; U.S. Department of Agriculture: Washington, DC, USA, 2023. [Google Scholar]
  114. Kabata-Pendias, A.; Motowicka-Terelak, T.; Piotrowska, M.; Terelak, H.; Witek, T. Ocena stopnia zanieczyszczenia gleb i roślin metalami ciężkimi i siarką. Ramowe Wytyczne Dla Rolnictwa. IUNG Puławy 1993, 53, 1–20. [Google Scholar]
Table 1. Biofertilizers tested in the field experiments.
Table 1. Biofertilizers tested in the field experiments.
SymbolRaw MaterialBacteria
Suspension biofertilizers
AsBmSewage sludge ash 1Bacillus megaterium 3
BsBmAnimal bones 2Bacillus megaterium
Granular biofertilizers
AgAfSewage sludge ashAcidithiobacillus ferrooxidans 4
ABgAfSewage sludge ash + animal bonesAcidithiobacillus ferrooxidans
ABgBmSewage sludge ash + animal bonesBacillus megaterium
AHgBmSewage sludge ash + dried animal blood 2Bacillus megaterium
1 from the ‘Łyna’ Municipal Wastewater Treatment Plant in Olsztyn, Poland; 2 from the meat industry; 3 from the Polish Collection of Microorganisms at the Institute of Immunology and Experimental Therapy of the Polish Academy of Sciences in Wrocław, Poland; 4 from Professor Zygmunt Sadowski, Wroclaw University of Science and Technology (strain isolated from the tailings impoundment “Iron Bridge”, Poland) [49].
Table 2. Basic data on the experiments performed.
Table 2. Basic data on the experiments performed.
ExperimentBiofertilizers TestedReference TreatmentsP Doses, kg ha−1P-Treatment Number (n)Test CropGrowing Season
IAsBm, BsBmno P, SP, PR, A + H2O0, 216 (24)Spring wheat2014
IIAsBmno P, SP, PR0, 17.6, 26.4, 35.210 (80)Spring wheat2015
IIIAgAf, ABgAfno P, SP0, 17.6, 26.4, 35.210 (40)Winter wheat2014/2015
IVABgBmno P, SP, ABg0, 17.6, 26.4, 35.210 (40)Winter wheat2015/2016
VAHgBmno P, SP, AHg0, 17.6, 26.4, 35.210 (40)Spring wheat2016
VIAHgBmno P, SP, AHg0, 17.6, 26.4, 35.210 (40)Winter wheat2016/2017
VIIAHgBmno P, SP, AHg0, 17.6, 26.4, 35.210 (40)Spring wheat2017
Table 3. Technological traits of wheat grain; means, medians, standard errors (SE), and p-values for ANOVA or Kruskal-Wallis tests for all phosphorus treatments in the individual experiments 1.
Table 3. Technological traits of wheat grain; means, medians, standard errors (SE), and p-values for ANOVA or Kruskal-Wallis tests for all phosphorus treatments in the individual experiments 1.
TraitsStatisticsExperiments
IIIIIIVVVIVII
Hectoliter (test) weight, kg/hLmean79.683.076.976.779.475.1
median79.783.176.976.779.475.1
SE0.080.060.050.080.080.12
p0.7710.8160.8510.8420.9910.719
Hardness indexmean87.495.050.959.067.454.0
median81.596.651.258.167.754.2
SE2.891.160.480.560.470.36
p0.4710.1880.6930.1330.3970.849
Zeleny (sedimentation) indexmean50.033.332.744.523.838.3
median45.532.632.444.623.938.3
SE0.480.490.360.340.250.42
p0.8600.9690.8550.8410.8420.817
Starch content, %mean67.370.869.968.169.468.3
median65.870.969.968.169.468.4
SE0.320.090.080.060.060.06
p0.8450.2220.8670.7940.9870.509
Wet gluten content, %mean33.226.424.328.221.326.3
median33.426.324.228.321.426.3
SE0.280.180.150.120.100.13
p0.8770.9400.9220.8870.9820.872
Protein content, %mean14.311.811.913.310.312.6
median14.211.711.913.310.312.6
SE0.060.060.050.040.040.05
p0.9960.8760.7820.9870.9800.883
1 no significant differences between phosphorus treatments in the individual experiments (p > 0.05).
Table 4. Contents of amino acids in wheat grain (g kg−1 DM); means, medians, standard errors (SE), and p-values for ANOVA or Kruskal-Wallis tests for all phosphorus treatments in the individual experiments 1.
Table 4. Contents of amino acids in wheat grain (g kg−1 DM); means, medians, standard errors (SE), and p-values for ANOVA or Kruskal-Wallis tests for all phosphorus treatments in the individual experiments 1.
Essential Amino AcidsStatisticsExperimentsNon-Essential Amino AcidsStatisticsExperiments
IIVIIV
Histidinemean2.992.74Alaninemean4.634.20
median2.992.75 median4.634.21
SE0.020.02 SE0.030.03
p0.9890.593 p0.9820.667
Isoleucinemean4.473.97Argininemean6.215.69
median4.446.96 median6.205.72
SE0.030.03 SE0.050.06
p0.9900.921 p0.9460.379
Leucinemean9.018.06Aspartic acidmean6.785.91
median8.938.05 median6.785.88
SE0.060.07 SE0.050.06
p0.9830.585 p0.7480.396
Lysinemean3.523.32Cysteinemean2.812.55
median3.523.28 median2.832.57
SE0.020.05 SE0.020.02
p0.9910.689 p0.7960.352
Methioninemean2.081.85Glutamic acidmean43.837.1
median2.101.88 median43.637.0
SE0.020.02 SE0.420.35
p0.4970.161 p0.9150.752
Phenylalaninemean6.455.60Glycinemean5.635.09
median6.415.62 median5.605.10
SE0.050.05 SE0.040.04
p0.9850.377 p0.9850.602
Threoninemean3.913.51Prolinemean14.212.2
median3.923.51 median14.112.3
SE0.030.03 SE0.140.11
p0.9180.576 p0.9980.692
Tryptophanmean1.531.41Serinemean6.615.77
median1.541.42 median6.595.77
SE0.010.01 SE0.060.07
p0.4370.617 p0.9920.523
Valinemean5.625.14Tyrosinemean3.613.23
median5.595.14 median3.603.22
SE0.030.04 SE0.030.05
p0.9920.903 p0.9880.697
1 no significant differences between phosphorus treatments in the individual experiments (p > 0.05).
Table 5. Contents of macroelements in wheat grain (g kg−1 DM); means, medians, standard errors (SE), and p-values for ANOVA or Kruskal-Wallis tests for all phosphorus treatments in the individual experiments 1.
Table 5. Contents of macroelements in wheat grain (g kg−1 DM); means, medians, standard errors (SE), and p-values for ANOVA or Kruskal-Wallis tests for all phosphorus treatments in the individual experiments 1.
ElementsStatisticsExperiments
IIIIIIIVV
P 2mean3.633.511.972.843.84
median3.623.491.982.843.83
SE0.0240.0270.0250.0140.018
p0.2910.1410.3590.7950.995
Cmean406409341416413
median405406341416413
SE0.461.521.850.250.28
p0.8950.3400.9100.4820.934
Nmean22.422.819.018.921.5
median22.322.618.718.721.5
SE0.120.090.100.120.06
p0.8360.4310.9100.8260.358
Kmean4.034.623.863.884.20
median4.004.293.823.874.219
SE0.0300.0240.0310.0200.019
p0.3950.7910.3860.9850.988
Camean0.490.330.290.320.33
median0.490.320.270.310.33
SE0.0050.0070.0170.0060.004
p0.8550.5160.9910.8470.608
Mgmean1.401.401.011.061.34
median1.391.391.001.061.34
SE0.0110.0090.0080.0040.006
p0.5290.2000.3640.6950.995
Smean1.351.381.181.161.34
median1.341.381.161.161.35
SE0.0100.0100.0100.0070.007
p0.2760.5440.3880.9090.511
1 no significant differences between phosphorus treatments in the individual experiments (p > 0.05); 2 detailed data are a part of a separate paper [42].
Table 6. Contents of microelements and potentially toxic elements in wheat grain (mg kg−1 DM); means, medians, standard errors (SE), and p-values for ANOVA or Kruskal-Wallis tests for all phosphorus treatments in the individual experiments 1.
Table 6. Contents of microelements and potentially toxic elements in wheat grain (mg kg−1 DM); means, medians, standard errors (SE), and p-values for ANOVA or Kruskal-Wallis tests for all phosphorus treatments in the individual experiments 1.
ElementsStatisticsExperiments
IIIIIIIVV
Bmean<LoD<LoD0.540.530.57
median<LoD<LoD<LoD<LoD<LoD
SE 0.0240.0140.022
p 0.5710.7200.749
Cu 2mean2.843.812.293.814.37
median2.793.802.293.814.12
SE0.0670.0510.0510.1130.276
p0.5360.5250.6080.9660.994
Fe 3mean39.756.359.632.740.8
median39.255.256.931.739.4
SE0.511.912.090.721.03
p0.9170.8820.5230.3480.385
Mnmean26.520.721.624.523.5
median26.920.422.224.923.3
SE0.510.260.360.250.18
p0.1330.3760.2170.6680.985
Momean1.011.991.841.211.70
median0.982.111.760.951.16
SE0.1270.1380.1800.2170.244
p0.0530.1220.5850.7320.512
Ni 2mean0.1070.0380.1970.1550.187
median0.0960.0210.1640.1260.059
SE0.0240.0050.0220.0140.043
p0.1310.2580.9220.4210.868
Zn 2mean22.240.525.624.926.3
median22.140.325.424.826.
SE0.420.520.470.380.27
p0.5970.2260.5760.4050.823
As 2mean<LoD0.0580.0610.0560.100
median<LoD<LoD<LoD<LoD0.076
SE 0.0030.0040.0020.009
p 0.2520.7760.4680.713
Al 3mean8.98<LoD<LoD2.692.51
median8.95<LoD<LoD2.112.05
SE0.353 0.3540.324
p0.721 0.1700.590
Cd 4mean0.0860.0390.0120.0160.036
median0.0820.0400.0110.0160.038
SE0.0040.0010.0010.0020.002
p0.4890.4520.6380.0850.463
Cr 2mean0.1930.0870.0820.2530.432
median0.141<LoD<LoD0.1680.292
SE0.0470.0150.0250.0430.071
p0.4770.2680.7540.2840.984
Pb 4mean0.0140.0460.0780.0190.038
median0.0120.0270.041<LoD<LoD
SE0.0010.0050.0100.0040.007
p0.5900.6860.8880.7250.869
1 no significant differences between phosphorus treatments in the individual experiments (p > 0.05); 2 a part of the data is published in [43]; 3 a part of the data is published in [56]; 4 a part of the data is published in [41].
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

Jastrzębska, M.; Kostrzewska, M.K.; Saeid, A. The Effect of Renewable Phosphorus Biofertilizers on Selected Wheat Grain Quality Parameters. Agriculture 2024, 14, 727. https://doi.org/10.3390/agriculture14050727

AMA Style

Jastrzębska M, Kostrzewska MK, Saeid A. The Effect of Renewable Phosphorus Biofertilizers on Selected Wheat Grain Quality Parameters. Agriculture. 2024; 14(5):727. https://doi.org/10.3390/agriculture14050727

Chicago/Turabian Style

Jastrzębska, Magdalena, Marta K. Kostrzewska, and Agnieszka Saeid. 2024. "The Effect of Renewable Phosphorus Biofertilizers on Selected Wheat Grain Quality Parameters" Agriculture 14, no. 5: 727. https://doi.org/10.3390/agriculture14050727

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