Review Article

Biosolubilization of Phosphate Rock Using Organic Amendments: An Innovative Approach for Sustainable Maize Production in Aridisols - A Review

Noor-us-Sabah1*, Mukkram Ali Tahir1, Ghulam Sarwar1, Muhammad Luqman2, Amir Aziz1, Muhammad Zeeshan Manzoor1 and Muhammad Aftab3

1Department of Soil and Environmental Sciences, College of Agriculture, University of Sargodha, Sargodha 40100, Pakistan; 2Department of Agriculture Extension, College of Agriculture, University of Sargodha, Sargodha 40100, Pakistan; 3Institute of Soil Chemistry and Environmental Sciences, AARI, Faisalabad, Pakistan.

Received | September 25, 2021; Accepted | January 15, 2022; Published | March 18, 2022

*Correspondence | Noor-us-Sabah, Department of Soil and Environmental Sciences, College of Agriculture, University of Sargodha, Sargodha 40100, Pakistan; Email: [email protected]

Citation | Sabah, N.U., M.A. Tahir, G. Sarwar, M. Luqman, A. Aziz, M.Z. Manzoor and M. Aftab. 2022. Biosolubilization of phosphate rock using organic amendments: an innovative approach for sustainable maize production in Aridisols - A review. Sarhad Journal of Agriculture, 38(2): 617-625.

DOI | https://dx.doi.org/10.17582/journal.sja/2022/38.2.617.625

Keywords | Phosphate rock, Solubilization, Organic amendments, Maize, Aridisols

Copyright: 2022 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Phosphate rock (PR) is the basic fundamental input required for manufacturing of all commercially available P containing fertilizers. At present, PR presents a trade name for more than 300 different P containing products available throughout the world. Carbonate, flouro, hydroxyl and sulpho apatites are the basic types of PR commonly found in rocks. There are two options for usage of PR. One is physically processed PR involving as such application of PR in raw form after grinding and sorting based on mesh size. Second option is chemically processed forms of PR by converting it into chemical P containing fertilizers. Problem associated with direct (as such) application of PR under high pH soils is occurrence of PR with alloy minerals (e.g. quartz, silica, iron and aluminum oxides etc.). Presence of these alloy minerals create hurdle in solubilization of PR thereby, lowering its solubility and P release.

Phosphorus; its importance and problem

Essentiality of P for plant growth is well known and well documented. For getting sustainable yield, exogenous application of P sources is compulsory. There are several functions of P in plants including involvement in cell metabolism, part of adenosine tri-phosphate (ATP), phospholipids, nucleic acid, DNA, RNA, role in synthesis of protein etc. Overall crop growth and yield particularly, root growth and development, formation of seeds and quality of crops is seriously affected due to deficiencies of P (Ezawa et al., 2002; Achal et al., 2007; Yadav and Pandey, 2018; Calle-Castañeda et al., 2018). Thus, provision of P is mandatory throughout the growing period of crops for getting sustainable yields (Grant et al., 2001). Many processes related to plant physiology such as photosynthesis, N-fixation, flower, fruit and seed formulation and crop maturity required an optimum supply of P. Plants deficient in P manifest symptoms like growth retardation, dark green, blue or purpling of leaves etc. (Brady and Weil, 2005).

Availability of P in soils

P exists in soils in two forms i.e. organic and inorganic. Generally, about 50 percent of total P is organic, however, variation exist in different soils (Brady and Weil, 2005). There is plenty of P present in agricultural soils ranging from 200-5000 mg kg-1 with an average of about 600 mg kg-1 (Gyaneshawar et al., 2002). However, less than 0.1% of this total P is plant available because of retention of this P with soil components such as Fe and Al oxides in low pH soils and Ca in high pH soils (Harris et al., 2006; Khan et al., 2010). Main factor responsible for availability of P to plants in soils is pH with maximum availability being noted at pH value of 6.5 to 7.5. At present, problem of low bioavailability of P to plants is among serious obstacle toward achieving agricultural sustainability as estimated yield losses due to shortage of P are 30-40% (Vance et al., 2003). Because of high pH and high Ca content of soils, insufficiency of P is also prevalent in Pakistan where more than 90% soils are declared as P deficient (having less than 100 mg kg-1 Olsen P), thus proper P management is essential for obtaining high yields (Ahmad et al., 2003; Aziz et al., 2006). Plants usually require higher supplies of P compared to native soil P content, therefore, exogenous application of P is done to fulfill this need. Total P present in soils are estimated to about 100-2000 mg kg-1. Of which, 350-7000 kg ha-1 occur in plough layer, presenting small fraction of total P present in soils (Morel, 2002).

 

Phosphate rock (PR)

Phosphate rock serves as main raw material for formulation of all commercially available P containing fertilizers. PR accounts for about 17.5 million tons of P source, 85% of which served as basic material for P fertilizers production (Cordell et al., 2009). Country wise PR production of the world is given in Figure 1 (Samreen and Kausar, 2019). Sedimentary rocks served as major source of phosphate rock being accounting for more than 80% PR (Uddin et al., 2012). From agronomic point of view, main concern is the phosphatic content of PR. Thus, more the P content of PR, more will be the credibility of PR. Conversion of PR to chemical fertilizer is impacted negatively by presence of impurities like carbonates, iron, magnesium, aluminum and chloride etc. However, such impurities do not matter in case if directly applied RP (Hammond and Day, 1992). High reactivity of flour apatite PR renders it most suitable to be used as P source (Khasawneh and Doll, 1978). Considerable deposits of PR existed in Khyber Pakhtunkhwa (KPK) province of Pakistan estimated to be 6.9 million ton as resource and 5.58 million tons PR serving as reserves (Sharif et al., 2013; Naseer and Muhammad, 2014; Abbasi and Manzoor, 2018).

PR could be employed in agriculture by two methods i.e. directly applied PR and PR used as a basic source of P fertilizers. Although direct application is cheaper, environmentally benign and preferred in organic farming but less reactivity and presence of impurities like Fe and Al content in low pH soils and Ca content in high pH soils renders it unsuitable for direct application (UNIDO and IFDC, 1998). In addition, not all types of PR are appropriate for all kind of soils and farming (Zapata, 2003). Low solubility of PR discouraged its use for direct application thus, compelling the scientists to explore other means of exploiting PR use in agriculture by enhancing its solubility and P recovery. Literature reported several methods of PR dissolution including use of organic amendments (FYM, pressmud, poultry manure, compost etc.), acid treatment of PR (partially), use of phosphorus solubilizing microorganisms (PSMs) etc. (Kumari and Phogat, 2008).

Factors affecting PR dissolution

Properties of PR: PR dissolution is greatly influenced by physio chemical properties of PR including mode of origin, particle size, thermodynamic stability, solubility and reactivity of PR (Vanlauwe et al., 2002).

Soil Factor: Solubilization of PR depends upon many soil and plants factors. Similarly, properties of PR also affect its dissolution ability. Various soil related parameters include proton provision ability of soil, pH of soil, CEC, soil Ca content, soil P concentration and organic fraction of soil. PR dissolution is more in soils with lower pH, less Ca on exchange sites and lower soil solution P (Vanlauwe et al., 2002). Soil with low pH (>5.5) values have greater ability of PR dissolution and P release (Bolan and Heldey, 1990). Higher organic matter proportion of soil also supports PR dissolution. This improvement can be attributed to higher CEC and release of organic acids from organic matter (Chien et al., 1990). Nying and Robinson (2006) also reported that PR dissolution is strongly affected by size of Ca sink in soil thereby by enhancing CEC and organic matter more effective dissolution could be accomplished. This can be attained by addition of organic amendments in soils.

Crop Factor: Differences exist among crops regarding P use from PR. Regarding crop factors influencing PR dissolution include P and Ca requirement of crop as well as ability of crop to acidify root surrounding area by secreting root exsudates. Different crops have varying ability to uptake P from PR dissolution. Crops like maize, buckwheat, rape seed, leguminous and cruciferous family have more affinity for taking up P by RP dissolution (Baligar et al., 2001; Hocking, 2001). Secretion of many organic acids by their roots seems to be responsible for PR solubilization, P release and subsequent uptake by plant roots. Thus, PR can be applied under high soil conditions by employing such crops having ability to release organic acids and thereby have greater affinity for PR dissolution and P release by taking up Ca such as maize (Flach et al., 1987).

Mechanism of solubilization of phosphate rock

Soil phosphate occurs as apatite form (calcium phosphate) being fixed with soil constituents like Ca in alkaline soils. PR has low solubility and thus, having low P release and solubilization under alkaline soil pH (Goldstein, 2000). Such apatite or fixed P can be released by lowering of pH governed by various kinds of organic acids secreted by soil microbes (PSMs). Thus, organic acid secretions by plant roots and many strains of soil microorganisms (Fankem et al., 2006) seems to be the basic mechanism responsible for PR solubilization and subsequent P release from Ca-phosphates (Vassilev et al., 2006). Organic acids like acetic, citric and oxalic acids result in rhizosphere acidification and thus dissociation of apatite form of P like Ca-phosphate take place (Hinsinger, 2001; Kumari et al., 2008). Additionally, some inorganic acids like H2SO4, HCl and HNO3 are also responsible for PR dissolution, thereby, commonly used for partial acidulation process of PR (Fekri et al., 2011). Mechanism of PR solubilization by acidulation can be depicted from following chemical reaction:

12HNO3+ Ca10 (PO4)6F2--->3Ca (H2PO4)2[Monocalcium phosphate] + 10Ca(NO3) 2 + 2HF

Use of organic amendments as a tool for solubilization of rock phosphate; an innovative approach

Use of FYM for PR solubilization: It has been reported that use of FYM in combination with PR via co-composting technique resulted in PR dissolution and subsequently release of P. The product thus obtained is known as phosphate rich organic manure (PROM) which can be utilized as a replacement of commercial P fertilizer. In addition to increased P solubility, this product also prevents re-fixation of P (Sekhar et al., 2001). It was reported that combined use of FYM (0.5-4.0 MT ha-1) and PR (40 kg ha-1) could result in substantial improvement in P solubility from RP dissolution depending on soil reaction (Sekhar and Aery, 2001). In an experiment, Hellal et al. (2013) also reported an enhanced PR dissolution and P release resulted from integrated use of phospho-compost prepared from PR and FYM in maize crop. Similarly, Sharif et al. (2011) also documented the beneficial effects of co-composting of FYM and PR on enhanced PR dissolution and P solubility.

Use of poultry manure (PM) for PR solubilization: Poultry dropping are well reported organic manure enriched with essential nutrients. Impact of PM in terms of improving PR dissolution and P release has also been reported extensively. Boateng et al. (2006) claimed that integration of PR with PM can improve nutrient availability to greater extent. Similar results were reported by Farhad et al. (2009). Khan and Sharif (2012) also suggested that composting of PR with PM amended with effective microorganisms (EM) resulted in greater PR dissolution and P release. Similarly, Akande et al. (2005) documented an improvement in yield and P content of maize by combined application of PR with poultry manures. However, Mahimairaja et al. (1995) discouraged the utilization of PM for making compost with PR due to high Ca content of poultry manures that served as impurity and lowered the reactivity of PR.

 

Use of Compost for PR solubilization: Literature suggested that PR co-composted with organic stuff substantially improved the RP dissolution and P release. Composting can be performed by using any organic materials like FYM, green manure, poultry droppings, city waste etc. (Ali et al., 2014). Hellal et al. (2013) documented that application of PROM made from composting of PR with organic materials resulted in improved nutrient composition of soil and subsequent uptake by plants. Similarly, enhanced P release from PR dissolution was also noticed by the use of PROM. Outcomes of Zafar et al. (2012), Ahmad et al. (2006) and Rizwan et al. (2006) also supported positive impact of composted PR regarding availability of P for plant use.

Use of pressmud for PR solubilization: Among organic amendments pressmud is found to be more effective mean of PR solubilization. Pressmud is considered as a bio active source for solubilization of PR and P release particularly in high pH soils (Mahimairaja et al., 1995; Aziz et al., 2010). Many researched reported the beneficial role of pressmud in dissolution of PR for P release (Aziz et al., 2006; Aziz et al., 2010; Qureshi et al., 2014; Sabah et al., 2016; Sabah et al., 2018a; 2018b). It was documented that it is the higher quantity of sulphur present in pressmud that trigger PR dissolution by lowering soil pH (Joggi et al., 2005).

Use of PSMs for PR solubilization: Use of microorganisms for PR dissolution was documented first time in 1903 (Khan et al., 2007). Afterward, wide range research was carried out in this regard and many types of PSMs were explored for their ability to solubilize P from PR (Aseri et al., 2009). There is a bulk of PSMs present in soil depending on soil types. Bacteria account for half of microbial population while fungi contribute to 0.1 to 0.5% of microbial population in soil (Chen et al., 2006). Similarly, plant growth promoting rhizobacteria (PGPRs) are also reported having such ability P solubilization from RP dissolution. Keeping in view this ability of PSMs and PGPRs, extensive research work was performed to explore the beneficial strains (Gyaneshwar et al., 2002). Possible mechanism responsible for PR dissolution is the secretion of many types of organic and inorganic (HCl) acids as well as chelating compounds in the rhizosphere that resulted in lowering of soil pH as described in Figure 2 (Kim et al., 1997; Deubel et al., 2000; Moharana et al., 2018). Similarly, PSMs also secret many enzymes (phosphatises and phytases) that also assist PR solubilization (Goenadi et al., 2000; Tarafdar et al., 2003). Various strains of PSMs reported for PR solubilization include Pseudomonas, Bacillus, Rhozobium, Enterobacter, Agrobacterium, Aspergillus, penicillium, Pseudomonas florescence etc. (Kpomblekou and Tabatabai, 1994; Rodriguez and Fraga, 1999; Vessey et al., 2004; Hilda and Fraga, 1999; Panda et al., 2013). Among PGPRs strains like Psedomonas, Azospirillum, Bacillus, Rhizobia, etc. are well reported (Kloepper, 1994; Hall et al., 1999; Chabot et al., 1993).

Conclusions and Recommendations

PR is a naturally occurring cheaper source of P. Direct application of PR is not effective in alkaline soils due to less reactivity. PR solubilization can be improved by the employment of organic amendments like FYM, poultry manure, compost and pressmud. It was found that pressmud proved more effective organic amendment in terms of PR dissolution. Similarly, use of PSMs and PGPRs can also improve the P release from RP by enhancing its dissolution. Such an improvement in P release from PR could encourage usage of PR as a substitute the costly commercial P sources in poor countries like Pakistan.

Novelty Statement

The study recommnds that organic amendments improve P release from PR through biosolubilization.

Author’s Contribution

Noor-us-Sabah: Designed and prepared the manuscript.

Mukkram Ali Tahir: Supervised the writeup.

Ghulam Sarwar: Technically assisted at every step.

Amir Aziz and Muhammad Zeeshan Manzoor: Helped in data collection.

Muhammad Luqman and Muhammad Aftab: Proof reading.

Conflict of interest

The authors have declared no conflict of interest.

References

Abbasi, K. and M. Manzoor. 2018. Biosolubilization of phosphorus from rock phosphate and other P fertilizers in response to phosphate solubilizing bacteria and poultry manure in a silt loam calcareous soil. J. Plant Nutr. Soil Sci., 181: 345-356. https://doi.org/10.1002/jpln.201800012

Achal, V., V.V. Savant and R.M. Sudhakara. 2007. Phosphate solubilization by wide type strain and UV-induced mutants of Aspergillus tubingensis. Soil Biol. Biochem., 39: 695-699. https://doi.org/10.1016/j.soilbio.2006.09.003

Ahmad, N., M. Abid, K. Hussain, M. Akram and M. Yousaf. 2003. Evaluation of nutrient status in rice growing areas of the Punjab. Asian J. Plant Sci., 2(5): 449-453. https://doi.org/10.3923/ajps.2003.449.453

Ahmad, R., A. Khalid, M. Arshad, Z.A. Zahir, and M. Naveed. 2006. Effect of raw (un-composted) and composted organic waste material on growth and yield of maize (Zea mays L.). Soil Environ., 25: 135-142.

Akande, M.O., J.A. Adediran and F.I. Oluwatoyinb. 2005. Effects of phosphate rock amended with poultry manure on soil available P and yield of maize and cowpea. Afr. J. Biotechnol., 4: 444-448.

Ali, A., M. Sharif, F. Wahid, Z.Q. Zhang, S.N.M. Shah, Rafiullah, S. Zaheer, F. Khan, and F. Rehman. 2014. Effect of Composted Phosphate rockwith Organic Materials on Yield and Phosphorus Uptake of Berseem and Maize. Am. J. Plant Sci., 5: 975-984. https://doi.org/10.4236/ajps.2014.57110

Alzoubi, M.M. and G. Maram. 2012. The Effect of Phosphate Solubilizing Bacteria and Organic Fertilization on Availability of Syrian Phosphate rockand Increase of Triple Superphosphate Efficiency. WJAS. 8(5): 473-478.

Aseri, G.K., N. Jain and J.C. Tarafdar. 2009. Hydrolysis of Organic Phosphate forms by Phosphatases and Phytase Producing Fungi of Arid and Semi-arid Soils of India. Am-Eurasian J. Agric. Environ. Sci., 5 (4): 564-570.

Aziz, T., Rahmatullah, M.A. Maqsood, M.A. Tahir, I. Ahmad and M.A. Cheema. 2006. Phosphorus utilization by six Brassica cultivars (Brassica juncea L.) from tri-calcium phosphate; a relatively insoluble P compound. Pak. J. Bot., 38: 1529-1538.

Aziz, T., S. Ullah, A. Sattar, M. Nasim, M. Farooq and M.M. Khan. 2010. Nutrient availability and maize (Zea mays L.) growth in soil amended with organic manures. Int. J. Agric. Biol., 12: 621-624.

Baligar, V.C., N.K. Fageria and Z.L. Ze. 2001. Nutrient use efficiency in plants. Com. Soil Sci. Plant Anal., 32: 921-950. https://doi.org/10.1081/CSS-100104098

Boateng, S.A., Zichermann, J. and Kornahrens M. 2006. Poultry manure effect on growth and yield of maize. West Afr. J. Appl. Ecol., 9: 1-11. https://doi.org/10.4314/wajae.v9i1.45682

Bolan, N.S., R.E. White and M.J. Hedley. 1990. A review of the use of phosphate rocks as fertilizers for direct application in Australia and New Zealand. Aus. J. Exp. Agric., 30: 297-313. https://doi.org/10.1071/EA9900297

Brady, N.C. and R.R. Weil. 2005. The nature and properties of soils. 13th Edition. Pearson Education, Inc. and Dorling Kindersley Publishing Inc., New York, pp. 137-192.

Calle-Castañeda, S.M., M.A. Márquez-Godoy and J.P. Hernández-Ortiz. 2018. Phosphorus recovery from high concentrations of low-grade phosphate rocks using the biogenic acid produced by the acidophilic bacteria Acidithiobacillus thiooxidans. Minerals Eng., 115:97-105. https://doi.org/10.1016/j.mineng.2017.10.014

Chabot, R., H. Antoun and M.P. Cescas. 1993. Stimulation de la croissance du mais et de la laitue romaine par desmicroorganismes dissolvant le phosphore inorganique. Can. J. Microbiol., 39: 941–947. https://doi.org/10.1139/m93-142

Chen, Y., P. Rekha, A. Arun, F. Shen, W.A. Lai and C.C. Young. 2006. Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl. Soil Ecol., 34 (1): 33-41. https://doi.org/10.1016/j.apsoil.2005.12.002

Chien, S.H., P.W.G. Sale and D.K. Friesen. 1990. A discussion of the methods for comparing the relative effectiveness of phosphate fertilizers varying in solubility. Fert. Res., 24: 149-157. https://doi.org/10.1007/BF01073583

Cordell, D., J.O. Drangert and S. White. 2009. Glob. Environ. Change, 19: 292-305. https://doi.org/10.1016/j.gloenvcha.2008.10.009

Deubel, A., A. Gransee and W. Merbach. 2000. Transformation of Organic Rhizodeposits by Rhizoplane Bacteria and its Influence on the Availability of Tertiary Calcium Phospate. J. Plant Nutr. Soil Sci., 163 (4): 387-392. https://doi.org/10.1002/1522-2624(200008)163:4<387::AID-JPLN387>3.0.CO;2-K

Ezawa, T., S.E. Smith and F.A. Smith. 2002. P metabolism and transport in AM fungi. Plant Soil, 244: 221-230. https://doi.org/10.1007/978-94-017-1284-2_21

Fankem, H., A. Nwaga, A. Dueubel, L. Dieng, W. Merbach and F.X. Etoa. 2006. Occurrence and Functioning of Phosphate Solubilizing Microorganisms from Oil Palm Tree (Elaeis guineensis) Rhizosphere in Cameroon. Afr. J. Biotechnol., 5(24): 2450-2460.

Farhad, W., M.F. Saleem, M.A. Cheema, and H.M. Hammad. 2009. Effect of poultry manure levels on the productivity of spring maize (Zea mays L.). JAPS., 19: 122-125.

Fekri, M., N. Gorgin and L. Sadegh. 2011. Phosphorus desorption kinetics in two calcareous soils amended with P fertilizer and organic matter. Environ. Earth Sci., https://doi.org/10.1007/s12665-010-0892-9

Flach, E.N., W. Quak and D.A. Van. 1987. A comparison of the rock phosphate-mobilising capacities of various crop species. Trop. Agric., 64: 347–352.

Goenadi, D.H., Siswanto and Y. Sugiarto. 2000. Bioactivation of poorly soluble phosphate rocks with a phosphorus-solubilizing fungus. Soil Sci. Soc. Am. J., 64: 927-932. https://doi.org/10.2136/sssaj2000.643927x

Goldstein, A.H. 2000. Bioprocessing of Phosphate rockOre: Essential Technical Considerations for the Development of a Successful Commercial Technology, Proceedings of 4th International Association for Technical Conference, pp. 220-242, ISBN 1-57498-079-3, New Orieans, USA, October 1-4, 2000.

Gyaneshwar, P., N.J. Kumar, L.J. Pareka and P.S. Podle. 2002. Role of Soil Microorganisms in Improving P Nutrition of Plants. Plant Soil, 245 (1): 83-93. https://doi.org/10.1023/A:1020663916259

Hall, J.A., D. Pierson, S. Ghosh and B.R. Glick. 1999. Root elongation in various agronomic crops by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Isr. J. Plant Sci., 44: 37-42. https://doi.org/10.1080/07929978.1996.10676631

Hammond, L.L. and D.P. Day. 1992. Phosphate rock standardization and product quality. In A.T. Bachik & A. Bidin, eds. Proceedings of a workshop on phosphate sources for acid soils in the humid tropics of Asia, pp. 73-89. Kuala Lumpur, Malaysian Society of Soil Science.

Harris, J.N., P.B. New and P.M. Martin. 2006. Laboratory tests can predict beneficial effects of phosphate-solubilizing bacteria on plants. Soil Biol. Biochnol., 38: 1521-1526. https://doi.org/10.1016/j.soilbio.2005.11.016

Hellal, F.A.A., N. Fuji and M.Z. Raffat. 2013.Influence of phosphocompost application on phosphorus availability and uptake by maize grown in red soil of Ishigaki Island, Japan. Agric. Sci., 4(2): 102-109. https://doi.org/10.4236/as.2013.42016

Hinsinger, P. 1998. How do plant roots acquire mineral nutrients? Adv. Agron., 64: 225-265. https://doi.org/10.1016/S0065-2113(08)60506-4

Hocking, P.J. 2001. Organic acids exuded from roots in phosphorus uptake and aluminum tolerance of plants in acid soils. Adv. Agron., 74: 63-93. https://doi.org/10.1016/S0065-2113(01)74031-X

Joggi, R.C., M.S. Aulakh, and R. Sharma. 2005. Impacts of elemental S applied under various temperature and moisture regimes on pH and available P in acidic, neutral and alkaline soils. Biol. Fertilizer Soils, 41: 52-58. https://doi.org/10.1007/s00374-004-0792-9

Khan, M.A., M. Sajid, Z. Hussain, A.R. Khan, B. Marwat, F. Wahid, and S. Bibi. 2013. How nitrogen and phosphorus influence the phenology of okra. Pak. J. Bot., 45(2): 479-482.

Khan, M.S., A. Zaidi, and P.A. Wani. 2007. Role of Phosphate-Solubilizing Microorganisms in Sustainable Agriculture-A Review. Agron. Sustain. Dev., 27(1): 29-43. https://doi.org/10.1051/agro:2006011

Khan, M.U. and M. Sharif. 2012. Solubility enhancement of phosphorus from phosphate rockthrough compositing with poultry litter. Sarhad J. Agric., 28(3): 415-420.

Khasawneh, F.E. and E.C. Doll. 1978. The use of phosphate rock for direct application to soils. Adv. Agron., 30: 159-206. https://doi.org/10.1016/S0065-2113(08)60706-3

Kim, K.V., D. Jordan and D. McDonald. 1997. Solubilization of Hydroxyapatite by Enterobacter Agglomerans and Cloned Escherichia in Culture Medium. Biol Ferti. Soils, 24(4): 347-352. https://doi.org/10.1007/s003740050256

Kloepper, J.W. and M.N. Schroth. 1998. Plant growth-promoting rhizobacteria on radishes. In: Station de Pathologie vegetale et Phyto-bacteriologie, editor. Proceedings of the 4th International Conference on Plant Pathogenic Bacteria Vol II. Tours: Gilbert-Clary. Pp. 879-882.

Kloepper, J.W., K. Lifshitz, and M.N. Schroth 1988. Pseudomonas inoculants to benefit plant production. ISI Atlas Sci. Anim. Plant Sci., pp. 60-64.

Kpomblekou, K. and K. Tabatabai. 1994. Effect of organic acids on release of phosphorus from phosphate rocks. Soil Sci., 158: 442-453. https://doi.org/10.1097/00010694-199415860-00006

Kumari, A., K.K. Kapoor, B.S. Kundu and R.K. Mehta. 2008. Identification of organic acids produced during rice straw decomposition and their role in phosphate rocksolubilization. J. Plants Soil Environ., 54(2): 72-77. https://doi.org/10.17221/2783-PSE

Kumari, K. and V.K. Phogat. 2008. Rock phosphate: its availability and solubilization in the soil - a review. Agric. Rev., 29(2): 108-116.

Mahimairaja, S., N.S. Bolan and M.J. Hedley. 1995. Dissolution of phosphate rock during the composting of poultry manure: An incubation experiment. Ferti. Res., 40: 93-104. https://doi.org/10.1007/BF00750093

Maharana, R., A. Basu, N.K. Dhal and T. Adak, 2021. Biosolubilization of rock phosphate by Pleurotus ostreatus with brewery sludge and its effect on the growth of maize (Zea mays L.). J. Plant Nutr., 44 (3): 395-410. https://doi.org/10.1080/01904167.2020.1822397

Matiullah K. and M. Sharif 2012. Solubility enhancement of phosphorus from phosphate rockthrough composting with poultry litter. Sarhad J. Agric., 28(3): 415-420.

Mengel, K. and E.A. Kirkby. 2001. Principles of Plant Nutrition. 5th Ed., Kluwer Academic Publishers, London. https://doi.org/10.1007/978-94-010-1009-2

Moharana, P.C., M.D. Meena and D.R. Biswasv. 2018. Role of Phosphate-Solubilizing Microbes in the Enhancement of Fertilizer Value of Rock Phosphate Through Composting Technology. Role of Rhizospheric Microbes in Soil. Volume 2, Springer. pp. 167-202. https://doi.org/10.1007/978-981-13-0044-8_6

Morel, C. 2002. Caractérisation de la phytodisponiblité du P du sol par la modélisation du transfert des ions phosphate entre le sol la solution. Habilitation à Diriger des Recherches. INPL-ENSA-IA Nancy. 80 pp. [Online] Available: http://www.bordeaux.inra.fr/tcem/ rubrique:Actualités [2004 May 04].

Naseer, M. and D. Muhammad. 2014. Direct and residual effect of hazara phosphate rock(hrp) on wheat and succeeding maize in alkaline calcareous soils. Pak. J. Bot., 46(5): 1755-1761.

Nying, C.S. and S.J. Robinson. 2006. Factors Influencing the Dissolution of Phosphate Rock in a Range of High P-Fixing Soils from Cameroon, Communications in Soil Science and Plant Analysis, 37: 2627-2645. https://doi.org/10.1080/00103620600823091

Panda, R., S.P. Panda, R.N. Kar and C.R. Panda. 2013. Solubilization of Uganda low grade Phosphate rockby Pseudomonas fluorescence. Res. J. Recent. Sci., 2: 250-254.

Pasandideh, M., M.J. Malakouti, and P. Keshavarz. 2003. Effect of sulfur and Thiobacillus inoculum on sulfur oxidation, pH, manure pit content and availability of phosphorus from biophosphate fertilizer. National Seminar on production and consumption of sulfur in Mashhad, Iran.

Qureshi, S.A., A. Rajput, M. Memon and M.A. Solangi. 2014. Nutrient composition of phosphate rockenriched compost from various organic wastes. E3 J. Sci. Res., 2(3): 47-51.

Rashid, M., S. Khalil, N. Ayub, S. Alam and F. Latif. 2004. Organic Acids Production and Phosphate Solubilization by Phosphate Solubilizing Microorganisms (PSM) under in vitro Condition. Pak. J. Biol. Sci., 7(2): 187-196. https://doi.org/10.3923/pjbs.2004.187.196

Rizwan, A., A. Naseer, Z.A. Zahir, M. Arshad, T. Sultan and M.A. Ullah. 2006. Integrated Use of Recycled Organic Waste and Chemical Fertilizers for Improving Maize Yield. Int. J. Agric. Biol., 6: 840-843.

Rodriguez, H. and R. Fraga. 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv., 17: 319-339. https://doi.org/10.1016/S0734-9750(99)00014-2

Sabah, N.U., G. Sarwar, M.A. Tahir and S. Muhammad. 2016. Comparative efficiency of high (triple super phosphate) and low (rock phosphate) grade P nutrition source enriched with organic amendment in maize crop. Pak. J. Bot., 48(6): 2243-2248.

Sabah, N.U., G. Sarwar, M.A. Tahir and S. Muhammad. 2018. Depicting the role of organic amendments for bio available phosphorus release from different sources of phosphate rockand uptake by maize crop. Pak. J. Bot., 50(1): 117-122.

Sabah, N.U., G. Sarwar, M.A. Tahir and S. Muhammad. 2018. Evaluation of de-waxed filter cake press mud for P-release from indigenous phosphate rock and its utilization by maize crop. Pak. J. Agric. Sci., 55(2): 361-366.

Samreen, S. and S. Kausar. 2019. Phosphorus Fertilizer: The Original and Commercial Sources. https://doi.org/10.5772/intechopen.82240

Sekhar, D.M.R. and N.C. Aery 2001. CURRENT SCIENCE. 80 (9).

Sekhar, D.M.R., Y. Dassin, L. Momani and A. Hamatteh. 2008. Phosphate rich organic manure as fertilizer. Nature Preced., https://doi.org/10.1038/npre.2008.2411.1

Sharif, M., K. Matiullah, B. Tanvir, A.H. Shah and F. Wahid. 2011. Response of fed dung composted with phosphate rockon yield and phosphorus and nitrogen uptake of maize crop. Afr. J. Biotechnol., 10(59): 12595-12601. https://doi.org/10.5897/AJB11.1240

Sharif, M., M.S. Sarir and F. Rabi. 2000. Biological and chemical transformation of phosphorus in some important soil series of NWFP. Sarhad J. Agri., 16(6): 587-592.

Sharif, M., T. Burni, F. Wahid, F. Khan, S. Khan, A. Khan and A. Shah. 2013. Effect of phosphate rock composted with organic materials on yield and phosphorus uptake of wheat and mung bean crops. Pak. J. Bot., 45(4): 1349-1356.

Taiz, L. and E. Zeiger. 1998. Plant Physiology. Second edition. Sinauer Associates, Inc. Publishers. Massachusetts. USA. pp. 792.

Tarafdar, J.C., M. Bareja and J. Panwar. 2003. Efficiency of Some Phosphatase Producing Soil-Fungi. Indian J. Microbiol., 43(1): 27-32.

Uddin, M., A. Kashem and K.T. Osman. 2012. Effect of organic and inorganic amendments on the phytoavailability of phosphorus to corn (Zea mays L.). Open J. Soil Sci., 2: 50-54. https://doi.org/10.4236/ojss.2012.21008

United Nations Industrial Development Organization (UNIDO) and IFDC. 1998. Fertilizer manual. Dordrecht, The Netherlands, Kluwer Academic Publishers. 615 pp.

Vance, C.P., C. Uhde-Stone, and D.L. Allan. 2003. Phosphorus acquisition and use: critical adaptations by plants for securing a non renewable resource. New phytol., 157: 423-427. https://doi.org/10.1046/j.1469-8137.2003.00695.x

Vanlauwe, B., Diels, J., Sanginga, N. and Merckx, R. 2002. Integrated Plant Nutrient Management in Sub-Saharan Africa, from Concept to Practice New York: CABI. https://doi.org/10.1079/9780851995762.0000

Vassilev, N., M. Vassilev and I. Nikolaeva. 2006. Simultaneous P-solubilzing and biocontrol activity of microorganisms: potentials and future trends. Appl. Microbial. Biotechnol., 71: 137-144. https://doi.org/10.1007/s00253-006-0380-z

Vessey, J.K., K. Pawlowski and B. Bergman. 2004. Root-based N2- fixing symbioses: Legumes, actinorhizal plants, Parasponia sp. and cycads. Plant Soil., 266: 205-230. https://doi.org/10.1007/s11104-005-0871-1

Yagodin, B.A. (Ed). 1984. Agricultural Chemistry. I. Mir Publishers, Moscow.

Yadav, C. and S. Pandey. 2018. Isolation and characterization of phosphate solubilizing bacteria from agriculture soil of Jaipur, Rajasthan. Int. J. Curr. Trends Sci. Technol., 8 (20):180-191.

Zafar, M., M.K. Abbasi, T. Arjumend and K. Jabran. 2012. Impact of compost, inorganic phosphorus fertilizers and their combination on maize growth, yield, nutrient uptake and soil properties. JAPS. 22(4): 1036-1041.

Zapata, F. and R.N. Roy. 2004. Use of phosphate rocks for sustainable Agriculture. Food and Agriculture Organization of the United Nations Rome, 2004 Fertilizer and Plant Nutrition Bulletin, 13.