Abstract
Phosphorous (P) is an important macronutrient for plant growth and often acts as a limiting nutrient. It is mostly provided to plants by inorganic resources, most of which cannot be utilized by plants either due to precipitation or immobilization. Phosphate-solubilizing bacteria (PSB) can improve P availability by dissolving inorganic and mineralizing organic P in soil, and their activities in soil can be stimulated by different organic sources. We conducted a pot trial to check the efficacy of PSB, individually and in combination with different organic amendments for improving growth and yield of mung bean. Seeds were inoculated with PSB strain “Psychrobacter sp.” along with soil supplementation of various amendments (farmyard manure, poultry manure, press mud and biogas slurry at 2% w/w each). Co-application of PSB and organic amendments proved to be more beneficial than their individual application. Maximum improvements in plant attributes, i.e., plant height (66%), root length (52%), number of nodules plant−1 (129%), root area (101%), pods dry biomass (89%), SPAD value (41%), carotenoid contents (58%), and NPK contents in roots (139, 380, and 132%) and grains (41, 89, and 266%) were observed in combined application of PSB and poultry manure. Furthermore, combined application improved soil biological health in terms of phosphatase activity, and among them, maximum acid and alkaline phosphatase activities were enhanced by 53 and 68%, respectively, under co-application of PSB and poultry manure. Hence, integration of PSB with different organic amendments can significantly improve P availability to plants, and can improve its growth.
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References
Aboksari HA, Hashemabadi D, Kaviani B (2021) Effects of an organic substrate on pelargonium peltatum and improvement of its morphological, biochemical, and flowering parameters by root-inoculated phosphate solubilizing microorganisms. Commun Soil Sci Plant Anal 52(15):1772–1789. https://doi.org/10.1080/00103624.2021.1892735
Adnan M, Fahad S, Saleem MH, Ali B, Mussart M, Ullah R, Arif M, Ahmad M, Shah WA, Romman M, Wahid F (2022) Comparative efficacy of phosphorous supplements with phosphate solubilizing bacteria for optimizing wheat yield in calcareous soils. Sci Rep 12(1):11997. https://doi.org/s41598-022-16035-3
Ahmad J, Anwar S, Shad AA, Marwat FY, Bibi H, Ahmad F, Noor W, Sadia B (2021) Yield and nutritional status of mungbean as influenced by molybdenum and phosphorus. Pak J Agric Res 34(1). https://doi.org/10.17582/journal.pjar/2021/34.1.144.153
Ahmad M, Adil Z, Hussain A, Mumtaz MZ, Nafees M, Ahmad I, Jamil M (2019) Potential of phosphate solubilizing Bacillus strains for improving growth and nutrient uptake in mungbean and maize crops. Pak J Agric Sci 56(2). https://doi.org/10.21162/PAKJAS/19.7285
Amanullah M, Khan I, Hussain Z, Kakar KM (2021) Pheno-morphological traits of mungbean as influenced by phosphorous and tillage under irrigated and un-irrigated conditions. Pure Appl Biol 3(2):55–59. https://doi.org/10.19045/bspab.2014.32001
Arnon DI (1949) Copper enzmes in chloroplasts. Phenol oxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Bi W, Zhang D, Weng B, Dong Z, Wang F, Wang W, Lin W, Yan D (2023) Research progress on the effects of droughts and floods on phosphorus in soil-plant ecosystems based on knowledge graph. HydroRes 6:29–35. https://doi.org/10.1016/j.hydres.2023.01.001
Cong WF, Suriyagoda LD, Lambers H (2020) Tightening the phosphorus cycle through phosphorus-efficient crop genotypes. Trend Plant Sci 25(10):967–975. https://doi.org/10.1016/j.tplants.2020.04.013
Cozzolino V, Monda H, Savy D, Di Meo V, Vinci G, Smalla K (2021) Cooperation among phosphate-solubilizing bacteria, humic acids and arbuscular mycorrhizal fungi induces soil microbiome shifts and enhances plant nutrient uptake. Chem Biol Technol Agric 8(1):1–8. https://doi.org/10.1186/s40538-021-00230-x
Dhuldhaj UP, Malik N (2022) Global perspective of phosphate solubilizing microbes and phosphatase for improvement of soil, food and human health. Cell Mol Biomedic Rep 2(3):173–186. https://doi.org/10.55705/cmbr.2022.347523.1048
Duhamel S, Diaz JM, Adams JC, Djaoudi K, Steck V, Waggoner EM (2021) Phosphorus as an integral component of global marine biogeochemistry. Nature Geosci 14(6):359–368 https://doi.org/articles/s41561-021-00755-8
Economic Survey of Pakistan. Pakistan Bureau of Statistics (2022) Economic survey of Pakistan. Pakistan Bureau of Statistics, Government of Pakistan
Epelde L, Jauregi L, Urra J, Ibarretxe L, Romo J, Goikoetxea I, Garbisu C (2018) Characterization of composted organic amendments for agricultural use. Front Sustain Food Syst 2:44. https://doi.org/10.3389/fsufs.2018.00044
Estrada-Bonilla GA, Durrer A, Cardoso EJ (2021) Use of compost and phosphate-solubilizing bacteria affect sugarcane mineral nutrition, phosphorus availability, and the soil bacterial community. Appl Soil Ecol 157:103760. https://doi.org/10.1016/j.apsoil.2020.103760
Faiza, Asghar HN, Zahir ZA, Zia MA (2020) Phosphorus-solubilizing rhizobacterium enhances growth, yield and oil content of sesame in a calcareous soil. Int J Agric Biol 24(6):1763–1772. https://doi.org/10.17957/IJAB/15.1620
Gan RY, Lui WY, Chan CL, Corke H (2017) Hot air drying induces browning and enhances phenolic content and antioxidant capacity in mung bean (Vigna radiata L.) sprouts. J Food Process Preserv 41(1):e12846. https://doi.org/10.1111/jfpp.12846
Guo S, Feng B, **ao C, Wang Q, Chi R (2021) Phosphate-solubilizing microorganisms to enhance phytoremediation of excess phosphorus pollution in phosphate mining wasteland soil. Bioremediat J 25(3):271–281. https://doi.org/10.1080/10889868.2021.1884528
Hou E, Wen D, Jiang L, Luo X, Kuang Y, Lu X, Chen C, Allen KT, He X, Huang X, Luo Y (2021) Latitudinal patterns of terrestrial phosphorus limitation over the globe. Ecol Lett 24(7):1420–1431. https://doi.org/10.1111/ele.13761
Huang Y, Lou C, Luo L, Wang XC (2021) Insight into nitrogen and phosphorus coupling effects on mixotrophic Chlorella vulgaris growth under stably controlled nutrient conditions. Sci Total Environ 752:141747. https://doi.org/10.1016/j.scitotenv.2020.141747
Imran S, Kalsoom S, Hussain Z, Ullah O, Nagra SA (2016) Nutritional and sensory evaluation of the formulated gluten free flour and its effect on the gastrointestinal symptoms of celiac patients. Pak J Zool 48(4). https://doi.org/10/0030-9923/2016/0004-1025
Iqbal N, Tanzeem-ul-Haq HS, Turan V, Iqbal M (2023) Soil amendments and foliar melatonin reduced pb uptake, and oxidative stress, and improved spinach quality in Pb-contaminated soil. Plants 12(9):1829. https://doi.org/10.3390/plants12091829
Jackson ML (1962) Soil chemical analysis. Prentice Hall
Jiang F, Zhang L, Zhou J, George TS, Feng G (2021) Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol 230(1):304–315. https://doi.org/10.1111/nph.17081
Jiao Y, Ouyang HL, Jiang YJ, Kong XZ, He W, Liu WX, Yang B, Xu FL (2017) Effects of phosphorus stress on the photosynthetic and physiological characteristics of Chlorella vulgaris based on chlorophyll fluorescence and flow cytometric analysis. Ecol Ind 78:131–141. https://doi.org/10.1016/j.ecolind.2017.03.010
Kalayu G (2019) Phosphate solubilizing microorganisms: promising approach as biofertilizers. Int J Agron:1–7. https://doi.org/10.1155/2019/4917256
Kavesh MA, Lahiri-Dutt K, Adhikari R (2023) Women and plant entanglements: pulses commercialization and care relations in Punjab, Pakistan. Oxford Dev Stud:1–3. https://doi.org/10.1080/13600818.2023.2177265
Khan F, Khan S, Fahad S, Faisal S, Hussain S, Ali S, Ali A (2014) Effect of different levels of nitrogen and phosphorus on the phenology and yield of maize varieties. Am J Plant Sci. https://doi.org/10.4236/ajps.2014.517272
Khan H, Akbar WA, Shah Z, Rahim HU, Taj A, Alatalo JM (2022) Coupling phosphate-solubilizing bacteria (PSB) with inorganic phosphorus fertilizer improves mungbean (Vigna radiata) phosphorus acquisition, nitrogen fixation, and yield in alkaline-calcareous soil. Heliyon 8(3):09081. https://doi.org/10.1016/j.heliyon.2022.e09081
Khan MA, Ramzani PM, Zubair M, Rasool B, Khan MK, Ahmed A, Khan SA, Turan V, Iqbal M (2020) Associative effects of lignin-derived biochar and arbuscular mycorrhizal fungi applied to soil polluted from Pb-acid batteries effluents on barley grain safety. Sci Total Environ 710:136294. https://doi.org/10.1016/j.scitotenv.2019.136294
Khan N, Bano A (2016) Modulation of phytoremediation and plant growth by the treatment with PGPR, Ag nanoparticle and untreated municipal wastewater. Int J Phytoremediat 18(12):1258–1269. https://doi.org/10.1080/15226514.2016.1203287
Korir H, Mungai NW, Thuita M, Hamba Y, Masso C (2017) Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Front Plant Sci 8:141. https://doi.org/10.3389/fpls.2017.00141
Kour D, Rana KL, Yadav N, Yadav AN (2019) Bioprospecting of phosphorus solubilizing bacteria from Renuka Lake ecosystems, lesser Himalayas. J Appl Biol Biotechnol 7(5):1–6. https://doi.org/10.7324/JABB.2019.70501
Kumar S, Lai L, Kumar P, Valentín Feliciano YM, Battaglia ML, Hong CO, Owens VN, Fike J, Farris R, Galbraith J (2019) Impacts of nitrogen rate and landscape position on soils and switchgrass root growth parameters. Agron J 111(3):1046–1059. https://doi.org/10.2134/agronj2018.08.0483
Lambers H (2022) Phosphorus acquisition and utilization in plants. Ann Rev Plant Biol 73:17–42. https://doi.org/10.1146/annurev-arplant-102720-125738
Li Y, Li Q, Guan G, Chen S (2020) Phosphate solubilizing bacteria stimulate wheat rhizosphere and endosphere biological nitrogen fixation by improving phosphorus content. PeerJ 8:9062. https://doi.org/10.7717/peerj.9062
Lin L, Li C, Ren Z, Qin Y, Wang R, Wang J, Cai J, Zhao L, Li X, Cai Y, **ong X (2023) Transcriptome profiling of genes regulated by phosphate-solubilizing bacteria Bacillus megaterium P68 in potato (Solanum tuberosum L.). Front Microbiol 14:1140752. https://doi.org/10.3389/fmicb.2023.1140752
McLaren TI, Smernik RJ, McLaughlin MJ, Doolette AL, Richardson AE, Frossard E (2020) The chemical nature of soil organic phosphorus: a critical review and global compilation of quantitative data. Adv Agron 160(1):51–124. https://doi.org/10.1016/bs.agron.2019.10.001
MNFSR (2017) Agriculture statistic of Pakistan. Federal bureau of statistics, economics survey of Pakistan, Ministry of national food security and research
Moharana PC, Meena MD, Biswas DR (2018) Role of phosphate-solubilizing microbes in the enhancement of fertilizer value of rock phosphate through composting technology: 167-202. In: Meena V (ed) Role of Rhizospheric Microbes in Soil. Springer, Singapore. https://doi.org/10.1007/978-981-13-0044-8_6
Muhammad G, Khan S, Khan MA, Anjum J, Alizai NA, Anjum K, Ghafoor A, Kakar H (2022) Biozote-p application under zero tillage drill wheat planting influenced yield and phosphorus use efficiency of wheat crop. J Appl Res Plant Sci 3(01):206–214. https://doi.org/10.38211/joarps.2022.3.1.25
Niazi MTH, Kashif SR, Asghar HN, Saleem M, Khan MY, Zahir ZA (2015) Phosphate solubilizing bacteria in combination with pressmud improve growth and yield of mash bean. JAPS: J Anim Plant Sci 25(4):1049–1054
Olsen SR, Sommers LE (1982) In: Methods of soil analysis, chemical and microbiological properties, edited, by Page, A. L., Miller, R. H., and Keeney, D. R., SSSA Madison, WI. Phosphorus. 2: 403–430.
Pande AS, Kaushik P, Pandey P, Negi A (2020) Isolation, characterization, and identification of phosphate-solubilizing Burkholderia cepacia from the sweet corn cv. Golden Bantam rhizosphere soil and effect on growth-promoting activities. Int J Veg Sci 26(6):591–607. https://doi.org/10.1080/19315260.2019.1692121
Poudyal S, Owen JS Jr, Sharkey TD, Fernandez RT, Cregg B (2021) Phosphorus requirement for biomass accumulation is higher compared to photosynthetic biochemistry for three ornamental shrubs. Sci Hort 275:109719. https://doi.org/10.1016/j.scienta.2020.109719
Qarni A, Billah M, Hussain K, Shah SH, Ahmed W, Alam S, Khan N (2021) Isolation and characterization of phosphate solubilizing microbes from rock phosphate mines and their potential effect for sustainable agriculture. Sustainability 13(4):2151. https://doi.org/10.3390/su13042151
R Core Team (2016) RStudio: integerated development for R. RStudio
Randall KF, Brennan N, Clipson R, Creamer B, Griffiths S, Storey F, Doyle E (2019) Soil bacterial community structure and functional responses across a long-term mineral phosphorus (Pi) fertilisation gradient differ in grazed and cut grasslands. Appl Soil Ecol 138:134–143. https://doi.org/10.1016/j.apsoil.2019.02.002
Rawat P, Das S, Shankhdhar D, Shankhdhar SC (2021) Phosphate solubilizing microorganisms: mechanism and their role in phosphate solubilization and uptake. J Soil Sci Plant Nutr 21(1):49–68. https://doi.org/10.1007/s42729-020-00342-7
Sarwar MJ, Zahir ZA, Asghar HN, Shabaan M, Ayyub M (2023) Co-application of organic amendments and Cd-tolerant rhizobacteria for suppression of cadmium uptake and regulation of antioxidants in tomato. Chemosphere:138478. https://doi.org/10.1016/j.chemosphere.2023.138478
Shabaan M, Asghar HN, Akhtar MJ, Saleem MF (2023) Assessment of cumulative microbial respiration and their ameliorative role in sustaining maize growth under salt stress. Plant Physiol Biochem 196:33–46. https://doi.org/10.1016/j.plaphy.2023.01.037
Shabaan M, Asghar HN, Zahir ZA, Sardar MF, Parveen R, Ali Q (2022a) Halotolerant rhizobacterial consortium confers salt tolerance to maize under naturally salt-affected soil. Soil Sci Soc Am J 86(5):1264–1279. https://doi.org/10.1002/saj2.20438
Shabaan M, Asghar HN, Zahir ZA, Zhang X, Sardar MF, Li H (2022b) Salt-tolerant PGPR confer salt tolerance to maize through enhanced soil biological health, enzymatic activities, nutrient uptake and antioxidant defense. Front Microbiol 13. https://doi.org/10.3389/fmicb.2022.901865
Shafique S, Attia U, Shafique S, Tabassum B, Akhtar N, Naeem A, Abbas Q (2023) Management of mung bean leaf spot disease caused by Phoma herbarum through Penicillium janczewskii metabolites mediated by MAPK signaling cascade. Sci Rep 13(1):3606. https://doi.org/10.1038/s41598-023-30709-6
Shrivastava M, Srivastava PC, D’Souza SF (2018) Phosphate-solubilizing microbes: diversity and phosphates solubilization mechanism: role of rhizospheric microbes in soil. Nutr Manag Crop Improv 2:137–165. https://doi.org/10.1007/978-981-13-0044-8_5
Siedliska A, Baranowski P, Pastuszka-Woźniak J, Zubik M, Krzyszczak J (2021) Identification of plant leaf phosphorus content at different growth stages based on hyperspectral reflectance. BMC Plant Biol 21:1–17. https://doi.org/10.1186/s12870-020-02807-4
Silva LID, Pereira MC, Carvalho AMXD, Buttros VH, Pasqual M, Doria J (2023) Phosphorus-solubilizing microorganisms: a key to sustainable agriculture. Agriculture 13(2):462. https://doi.org/10.3390/agriculture13020462
Sönmez OS, Turan V, Kaya C (2016) The effects of sulfur, cattle, and poultry manure addition on soil phosphorus. Turk J Agric Forest 40(4):536–541. https://doi.org/10.3906/tar-1601-41
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1(4):301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Thonar C, Lekfeldt JDS, Cozzolino V, Kundel D, Kulhánek M, Mosimann C, Mäder P (2017) Potential of three microbial bio-effectors to promote maize growth and nutrient acquisition from alternative phosphorous fertilizers in contrasting soils. Chem Biol Technol Agric 4:1–16. https://doi.org/10.1186/s40538-017-0088-6
Turan V (2019) Confident performance of chitosan and pistachio shell biochar on reducing Ni bioavailability in soil and plant plus improved the soil enzymatic activities, antioxidant defense system and nutritional quality of lettuce. Ecotoxicol Environ Safe 183:109594. https://doi.org/10.1016/j.ecoenv.2019.109594
Turan V (2020) Potential of pistachio shell biochar and dicalcium phosphate combination to reduce Pb speciation in spinach, improved soil enzymatic activities, plant nutritional quality, and antioxidant defense system. Chemosphere 245:125611. https://doi.org/10.1016/j.chemosphere.2019.125611
Turan V (2021) Arbuscular mycorrhizal fungi and pistachio husk biochar combination reduces Ni distribution in mungbean plant and improves plant antioxidants and soil enzymes. Physiol Planta 173(1):418–429. https://doi.org/10.1111/ppl.13490
Turan V (2022) Calcite in combination with olive pulp biochar reduces Ni mobility in soil and its distribution in chili plant. Int J Phytorem 24(2):166–176. https://doi.org/10.1080/15226514.2021.1929826
Turan V, Schröder P, Bilen S, Insam H, Fernández-Delgado Juárez M (2019) Co-inoculation effect of Rhizobium and Achillea millefolium L. oil extracts on growth of common bean (Phaseolus vulgaris L.) and soil microbial-chemical properties. Sci Rep 9(1):15178. https://doi.org/10.1038/s41598-019-51587-x
Uebersax MA, Cichy KA, Gomez FE, Porch TG, Heitholt J, Osorno JM, Kamfwa K, Snapp SS, Bales S (2022) Dry beans (Phaseolus vulgaris L.) as a vital component of sustainable agriculture and food security-a review. Leg Sci:155. https://doi.org/10.1002/leg3.155
Ullah A, Shah TM, Farooq M (2020) Pulses production in Pakistan: status, constraints and opportunities. Int J Plant Prod 14(4):549–569. https://doi.org/10.1007/s42106-020-00108-2
Vinci G, Cozzolino V, Mazzei P, Monda H, Savy D, Drosos M, Piccolo A (2018) Effects of Bacillus amyloliquefaciens and different phosphorus sources on Maize plants as revealed by NMR and GC-MS based metabolomics. Plant Soil 429:437–450. https://doi.org/10.1007/s11104-018-3701-y
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37(1):29–38
Wang K, Hou J, Zhang S, Hu W, Yi G, Chen W, Cheng L, Zhang Q (2023) Preparation of a new biochar-based microbial fertilizer: nutrient release patterns and synergistic mechanisms to improve soil fertility. Sci Total Environ 860:160478. https://doi.org/10.1016/j.scitotenv.2022.160478
Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Sci Soc Am J 29(6):677–678. https://doi.org/10.2136/sssaj1965.03615995002900060025x
Wolf B (1982) A comprehensive system of leaf analysis and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13:1035–1059. https://doi.org/10.1080/00103628209367332
Xu ZL, Lin S, Onofrio N, Zhou L, Shi F, Lu W, Lau SP (2018) Exceptional catalytic effects of black phosphorus quantum dots in shuttling-free lithium sulfur batteries. Nat Commun 9(1):4164 https://www.nature.com/articles/s41467-018-06629-9
Yaseen R, Aziz O, Saleem MH, Riaz M, Zafar-ul-Hye M, Rehman M, Ali S, Rizwan M, Nasser Alyemeni M, El-Serehy HA, Al-Misned FA (2020) Ameliorating the drought stress for wheat growth through application of ACC-deaminase containing rhizobacteria along with biogas slurry. Sustain 12(15):6022. https://doi.org/10.3390/su12156022
Yi-Shen Z, Shuai S, FitzGerald R (2018) Mung bean proteins and peptides: nutritional, functional and bioactive properties. Food Nutr Res 62. https://doi.org/10.29219/fnr.v62.1290
Yong TW, ** CH, Qian DO, Qing DU, Feng YA, Wang XC, Liu WG, Yang WY (2018) Optimized nitrogen application methods to improve nitrogen use efficiency and nodule nitrogen fixation in a maize-soybean relay intercrop** system. J Integr Agric 17(3):664–676. https://doi.org/10.1016/S2095-3119(17)61836-7
Zeng Q, Ding X, Wang J, Han X, Iqbal HM, Bilal M (2022) Insight into soil nitrogen and phosphorus availability and agricultural sustainability by plant growth-promoting rhizobacteria. Environ Sci Pollut Res 29(30):45089–45106. https://doi.org/10.1007/s11356-022-20399-4
Zhu J, Li M, Whelan M (2018) Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Sci Total Environ 612:522–537. https://doi.org/10.1016/j.scitotenv.2017.08.095
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Rabia Khalid performed the experiment and conducted the analysis.
Aqsa Khalid assisted during the laboratory analyses.
Muhammad Shabaan assisted during the experiment and manuscript write up.
Hafiz Naeem Asghar supervised the student and critically reviewed the data.
Zahir Ahmad Zahir co-supervised the students and critically reviewed the data.
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Khalid, R., Khalid, A., Shabaan, M. et al. Phosphorous (P)-Solubilizing Rhizobacteria Improve P Availability to Mung Bean via Enhanced Soil Phosphatase Activity and Improve Its Growth. J Soil Sci Plant Nutr 23, 6155–6166 (2023). https://doi.org/10.1007/s42729-023-01473-3
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DOI: https://doi.org/10.1007/s42729-023-01473-3