افزایش بهره‌وری محصولات کشاورزی با باکتری‌های محرک رشد گیاه و ذرات نانو: سازوکارها، چالش‌ها و جهت‌گیری‌های آینده

نوع مقاله : مقاله مروری

نویسندگان

1 محقق پسادکترا، موسسه تحقیقات خاک و آب کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، کرج، ایران.

2 استاد موسسه تحقیقات خاک و آب کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، کرج، ایران.

3 دانشیار موسسه تحقیقات خاک و آب کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، کرج، ایران.

4 گروه علوم خاک، دانشگاه آزاد اسلامی، واحد اصفهان (خوراسگان)، اصفهان، ایران

10.22092/sbj.2025.368425.277

چکیده

در دهه‌های اخیر، توجه به کشاورزی پایدار و بهره‌برداری مؤثر از منابع طبیعی به طور فزاینده‌ای افزایش یافته است. باکتری‌های محرک رشد گیاه (PGPR) و ذرات نانو به عنوان دو فناوری نوین در زیست‌فناوری کشاورزی، توانسته‌اند به بهبود رشد و کیفیت محصولات کشاورزی کمک شایانی کنند.PGPR ها، گروه متنوعی از باکتری‌های مفید خاکزی هستند که از طریق سازوکارهای مستقیم و غیرمستقیم، رشد گیاهان را بهبود می‌بخشند. از سوی دیگر، ذرات نانو با ویژگی‌های فیزیکی و شیمیایی منحصربه‌فرد خود، نقش‌های متعددی در کشاورزی ایفا می‌کنند و می‌توانند به عنوان حامل‌های مؤثر مواد مغذی و آفت‌کش‌ها عمل کرده و مستقیماً بر فرآیندهای فیزیولوژیکی گیاه تأثیر بگذارند. بررسی‌ها نشان می‌دهد که استفاده ترکیبی از PGPR و نانوذرات می‌تواند اثرات هم‌افزایی قابل توجهی بر عملکرد محصولات کشاورزی داشته باشد. به عنوان مثال، کاربردBacillus subtilis با کود NPK در مزارع کلزا منجر به افزایش حدود 46 درصدی عملکرد دانه در دو سال متوالی شده است. همچنین، استفاده از نانوذرات اکسید روی، آهن و Zn-Fe همراه با Azotobacter در گندم، افزایش چشمگیر 88 درصدی در عملکرد دانه را نشان داده است. در شرایط تنش آلودگی خاک، ترکیب Actinobacterium sp. و نانوذرات سلنیوم موجب افزایش 74 درصدی زیتوده در سویا گردید. علاوه بر این، استفاده از نانوذرات نقره با Bacillus pumilus و Pseudomonas moraviensis وزن تر پیاز را به ترتیب 75 و 33 درصد افزایش داده است. این اثرات هم‌افزایی احتمالاً از طریق بهبود جذب مواد مغذی، تولید هورمون‌های رشد گیاهی، افزایش تحمل به تنش و بهبود کلونیزاسیون ریشه، بهبود جذب مواد مغذی و تحریک سیستم ایمنی گیاه صورت می‌گیرد. با وجود این نتایج امیدوارکننده، استفاده از این فناوری‌ها با چالش‌هایی نظیر سمیت احتمالی برخی نانوذرات، اثرات بلندمدت زیست‌محیطی و نیاز به تدوین پروتکل‌های استاندارد برای تولید و مصرف همراه است. بنابراین، تحقیقات بیشتری برای بهینه‌سازی کاربرد این ترکیبات و درک کامل مکانیسم‌های عمل آن‌ها ضروری است.

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

Enhancing agricultural productivity using PGPR and nanoparticles: mechanisms, challenges, and future directions

نویسندگان [English]

  • Bahman Khoshrou 1
  • Alireza Fallah Nosratabad 2
  • Houshang Khosravi 3
  • Ahmad Asgharzadeh 3
  • Laleh Faridian 4
1 Postdoctoral Researcher, Soil and Water Research Institute (SWRI), Agricultural Research, Education and Extension Organization (AREEO), Karaj 31785-311, Iran.
2 Professor of Soil and Water Research Institute (SWRI), Agricultural Research, Education and Extension Organization (AREEO), Karaj 31785-311, Iran.
3 Associate Professor of Soil and Water Research Institute (SWRI), Agricultural Research, Education and Extension Organization (AREEO), Karaj 31785-311, Iran.
4 Department of Soil Science, Islamic Azad University, Isfahan (Khorasgan) Branch, Isfahan, Iran
چکیده [English]

Background and objective:The growing global population and increasing food demand necessitate sustainable agricultural practices that enhance productivity while minimizing environmental impact. Conventional agriculture's reliance on synthetic inputs has led to significant environmental degradation. In this context, integrating biotechnological approaches, particularly using plant growth-promoting bacteria (PGPR) and nanotechnology, offers a promising strategy. PGPR, a diverse group of rhizosphere bacteria, promote plant growth through direct mechanisms like enhancing nutrient availability (nitrogen fixation, phosphorus solubilization, potassium mobilization), producing phytohormones (auxins, gibberellins, cytokinins), and synthesizing siderophores. Indirect mechanisms involve suppressing pathogens through antibiotics, lytic enzymes, and induced systemic resistance (ISR). Nanoparticles, with their unique physicochemical properties (high surface area-to-volume ratio, quantum effects, enhanced reactivity), offer advantages in agriculture. They act as carriers for targeted delivery of nutrients and agrochemicals, improving efficiency and reducing contamination. They also directly influence plant physiological processes. Combining PGPR and nanoparticles shows promising synergistic effects, potentially leading to greater improvements in plant growth and yield. This synergy stems from enhanced bacterial colonization, improved nutrient delivery, and direct effects on plant physiology. This study aims to: (1) review the mechanisms by which PGPR and nanoparticles influence plant growth; (2) investigate their synergistic interactions; (3) analyze their practical applications; (4) discuss challenges and limitations; and (5) provide future research recommendations for optimizing their application in sustainable agriculture.
Material and Methods:This study employed a comprehensive literature review of existing research on PGPR and nanoparticle applications in agriculture. Scientific articles, reports, books, reviews, and conference proceedings were collected from databases like Scopus, Web of Science, PubMed, Google Scholar, and Sciencedirect. Keywords and Boolean operators were used for the search, including "plant growth-promoting bacteria," "PGPR," "nanoparticles," "nanotechnology in agriculture," "Nutrient uptake," "Plant hormones," "Biotic/abiotic stress," "Sustainable agriculture," "Nanofertilizers," and related terms. The collected literature was critically evaluated for relevance, methodological rigor, and scientific quality. Studies investigating the synergistic effects of combining PGPR and nanoparticles were prioritized. Information extracted included types of PGPR and nanoparticles, application methods, plant species, experimental conditions, and measured parameters (plant growth, yield, nutrient uptake, stress tolerance).
Results:The literature review provides compelling evidence of the beneficial effects of PGPR and nanoparticles on plant growth and yield. PGPR have consistently been shown to enhance nutrient availability, stimulate root development, improve water use efficiency, and increase plant resistance to various biotic and abiotic stresses. Numerous studies have demonstrated the ability of PGPR to fix atmospheric nitrogen, solubilize insoluble phosphorus, and mobilize potassium, making these essential nutrients available to plants. Furthermore, PGPR are known to produce various phytohormones, such as auxins, gibberellins, and cytokinins, which play crucial roles in regulating plant growth and development, including cell elongation, cell division, and differentiation. The production of siderophores by PGPR has also been shown to improve iron uptake by plants, especially in calcareous soils. Nanoparticles, with their unique properties, serve as effective carriers for delivering nutrients, pesticides, and other agrochemicals to plants, improving their efficiency and reducing environmental contamination. Studies have also demonstrated the direct effects of nanoparticles on plant physiological processes, such as enhancing photosynthesis by improving chlorophyll content and photosynthetic efficiency, and influencing stomatal regulation. The combined application of PGPR and nanoparticles consistently results in synergistic effects, leading to greater improvements in plant growth and yield compared to the application of either technology alone. This synergy can be attributed to several factors. Nanoparticles can enhance the colonization of plant roots by PGPR by providing a protective microenvironment and improving bacterial attachment. Conversely, PGPR can facilitate the uptake and translocation of nanoparticles within the plant. The combination of PGPR and nanoparticles has been shown to improve plant tolerance to various abiotic stresses, such as drought, salinity, and heavy metal toxicity.
Conclusion:The combined application of PGPR and nanoparticles represents a promising and sustainable approach for enhancing agricultural productivity and minimizing environmental impact. The synergistic interactions between these two technologies offer significant potential for improving plant growth, yield, and quality. PGPR contribute by enhancing nutrient availability, producing phytohormones, and inducing systemic resistance, while nanoparticles act as efficient delivery systems for nutrients and other agrochemicals and directly influence plant physiological processes. The combined application of these technologies often results in greater improvements in plant growth and yield compared to individual applications, demonstrating a clear synergistic effect. However, several challenges need to be addressed before widespread adoption of this approach. These challenges include the potential toxicity of certain nanoparticles to plants and soil microorganisms, the need for further research on the long-term environmental impacts of nanoparticles, the cost-effectiveness of nanoparticle production and application, and the development of standardized protocols for application. Furthermore, understanding the precise mechanisms of interaction between specific PGPR strains and different types of nanoparticles is crucial. Future research should focus on: (1) elucidating the complex interactions between PGPR, nanoparticles, plants, and the soil microbiome at the molecular level; (2) conducting comprehensive risk assessments to evaluate the potential environmental and human health impacts of nanoparticles used in agriculture; (3) developing sustainable and cost-effective methods for producing and applying nanoparticles in agriculture; (4) optimizing the application methods and formulations of PGPR and nanoparticles for different crops and environmental conditions; (5) establishing clear regulatory frameworks for the use of nanoparticles in agriculture; (6) investigating the long-term effects of repeated applications of nanoparticles on soil health and ecosystem functioning; and (7) exploring the potential of using nanobiosensors for monitoring the effects of nanoparticles in the environment. By addressing these challenges and pursuing these research directions, the synergistic potential of PGPR and nanoparticles can be fully exploited to contribute to a more sustainable and productive agricultural future.

کلیدواژه‌ها [English]

  • Food security
  • Nano-fertilizers
  • Nutrient uptake
  • Sustainable agriculture
  • Synergy
  1. Adesemoye, A.O., Torbert, H.A. and Kloepper, J.W., 2009. Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Canadian Journal of Microbiology, 55(8), pp.876–884.
  2. Aghaei, F., Sharifi, R.S. and Farzaneh, S., 2024. Effects of Nano Iron-Silicon Oxide on Yield and Some Biochemical and Physiological Characteristics of Triticale Under Salinity Stress. Silicon, pp.1-13.
  3. Aizawa, S., 2014. Sinorhizobium meliloti-nitrogen-fixer in the grassland. The Flagellar World: Electron Microscopic Images of Bacterial Flagella and Related Surface Structures. First Edition, Academic Press, pp.82–83.
  4. Akhtar, N., Ilyas, N., Hayat, R., Yasmin, H., Noureldeen, A. and Ahmad, P., 2021. Synergistic effects of plant growth promoting rhizobacteria and silicon dioxide nano-particles for amelioration of drought stress in wheat. Plant Physiology and Biochemistry, 166, pp.160–176.
  5. Al-Hasani, F.J., Hamad, Q.A. and Faheed, N.K., 2024. Enhancing the cell viability and antibacterial properties of alginate-based composite layer by adding active particulates. Discover Applied Sciences, 6(2), p.70.
  6. Ali, S., Shafique, O., Mahmood, T., Hanif, M.A., Ahmed, I. and Khan, B.A., 2018. A review about perspectives of nanotechnology in agriculture. Pakistan Journal of Agricultural Research, 30(2), pp.116–121.
  7. Anal, A.K., Singh, H. and Khare, S.K., 2003. Effect of process parameters on microencapsulation of probiotic bacteria using alginate. Process Biochemistry, 38(11), pp.1713–1718.
  8. Artursson, V., Finlay, R.D. and Jansson, J.K., 2006. Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environmental Microbiology, 8(1), pp.1–10.
  9. Bashan, Y., 1986. Alginate beads as synthetic inoculant carriers for the slow release of bacteria that affect plant growth. Applied and Environmental Microbiology, 51, pp.1089–1098.
  10. Bashan, Y., de-Bashan, L.E. and Prabhu, S.R., 2016. Superior polymeric formulations and emerging innovative products of bacterial inoculants for sustainable agriculture and the environment. In: Agriculturally important microorganisms: Commercialization and regulatory requirements in Asia. Singapore: Springer Singapore, pp.15–46.
  11. Beck, D.P., Materon, L.A. and Afandi, F., 1993. Practical Rhizobium-Legume Technology Manual. Technical Manual No. 19. ICARDA, Aleppo, Syria.
  12. Bhattacharyya, P. and Jha, D.K., 2012. Plant growth-promoting rhizobacteria: A critical review. Biotechnology Advances, 30(4), pp.965–979.
  13. Cao, Y., Glass, A.D. and Crawford, N.M., 2022. Understanding the transport and regulation of potassium and its importance for plant nutrition: Insights from genetic and molecular tools. Plant Physiology, 188(1), pp.27–38.
  14. Cassidy, M.B., Lee, H. and Trevors, J.T., 1996. Environmental applications of immobilized microbial cells: a review. Journal of Industrial Microbiology and Biotechnology, 16, pp.79–101.
  15. Chen, J., Dou, Z., Zhang, Y. and Shi, J., 2020. Enhanced phosphorus availability by hydroxyapatite nanoparticles and phosphate-solubilizing bacteria. Environmental Science and Pollution Research, 27(4), pp.4290–4298.
  16. Chen, J., Li, J., Zhang, H., Hu, J. and Li, W., 2018. Effects of potassium-solubilizing bacteria on potassium availability and microbial activity in a black soil in Northeast China. Frontiers in Microbiology, 9, p.1565.
  17. Chhipa, H. and Joshi, P., 2016. Nanofertilizers, nanopesticides, nanosensors in agriculture. Environmental Chemistry Letters, 14(2), pp.229–240.
  18. Corbo, M.R., Bevilacqua, A., Speranza, B., Di Maggio, B., Gallo, M. and Sinigaglia, M., 2016. Use of alginate beads as carriers for lactic acid bacteria in a structured system and preliminary validation in a meat product. Meat Science, 111, pp.98–203.
  19. Cui, S. and Zhou, K., 2017. A comparison of the predictive potential of various vegetation indices for leaf chlorophyll content. Earth Science Informatics, 10, pp.169–181.
  20. Das, S., Dash, P. and Mishra, S., 2021. Synergistic effect of nanoparticles and PGPR on growth and stress tolerance in plants. Plant and Soil, 466(1), pp.101–120.
  21. Devi, S.H., Bhupenchandra, I., Sinyorita, S., Chongtham, S.K. and Devi, E.L., 2021. Mycorrhizal fungi and sustainable agriculture. Nitrogen in Agriculture− Physiological, Agricultural and Ecological Aspects, pp.1–19.
  22. Dobermann, A., 2005. Nitrogen use efficiency – state of the art. Agronomy & Horticulture Faculty Publications, 316, pp.1–16.
  23. Draget, K.I., Taylor, C., Smidsrød, O. and Stokke, B.T., 2020. Alginates. In: Handbook of Hydrocolloids. Woodhead Publishing, pp.649–689.
  24. Dzul Rashidi, N.F., Jamali, N.S., Mahamad, S.S., Ibrahim, M.F., Abdullah, N., Ismail, S.F. and Siajam, S.I., 2020. Effects of alginate and chitosan on activated carbon as immobilisation beads in biohydrogen production. Processes, 8(10), p.1254.
  25. Elmer, W.H. and White, J.F., 2018. The use of soil amendments and beneficial microbes to manage plant diseases. Biological Control, 121, pp.476–486.
  26. Etesami, H., Jeong, B.R. and Glick, B.R., 2021. Contribution of arbuscular mycorrhizal fungi, phosphate–solubilizing bacteria, and silicon to P uptake by plant. Frontiers in Plant Science, 12, p.699618.
  27. Fageria, N.K., Baligar, V.C. and Clark, R.B., 2001. Physiology of Crop Production. New York: CRC Press.
  28. Fallah Nosratabab, A., Khoshru, B., 2024. Potentials and challenges of biofertilizers in sustainable Soil Biology Journal, 12 (1), 19-63.
  29. Feichtmeier, N.S., Walther, P. and Leopold, K., 2015. Uptake, effects, and regeneration of barley plants exposed to gold nanoparticles. Environmental Science and Pollution Research, 22, pp.8549–8558.
  30. Fenice, M., Selbman, L., Federici, F. and Vassilev, N., 1999. Application of encapsulated Penicillium variabile P16 in solubilization of rock phosphate. Bioresource Technology, 73, pp.157–162.
  31. Fouda, M.M., Abdelsalam, N.R., El-Naggar, M.E., Zaitoun, A.F., Salim, B.M., Bin-Jumah, M., Allam, A.A., Abo-Marzoka, S.A. and Kandil, E.E., 2020. Impact of high throughput green synthesized silver nanoparticles on agronomic traits of onion. International Journal of Biological Macromolecules, 149, pp.1304–1317.
  32. Francis, D.V., Abdalla, A.K., Mahakham, W., Sarmah, A.K. and Ahmed, Z.F., 2024. Interaction of plants and metal nanoparticles: Exploring its molecular mechanisms for sustainable agriculture and crop improvement. Environment International, p.108859.
  33. Franken, P., 2012. The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Applied Microbiology and Biotechnology, 96, pp.1455–1464.
  34. Ghazy, N.A., Abd El-Hafez, O.A., El-Bakery, A.M. and El-Geddawy, D.I., 2021. Impact of silver nanoparticles and two biological treatments to control soft rot disease in sugar beet (Beta vulgaris L). Egyptian Journal of Biological Pest Control, 31, pp.1–12.
  35. Gill, S.S., Gill, R., Trivedi, D.K., Anjum, N.A., Sharma, K.K., Ansari, M.W., et al., 2016. Piriformospora indica: potential and significance in plant stress tolerance. Frontiers in Microbiology, 7, p.332.
  36. Glaeser, S.P., Imani, J., Alabid, I., Guo, H., Kumar, N., Kampfer, P., et al., 2016. Non-pathogenic rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica. The ISME Journal, 10, pp.871–884.
  37. Guzmán-Guzmán, P., Kumar, A., de Los Santos-Villalobos, S., Parra-Cota, F.I., Orozco-Mosqueda, M.D.C., Fadiji, A.E., Hyder, S., Babalola, O.O. and Santoyo, G., 2023. Trichoderma species: Our best fungal allies in the biocontrol of plant diseases—A review. Plants, 12(3), p.432.
  38. Hao, Y., Yu, Y., Sun, G., Gong, X., Jiang, Y., Lv, G., Zhang, Y., Li, L., Zhao, Y., Sun, D. and Gu, W., 2023. Effects of multi-walled carbon nanotubes and nano-silica on root development, leaf photosynthesis, active oxygen and nitrogen metabolism in maize. Plants, 12(8), p.1604.
  39. Hatami, M. and Ghorbanpour, M., 2024. Metal and metal oxide nanoparticles-induced reactive oxygen species: Phytotoxicity and detoxification mechanisms in plant cell. Plant Physiology and Biochemistry, p.108847.
  40. Hayat, R., Ali, S., Amara, U., Khalid, R. and Ahmed, I., 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology, 60(4), pp.579–598.
  41. He, Y., Wu, Z., Tu, L., Han, Y., Zhang, G. and Li, C., 2015. Encapsulation and characterization of slow-release microbial fertilizer from the composites of bentonite and alginate. Applied Clay Science, 109–110, pp.68–75.
  42. Hodge, A. and Storer, K., 2015. Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil, 386(1–2), pp.1–19.
  43. Hussain, A., Al-Dakheel, A.J., Rehman, S.U., et al., 2018. Role of potassium-solubilizing microorganisms to enhance soil fertility, plant growth, and potassium content. Sustainable Agriculture Research, 7(4), pp.1–11.
  44. Ivanova, E., Chipeva, V., Ivanova, I., Dousset, X. and Poncelet, D., 2002. Encapsulation of lactic acid bacteria in calcium alginate beads for bacteriocin production. Journal of Culture Collection, 3, pp.53–58.
  45. Ivanova, E., Teunou, E. and Poncelet, D., 2005. Alginate-based macro capsules as inoculants carriers for production of nitrogen biofertilizers. Proceedings of the Balkan Scientific Conference of Biology, Plovdiv, Bulgaria, pp.90–108.
  46. Jahangir, S., Javed, K. and Bano, A., 2020. Nanoparticles and plant growth promoting rhizobacteria (PGPR) modulate the physiology of onion plant under salt stress. J. Bot., 52(4), pp.1473–1480.
  47. Jangir, P., Shekhawat, P.K., Bishnoi, A., Ram, H. and Sonin, P., 2021. Role of Serendipita indica in enhancing drought tolerance in crops. Physiological and Molecular Plant Pathology, 116, p.101691.
  48. Jha, S. and Yadav, A., 2023. Assessment of carbon and fullerene nanomaterials for sustainable crop plants growth and production. In Engineered Nanomaterials for Sustainable Agricultural Production, Soil Improvement and Stress Management (pp.145–160). Academic Press.
  49. John, R.P., Tyagi, R.D., Brar, S.K., Surampalli, R.Y. and Prevost, D., 2011. Bio-encapsulation of microbial cells for target agricultural delivery. Rev. Biotechnol., 31, pp.211–226.
  50. Jordan, D.C. Family III Rhizobiaceae. In: Bergey’s Manual of Systematic Bacteriology, pp.234–242.
  51. Kalayu, G., 2019. Phosphate solubilizing microorganisms: promising approach as biofertilizers. International Journal of Agronomy, 2019(1), p.4917256.
  52. Kalia, A., Sood, S. and Bhardwaj, S., 2022. Role of plant growth-promoting rhizobacteria in enhancing ZnO nanoparticle uptake by wheat. Environmental Nanotechnology, Monitoring & Management, 18, 100711.
  53. Kalra, Y.P., 1998. Handbook of Reference Methods for Plant Analysis. Boca Raton, Florida, USA: CRC Press.
  54. Kapoor, D., Yadav, S., Sharma, M.M.M. and Sharma, P., 2023. Interaction between metal nanoparticles and PGPR on the plant growth and development. In Nanomaterials and Nanocomposites Exposures to Plants: Response, Interaction, Phytotoxicity and Defense Mechanisms (pp.327–351). Singapore: Springer Nature Singapore.
  55. Katarína, K., Masarovičová, E. and Jampílek, J., 2021. Risks and benefits of metal-based nanoparticles for vascular plants. In Handbook of Plant and Crop Physiology (pp.922–963). CRC Press.
  56. Khan, I., Awan, S.A., Rizwan, M., Hassan, Z.U., Akram, M.A., Tariq, R., Brestic, M. and Xie, W., 2022. Nanoparticle’s uptake and translocation mechanisms in plants via seed priming, foliar treatment, and root exposure: A review. Environmental Science and Pollution Research, 29(60), pp.89823-89833.
  57. Khan, M.S., Zaidi, A. and Wani, P.A., 2009. Role of phosphate-solubilizing microorganisms in sustainable agriculture—a review. Sustain. Dev., 27(1), pp.29–43.
  58. Khoshru, B., Fallah Nosratabad, A., Mahjenabadi, V.A.J., Knežević, M., Hinojosa, A.C., Fadiji, A.E., Enagbonma, B.J., Qaderi, S., Patel, M., Baktash, E.M. and Dawood, M.F.A.M., 2024. Multidimensional role of Pseudomonas: from biofertilizers to bioremediation and soil ecology to sustainable agriculture. Journal of Plant Nutrition, pp.1–27.
  59. Khosravi, H., Khoshru, B., Nosratabad, A.F. and Mitra, D., 2024. Exploring the landscape of biofertilizers containing plant growth-promoting rhizobacteria in Iran: Progress and research prospects. Current Research in Microbial Sciences, p.100268.
  60. Kim, Y.J., Park, H.G., Yang, Y.L., Yoon, Y., Kim, S. and Oh, E., 2005. Multifunctional drug delivery system using starch-alginate beads for controlled release. Pharm. Bull., 28, pp.394–397.
  61. Klute, A., 1986. Methods of Soil Analysis. Part 1. Physical and Mineralogical Methods. Second Edition. ASA-CSSA-SSSA Publisher, Madison, Wisconsin, USA.
  62. Kowalska, E., Ziarno, M., Ekielski, A. and Żelaziński, T., 2022. Materials used for the microencapsulation of probiotic bacteria in the food industry. Molecules, 27(10), p.3321.
  63. Kumar, S., Nehra, M. and Dilbaghi, N., 2021. Nanotechnology-based sustainable agriculture: Current status and future implications. Biotechnology Reports, 30, e00677.
  64. Kumaresan, G. and Reetha, D., 2012. Development of gel-based formulation enriched with different additives for long term survival of Azospirillum International Journal of Recent Scientific Research, 3, p.11.
  65. Lahuta, L.B., Szablińska-Piernik, J., Głowacka, K., Stałanowska, K., Railean-Plugaru, V., Horbowicz, M., Pomastowski, P. and Buszewski, B., 2022. The effect of bio-synthesized silver nanoparticles on germination, early seedling development, and metabolome of wheat (Triticum aestivum). Molecules, 27(7), p.2303.
  66. Lambers, H., 2022. Phosphorus acquisition and utilization in plants. Annual Review of Plant Biology, 73(1), pp.17–42.
  67. Lateef, A., Nazir, R., Jamil, N. and Shah, R., 2021. Sustainable agricultural practices through application of bio-nanofertilizers: An emerging perspective. Environmental Research, 197, 111023.
  68. Lee, B.B., Ibrahim, R., Chu, S.Y., Zulkifli, N.A. and Ravindra, P., 2015. Alginate liquid core capsule formation using the simple extrusion dripping method. Journal of Polymer Engineering, 35(4), pp.311–318.
  69. Ley, J., Barrio-Duque, A.D., Samad, A., Antonielli, L., Sessitsch, A. and Compant, S., 2019. Beneficial endophytic bacteria-Serendipita indica interaction for crop enhancement and resistance to phytopathogens. Microbiol., 10, p.3398.
  70. López-Valdez, F., Fernández-Luqueño, F. and de la Rosa, G., 2021. Nanotechnology and plant-microbe interactions: A strategy for improving agricultural sustainability. Frontiers in Microbiology, 12, 671791.
  71. Lucy, M., Reed, E. and Glick, B.R., 2004. Applications of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek, 86(1), pp.1–25.
  72. Mahanty, T., Bhattacharjee, S., Goswami, M. and Tribedi, P., 2022. Nano-biofertilizer and nano-biopesticide: A sustainable approach for agricultural applications. Frontiers in Microbiology, 13, 854932.
  73. Malusá, E., Sas-Paszt, L. and Ciesielska, J., 2012. Technologies for beneficial microorganisms inocula used as biofertilizers. The Scientific World Journal, 2012, pp.1–12.
  74. Marschner, P., 2012. Marschner's Mineral Nutrition of Higher Plants. 3rd ed. London: Academic Press.
  75. Martinez, Y., Ribera, J., Schwarze, F.W. and De France, K., 2023. Biotechnological development of Trichoderma-based formulations for biological control. Applied Microbiology and Biotechnology, 107(18), pp.5595–5612.
  76. Martínez-Cano, B., Mendoza-Meneses, C.J., García-Trejo, J.F., Macías-Bobadilla, G., Aguirre-Becerra, H., Soto-Zarazúa, G.M. and Feregrino-Pérez, A.A., 2022. Review and perspectives of the use of alginate as a polymer matrix for microorganisms applied in agro-industry. Molecules, 27(13), p.4248.
  77. Mazhar, Z., Akhtar, J., Alhodaib, A., Naz, T., Zafar, M.I., Iqbal, M.M., Fatima, H. and Naz, I., 2023. Efficacy of ZnO nanoparticles in Zn fortification and partitioning of wheat and rice grains under salt stress. Scientific Reports, 13(1), p.2022.
  78. Meirelles, L.N., Mesquita, E., Corrêa, T.A., Bitencourt, R.D.O.B., Oliveira, J.L., Fraceto, L.F., Camargo, M.G. and Bittencourt, V.R.E.P., 2023. Encapsulation of entomopathogenic fungal conidia: evaluation of stability and control potential of Rhipicephalus microplus. Ticks and Tick-Borne Diseases, 14(4), p.102184.
  79. Mendoza, J., Romero-Perdomo, F., Hernandez, J.P. and Uribe-Velez, D., 2021. Bacillus strains immobilized in alginate macro beads enhance drought stress adaptation of guinea grass. Rhizosphere, 19(14), p.100385.
  80. Menossi, M., Casalongué, C. and Alvarez, V.A., 2022. Bio-nanocomposites for modern agricultural applications. In Handbook of Consumer Nanoproducts (pp.1201–1237). Singapore: Springer Nature Singapore.
  81. Merinero, M., Alcudia, A., Begines, B., Martínez, G., Martín-Valero, M.J., Pérez-Romero, J.A., Mateos-Naranjo, E., Redondo-Gómez, S., Navarro-Torre, S., Torres, Y. and Merchán, F., 2022. Assessing the biofortification of wheat plants by combining a plant growth-promoting rhizobacterium (PGPR) and polymeric Fe-nanoparticles: allies or enemies?. Agronomy, 12(1), p.228.
  82. Mukherjee, A., Majumdar, S. and Servin, A., 2020. Interaction of engineered nanomaterials with soil microbiota and plants: A review. Frontiers in Microbiology, 11, 606084.
    Patel, S., Singh, M. and Husain, M., 2021. Silver nanoparticles: Mechanisms of antimicrobial action and their potential application in agriculture. Journal of Applied Microbiology, 131(4), pp.1867–1883.
  83. Narayan, O.M., Verma, N., Jogawat, A., Dua, M. and Johri, A.K., 2021. Sulfur transfer from the endophytic fungus Serendipita indica improves maize growth and requires the sulfate transporter. Plant Cell, 33(4), pp.1268–1285.
  84. Nascimento, F.C., Santos, C.H., Kandasamy, S. and Rigobelo, E., 2019. Efficacy of alginate-and clay-encapsulated microorganisms on the growth of Araçá-Boi seedlings (Eugenia stipitata). Acta Scientiarum. Biological Sciences, 41, p.43936.
  85. Nechitailo, G.S., Bogoslovskaya, O.A., Ol’khovskaya, I.P. and Glushchenko, N.N., 2018. Influence of iron, zinc, and copper nanoparticles on some growth indices of pepper plants. Nanotechnologies in Russia, 13, pp.161–167.
  86. Nedović, V.A., Kalusevic, A., Manojlovic, V., Levic, S., Bugarski, B. and Gӧkmen, V., 2017. Encapsulation of food bioactive compounds. In Food Bioactive Compounds (pp.285–325). Cham: Springer.
  87. Page, A.L., Miller, R.H. and Keeney, D.R., 1982. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties. ASA-CSSA-SSSA Publisher, Madison, Wisconsin, USA.
  88. Park, J.K. and Chang, H.N., 2000. Microencapsulation of microbial cells. Biotechnol Adv, 18, pp.303–319.
  89. Pavithran, R.K., Reddy, S.G., Kumar, B.S. and Kugabalasooriar, S., 2024. Enhancing sustainability in agriculture: natural polymer-based controlled release systems for effective pest management and environmental protection. ES Food & Agroforestry, 18, p.1276.
  90. Perret, X., Staehelin, C. and Broughton, W.J., 2000. Molecular basis of symbiotic promiscuity. Microbiology and Molecular Biology Reviews, 64(1), p.1.
  91. Pitaktamrong, P., Kingkaew, J., Yooyongwech, S., Cha-um, S. and Phisalaphong, M., 2018. Development of arbuscular mycorrhizal fungi-organic fertilizer pellets encapsulated with alginate film. Engineering Journal, 22(6), pp.65–79.
  92. Rai, M., Bonde, S., Yadav, A. and Ingle, A.P., 2021. Nanotechnology in biofertilizers: Recent trends and future perspectives. Environmental Chemistry Letters, 19(3), pp.1911–1928.
    Shaikh, S., Nazam, N. and Rizvi, M.A., 2023. Nanoparticles and their bio-interaction with plant growth-promoting rhizobacteria: Implications for sustainable agriculture. Journal of Nanobiotechnology, 21(1), 115.
  93. Rai, P.K., Lee, S.S., Zhang, M. and Tsang, D.C.W., 2021. Nanoparticles and plant–microbe interactions: Synergistic effects on plant growth and sustainability. Journal of Hazardous Materials, 403, 123102.
  94. Rai, P.K., Rai, A., Sharma, N.K., Singh, T. and Kumar, Y., 2023. Limitations of biofertilizers and their revitalization through nanotechnology. Journal of Cleaner Production, p.138194.
  95. Rajput, V., Minkina, T., Sushkova, S., Behal, A., Maksimov, A., Blicharska, E., Ghazaryan, K., Movsesyan, H. and Barsova, N., 2020. ZnO and CuO nanoparticles: a threat to soil organisms, plants, and human health. Environmental Geochemistry and Health, 42, pp.147–158.
  96. Rajput, V.D., Minkina, T. and Mandzhieva, S., 2021. Effects of metal oxide nanoparticles on soil, plants, and growth promoting rhizobacteria. Ecotoxicology and Environmental Safety, 208, 111687.
  97. Regnault-Roger, C., 2011. Trends for commercialization of biocontrol agent (biopesticide) products. In Plant Defence: Biological Control (pp.139–160). Dordrecht: Springer Netherlands.
  98. Rehmanullah, Muhammad, Z., Inayat, N. and Majeed, A., 2020. Application of nanoparticles in agriculture as fertilizers and pesticides: challenges and opportunities. In New Frontiers in Stress Management for Durable Agriculture (pp.281–293).
  99. Rezaei Cherati, S., Anas, M., Liu, S., Shanmugam, S., Pandey, K., Angtuaco, S., Shelton, R., Khalfaoui, A.N., Alena, S.V., Porter, E. and Fite, T., 2022. Comprehensive risk assessment of carbon nanotubes used for agricultural applications. ACS Nano, 16(8), pp.12061–12072.
  100. Richardson, A.E. and Simpson, R.J., 2011. Soil microorganisms mediating phosphorus availability: update on microbial phosphorus. Plant Physiology, 156(3), pp.989–996.
  101. Rizwan, M., Ali, S., ur Rehman, M.Z., Riaz, M., Adrees, M., Hussain, A., Zahir, Z.A. and Rinklebe, J., 2021. Effects of nanoparticles on trace element uptake and toxicity in plants: A review. Ecotoxicology and Environmental Safety, 221, p.112437.
  102. Rossi, L., Fedenia, L.N., Sharifan, H., Ma, X. and Lombardini, L., 2019. Effects of foliar application of zinc sulfate and zinc nanoparticles in coffee (Coffea arabica L.) plants. Plant Physiology and Biochemistry, 135, pp.160–166.
  103. Rui, M., Ma, C., Tang, X., Yang, J., Jiang, F., Pan, Y., Xiang, Z., Hao, Y., Rui, Y., Cao, W. and Xing, B., 2017. Phytotoxicity of silver nanoparticles to peanut (Arachis hypogaea L.): physiological responses and food safety. ACS Sustainable Chemistry & Engineering, 5(8), pp.6557–6567.
  104. Saberi Riseh, R., Ebrahimi-Zarandi, M., Gholizadeh Vazvani, M. and Skorik, Y.A., 2021. Reducing drought stress in plants by encapsulating plant growth-promoting bacteria with polysaccharides. International Journal of Molecular Science, 22, p.12979.
  105. Saberi Riseh, R., Skorik, Y.A., Kumar Thakur, V., Moradi Pour, M., Tamanadar, E. and Shahidi Noghabi, S., 2021. Encapsulation of plant biocontrol bacteria with alginate as a main polymer material. International Journal of Molecular Sciences, 22, p.11165.
  106. Schoebitz, M., Roldan, A. and Lopez, M.D., 2013. Bioencapsulation of microbial inoculants for better soil-plant fertilization. Agronomy for Sustainable Development, 33, pp.751–765.
  107. Schwartz, A.R., Ortiz, I., Maymon, M., Herbold, C.W., Fujishig, N.A., Vijanderan, J.A., Villella, W., Hanamoto, K., Diener, A., Sanders, E.R., DeMason, D.A. and Hirsch, A.M., 2013. Bacillus simplex—A little known PGPB with anti-fungal activity—alters pea legume root architecture and nodule morphology when coinoculated with Rhizobium leguminosarum Viciae. Agronomy, 3, pp.595–620.
  108. Shang, Y., Hasan, M. and Akin, D., 2022. Nanoparticle-induced biofilm formation by plant growth-promoting bacteria: Mechanisms and applications. Environmental Nanotechnology, Monitoring & Management, 19, 100733.
  109. Sharma, M., Schmid, M., Rothballer, M., Hause, G., Zuccaro, A., Imani, J. et al., 2008. Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiol., 10, pp.2235–2246.
  110. Sharma, S.B., Sayyed, R.Z., Trivedi, M.H. and Gobi, T.A., 2021. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus, 2(1), pp.587–612.
  111. Siddhanta, S., Paidi, S.K., Bushley, K., Prasad, R. and Barman, I., 2017. Exploring morphological and biochemical linkages in fungal growth with label-free light sheet microscopy and Raman spectroscopy. Chem Phys Chem, 18, pp.72–78.
  112. Silva, D., Ribeiro, A.J. and Reis, C.P., 2022. Microencapsulation of probiotics: a review of the different methods and their applications. Foods, 11(13), p.1952.
  113. Singh, J., Kumar, V. and Kim, K.H., 2020. Nanoparticle-based fertilizers and their application in modern agriculture. Environmental Nanotechnology, Monitoring & Management, 14, 100308.
  114. Singhal, U., Khanuja, M., Prasad, R. and Varma, A., 2017. Impact of synergistic association of ZnO-nanorods and symbiotic fungus Piriformospora indica DSM 11827 on Brassica oleracea var. botrytis (broccoli). Frontiers in Microbiology, 8, p.1909.
  115. Sivakumar, P.K., Parthasarthi, R., and Lakshmipriya, V.P., 2014. Encapsulation of plant growth promoting inoculant in bacterial alginate beads enriched with humic acid. International Journal of Current Microbiology and Applied Sciences, 3, p.6.
  116. Smit, E., Wolters, A.C., Lee, H., Trevors, J.T., and van Elsas, J.D., 1996. Interaction between a genetically marked Pseudomonas fluorescens strain and bacteriophage øR2f in soil: Effects of nutrients, alginate encapsulation, and the wheat rhizosphere. Microbial Ecology, 31, pp.125–140.
  117. Smith, S.E., and Read, D.J., 2008. Mycorrhizal Symbiosis. 3rd ed. San Diego: Academic Press.
  118. Soares da Costa, L., Henrique Grazziotti, P., Christofaro Silva, A., and et al., 2019. Alginate gel entrapped ectomycorrhizal inoculum promoted growth of Eucalyptus clones cutting under nursery conditions. Canadian Journal of Forest Research.
  119. Sutulienė, R., Ragelienė, L., Duchovskis, P., and Miliauskienė, J., 2022. The effects of nano-copper, -molybdenum, -boron, and -silica on pea (Pisum sativum L.) growth, antioxidant properties, and mineral uptake. Journal of Soil Science and Plant Nutrition, pp.1–14.
  120. Syers, J.K., Johnston, A.E., and Curtin, D., 2008. Efficiency of soil and fertilizer phosphorus use. FAO Fertilizer and Plant Nutrition Bulletin, 18(108), pp.5–50.
  121. Szekalska, M., Puciłowska, A., Szymańska, E., Ciosek, P., and Winnicka, K., 2016. Alginate: current use and future perspectives in pharmaceutical and biomedical applications. International Journal of Polymer Science, 2016(1), p.7697031.
  122. Takei, T., Yoshida, M., Hatate, Y., Shiomori, K., and Kiyoyma, Sh., 2008. Lactic acid bacteria-enclosing poly (ɛ-caprolactone) microcapsules as soil bioamendment. Journal of Bioscience and Bioengineering, pp.268–272.
  123. Tariq, A., Pan, K., Olatunji, O.A., Graciano, C., Li, Z., Sun, F., Sun, X., and et al., 2017. Phosphorus application improves drought tolerance of Phoebe zhennan. Frontiers in Plant Science, 8, p.5644.
  124. Timmusk, S., Seisenbaeva, G., and Behers, L., 2018. Titania (TiO2) nanoparticles enhance the performance of growth-promoting rhizobacteria. Scientific Reports, 8(1), p.617.
  125. Trevors, J.T., van Elsas, J.D., Lee, H., and Wolters, A.C., 1993. Survival of alginate encapsulated Pseudomonas fluorescens cells in soil. Applied Microbiology and Biotechnology, 39, pp.637–643.
  126. Tripathi, D.K., Singh, S., Singh, V.P. and Prasad, S.M., 2022. Zinc oxide nanoparticles and their interactions with beneficial soil microbes: A review on mechanisms and applications. Environmental Nanotechnology, Monitoring & Management, 18, 100732.
  127. Van Wylick, A., De Laet, L., Peeters, E., and Rahier, H., 2023. Encapsulation of fungal spores for fungi-mediated self-healing concrete. In MATEC Web of Conferences (Vol. 378, p.02002). EDP Sciences.
  128. Varma, A., Verma, S., Sahay, N., Bütehorn, B., and Franken, P., 1999. Piriformospora indica: a cultivable plant-growth-promoting root endophyte. Applied and Environmental Microbiology, 65, pp.2741–2744.
  129. Vassilev, N., Vassileva, M., Martos, V., Garcia del Moral, L.F., Kowalska, J., Tylkowski, B., and Eligio, M., 2020. Formulation of microbial inoculants by encapsulation in natural polysaccharides: focus on beneficial properties of carrier additives and derivatives. Frontiers in Plant Science, 11, p.270.
  130. Vejan, P., Khadiran, T., Abdullah, R., and Ahmad, N., 2021. Controlled release fertilizer: A review on developments, applications, and potential in agriculture. Journal of Controlled Release, 339, pp.321–334.
  131. Vejan, P., Khadiran, T., Abdullah, R., Ismail, S., and Dadrasnia, A., 2019. Encapsulation of plant growth promoting rhizobacteria—prospects and potential in agricultural sector: a review. Journal of Plant Nutrition, 42(19), pp.2600–2623.
  132. Verma, K.K., Joshi, A., Song, X.P., Singh, S., Kumari, A., Arora, J., Singh, S.K., Solanki, M.K., Seth, C.S., and Li, Y.R., 2024. Synergistic interactions of nanoparticles and plant growth promoting rhizobacteria enhancing soil-plant systems: a multigenerational perspective. Frontiers in Plant Science, 15, p.1376214.
  133. Vessey, J.K., 2003. Plant growth promoting rhizobacteria as biofertilizers. Plant and Soil, 255(2), pp.571–586.
  134. Vitousek, P.M., Menge, D.N.L., Reed, S.C., and Cleveland, C.C., 2013. Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Biological Sciences, 368, p.1621.
  135. Wang, N., Wang, B., Wan, Y., Gao, B., and Rajput, V.D., 2023. Alginate-based composites as novel soil conditioners for sustainable applications in agriculture: A critical review. Journal of Environmental Management, 348, p.119133.
  136. Wang, P., Menzies, N.W. and Lombi, E., 2023. Silicon nanoparticles in agriculture: Potential benefits and risks for plant growth and soil health. Frontiers in Plant Science, 14, 1187321.
  137. Wang, Q., Liu, J., and Zhu, H., 2018. Genetic and molecular mechanisms underlying symbiotic specificity in legume-rhizobium interactions. Plant Science, 9, p.313.
  138. Wang, Y., Zhang, X. and Li, J., 2023. Synergistic effects of PGPR and TiO2 nanoparticles on plant growth and stress tolerance. Science of The Total Environment, 866, 161380.
  139. Weir, S.C., Dupuis, S.P., Providenti, M.A., Lee, H., and Trevors, J.T., 1995. Nutrient enhanced survival of and phenanthrene mineralization by alginate-encapsulated and free Pseudomonas sp. UG14Lr cells in creosote-contaminated soil slurries. Applied Microbiology and Biotechnology, 43, pp.946–951.
  140. Westerman, R.L., 1990. Soil Testing and Plant Analysis. 3rd ed. Book Series No. 3, SSSA, USA.
  141. Wiwattanapatapee, R., Chumthong, A., Penagnoo, A., and Kanjanamaneesathian, M., 2013. Preparation and evaluation of Bacillus megaterium alginate microcapsules for control of rice sheath blight disease. World Journal of Microbiology and Biotechnology, 29, pp.1487–1497.
  142. Wu, Z., Zhao, Y., Kaleem, I., and Li, C., 2011. Preparation of calcium–alginate microcapsuled microbial fertilizer coating Klebsiella oxytoca Rs-5 and its performance under salinity stress. European Journal of Soil Biology, 47, pp.152–159.
  143. Xin, X., Zhao, F., Rho, J.Y., Goodrich, S.L., Sumerlin, B.S., and He, Z., 2020. Use of polymeric nanoparticles to improve seed germination and plant growth under copper stress. Science of the Total Environment, 745, p.141055.
  144. Yan, A., and Chen, Z., 2019. Impacts of silver nanoparticles on plants: a focus on the phytotoxicity and underlying mechanism. International Journal of Molecular Sciences, 20(5), p.1003.
  145. Younes, N.A., Dawood, M.F., and Wardany, A.A., 2019. Biosafety assessment of graphene nanosheets on leaf ultrastructure, physiological, and yield traits of Capsicum annuum L. and Solanum melongena L. Chemosphere, 228, pp.318–327.
  146. Young, C.C., Rekha, P.D., Lai, W.A., and Arun, A.B., 2006. Bioencapsulation of plant growth-promoting bacteria in alginate beads enriched with humic acid. Biotechnology and Bioengineering, 1, pp.76–83.
  147. Zahedi, S.M., Abolhassani, M., Hadian-Deljou, M., Feyzi, H., Akbari, A., Rasouli, F., Koçak, M.Z., Kulak, M., and Gohari, G., 2023. Proline-functionalized graphene oxide nanoparticles (GO-pro NPs): A new engineered nanoparticle to ameliorate salinity stress on grape (Vitis vinifera L. cv Sultana). Plant Stress, 7, p.100128.
  148. Zhang, H., Wang, R., Chen, Z., Cui, P., Lu, H., Yang, Y., and Zhang, H., 2021. The effect of zinc oxide nanoparticles for enhancing rice (Oryza sativa L.) yield and quality. Agriculture, 11(12), p.1247.
  149. Zhang, Y., Li, X. and Chen, G., 2024. Controlled release of nanoparticles for agricultural applications: Enhancing plant growth while minimizing environmental impact. Journal of Agricultural and Food Chemistry, 72(4), pp.1123–1135.
  150. Zhao, L., Huang, Y. and Hu, J., 2021. Nanotechnology for sustainable agriculture: Applications and perspectives. Science of the Total Environment, 755, 142466.
  151. Zohar-Perez, C., Ritte, E., Chernin, L., Chet, I., and Nussinovitch, A., 2002. Preservation of chitinolytic Pantoea agglomerans in a viable form by cellular dried alginate-based carriers. Biotechnology Progress, 18, pp.1133–1140.