Recent Advances in Encapsulation Techniques of Plant Growth-Promoting Microorganisms and Their Prospects in the Sustainable Agriculture

In addition to changing global demography and global warming, agricultural production systems around the world are threatened by intensive agricultural practices (overuse of land and excessive use of chemical fertilizers and pesticides) that deplete soils by affecting their dynamics and their fertility, pollute the environment, lower production, and alter biodiversity on a large scale. The use of bioformulations based on PGPMs (plant growth-promoting microorganisms) seems to be a promising and sustainable strategy to overcome these threats, thanks to their tolerance to various biotic and abiotic stresses and via their beneficial effects in promising plant growth, pest protection, bioremediation, and restoration of degraded lands. In recent years, particular attention has been paid to encapsulated formulations because they offer several advantages over conventional bioformulation (liquid and solid) related to shelf life, problems of survival and viability in the environment, and the efficiency of rhizospheric colonization. This review focuses on the types of encapsulations and the different technologies used in this process as well as the most commonly used substrates and additives. It also provides an overview on the application of encapsulated bioformulations as biofertilizers, biopesticides, or other biostimulators and summarizes the knowledge of the scientific literature on the development of nanoencapsulation in this sector.

[1]  V. Thakur,et al.  Encapsulation of Plant Biocontrol Bacteria with Alginate as a Main Polymer Material , 2021, International journal of molecular sciences.

[2]  Roohallah Saberi-Riseh,et al.  A novel encapsulation of Streptomyces fulvissimus Uts22 by spray drying and its biocontrol efficiency against Gaeumannomyces graminis, the causal agent of take-all disease in wheat. , 2021, Pest management science.

[3]  R. E. Krishnankutty,et al.  Evaluation of plant probiotic performance of Pseudomonas sp. encapsulated in alginate supplemented with salicylic acid and zinc oxide nanoparticles. , 2020, International journal of biological macromolecules.

[4]  M. Fomina,et al.  Microbial Interaction with Clay Minerals and Its Environmental and Biotechnological Implications , 2020, Minerals.

[5]  Anant V. Patel,et al.  Formulating bacterial endophyte: Pre-conditioning of cells and the encapsulation in amidated pectin beads , 2020, Biotechnology reports.

[6]  Pratyoosh Shukla,et al.  Techniques for improving formulations of bioinoculants , 2020, 3 Biotech.

[7]  M. Vassileva,et al.  Formulation of Microbial Inoculants by Encapsulation in Natural Polysaccharides: Focus on Beneficial Properties of Carrier Additives and Derivatives , 2020, Frontiers in Plant Science.

[8]  V. Dragović-Uzelac,et al.  Advanced Technologies for the Extraction of Marine Brown Algal Polysaccharides , 2020, Marine drugs.

[9]  Yangchao Luo,et al.  Chitosan-based hydrogel beads: Preparations, modifications and applications in food and agriculture sectors - A review. , 2020, International journal of biological macromolecules.

[10]  Prateek,et al.  Graphite modified sodium alginate hydrogel composite for efficient removal of malachite green dye. , 2020, International journal of biological macromolecules.

[11]  P. Zhou,et al.  Microencapsulation of Bacillus megaterium NCT-2 and its effect on remediation of secondary salinization soil , 2019, Journal of microencapsulation.

[12]  Roohallah Saberi-Rise,et al.  The effect of Bacillus subtilis Vru1 encapsulated in alginate - bentonite coating enriched with titanium nanoparticles against Rhizoctonia solani on bean. , 2019, International journal of biological macromolecules.

[13]  Rosazlin Abdullah,et al.  Encapsulation of plant growth promoting Rhizobacteria—prospects and potential in agricultural sector: a review , 2019, Journal of Plant Nutrition.

[14]  R. Mohammadinejad,et al.  Investigating the formulation of alginate- gelatin encapsulated Pseudomonas fluorescens (VUPF5 and T17-4 strains) for controlling Fusarium solani on potato. , 2019, International journal of biological macromolecules.

[15]  F. R. Rosado,et al.  Shelf Life of Azospirillum brasilense in Alginate Beads Enriched With Trehalose and Humic Acid , 2019, Journal of Agricultural Science.

[16]  M. Sohail,et al.  Chitosan oligosaccharide (COS): An overview. , 2019, International journal of biological macromolecules.

[17]  P. Dandge,et al.  Alleviation of salinity stress in rice plant by encapsulated salt tolerant plant growth promoting bacteria Pantoea agglomerans strain KL and its root colonization ability , 2019, Archives of Agronomy and Soil Science.

[18]  M. Ferrero,et al.  Development of low-cost formulations of plant growth-promoting bacteria to be used as inoculants in beneficial agricultural technologies. , 2019, Microbiological research.

[19]  D. Naik,et al.  Nanotechnology application in agriculture: A review , 2019 .

[20]  J. J. Perez,et al.  A novel, green, low-cost chitosan-starch hydrogel as potential delivery system for plant growth-promoting bacteria. , 2018, Carbohydrate polymers.

[21]  V. Thakur,et al.  Recent progress in sodium alginate based sustainable hydrogels for environmental applications , 2018, Journal of Cleaner Production.

[22]  G. Lucchesi,et al.  Alginate-perlite encapsulated Pseudomonas putida A (ATCC 12633) cells: Preparation, characterization and potential use as plant inoculants. , 2018, Journal of biotechnology.

[23]  T. Sa,et al.  Evaluation of chitosan and alginate immobilized Methylobacterium oryzae CBMB20 on tomato plant growth , 2018 .

[24]  A. Sessitsch,et al.  Maintenance and assessment of cell viability in formulation of non‐sporulating bacterial inoculants , 2017, Microbial biotechnology.

[25]  T. Prasad,et al.  Plant growth promoting rhizobacteria for sustainable agricultural practices with special reference to biotic and abiotic stresses , 2018, Plant Growth Regulation.

[26]  P. Guerrero,et al.  Chitosan as a bioactive polymer: Processing, properties and applications. , 2017, International journal of biological macromolecules.

[27]  F. Olivares,et al.  Plant growth promoting bacteria and humic substances: crop promotion and mechanisms of action , 2017, Chemical and Biological Technologies in Agriculture.

[28]  S. Jurić,et al.  Kinetics and Mechanisms of Chemical and Biological Agents Release from Biopolymeric Microcapsules. , 2017, Journal of agricultural and food chemistry.

[29]  G. Simó,et al.  Research progress in coating techniques of alginate gel polymer for cell encapsulation. , 2017, Carbohydrate polymers.

[30]  B. Ye,et al.  Preparation and characterization of monodisperse microcapsules with alginate and bentonite via external gelation technique encapsulating Pseudomonas putida Rs-198 , 2017, Journal of biomaterials science. Polymer edition.

[31]  C. Pereira,et al.  Beneficial rhizobacteria immobilized in nanofibers for potential application as soybean seed bioinoculants , 2017, PloS one.

[32]  S. Nardi,et al.  Soil-root cross-talking: The role of humic substances , 2017 .

[33]  K. Ramkumar,et al.  Preparation of collagen peptide functionalized chitosan nanoparticles by ionic gelation method: An effective carrier system for encapsulation and release of doxorubicin for cancer drug delivery. , 2017, Materials science & engineering. C, Materials for biological applications.

[34]  B. Ye,et al.  Viability evaluation of alginate-encapsulated Pseudomonas putida Rs-198 under simulated salt-stress conditions and its effect on cotton growth , 2016 .

[35]  Bruna Alice Gomes de Melo,et al.  Humic acids: Structural properties and multiple functionalities for novel technological developments. , 2016, Materials science & engineering. C, Materials for biological applications.

[36]  N. Bashan Inoculant formulations are essential for successful inoculation with plant growth-promoting bacteria and business opportunities. , 2016 .

[37]  Genlin Zhang,et al.  Encapsulation and characterization of slow-release microbial fertilizer from the composites of bentonite and alginate , 2015 .

[38]  V. Bini,et al.  Insights in Behavior of Variably Formulated Alginate-Based Microcapsules for Cell Transplantation , 2015, BioMed research international.

[39]  G. Gupta,et al.  Plant Growth Promoting Rhizobacteria (PGPR): Current and Future Prospects for Development of Sustainable Agriculture , 2015 .

[40]  S. Karlović,et al.  Improving the controlled delivery formulations of caffeine in alginate hydrogel beads combined with pectin, carrageenan, chitosan and psyllium. , 2015, Food chemistry.

[41]  A. Ting,et al.  Biocontrol of Fusarium oxysporum f.sp. cubense tropical race 4 by formulated cells and cell-free extracts of Streptomyces griseus in sterile soil environment , 2015 .

[42]  A. Margaritis,et al.  Biopolymer nanoparticle production for controlled release of biopharmaceuticals , 2014, Critical reviews in biotechnology.

[43]  A. Sosnik Alginate Particles as Platform for Drug Delivery by the Oral Route: State-of-the-Art , 2014, ISRN pharmaceutics.

[44]  Zhansheng Wu,et al.  Root colonization of encapsulated Klebsiella oxytoca Rs-5 on cotton plants and its promoting growth performance under salinity stress , 2014 .

[45]  Y. Bashan,et al.  Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013) , 2014, Plant and Soil.

[46]  Anant V. Patel,et al.  Review of encapsulation methods suitable for microbial biological control agents , 2013 .

[47]  Sapna S. Mishra,et al.  Preparation, characterization, and insecticidal activity evaluation of three different formulations of Beauveria bassiana against Musca domestica , 2013, Parasitology Research.

[48]  R. Surampalli,et al.  EFFECT OF EMULSION FORMULATION OF SINORHIZOBIUM MELILOTI AND PRE-INOCULATED SEEDS ON ALFALFA NODULATION AND GROWTH: A POUCH STUDY , 2013 .

[49]  A. Rasool,et al.  Effects of free and encapsulated co-culture bacteria on cotton growth and soil bacterial communities , 2012 .

[50]  D. Poncelet,et al.  Starch filler and osmoprotectants improve the survival of rhizobacteria in dried alginate beads , 2012, Journal of microencapsulation.

[51]  Youfu Zhao,et al.  Controlled release of Pantoea agglomerans E325 for biocontrol of fire blight disease of apple. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[52]  A. Sari,et al.  Antimony(III) Adsorption from Aqueous Solution Using Raw Perlite and Mn-Modified Perlite: Equilibrium, Thermodynamic, and Kinetic Studies , 2012 .

[53]  E. Malusá,et al.  Technologies for Beneficial Microorganisms Inocula Used as Biofertilizers , 2012, TheScientificWorldJournal.

[54]  Chun Xing Li,et al.  Encapsulation of R. planticola Rs-2 from alginate-starch-bentonite and its controlled release and swelling behavior under simulated soil conditions , 2012, Journal of Industrial Microbiology & Biotechnology.

[55]  Armando Garcia Anhydrobiosis in bacteria: From physiology to applications , 2011, Journal of Biosciences.

[56]  Rojan P John,et al.  Bio-encapsulation of microbial cells for targeted agricultural delivery , 2011, Critical reviews in biotechnology.

[57]  Minaxi,et al.  Efficacy of rhizobacterial strains encapsulated in nontoxic biodegradable gel matrices to promote growth and yield of wheat plants , 2011 .

[58]  André Henrique Rosa,et al.  Paraquat-loaded alginate/chitosan nanoparticles: preparation, characterization and soil sorption studies. , 2011, Journal of hazardous materials.

[59]  D. Dowling,et al.  Alginate beads as a storage, delivery and containment system for genetically modified PCB degrader and PCB biosensor derivatives of Pseudomonas fluorescens F113 , 2011, Journal of applied microbiology.

[60]  Yimin Li,et al.  Carboxylmethylcellulose/bentonite composite gels: Water sorption behavior and controlled release of herbicide , 2009 .

[61]  M. Albareda,et al.  Alternatives to peat as a carrier for rhizobia inoculants: Solid and liquid formulations , 2008 .

[62]  Jing Chen,et al.  New advances in plant growth-promoting rhizobacteria for bioremediation. , 2007, Environment international.

[63]  A. Arun,et al.  Effect of free and encapsulated Pseudomonas putida CC-FR2-4 and Bacillus subtilis CC-pg104 on plant growth under gnotobiotic conditions. , 2007, Bioresource technology.

[64]  A. Arun,et al.  Encapsulation of plant growth‐promoting bacteria in alginate beads enriched with humic acid , 2006, Biotechnology and bioengineering.

[65]  P. White,et al.  Preservation of micro-organisms by drying; a review. , 2006, Journal of microbiological methods.

[66]  S. K. Brar,et al.  Recent advances in downstream processing and formulations of Bacillus thuringiensis based biopesticides , 2006 .

[67]  P. Trivedi,et al.  Carrier-based Preparations of Plant Growth-promoting Bacterial Inoculants Suitable for use in Cooler Regions , 2005 .

[68]  J. Karkalas,et al.  Starch-composition, fine structure and architecture , 2004 .

[69]  J. Streeter Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation , 2003, Journal of applied microbiology.

[70]  Y. Bashan,et al.  Alginate microbeads as inoculant carriers for plant growth-promoting bacteria , 2002, Biology and Fertility of Soils.

[71]  J. Traquair,et al.  Formulation of a Streptomyces Biocontrol Agent for the Suppression of Rhizoctonia Damping-off in Tomato Transplants , 2002 .

[72]  J. Usall,et al.  Effect of protective agents, rehydration media and initial cell concentration on viability of Pantoea agglomerans strain CPA‐2 subjected to freeze‐drying , 2000, Journal of applied microbiology.

[73]  J. Benoit,et al.  Rhizobacteria microencapsulation: properties of microparticles obtained by spray-drying. , 1999, Journal of microencapsulation.

[74]  H. D. Burges,et al.  Formulation of Microbial Biopesticides , 1998, Springer Netherlands.

[75]  G. Reineccius,et al.  Off-flavors in foods. , 1991, Critical reviews in food science and nutrition.

[76]  F. Otey,et al.  Starch–borate complexes for EPTC encapsulation , 1984 .