Abstract
Bioinoculants are eco-friendly microorganisms having a variety of products commonly utilized for improving the potential of soil and providing the nutrient requirements to the host plant. The usage of chemical fertilizers is not beneficial because it affects the soil microbial communities on large scale. The toxicity of chemical fertilizer decreases the fertility of soil and causes microbial disruption. Bioinoculants that are used as PGPR play an important role in the enhancement of crop production and beneficial for both producers and consumers economically by protecting the soil during unfavourable conditions. The utilization of PGPR in the bioinoculant form imparts successfully sustain agricultural yield production and such formulated products contain living microbial cells of bioinoculants that also helps in seed treatment and enhances the mobilization process of nutrients by the low-cost process. This review mainly focuses on different bioinoculant formulations related to its recent approaches such as metabolite formulations, liquid formulations, solid carrier-based formulations and synthetic polymer-based formulations. This review also gives an overview of some aspects of the bioinoculant efficiency and their appropriate formulation, production and storage condition of microbial cells.
Similar content being viewed by others
References
Aini N, Yamika WSD, Ulum B (2019) Effect of nutrient concentration, PGPR and AMF on plant growth, yield, and nutrient uptake of hydroponic lettuce. Int J Agric Biol 21(1):175–183. https://doi.org/10.17957/IJAB/15.0879
Ali Z, Abul-Faraj A, Li L, Ghosh N, Piatek M, Mahjoub A et al (2015) Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol Plant 8:1288–1291. https://doi.org/10.1016/j.molp.2015.02.011
Andersen MM, Landes X, Xiang W, Anyshchenko A, Falhof J, Østerberg JT et al (2015) Feasibility of new breeding techniques for organic farming. Trends Plant Sci 20:426–434. https://doi.org/10.1016/j.tplants.2015.04.011
Aremu BR, Alori ET, Kutu RF, Babalola OO (2017) Potentials of microbial inoculants in soil productivity: an outlook on African legumes. In: Panpatte DG, Jhala YK, Vyas RVS (eds) Microorganisms for green revolution HN. Springer, Singapore, pp 53–75. https://doi.org/10.1007/978-981-10-6241-4_3
Arora NK, Mishra J (2016) Prospecting the roles of metabolites and additives in future bioformulations for sustainable agriculture. Appl Soil Ecol 107:405–407. https://doi.org/10.1016/j.apsoil.2016.05.020
Arora NK, Verma M, Mishra J (2017) Rhizobial bioformulations: past, present and future. In: Mehnaz S (ed) Rhizotrophs: plant growth promotion to bioremediation. Springer, Singapore, pp 69–99. https://doi.org/10.1007/978-981-10-4862-3_4
Bahadur I, Maurya BR, Kumar A, Meena VS, Raghuwanshi R (2016) Towards the soil sustainability and potassium-solubilizing microorganisms. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 255–266. https://doi.org/10.1007/978-81-322-2776-2_18
Baloglu MC, Kavas M, Gürel S, Gurel E (2018) The use of microorganisms for gene transfer and crop improvement. In: Prasad R, Gill SS, Tuteja N (eds) Crop improvement through microbial biotechnology pp 1–25. Elsevier, Berlin. https://doi.org/10.1016/B978-0-444-63987-5.00001-3
Bashan Y, de-Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378(1–2):1–33. https://doi.org/10.1007/s11104-013-1956-x
Bashan Y, Hernandez JP, Leyva LA, Bacilio M (2002) Alginate microbeads as inoculant carriers for plant growth-promoting bacteria. Biol Fert Soils 35(5):359–368. https://doi.org/10.1007/s00374-002-0481-5
Berninger T, Gonzalez Lopez O, Bejarano A, Preininger C, Sessitsch A (2018) Maintenance and assessment of cell viability in formulation of non-sporulating bacterial inoculants. Microb biotechnol 11(2):277–301. https://doi.org/10.1111/1751-7915.12880
Bextine BR, Thorvilson HG (2002) Field applications of bait-formulated Beauveria bassiana alginate pellets for biological control of the red imported fire ant (Hymenoptera: Formicidae). Environ entomol 31(4):746–752. https://doi.org/10.1603/0046-225X-31.4.746
Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6(1):1–16. https://doi.org/10.1038/srep34768
Bhattacharyya C, Roy R, Tribedi P, Ghosh A, Ghosh A (2020) Biofer-tilizers as substitute to commercial agrochemicals. In: Majeti N, Vara P (eds) Agrochemicals detection, treatment and remediation butterworth-heinemann, pp 263–290. https://doi.org/10.1016/B978-0-08-103017-2.00011-8
Ceglie FG, Bustamante MA, Amara MB, Tittarelli F (2015) The challenge of peat substitution in organic seedling production: optimization of growing media formulation through mixture design and response surface analysis. PLoS ONE 10(6):e0128600. https://doi.org/10.1371/journal.pone.0128600
Chandra D, Barh A, Sharma IP (2018) Plant growth promoting bacteria: a gateway to sustainable agriculture. Microbial Biotechnol Environ Monitor Cleanup 2018:318–338. https://doi.org/10.4018/978-1-5225-3126-5.ch020
Chaudhary T, Shukla P (2019) Bioinoculants for bioremediation applications and disease resistance: innovative perspectives. Indian J Microbiol 59(2):129–136. https://doi.org/10.1007/s12088-019-00783-4
Covarrubias SA, Bashan LE, Moreno M, Bashan Y (2012) Alginate beads provide a beneficial physical barrier against native microorganisms in wastewater treated with immobilized bacteria and microalgae. Appl Microbiol Biotechnol 93(6):2669–2680. https://doi.org/10.1007/s00253-011-3585-8
Dangi AK, Sharma B, Hill RT, Shukla P (2019) Bioremediation through microbes: systems biology and metabolic engineering approach. Crit Rev Biotechnol 39(1):79–98. https://doi.org/10.1080/07388551.2018.1500997
Dangi AK, Sharma B, Khangwal I, Shukla P (2018) Combinatorial interactions of biotic and abiotic stresses in plants and their molecular mechanisms: systems biology approach. Mol Biotechnol 60(8):636–650. https://doi.org/10.1007/s12033-018-0100-9
de-Bashan LE, Hernandez JP, Bashan Y (2012) The potential contribution of plant growth-promoting bacteria to reduce environmental degradation—a comprehensive evaluation. Appl Soil Ecol 61:171–189. https://doi.org/10.1016/j.apsoil.2011.09.003
Frederix M, Edwards A, Swiderska A (2014) Mutation of praR in Rhizobium leguminosarum enhances root biofilms, improving nodulation competitiveness by increased expression of attachment proteins. Mol microbial 93(3):464–478. https://doi.org/10.1111/mmi.12670
Gopi GK, Meenakumari KS, Nysanth NS, Subha P (2019) An optimized standard liquid carrier formulation for extended shelf-life of plant growth promoting bacteria. Rhizosphere 11:100160. https://doi.org/10.1016/j.rhisph.2019.100160
Imam J, Shukla P, Prasad Mandal N, Variar M (2017) Microbial interactions in plants: perspectives and applications of proteomics. Curr Protein Pept Sci 18(9):956–965. https://doi.org/10.2174/1389203718666161122103731
Imam J, Singh PK, Shukla P (2016) Plant microbe interactions in post genomic era: perspectives and applications. Front Microbiol 7:1488. https://doi.org/10.3389/fmicb.2016.01488
Imam J, Variar M, Shukla P (2013) Role of enzymes and proteins in plant-microbe interaction: a study of M oryzae versus rice. In: Shukla P, Pletschke BI (eds) Advances in enzyme biotechnology, pp 137–145. Springer, New Delhi. https://doi.org/10.1007/978-81-322-1094-8_10
John RP, Tyagi RD, Brar SK, Prevost D, Surampalli RY (2013) Effect of emulsion formulation of Sinorhizobium meliloti and pre-inoculated seeds on alfalfa nodulation and growth: a pouch study. J Plant Nutr 36(2):231–242. https://doi.org/10.1080/01904167.2012.739243
Kaushal M, Wani SP (2015) Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann Microbiol. https://doi.org/10.1007/s13213-015-1112-3
Kim YC, Glick BR, Bashan Y, Ryu CM (2012) Enhancement of plant drought tolerance by microbes. In: Aroca R (ed) Plant responses to drought stress. Springer, Berlin, Heidelberg, pp 383–413. https://doi.org/10.1007/978-3-642-32653-0_15
Kumar BK, Ismail S, Patil VD (2017) Role of microbial solubilisers on major nutrient uptake—a review. J Pharmacogn Phytochem 6(5):641–644
Kumar V, Baweja M, Singh PK, Shukla P (2016) Recent developments in systems biology and metabolic engineering of plant–microbe interactions. Front Plant Sci 7:1421. https://doi.org/10.3389/fpls.2016.01421
Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228(3):367–381. https://doi.org/10.1007/s00425-008-0772-7
Lakey JR, Krishnan R, Botvinick EL (2017) Methods of manipulating alginate microcapsule size and permeability. US Patent Application 15(204), 916
Lalitha S (2017) Plant growth-promoting microbes: a boon for sustainable agriculture. In: Dhanarajan A (ed) Sustainable agriculture towards food security. Springer, Singapore, pp 125–158. https://doi.org/10.1007/978-981-10-3473-2_18
Li P, Muuller M, Chang MW, Frettlooh M, Schoonherr H (2017) Encapsulation of autoinducer sensing reporter bacteria in reinforced alginate-based microbeads. ACS App Mater Interfaces 9(27):22321–22331. https://doi.org/10.1021/acsami.7b07166
Lopez BR, Bashan Y, Trejo A, de Bashan LE (2013) Amendment of degraded desert soil with wastewater debris containing immobilized Chlorella sorokiniana and Azospirillum brasilense significantly modifies soil bacterial community structure, diversity, and richness. Biol fertil soil 49(8):1053–1063. https://doi.org/10.1007/s00374-013-0799-1
Ma Y (2019) Seed coating with beneficial microorganisms for precision agriculture. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2019.107423
Mahanty T, Bhattacharjee S, Goswami M, Bhattacharyya P, Das B, Ghosh A, Tribedi P (2017) Biofertilizers: a potential approach for sustainable agriculture development. Environ Sci Pollut Res 24(4):3315–3335. https://doi.org/10.1007/s11356-016-8104-0
Maillet F, Poinsot V, André O et al (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469(7328):58. https://doi.org/10.1038/nature09622
Malusa E, Sas-Paszt L, Ciesielska J (2012) Technologies for beneficial microorganisms inocula used as biofertilizers. Sci World J. https://doi.org/10.1100/2012/491206
Meena VS, Meena SK, Verma JP (2017) Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: a review. Ecol eng 107:8–32. https://doi.org/10.1016/j.ecoleng.2017.06.058
Mutturi S, Sahai V, Bisaria VS (2017) Fed-batch cultivation for high density culture of Pseudomonas spp. for bioinoculant preparation. In: Varma A, Sharma AK (eds) Modern tools and techniques to understand microbes. Springer, Cham, pp 381–400. https://doi.org/10.1007/978-3-319-49197-4_24
Pathak D, Lone R, Koul KK (2017) Arbuscular mycorrhizal fungi (amf) and plant growth-promoting rhizobacteria (pgpr) association in potato (Solanum tuberosum L.): a brief review. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics and plant health. Springer, Singapore, pp 401–420. https://doi.org/10.1007/978-981-10-3473-2_18
Perez-Garcia A, Romero D, De Vicente A (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotechnol 22(2):187–193. https://doi.org/10.1021/bp025532t
Puri A, Padda KP, Chanway CP (2017) Beneficial effects of bacterial endophytes on forest tree species. In: Maheshwari D, Annapurna K (eds) Endophytes: crop productivity and protection. Sustainable development and biodiversity, vol 16. Springer, Cham, pp 111–132. https://doi.org/10.1007/978-3-319-66544-3_6
Qiu Z, Egidi E, Liu H (2019) New frontiers in agriculture productivity: optimised microbial inoculants and in situ microbiome engineering. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2019.03.010
Rani U, Kumar V (2019) Microbial bioformulations: present and future aspects. In: Prasad R, Kumar V, Kumar M, Choudhary D (eds) Nanobiotechnology in bioformulations. Springer, Cham, pp 243–258. https://doi.org/10.1007/978-3-030-17061-5_10
Reddy CA, Saravanan RS (2013) Polymicrobial multi-functional approach for enhancement of crop productivity. Adv Appl Microbiol 82:53–113. https://doi.org/10.1016/B978-0-12-407679-2.00003-X
Rekha PD, Lai WA, Arun AB, Young CC (2007) Effect of free and encapsulated Pseudomonas putida CC-FR2-4 and Bacillus subtilis CC-pg104 on plant growth under gnotobiotic conditions. Bioresour Technol 98(2):447–451
Sabaratnam S, Traquair JA (2002) Formulation of a Streptomyces biocontrol agent for the suppression of Rhizoctonia damping-off in tomato transplants. Biol Control 23(3):245–253. https://doi.org/10.1006/bcon.2001.1014
Sahu PK, Gupta A, Singh M (2018) Bioformulation and fluid bed drying. A new approach towards an improved biofertilizer formulation. In: Sengar RS, Singh A (eds) Eco-friendly agro-biological techniques for enhancing crop productivity. Springer, Singapore, pp 47–62. https://doi.org/10.1007/978-981-10-6934-5_3
Schoebitz M, Belchi MDL (2016) Encapsulation techniques for plant growth-promoting rhizobacteria. In: Arora NK, Mehnaz S, Balestrini R (eds) Bioformulations for sustainable agriculture. Springer, India, pp 251–265
Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 140(3–4):339–353. https://doi.org/10.1016/j.agee.2011.01.017
Singh P (2018) Development and characterization of cellulose based systems for the entrapment and delivery of probiotic bacteria (Doctoral dissertation, 00500: Universidade de Coimbra)
Surendra KA, Baby A (2016) Enhanced shelf life of Azospirillum and PSB (Phosphate solubilizing Bacteria) through addition of chemical additives in liquid formulations. Int J Sci Environ Technol 5(4):2023–2029
Suyal DC, Soni R, Sai S, Goel R (2016) Microbial inoculants as biofertilizer. In: Singh DP, Singh HB, Prabha R (eds) Microbial inoculants in sustainable agricultural productivity. Springer, New Delhi, pp 311–318
Tahir HAS, Gu Q, Wu H, Niu Y, Huo R, Gao X (2017) Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci Rep 7:40481. https://doi.org/10.1038/srep40481
Tang Y, Kang H, Qin Z, Zhang K, Zhong Y, Li H, Mo L (2020) Significance of manganese resistant Bacillus cereus strain WSE01 as a bioinoculant for promotion of plant growth and manganese accumulation in Myriophyllum verticillatum. Sci Total Environ 707:135867. https://doi.org/10.1016/j.scitotenv.2019.135867
Tewari S, Arora NK (2016) Exopolysaccharides based bioformulation from Pseudomonas aeruginosa combating saline stress. Recent Trends PGPR Res Sustain Crop Product 2016:93
Timmusk S, Behers L, Muthoni J, Muraya A, Aronsson AC (2017) Perspectives and challenges of microbial application for crop improvement. Front Plant Sci 8:49. https://doi.org/10.3389/fpls.2017.00049
Timmusk S, El-Daim IAA, Copolovici L et al (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS ONE 9(5):e96086. https://doi.org/10.1371/journal.pone.0096086
Trejo A, De-Bashan LE, Hartmann A et al (2012) Recycling waste debris of immobilized microalgae and plant growth-promoting bacteria from wastewater treatment as a resource to improve fertility of eroded desert soil. Environ Exper Bot 75:65–73. https://doi.org/10.1016/j.envexpbot.2011.08.007
Trivedi P, Pandey A (2008) Recovery of plant growth-promoting rhizobacteria from sodium alginate beads after 3 years following storage at 4 C. J Ind Microbiol Biotechnol 35(3):205–209. https://doi.org/10.1007/s10295-007-0284-7
Trivedi P, Pandey A, Palni LMS (2005) Carrier-based preparations of plant growth-promoting bacterial inoculants suitable for use in cooler regions. World J Microbiol Biotechnol 21(6–7):941–945. https://doi.org/10.1007/s11274-004-6820-y
Wang Y, Ren W, Li Y et al (2019) Nontargeted metabolomic analysis to unravel the impact of di (2-ethylhexyl) phthalate stress on root exudates of alfalfa (Medicago sativa). Sci Total Environ 646:212–219. https://doi.org/10.1016/j.scitotenv.2018.07.247
Warra AA, Prasad MNV (2020) African perspective of chemical usage in agriculture and horticulture—their impact on human health and environment. In: Majeti N, Vara P (eds) Agrochemicals detection, treatment and remediation butterworth-heinemann, pp 401–436. https://doi.org/10.1016/B978-0-08-103017-2.00016-7
Wu Z, He Y, Chen L et al (2014) Characterization of Raoultella planticola Rs-2 microcapsule prepared with a blend of alginate and starch and its release behavior. Carbohyd Polym 110:259–267. https://doi.org/10.1016/j.carbpol.2014.04.011
Yabur R, Bashan Y, Hernández-Carmona G (2007) Alginate from the macroalgae Sargassum sinicola as a novel source for microbial immobilization material in wastewater treatment and plant growth promotion. J Appl Phycol 19(1):43–53. https://doi.org/10.1007/s10811-006-9109-8
Young CC, Rekha PD, Lai WA, Arun AB (2006) Encapsulation of plant growth-promoting bacteria in alginate beads enriched with humic acid. Biotechnol Bioeng 95(1):76–83. https://doi.org/10.1002/bit.20957
Zago SL, dos Santos MF, Konrad D, Fiorini A, Rosado FR, Missio RF, Vendruscolo ECG (2019) Shelf life of Azospirillum brasilense in alginate beads enriched with trehalose and humic acid. J Agric Sci 11:6. https://doi.org/10.5539/jas.v11n6p269
Zaidi A, Khan MS, Saif S et al (2017) Role of nitrogen-fixing plant growth-promoting rhizobacteria in sustainable production of vegetables. Current perspective. In: Zaidi A, Khan MS (eds) Microbial strategies for vegetable production. Springer, Cham, pp 49–79. https://doi.org/10.1007/978-3-319-54401-4_3
Zhang S, Moyne AL, Reddy MS, Kloepper JW (2002) The role of salicylic acid in induced systemic resistance elicited by plant growth-promoting rhizobacteria against blue mold of tobacco. Biol Control 25(3):288–296. https://doi.org/10.1016/S1049-9644(02)00108-1
Zohar-Perez C, Ritte E, Chernin L (2002) Preservation of chitinolytic Pantoaeag glomerans in a viable form by cellular dried alginate-based carriers. Biotechnol Progress 18(6):1133–1140. https://doi.org/10.1021/bp025532t
Acknowledgements
The author, TC acknowledges Maharshi Dayanand University, Rohtak, India for University Research Scholarship (URS). PS acknowledges Department of Science and Technology, New Delhi, Govt. of India, FIST grant (Grant no. 1196 SR/FST/LS-I/ 2017/4) and Department of Biotechnology, Government of India (Grant no. BT/PR27437/BCE/8/1433/2018).
Author information
Authors and Affiliations
Contributions
TC wrote the manuscript with contributions from MD, AKS and GG. The manuscript was edited by PS, RG, AP.
Corresponding author
Ethics declarations
Conflict of interest
The Authors don’t have any conflict of interest.
Ethical statement
This review article does not contain any studies with human participants or animals performed by any of the authors.
Rights and permissions
About this article
Cite this article
Chaudhary, T., Dixit, M., Gera, R. et al. Techniques for improving formulations of bioinoculants. 3 Biotech 10, 199 (2020). https://doi.org/10.1007/s13205-020-02182-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-020-02182-9