Keywords
Biofertilizer
Biopesticide
Soil biodiversity
Soil microbiome
How to Cite
Abstract
Microbial inoculants can be an efficient tool to manage the soil and plant microbiomes providing direct beneficial effects, and for modulating native soil and plant-associated microbiota. However, the application of soil microbial inoculants as biofertilizers and biopesticides in agriculture is still limited by factors related to their formulation, application method, and the knowledge about the impact and interactions between microbial inoculants and native soil and plant host microbiomes. The review is thus describing and discussing three major aspects related to microbial-based product exploitation, namely: i) the discovery and screening of beneficial microbial strains; ii) the opportunities and challenges associated with strain multifunctional features; iii) the fermentation and formulation strategies also based on the use of wastes as growth substrates and the technical and regulatory challenges faced in their path to field application. All these issues are addressed in activities performed by the EXCALIBUR project (www.excaliburproject.eu), which aims to expand the current concept about microbiomes interactions, acknowledging their interactive network that can impact agricultural practices as well as on all living organisms within an ecosystem.
References
Berg G, Rybakova D, Fischer D, Cernava T, Vergès MC, Charles T, et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome 2020; 8(1): 1-22, , doi:10.1186/s40168-020-00875-0.
Kinross JM, Darzi AW, Nicholson JK. Gut microbiome-host interactions in health and disease. Genome Med 2011; 3(3): 1-12, doi:10.1186/gm228.
Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol 2015; 31(1): 69, doi:10.1097/MOG.0000000000000139.
Pannaraj PS, Li F, Cerini C, Bender JM, Yang S, Rollie A, et al. Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatr 2017; 171(7): 647-654, doi:10.1001/jamapediatrics.2017.0378.
Turner TR, James EK, Poole PS. The plant microbiome. Genome Biol 2013; 14(6): 1-10, doi:10.1186/gb-2013-14-6-209.
Compant S, Brader G, Muzammil S, Sessitsch A, Lebrihi A, Mathieu F. Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases. BioControl 2013; 58: 435-455, doi:10.1007/s10526-012-9479-6.
Berg G, Grube M, Schloter M, Smalla K. The plant microbiome and its importance for plant and human health. Front Microbiol 2014; 5: 1, doi:10.3389/fmicb.2014.00491.
Berg G, Grube M, Schloter M, Smalla K. Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 2014b; 5: 148, doi:10.3389/fmicb.2014.00148.
Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science 2008; 320(5883): 1647-1651, doi:10.1126/science.1155725.
Barko PC, McMichael MA, Swanson KS, Williams DA. The gastrointestinal microbiome: a review. J Vet Intern Med 2012; 32(1): 9-25, doi:10.1111/jvim.14875.
Seedorf H, Griffin NW, Ridaura VK, Reyes A, Cheng J, Rey FE, et al. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 2014; 159(2): 253-66, doi: 10.1016/j.cell.2014.09.008.
Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat EVL, Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Ann Rev Plant Biol. 2013; 64: 807–838, doi:10.1146/annurev-arplant-050312-120106.
Blaser MJ, Cardon ZG, Cho MK, Dangl JL, Donohue TJ, Green JL, et al. Toward a predictive understanding of Earth’s microbiomes to address 21st century challenges. 2016; 7(3): e00714-16, doi:10.1128/mBio.00714-16.
Berg G. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 2009; 84(1): 11-8, doi: 10.1007/s00253-009-2092-7.
Berg G, Kusstatscher P, Abdelfattah A, Cernava T, Smalla K. Microbiome Modulation—Toward a Better Understanding of Plant Microbiome Response to Microbial Inoculants. Front Microbiol 2021; 12: 803, doi:10.3389/fmicb.2021.650610.
Bashan Y, Prabhu SR, de-Bashan LE, Kloepper JW. Disclosure of exact protocols of fermentation, the identity of microorganisms within consortia, formation of advanced consortia with microbe-based products. Biol Fertil Soils 2020; 56: 443–445, doi:10.1007/s00374-020-01464-x.
Malusá E, Canfora L, Pinzari F, Tartanus M, Łabanowska BH. Improvement of Soilborne Pests Control with Agronomical Practices Exploiting the Interaction of Entomophagous Fungi. In Singh D, Singh H, Prabha R, Eds.; Plant Microbe Interactions in Agro Ecological Perspectives. Springer: Singapore, 2017; doi:10.1007/978-981-10-5813-4_29.
Canfora L, Costa C, Pallottino F, Mocali S. Trends in Soil Microbial Inoculants Research: A Science Mapping Approach to Unravel Strengths and Weaknesses of their Application. Agriculture, 2021; 11: 158, doi.org/10.3390/ agriculture11020158.
Kaminsky LM, Trexler RV, Malik RJ, Hockett KL, Bell TH. The inherent conflicts in developing soil microbial inoculants. Trends Biotechnol. 2019; 37: 140–151, doi:10.1016/j.tibtech.2018.11.011.
Hamonts K, Trivedi P, Garg A, Janitz C, Grinyer J, Holford P, et al. Field study reveals core plant microbiota and relative importance of their drivers. Environ Microbiol 2018; 20(1): 124-140, doi:10.1111/1462-2920.14031.
Singh BK, Liu H, Trivedi P. Eco-holobiont: a new concept to identify drivers of host-associated microorganisms. Environ Microbiol 2020; 22(2): 564-567, doi:10.1111/1462-2920.14900.
Flandroy L, Poutahidis T, Berg G, Clarke G, Dao MC, Decaestecker E, et al. The impact of human activities and lifestyles on the interlinked microbiota and health of humans and of ecosystems. Sci Total Environ 2018; 627: 1018-1038, doi:10.1016/j.scitotenv.2018.01.288.
Carrion VJ, Cordovez V, Tyc O, Etalo DW, de Bruijn I, de Jager VCL, et al. Involvement of Burkholderiaceae and sulfurous volatiles in disease-suppressive soils. ISME J 2018; 12(9): 2307-2321, doi: 10.1038/s41396-018-0186-x.
Cernava T. How microbiome studies could further improve biological control. Biol Control 2021; 104669, doi:10.1016/j.biocontrol.2021.104669.
Matsumoto H, Fan X, Wang Y, Kusstatscher P, Duan J, Wu S, et al. Bacterial seed endophyte shapes disease resistance in rice. Nat Plants 2021; 7(1): 60-72. doi:10.1038/s41477-020-00826-5.
Agrahari RK, Singh P, Koyama H, Panda SK. Plant-microbe interactions for sustainable agriculture in the post-genomic era. Curr Genomics 2020; 21(3): 168-178, doi: 10.2174/1389202921999200505082116.
Berg G. Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 2009; 84: 11–18, doi:10.1007/s00253-009-2092-7.
Opelt K, Berg C, Berg G. The bryophyte genus Sphagnum is a reservoir for powerful and extraordinary antagonists and potentially facultative human pathogens. FEMS Microbiol Ecol 2007; 61: 38–53, doi:10.1111/j.1574-6941.2007.00323.x.
Shcherbakov A, Bragina A, Kuz’mina EI, Berg K, Muntian A, Makarova N, et al. Bacterial endophytes from Sphagnum mosses as a promising objects for agricultural microbiology. Mikrobiologiia 2013; 82, 312–322, doi:10.7868/S0026365613030130.
Wicaksono WA, Cernava T, Berg C, Berg G. Bog ecosystems as a playground for plant–microbe coevolution: bryophytes and vascular plants harbour functionally adapted bacteria. Microbiome 2021; 9(1): 1-16, doi:10.1186/s40168-021-01117-7.
Köberl M, Schmidt R, Ramadan EM, Bauer R, Berg G. The microbiome of medicinal plants: diversity and importance for plant growth, quality and health. Front Microbiol 2013; 4: 400, doi:10.3389/fmicb.2013.00400.
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev. 2015; 79: 293–320, doi:10.1128/MMBR.00050-14.
Rai AK, Singh DP, Prabha R, Kumar M, Sharma L. Microbial Inoculants: Identification, Characterization, and Applications in the Field. In: Singh DP, Singh HB, Prabha R, Eds. Microbial Inoculants in Sustainable Agricultural Productivity: Vol. 1: Research Perspectives, New Delhi: Springer India 2016; pp. 103–115, doi:10.1007/978-81-322-2647-5_6.
Berg G, Fritze A, Roskot N, Smalla K. Evaluation of potential biocontrol rhizobacteria from different host plants of Verticillium dahliae Kleb. J Appl Microbiol 2001; 91: 963–971, doi:10.1046/j.1365-2672.2001.01462.x.
Cardinale M, Grube M, Erlacher A, Quehenberger J, Berg G. Bacterial networks and co‐occurrence relationships in the lettuce root microbiota. Environ Microbiol 2015; 17: 239–252, doi:10.1111/1462-2920.12686.
Pérez-Jaramillo JE, Mendes R, Raaijmakers JM. Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol 2016; 90: 635–644, doi:10.1007/s11103-015-0337-7.
Kusstatscher P, Cernava T, Harms K, Maier J, Eigner H, Berg G, et al. Disease incidence in sugar beet fields is correlated with microbial diversity and distinct biological markers. Phytobiomes J 2019; 3(1): 22-30, doi:10.1094/PBIOMES-01-19-0008-R.
Raaijmakers JM, Mazzola M. Soil immune responses. Science 2016; 352: 1392–1393, doi:10.1126/science.aaf3252.
Pugliese M, Liu B, Gullino ML, Garibaldi A. Selection of antagonists from compost to control soil-borne pathogens. J Plant Dis Prot 2008; 115: 220–228, doi:10.1007/BF03356267.
Wolfgang A, Zachow C, Müller H, Grand A, Temme N, Tilcher R, et al. Understanding the impact of cultivar, seed origin, and substrate on bacterial diversity of the sugar beet rhizosphere and suppression of soil-borne pathogens. Front Plant Sci 2020; 11: 1450, doi:10.3389/fpls.2020.560869.
Berg G, Grube M, Schloter M, Smalla K. Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 2014; 5: 148, doi:10.3389/fmicb.2014;00148.
Lugtenberg B, Kamilova F. Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 2019; 63: 541–556, doi:10.1146/annurev.micro.62.081307.162918.
Raymaekers K, Ponet L, Holtappels D, Berckmans B, Cammue BP. Screening for novel biocontrol agents applicable in plant disease management–a review. Biol Control 2020; 144: 104240, doi:10.1016/j.biocontrol.2020.104240.
Han SH, Kang BR, Lee JH, Kim HJ, Park JY, Kim JJ, et al. Isolation and characterization of oligotrophic bacteria possessing induced systemic disease resistance against plant pathogens. Plant Pathol J 2012; 28(1): 68-74, doi:10.5423/PPJ.NT.11.2011.0218.
Zachow C, Müller H, Tilcher R, Donat C, Berg G. Catch the best: novel screening strategy to select stress protecting agents for crop plants. Agronomy 2013; 3: 794–815, doi:10.3390/agronomy3040794.
Hu J, Wei Z, Friman VP, Gu S, Wang X, Eisenhauer N, et al. Probiotic diversity enhances rhizosphere microbiome function and plant disease suppression. MBio 2016; 7, doi:10.1128/mBio.01790-16.
Yasmin S, Zaka A, Imran A, Zahid MA, Yousaf S, Rasul G, et al. Plant growth promotion and suppression of bacterial leaf blight in rice by inoculated bacteria. PloS One 2016; 11: e0160688, doi:10.1371/journal.pone.0160688.
Baas P, Bell C, Mancini L, Lee MN, Conant RT, Wallenstein MD. Phosphorus mobilizing consortium Mammoth PTM enhances plant growth. PeerJ 2016; 4: e2121, doi:10.7717/peerj.2121.
Timm CM, Pelletier DA, Jawdy SS, Gunter LE, Henning JA, Engle N, et al. Two poplar-associated bacterial isolates induce additive favorable responses in a constructed plant-microbiome system. Front Plant Sci 2016; 7: 497, doi:10.3389/fpls.2016.00497.
Loján P, Demortier M, Velivelli SL, Pfeiffer S, Suárez JP, De Vos P, et al. Impact of plant growth‐promoting rhizobacteria on root colonization potential and life cycle of Rhizophagus irregularis following co‐entrapment into alginate beads. J Appl Microbiol 2017; 122: 429–440, doi:10.1111/jam.13355.
Frey-Klett P, Garbaye J, Tarkka M. The mycorrhiza helper bacteria revisited. New Phytol 2007; 176: 22–36, doi:10.1111/j.1469-8137.2007.02191.x.
Rojas-Solís D, Zetter-Salmón E, Contreras-Pérez M, del Carmen Rocha-Granados M, Macías-Rodríguez L, Santoyo G. Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 endophytes produce antifungal volatile organic compounds and exhibit additive plant growth-promoting effects. Biocatal Agric Biotechnol 2018; 13: 46–52, doi:10.1016/j.bcab.2017.11.007.
Köhl J, Postma J, Nicot P, Ruocco M, Blum B. Stepwise screening of microorganisms for commercial use in biological control of plant-pathogenic fungi and bacteria. Biol Control 2011; 57: 1–12, doi:10.3390/agronomy3040794.
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol. 2013; 11(11): 789-99, doi: 10.1038/nrmicro3109.
French E, Kaplan I, Iyer-Pascuzzi A, Nakatsu CH, Enders. Emerging strategies for precision microbiome management in diverse agroecosystems. Nat. Plants 2021; 7(3): 256-267, doi: 10.1038/s41477-020-00830-9.
Compant S, Clement C, Sessitsch A. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 2010; 42(5): 669-678, doi: 10.1016/j.soilbio.2009.11.024.
Gianinazzi S, Gollotte A, Binet M-N, Van Tuinen T, Redecker D, Wipf D. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 2010; 20: 519-530, doi: 10.1007/s00572-010-0333-3.
Bhattacharyya PN, Jha DK. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J. Microbiol. Biotechnol. 2012; 28: 1327–1350, doi: 10.1007/s11274-011-0979-9.
Ahmad M, Pataczek L, Hilger TH, Zahir ZA, Hussain A, Rasche F, et al. Perspectives of microbial inoculation for sustainable development and environmental management. Front. Microbiol. 2018; 9: 2992, doi: 10.3389/fmicb.2018.02992.
Alori ET, Glick BR, Babalola OO. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front. Microbiol. 2017; 8: 971, doi: 10.3389/fmicb.2017.00971.
Smith SE, Read D. Mycorrhizal Symbiosis, 3rd ed. Elsevier Ltd 2008; pp. 1-787, doi: 10.1016/B978-0-12-370526-6.X5001-6.
De Bruijn FJ. Biological Nitrogen Fixation, Wiley Blackwell, Hoboken, NJ 2015; pp. 1-1196, doi: 10.1002/9781119053095.
Barber NA, Gordon NLS. How do belowground organisms influence plant–pollinator interactions? J Plant Ecol 2015; 8(1): 1-11, doi: 10.1093/jpe/rtu012.
Cesa-Luna C, Baez A, Quintero-Hernandez V, de la Cruz-Enriquez J, Castaneda-Antonio MD, Munoz-Rojas J. The importance of antimicrobial compounds produced by beneficial bacteria on the biocontrol of phytopathogens. Acta Biol Colombiana 2020; 25(1): 140-145, doi: 10.15446/abc.v25n1.76867.
Veliz EA, Martinez-Hidalgo P, Hirsch AM. Chitinase-producing bacteria and their role in biocontrol. AIMS Microbiol 2017; 3(3): 689-705, doi: 10.3934/microbiol.2017.3.689.
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM. Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 2014; 52: 347–75, doi: 10.1146/annurev-phyto-082712-102340.
Fuchs B, Krischke M, Mueller MJ, Krauss J. Herbivore-specific induction of defence metabolites in a grass-endophyte association. Funct Ecol 2017; 31(2): 318-324, doi: 10.1111/1365-2435.12755.
Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ. Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 2012; 38(6): 651-664, doi: 10.1007/s10886-012-0134-6.
Lacey LA, Grzywacz D, Shaprio-Ilan DI, Frutos R, Brownbridge M, Goettel MS. Insect pathogens as biological control agents: Back to the future. J Invertebr Pathol 2015; 132: 1-41, doi:10.1016/j.jip.2015.07.009.
Jaber LR, Ownley BH. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 2018; 116: 36-45, doi: 10.1016/j.biocontrol.2017.01.018.
Cachapa JC, Meyling NV, Burow M, Hauser TP. Induction and priming of plant defense by root-associated insect-pathogenic fungi. J Chem Ecol 2021; 47(1): 112-122, doi: 10.1007/s10886-020-01234-x.
Rasmann S, Bennett A, Biere A, Karley A, Guerrieri E. Root symbionts: Powerful drivers of plant above- and belowground indirect defenses. Insect Sci 2018; 24(6): 947-960, doi: 10.1111/1744-7917.12464.
Bhattacharyya C, Bakshi U, Mallick I, Mukherji S, Bera B, Ghosh A. Genome-guided insights into the plant growth promotion capabilities of the physiologically versatile Bacillus aryabhattai strain AB211. Front Microbiol 2017; 21(8): 411, doi: 10.3389/fmicb.2017.00411.
Shah F, Rineau F, Canbäck B, Johansson T, Tunlid A. The molecular components of the extracellular protein-degradation pathways of the ectomycorrhizal fungus Paxillus involutus. New Phytol 2013; 200(3): 875-887, doi: 10.1111/nph.12425.
Pinzari F, Jungblut AD, Cuadros. Fungal taste for minerals: the ectomycorrhizal fungus Paxillus involutus triggers specific genes when extracting potassium from different silicates. bioRxiv 2021; doi: 10.1101/2021.03.05.434133.
Nadeem SM, Ahmadb M, Zahir ZA, Javaid A, Ashraf M. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 2014; 32: 429-448, doi:10.1016/j.biotechadv.2013.12.005.
Aguilar-Paredes A, Valdes G, Nuti M. Ecosystem functions of microbial consortia in sustainable agriculture. Agronomy 2020; 10(12): 1902, doi: 10.3390/agronomy10121902.
Lareen A, Burton F, Schäfer P. Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 2016; 90(6): 575-87, doi: 10.1007/s11103-015-0417-8.
Meena KK, Mesapogu S, Kumar M, Yandigeri MS, Singh G, Saxena AK. Co-inoculation of the endophytic fungus Piriformospora indica with the phosphate solubilizing bacterium Pseudomonas striata affects population dynamics and plant growth in chickpea. Biol Fertil Soils 2010; 46:169–174, doi:10.1007/s11104-013-1956-x.
Bashan Y, de-Bashan LE, Prabhu SR, Hernandez JP. Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998-2013). Plant Soil, 2014; 378: 1-33, doi:10.1007/s11104-013-1956-x.
Vassilev N, Vassileva M, Martos V, Garcia Del Moral LF, Kowalska J, Tylkowski B, et al. Formulation of microbial inoculants by encapsulation in natural polysaccharides: Focus on beneficial properties of carrier additives and derivates. Frontiers in Plant Science, 2020; 11: 270, doi: 10.3389/fpls.2020.00270.
Vassileva M, Flor-Peregrin E, Malusá E, Vassilev N. Towards better understanding of the interactions and efficient application of plant beneficial prebiotics, probiotics, postbiotics and synbiotics. Front Plant Sci 2020; 11: 1068, doi: 10.3389/fpls.2020.01068.
Cordovez V, Dini-Andreote F, Carrión VJ, Raaijmakers JM. Ecology and Evolution of Plant microbiomes. Annu Rev Microbiol 2019; 8: 69-88, doi:10.1146/annurev-micro-090817-062524.
Song C, Jin K, Raaijmakers JM. Designing a home for beneficial plant microbiomes. Curr Opin Plant Biol 2021; 5: 62:102025, doi:10.1016/j.pbi.2021.102025.
Berg G, Müller. BFC technology to formulate microbes/consortia. PCT/EP2018/075760, 2018.
Vassileva M, Malusà E, Sas-Paszt L, Trzcinski P, Galvez A, Flor-Peregrin E, et al. Fermentation Strategies to Improve Soil Bio-Inoculant Production and Quality. Microorganisms 2021; 9: 1254, doi:10.3390/microorganisms9061254.
Vassilev N, de Oliveira Mendes G. Solid-State Fermentation and plant-beneficial microorganisms," in Current Developments in Biotechnology and Bioengineering - Current advances in Solid-State Fermentation, eds Pandey A, Larroche C, Soccol CR. (Elsevier), 2018; pp. 435-450, doi:10.3390/microorganisms9061254.
Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 2011; 332(6033): 1097-1100, doi: 10.1126/science.1203980.
Ben Rebah F, Prevost D, Yezza A, Tyagi RD. Agro-indusrial waste materials and wastewater sludge for rhizobial inoculant production: A review. Biores Technol 2007; 98: 3535-3546, doi:10.3390/microorganisms9061254.
Vassilev N, Vassileva M, Lopez A, Martos V, Reyes A, Maksimovic I, et al. Unexploited potential of some biotechnological techniques for biofertilizer production and formulation. Appl Microbiol Biotechnol 2015; 99: 4983-4996, doi:10.1007/s00253-015-6656-4.
Lu KH, Jin Q, Lin YB, Lu WW, Li SS, Zhou CH, et al. Cell-free Fermentation Broth of Bacillus velezensis Strain S3-1 Improves Pak Choi Nutritional Quality and Changes the Bacterial Community Structure of the Rhizosphere Soil. Front Microbiol 2020; 11: 2043, doi: 10.3389/fmicb.2020.02043.
Ijdo M, Cranenbrouck S, Declerck S. Methods for large-scale production of AM fungi: past, present and future. Mycorrhiza 2011; 21: 1-16, doi:10.1007/s00572-010-0337-z.
Jarstfer AG, Sylvia DM. Aeroponic culture of VAM fungi. In: Mycorrhiza: structure, function, molecular biology and biotechnology, Varma A, Hock B (eds). Springer-Verlag: Berlin, 1994; 427–441, doi:10.1007/978-3-662-03779-9.
Feldmann F, Grotkass C. Directed inoculum production— Shall we be able to design populations of arbuscular mycorrhizal fungi to achieve predictable symbiotic effectiveness? In: Mycorrhizal technology in agriculture: from genes to bioproducts, Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds). 2002; Birkhäuser Verlag: Basel; 223–233, doi: 10.1007/978-3-0348-8117-3.
Declerck S, Strullu DG, Plenchette C. In vitro mass-production of the arbuscular mycorrhizal fungus, Glomus versiforme, associated with Ri T-DNA transformed carrot roots. Mycol Res 1996; 100: 1237-1242, doi:10.1016/S0953-7562(96)80186-9.
Rosikiewicz P, Bonvin J, Sanders IR. Cost-efficient production of in vitro Rhizophagus irregularis. Mycorrhiza 2017; 27: 477–486, doi:10.1007/s00572-017-0763-2.
Canfora L, Abu-Samra N, Tartanus M, Łabanowska BH, Benedetti A, Pinzari F, et al. Co-inoculum of Beauveria brongniartii and B. bassiana shows in vitro different metabolic behaviour in comparison to single inoculums. Sci Rep 2017; 7: 1–15, doi:10.1038/s41598-017-12700-0.
Inglis GD, Johnson DL, Chen, KJ, Goettel MS. Use of pathogen combinations to overcome the constraints of temperature on entomopathogenic hyphomycetes against grasshoppers. Biol Control 1997; 8: 143–152, doi:10.1006/bcon.1996.0495.
Kaminsky LM, Trexler RV, Malik RJ, Hockett KL, Bell TH. The inherent conflicts in developing soil microbial inoculants. Trends Biotechnol 2019; 37(2): 140-151, doi:10.1016/j.tibtech.2018.11.011.
Malusá E, Sas-Paszt L, Ciesielska J. Technologies for beneficial microorganisms inocula used as biofertilizers. The Sci World J Vol. 2012, doi:10.1100/2012/491206.
Razinger J, Praprotnik E, Schroers HJ. Bioaugmentation of entomopathogenic fungi for sustainable Agriotes larvae (wireworms) management in maize. Front Plant Sci 2020; 11: 535005, doi: 10.3389/fpls.2020.535005.
Kowalska J, Tyburski J, Matysiak K, Tylkowski B, Malusá E. Field Exploitation of Multiple Functions of Beneficial Microorganisms for Plant Nutrition and Protection: Real Possibility or Just a Hope? Front Microbiol 2020; 11: 1904, doi: 10.3389/fmicb.2020.01904.
Regulation EC. 1107/2009. Regulation (EC) 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market. Offi J Eur Union 2009; 309: 1–50.
Lopes R, Tsui S, Gonçalves P, de Queiroz MV. A look into a multifunctional toolbox: endophytic Bacillus species provide broad and underexploited benefits for plants. World J Microbiol Biotechnol 2018; 34: 94, doi:10.1007/s11274-018-2479-7.
Chandler D, Bailey AS, Tatchell GM, Davidson G, Greaves J, Grant WP. The development, regulation and use of biopesticides for integrated pest management. Philos Trans R Soc Lond Ser 2011; B366: 1987–1998, doi: 10.1098/rstb.2010.0390.
Keswani C, Dilnashin H, Birla H, and Singh SP. Re-addressing the commercialization and regulatory hurdles for biopesticides in India. Rhizosphere 2019; 11: 100155, doi: 10.1016/j.rhisph.2019.100155.
Regulation EU. 2019/1009. Regulation (EU) 2019/1009 of the European Parliament and of the Council of 5 June 2019 laying down rules on the making available on the market of EU fertilising products and amending Regulations (EC) No 1069/2009 and (EC) No 1107/2009 and repealing Regulation (EC) No 2003/2003. Offi J Eur Union 2019; 62: 1–114.
Deising HB, Gase I, Kubo Y. The unpredictable risk imposed by microbial secondary metabolites: how safe is biological control of plant diseases? J Plant Dis Prot 2018; 124: 413-419, doi:10.1007/s41348-017-0109-5.
Raimi A, Roopnarain A, Chirima GJ, Adeleke R. Insights into the microbial composition and potential efficiency of selected commercial biofertilisers. Helyon 2020; 6: E04342, doi:10.1016/j.heliyon.2020.e04342.
Berg G, Eberl L, Hartmann A. The rhizosphere as a reservoir for oportunistic human pathogenic bacteria. Environ Microbiol 2005; 7: 1673-1685, doi:10.1111/j.1462-2920.2005.00891.x.
Manfredini A, Malusà E, Costa C, Pallottino F, Mocali S, Pinzari F, et al. Current methods, common practices and perspectives in tracking and monitoring bioinoculants in soil. Front Microbiol 2021; 12, doi: 10.3389/fmicb.2021.698491.
Mawarda PC, Le Roux X, van Elsas DJ, Salles JF. Deliberate introduction of invisible invaders: A critical appraisal of the impact of microbial inoculants on soil microbial communities. Soil Biol Biochem 2020; 148: 107874, doi:10.1016/j.soilbio.2020.107874.
Tartanus M, Furmanczyk EM, Canfora L, Pinzari F, Tkaczuk C, Majchrowska-Safaryan A, et al. Biocontrol of Melolontha spp. Grubs in Organic Strawberry Plantations by Entomopathogenic Fungi as Affected by Environmental and Metabolic Factors and the Interaction with Soil Microbial Biodiversity. Insects 2021; 12(2): 127, doi:10.3390/insects12020127.
Adesemoye AO, Torbert HA, Kloepper JW. Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient anagement system. Can J Microbiol 2008; 54: 876–86, doi:10.1139/W08-081.
Kowalska J, Tyburski J, Matysiak K, Tylkowski B, Malusá E. Field exploitation of multiple functions of beneficial microorganisms for plant nutrition and protection: real possibility or just a hope? Front Microbiol 2020; 11: 1904, doi:10.3389/fmicb.2020.01904.
Herbst M, Razinger J, Ugrinović K, Škof M, Schroers HJJ, Hommes M, et al. Evaluation of low risk methods for managing Delia radicum, cabbage root fly, in broccoli production. Crop Prot 2017; 96: 273–280, doi:10.1016/j.cropro.2017.02.023.
Rasool S, Vidkjær NH, Hooshmand K, Jensen B, Fomsgaard IS, Meyling NV. Seed inoculations with entomopathogenic fungi affect aphid populations coinciding with modulation of plant secondary metabolite profiles across plant families. New Phytol 2021; 229(3): 1715-1727, doi:10.1111/nph.16979.
Susič N, Žibrat U, Sinkovič L, Vončina A, Razinger J, Knapič M, et al. From genome to field—observation of the multimodal nematicidal and plant growth-promoting effects of Bacillus firmus I-1582 on tomatoes using hyperspectral remote sensing. Plants 2020; 9(5): 592, doi:10.3390/plants9050592.
Kabaluk JT, Ericsson JD. Environmental and Behavioral Constraints on the Infection of Wireworms by Metarhizium anisopliae. Environ Entomol 2007; 36: 1415–1420, doi:10.1603/0046-225X(2007)36[1415:EABCOT]2.0.CO;2.
Meyling NV, Pell JK. Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol Entomol 2006; 31: 162–171, doi:10.1111/j.0307-6946.2006.00781.x.
Hohmann P, Schlaeppi K, Sessitsch A. miCROPe 2019 – emerging research priorities towards microbe-assisted crop production. FEMS Microbiol Ecol 2019; 96(10): fiaa177, doi: 10.1093/femsec/fiaa177.
Díaz ASL, Macheda D, Saha H, Ploll U, Orine D, Biere A. Tackling the context-dependency of microbial-induced resistance. Agronomy 2021; 11: 1293, doi:10.3390/agronomy11071293.
Tyc O, van den Berg M, Gerards S, van Veen JA, Raaijmakers JM, de Boer W, et al. Impact of interspecific interactions on antimicrobial activity among soil bacteria. Front Microbiol 2014; 5: 567, doi: 10.3389/fmicb.2014.00567.
Robert-Seilaniantz A, Grant M, Jones JDG. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 2011; 49: 317-43, doi: 10.1146/annurev-phyto-073009-114447.
Pozo MJ, Lopez-Raez JA, Azcon-Aguilar C, Garcia-Garrido JM. Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 2015; 205(4): 1431-1436, doi: 10.1111/nph.13252.
Xu X, Jeger M. More Ecological Research Needed for Effective Biocontrol of Plant Pathogens, in: Al., A.D.C. et (Ed.), Progress in Biological Control, 2020; 21: How Research Can Stimulate the Development of Commercial Biological Control Against Plant Diseases. Springer, doi:10.1007/978-3-030-53238-3_2.
Razinger J, Žerjav M, Zemljič-Urbančič M, Modic Š, Lutz M, Schroers HJ, et al. Comparison of cauliflower–insect–fungus interactions and pesticides for cabbage root fly control. Insect Sci 2017; 24: 1057–1064, doi:10.1111/1744-7917.12534.
Mazzola M, Manici LM. Apple replant disease: role of microbial ecology in cause and control. Annu Rev Phytopathol 2012; 50: 45–65, , doi:10.1146/annurev-phyto-081211-173005.
Deakin G, Fernández-Fernández F, Bennett J, Passey T, Harrison N, Tilston ELEL, et al. The effect of rotating apple rootstock genotypes on apple replant disease and rhizosphere microbiome. Phytobiomes J 2019; 3: 273–285, doi:10.1094/PBIOMES-03-19-0018-R.
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.