Abstract
Plant-associated microorganisms fulfill important functions for plant growth and health. Direct plant growth promotion by microbes is based on improved nutrient acquisition and hormonal stimulation. Diverse mechanisms are involved in the suppression of plant pathogens, which is often indirectly connected with plant growth. Whereas members of the bacterial genera Azospirillum and Rhizobium are well-studied examples for plant growth promotion, Bacillus, Pseudomonas, Serratia, Stenotrophomonas, and Streptomyces and the fungal genera Ampelomyces, Coniothyrium, and Trichoderma are model organisms to demonstrate influence on plant health. Based on these beneficial plant–microbe interactions, it is possible to develop microbial inoculants for use in agricultural biotechnology. Dependent on their mode of action and effects, these products can be used as biofertilizers, plant strengtheners, phytostimulators, and biopesticides. There is a strong growing market for microbial inoculants worldwide with an annual growth rate of approximately 10%. The use of genomic technologies leads to products with more predictable and consistent effects. The future success of the biological control industry will benefit from interdisciplinary research, e.g., on mass production, formulation, interactions, and signaling with the environment, as well as on innovative business management, product marketing, and education. Altogether, the use of microorganisms and the exploitation of beneficial plant–microbe interactions offer promising and environmentally friendly strategies for conventional and organic agriculture worldwide.
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References
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:234–266
Banerjee M, Yesmin L (2002) Sulfur-oxidizing plant growth promoting Rhizobacteria for enhanced canola performance. US Patent
Bauer WD, Mathesius U (2004) Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol 7:429–433
Bhattacharjee RB, Sing A, Mukhopadyay SN (2008) Use of nitrogen-fixing bacteria as biofertilizer for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209
Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K (2002) Plant-dependent genotypic and phenotypic diversity of antagonistic Rhizobacteria isolated from different Verticillium host plants. Appl Environ Microbiol 68:3328–3338
Berg G, Eberl L, Hartmann A (2005a) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 71:4203–4213
Berg G, Krechel A, Ditz M, Faupel A, Ulrich A, Hallmann J (2005b) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51:215–229
Berg G, Opelt K, Zachow C, Lottmann J, Götz M, Costa R, Smalla K (2006) The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol Ecol 56:250–261
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13
Bolckmans K (2008) Biocontrol files. Can Bull Ecol Pest Manag 13:1–10
Cassán F, García Salamone I (eds) (2008) Azospirillum sp: cell physiology, plant response, agronomic and environmental research in Argentina. Asociación Argentina de Microbiología, Buenos Aires
Castro-Sowinski S, Herschkovitz Y, Okon Y, Jurkevitch E (2007) Effects of inoculation with plant growth-promoting Rhizobacteria on resident rhizosphere microorganisms. FEMS Microbiol Lett 276:1–11
Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant growth-promoting Rhizobacteria to promote soybean growth. Soil Sci Soc Am J 63:1670–1680
Chet I, Chernin L (2002) Biocontrol, microbial agents in soil. In: Bitton G (ed) Encyclopedia of environmental microbiology. Willey, New York, pp 450–465
Choi O, Kim J, Kim J, Jeong Y, Moon J, Seuk Park C, Hwang I (2008) Pyrroloquinoline quinone is a plant growth promotion factor produced by Pseudomonas fluorescens B16. Plant Physiol 146:657–668
Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959
Conn KL, Lazarovits G (2000) Soil factors influencing the efficacy of liquid swine manure added to soil to kill Verticillium dahliae. Can J Plant Pathol 21:400–406
Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7:210–216
Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592
Danhorn T, Fuqua C (2004) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–22
De Vleeschauwer D, Höfte M (2007) Using Serratia plymuthica to control fungal pathogens of plant. CAB Reviews 2:46
De Werra P, Péchy-Tarr M, Keel C, Maurhofer M (2009) Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0. Appl Environ Microbiol 75:4162–4174
Dobbelare S, Vanderleydern J, Okon Y (2003) Plant-growth promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149
Dobbelaere S, Okon Y (2007) The plant growth promoting effects and plant responses. In: Elmerich C, Newton WE (eds) Nitrogen fixation: origins, applications and research progress. Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations, vol V. Heidelberg, Springer, pp 145–170
Egamberdieva D, Kamilova F, Validov S, Gafurova L, Kucharova Z, Lugtenberg B (2008) High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environ Microbiol 10:1–9
Ehlers RU (2006) Einsatz der Biotechnologie im biologischen Pflanzenschutz. Schr.reihe Dtsch Phytomed Ges 8:17–31
Emmert EAB, Handelsman J (1999) Biocontrol of plant disease: a (gram+) positive perspective. FEMS Microbiol Lett 171:1–9
Fürnkranz M, Müller H, Berg G (2009) Characterization of plant growth promoting bacteria from crops in Bolivia. Journal of Plant Diseases and Protection, in press
Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 252:1–7
Gunnell D, Eddleston M, Phillips MR, Konradsen F (2007) The global distribution of fatal pesticide self-poisoning: systematic review. BMC Public Health 21(7):357
Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319
Hallmann J, Rodríguez-Kábana R, Kloepper JW (1999) Chitin-mediated changes in bacterial communities of the soil, rhizosphere and within roots of cotton in relation to nematode control. Soil Biol Biochem 31:551–560
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56
Hartmann A, Gantner S, Schuhegger R, Steidle A, Dürr C, Schmid M, Langebartels C, Dazzo FB, Eberl L (2004) N-acyl homoserine lactones of rhizosphere bacteria trigger systemic resistance in tomato plants. In: Lugtenberg B, Tikhonovich I, Provorov N (eds) Biology of molecular plant–microbe interactions, vol 4. APS, St. Paul, pp 554–556
Jacobsen BJ, Zidack NK, Larson BJ (2004) The role of Bacillus-based biological control agents in integrated pest management systems: plant diseases. Phytopathology 94:1272–1275
Jäderlund L, Hellman M, Sundh I, Bailey MJ, Jansson JK (2008) Use of a novel nonantibiotic triple marker gene cassette to monitor high survival of Pseudomonas fluorescens SBW25 on winter wheat in the field. FEMS Microbiol Ecol 63:156–168
Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B (2005) Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7:1809–1817
Kamilova F, Kravchenko LV, Shaposhnikov AI, Makarova N, Lugtenberg B (2006) Effects of the tomato pathogen Fusarium oxysporum f. sp. radicis-lycopersici and of the biocontrol bacterium Pseudomonas fluorescens WCS365 on the composition of organic acids and sugars in tomato root exudate. Mol Plant Microbe Interact 19:1121–1126
Katiyar V, Goel R (2004) Siderophore mediated plant growth promotion at low temperature by mutant of fluorescent pseudomonad. Plant Growth Regul 42:239–244
Leach AW, Mumford JD (2008) Pesticide environmental accounting: a method for assessing the external costs of individual pesticide applications. Environ Pollut 151:139–47
Long SR (2001) Genes and signals in Rhizobium–legume symbiosis. Plant Physiol 125:69–72
Loper JE, Kobayashi DY, Paulsen IT (2007) The genomic sequence of Pseudomonas fluorescens Pf-5: insights into biological control. Phytopathology 97:233–238
Lugtenberg BJJ, Chin-A-Woeng TFC, Bloemberg GV (2002) Microbe–plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383
McSpadden Gardener BB, Fravel D (2002) Biological control of plant pathogens: research, commercialization, and application in the USA. Plant Health Progr. doi:10.1094/PHP-2002-0510-01-RV
Miller SA, Beed FD, Harmon CL (2009) Plant disease diagnostic capabilities and networks. Annu Rev Phytopathol, in press
Morrissey JP, Dow JM, Mark L, O’Gara F (2004) Are microbes at the root of a solution to world food production? EMBO Rep 5:922–926
Müller H, Westendorf C, Leitner E, Chernin L, Riedel K, Schmidt S, Eberl L, Berg G (2009) Quorum-sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. FEMS Microbiol Ecol 67:468–467
Okon Y (1994) Azospirillum/plant associations. CRC, Boca Raton, p 175
Opelt K, Berg C, Berg G (2007) The bryophyte genus Sphagnum is a reservoir for powerful and extraordinary antagonists and potentially facultative human pathogens. FEMS Microbiol Ecol 61:38–53
Parke JL, Gurian-Sherman D (2001) Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 39:225–258
Parniske M, Fischer HM, Hennecke H, Werner D (1991) Accumulation of the phytoalexine glycollein I in soybean nodules infected by Bradyrhizobium japonicum nifA mutant. Z Naturforsch 46:318–320
Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teubner LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894
Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ (2006) The Janus factor of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183
Raaijmakers JM, de Bruijn I, de Kock MJ (2006) Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol Plant Microbe Interact 19:699–710
Rahme LG, StevensEJ WSF, Shao J, Tompkins RG, Ausubel FM (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268:1899–1902
Ribbeck-Busch K, Roder A, Hasse D, de Boer W, Martínez JL, Hagemann M, Berg G (2005) A molecular biological protocol to distinguish potentially human pathogenic Stenotrophomonas maltophilia from plant-associated Stenotrophomonas rhizophila. Environ Microbiol 7:1853–1858
Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9
Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, Berg G, van der Lelie D, Dow JM (2009) Versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Microbiol Rev 7:514–525
Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting Rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotech 34:635–648
Scherwinski K, Grosch R, Berg G (2008) Effect of bacterial antagonists on lettuce: active biocontrol of Rhizoctonia solani and negligible, short-term effect on non-target microbes. FEMS Microbiol Ecol 64:106–116
Schrey SD, Tarkka MT (2008) Friends and foes: streptomycetes as modulators of plant disease and symbiosis. Antonie Van Leeuwenhoek 94:11–19
Smith KP, Handelsman J, Godman RM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc Natl Acad Sci U S A 9:4786–4790
Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448
Thakore Y (2006) The biopesticide market for global agricultural use. Ind Biotechnol 2:194–208
Unno Y, Okubo K, Wasaki J, Shinano T, Osaki M (2005) Plant growth promotion abilities and microscale bacterial dynamics in the rhizosphere of lupin analysed by phytate utilization ability. Environ Microbiol 7:396–404
Van Loon LC (2007) Plant responses to plant growth promoting bacteria. Eur J Plant Pathol 119:243–254
Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81:357–364
Weller DM, Raaijmakers JM, Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348
Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256
Whipps J (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511
Winding A, Binnerup SJ, Pritchard H (2004) Non-target effects of bacterial biological control agents suppressing root pathogenic fungi. FEMS Microbiol Ecol 47:129–141
Zabetakis I (1997) Enhancement of flavour biosynthesis from strawberry (Fragaria x ananassa) callus cultures by Methylobacterium species. Plant Cell Tiss Organ Cult 50:179–183
Zachow C, Berg C, Müller H, Meincke R, Komon-Zelazowska M, Druzhinina IS, Kubicek CP, Berg G (2009a) Fungal diversity in the rhizosphere of endemic plant species of Tenerife (Canary Islands): relationship to vegetation zones and environmental factors. ISME J 3:79–92
Zachow C, Pirker H, Westendorf C, Tilcher R, Berg G (2009b) Caenorhabditis elegans provides a valuable tool to evaluate the human pathogenic potential of bacterial biocontrol agents. Eur J Plant Pathol, in press
Acknowledgement
I would like to thank my coworkers in biocontrol research projects for the fruitful discussions especially in our platform “Arbeitskreis für Biologische Bekämpfung von Pflanzenkrankheiten” of the Deutsche Phytomedizinische Gesellschaft. The research was funded by the Deutsche Forschungsgemeinschaft, by the Federal Ministry of Consumer Protection, Food and Agriculture (Germany), and by the Austrian Science Foundation FWF (Austria).
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Berg, G. Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84, 11–18 (2009). https://doi.org/10.1007/s00253-009-2092-7
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DOI: https://doi.org/10.1007/s00253-009-2092-7