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Plant Growth-Promoting Bacteria: Fundamentals and Exploitation

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Bacteria in Agrobiology: Crop Ecosystems

Abstract

Many plant-beneficial rhizobacteria have been described in the literature. These have been isolated from the plant root, where they usually live under conditions of nutrient starvation and at a low pH. In order to be beneficial, they usually need to colonize the root efficiently. Moreover, they have to multiply fast in order to be competitive with other organisms. To this end, traits such as chemotaxis to, and fast utilization of, the nutrients secreted by the root are required. These nutrients mainly consist of organic acids and sugars. Some plant-beneficial bacteria promote plant growth directly, e.g., by making nutrients available to the plant or by stimulating the growth of plants by production of hormones. Other plant-beneficial bacteria stimulate plant growth indirectly, e.g., by degrading environmental pollutants which inhibit plant growth or by controlling the growth of pathogens.

Commercialization of microbes is a complex and long-lasting process. Firstly, industry must see opportunities for making a profit. Secondly, the bacterium as well as the final product must be efficient and safe with respect to humans, animals, as well as nontarget organisms. Fast up scaled production of the organism against a reasonable price is another important prerequisite. Finally, the microbe must be formulated and packed in a form that is stable for many months and which is consistent with agricultural practice.

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References

  • /414/EEC: Council Directive of 15 July 1991 concerning the placing of plant protection products on the market. Official Journal L 230, 19/08/1991, 0001–0032

    Google Scholar 

  • /36/EC: Commission Directive of 16 May 2001 amending Council Directive 91/414/EEC concerning the placing of plant protection products on the market. Official Journal L 164, 20/06/2001, 0001–0038

    Google Scholar 

  • /25/EC: Commission Directive of 14 March 2005 amending Annex VI to Directive 91/414/EEC as regards plant protection products containing microorganisms Official Journal L 90, 08/04/2005, 0001–0034

    Google Scholar 

  • Achouak W, Conrod S, Cohen V, Heulin T (2004) Phenotypic variation of Pseudomonas brassicacearum as a plant root-colonisation strategy. Mol Plant Microbe Interact 17:872–879

    PubMed  CAS  Google Scholar 

  • Adesina MF, Grosch R, Lembke A, Vatchev TD, Smalla K (2009) In vitro antagonists of Rhizoctonia solani tested on lettuce: rhizosphere competence, biocontrol efficiency and rhizosphere microbial community response. FEMS Microbiol Ecol 69:62–74

    PubMed  CAS  Google Scholar 

  • Ahn SJ, Yang CH, Cooksey DA (2007) Pseudomonas putida 06909 genes expressed during colonization on mycelia surfaces and phenotypic characterization of mutants. J Appl Microbiol 103:120–132

    PubMed  CAS  Google Scholar 

  • Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: the European situations. Eur J Plant Pathol 114:329–341

    Google Scholar 

  • Andersen JB, Koch B, Nielsen TH, Sorensen D, Hanse M (2003) Surface motility in Pseudomonas sp. DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum. Microbiology 149:37–46

    PubMed  CAS  Google Scholar 

  • Anonymous (1998) Sichere Biotechnologie. Eingruppierung biologischer Agenzien: Bacterien, BG Chemie, Merkblatt B 006 8/98 ZH 1/346. Jedermann-Verlag, Dr. Otto Pfeffer oHG, Heidelberg, Germany

    Google Scholar 

  • Autret N, Charbit A (2005) Lessons from signature tagged mutagenesis on the infectious mechanisms of pathogenic bacteria. FEMS Microbiol Rev 29:703–717

    PubMed  CAS  Google Scholar 

  • Bakker PAHM, Ran LX, Pieterse CMJ, Van Loon LC (2003) Understanding the involvement of rhizobacteria-mediated induction of systemic resistance in biocontrol of plant disease. Can J Plant Pathol 25:5–9

    Google Scholar 

  • Barea JM, Navarra E, Montoya E (1976) Production of plant-growth regulators by rhizosphere phosphate solubilizing bacteria. J Appl Bacteriol 40:129–134

    PubMed  CAS  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    CAS  Google Scholar 

  • Berg G, Eberl L, Hartmann A (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7:1673–1685

    PubMed  CAS  Google Scholar 

  • Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Am Soc Agron 64:1644–1655

    CAS  Google Scholar 

  • Bloemberg GV (2007) Microscopic analysis of plant-bacterium interactions using auto fluorescent proteins. Eur J Plant Pathol 119:301–309

    CAS  Google Scholar 

  • Bloemberg GV, Lugtenberg BJJ (2004) Bacterial biofilms on plants: relevance and phenotypic aspects. In: Ghannoum M, O’Toole GA (eds) Microbial biofilms. ASM Press, Washington DC, pp 141–159

    Google Scholar 

  • Bloemberg GV, O’Toole GA, Lugtenberg BJJ, Kolter R (1997) Green fluorescent protein as a marker for Pseudomonas spp. Appl Environ Microbiol 63:4543–4551

    PubMed  CAS  Google Scholar 

  • Bloemberg GV, Wijfjes AHM, Lamers GEM, Stuurman N, Lugtenberg BJJ (2000) Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. Mol Plant Microbe Interact 13:1170–1176

    PubMed  CAS  Google Scholar 

  • Blumer C, Haas D (2000) Mechanisms, regulation and ecological role of bacterial cyanide byiosynthesis. Arch Microbiol 173:170–177

    PubMed  CAS  Google Scholar 

  • Boiero L, Perrig D, Masciarelli O, Penna C, Cassan F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880

    PubMed  CAS  Google Scholar 

  • Boldt TS, Sorensen J, Karlson U, Molin S, Ramos C (2004) Combined use of different Gfp reporters for monitoring single-cell activities of a genetically modified PCB degrader in the rhizosphere of alfalfa. FEMS Microbiol Ecol 48:139–148

    PubMed  CAS  Google Scholar 

  • Bolwerk A, Lagopodi AL, Wijfjes AHM, Lamers GEM, Chin-A-Woeng TFC, Lugtenberg BJJ, Bloemberg GV (2003) Interactions in the tomato rhizosphere of two Pseudomonas biocontrol strains with the phytopathogenic fungus Fusarium oxysporum f. sp. radicis-lycopersici. Mol Plant Microbe Interact 11:983–993

    Google Scholar 

  • Braun PG, Hildebrand PD, Ells TC, Kobayashi DY (2001) Evidence and characterization of a gene cluster required for the production of viscosin, a lipopeptide biosurfactant, by a strain of Pseudomonas fluorescens. Can J Microbiol 47:294–301

    PubMed  CAS  Google Scholar 

  • Burges HD (1998) Formulation of microbial pesticidas. Kluwer Academic Publisher, Dordrecht, The Netherlands

    Google Scholar 

  • Camacho Carvajal MM (2001) Molecular characterization of the roles of type 4 pili, NDH-I and PyrR in rhizosphere colonization of Pseudomonas fluorescens WCS365. PhD Thesis Univ. Leiden, The Netherlands.

    Google Scholar 

  • Camacho Carvajal MM, Lugtenberg BJJ, Bloemberg GV (2002) Characterization of NADH dehydrogenase of Pseudomonas fluorescens WCS365 and their role in competitive root colonization. Mol Plant Microbe Interact 15:662–671

    PubMed  Google Scholar 

  • Cases I, De Lorenzo V (2005) Genetically modified organisms for the environment: stories of success and failure and what we have learned from them. Int Microbiol 8:213–222

    PubMed  CAS  Google Scholar 

  • Castoria R, Wright SAI (2009) Host responses to biological control agents. In: Prusky D, Gullino ML (eds) Post-harvest pathology, vol 2. Springer, The Netherlands, pp 171–181

    Google Scholar 

  • Cazorla FM, Duckett SB, Bergström ET, Noreen S, Odijk R, Lugtenberg BJJ, Thomas-Oates J, Bloemberg GV (2006) Biocontrol of avocado dematophora root rot by antagonistic Pseudomonas fluorescens PCL1606 correlates with the production of 2-hexyl 5-propyl resorcinol. Mol Plant Microbe Interact 19:418–428

    PubMed  CAS  Google Scholar 

  • Cherry A (2005) Biopesticides, a global perspective. Workshop “Development of biopesticide registration and risk assessments for Ghana” Accra, Ghana, 27-30 June. http://www.fao.org/docs/eims/upload/agrotech/2003/global_perpective.pdf.

  • Chin-A-Woeng TFC, Bloemberg GV, Van der Bij AJ, Van der Drift KMGM, Schripsema J, Kroon B, Scheffer RJ, Keel C, Bakker PAHM, Tichy HV, de Bruijn FJ, Thomas-Oates JE, Lugtenberg BJJ (1998) Biocontrol by phenazine-1-carboxamide-producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicis-lycopersisi. Mol Plant Microbe Interact 11:1069–1077

    CAS  Google Scholar 

  • Chin-A-Woeng TFC, Bloemberg GV, Mulders IHM, Dekkers LC, Lugtenberg BJJ (2000) Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato root rot. Mol Plant Microbe Interact 12:1340–1345

    Google Scholar 

  • Cohen AC, Bottini R, Piccoli PN (2008) Azospirillum brasilense SP245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul 54:97–103

    CAS  Google Scholar 

  • Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18

    PubMed  Google Scholar 

  • Cotter SE, Surana NK, StGeme JW III (2005) Trimeric autotransporters: a distinct subfamily of autotransporter proteins. Trends Microbiol 13:199–205

    PubMed  CAS  Google Scholar 

  • De Bruijn FJ, Hilgert U, Stigter J, Schneider M, Meyer H, Klosse U, Pawlowski K (1990) Regulation of nitrogen fixation and assimilation genes in the free-living versus symbiotic state. In: Gresshoff PM, Roth LE, Stacey G, Newton W (eds) Nitrogen fixation: achievements and objectives. Chapman and Hall, New York and London, pp 33–44

    Google Scholar 

  • De Souza JT, Arnould C, Deulvot C, Lemanceau P, Gianinazzi-Pearson V, Raaijmakers JM (2003) Effect of 2, 4 diacetylphloroglucinol on Pythium: cellular responses and variation in sensitivity among propagules and species. Phytopathology 93:966–975

    PubMed  Google Scholar 

  • De Weert S, Bloemberg G (2007) Rhizosphere competence and the role of root colonisation in biocontrol. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, The Netherlands, pp 317–333

    Google Scholar 

  • De Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, Mot R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe Interact 15:1173–1180

    PubMed  Google Scholar 

  • De Weert S, Kuiper I, Lagendijk EL, Lamers GEM, Lugtenberg BJJ (2004a) Role of chemotaxis towards fusaric acid in colonisation of hyphae of Fusarium oxysporum f. sp. radicis lycopersici by Pseudomonas fluorescens WCS365. Mol Plant Microbe Interact 16:1185–1191

    Google Scholar 

  • De Weert S, Dekkers LC, Kuiper I, Bloemberg GV, Lugtenberg BJJ (2004b) Generation of enhanced competitive root tip colonizing Pseudomonas bacteria through accelerated evolution. J Bacteriol 186:3153–3159

    PubMed  Google Scholar 

  • De Weert S, Dekkers LC, Bitter W, Tuinman S, Wijfjes AHM, van Boxtel R, Lugtenberg BJJ (2006) The two-component colR/S system of Pseudomonas fluorescens WCS365 plays a role in rhizosphere competence through maintaining the structure and function of the outer membrane. FEMS Microbiol Ecol 58:205–213

    PubMed  Google Scholar 

  • De Weert S, Kuiper I, Kamilova F, Mulders IHM, Bloemberg GV, Kravchenko L, Azarova T, Eijkemans K, Preston GM, Rainey P, Tikhonovich I, Wijfjes AHM, Lugtenberg B (2007) The role of competitive root tip colonization in the biological control of tomato foot and root rot. In: Chincolkar SB, Mukerji KG (eds) Biological control of plant diseases. The Haworth Press, Inc New York, London, Oxford, pp 103–122

    Google Scholar 

  • De Weger LA, Van der Vlugt CI, Wijfjes AH, Bakker PA, Schippers B, Lugtenberg BJJ (1987) Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonisation of potato roots. J Bacteriol 169:2769–2773

    PubMed  Google Scholar 

  • De Werra P, Baehler E, Huser A, Keel C, Maurhofer M (2008) Detection of plant-modulated alterations in antifungal gene expression in Pseudomonas fluorescens CHA0 on roots by flow cytometry. Appl Environ Microbiol 74:1339–1349

    PubMed  Google Scholar 

  • Dekkers LC, de Weger LA, Wijffelman CA, Spaink HP, Lugtenberg BJJ (1998) A two-component system plays an important role in the root-colonising ability of Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact 11:45–56

    PubMed  CAS  Google Scholar 

  • Dekkers LC, Mulders CHM, Phoelich CC, Chin-A-Woeng TFC, Wijfjes AHM, Lugtenberg BJJ (2000) The sss colonization gene of the tomato-Fusarium f.sp. radicis-lycopersici biocontrol strain Pseudomonas fluorescens WCS365 can improve root colonization of other wild type Pseudomonas spp. bacteria. Mol Plant Microbe Interact 13:1177–1183

    PubMed  CAS  Google Scholar 

  • Dikin A, Sijam K, Kadir J, Seman IA (2007) Mode of action of antimicrobial substances from Burkholderia multivorans and Microbacterium testaceum against Schizophyllum commune Fr. Int J Agric Biol 9:311–314

    Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, VandeBroek A, VanderLeyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA productions on wheat. Plant Soil 212:155–164

    CAS  Google Scholar 

  • Dong Y-H, Zhang X-F, Xu J-L, Zhang L-H (2004) Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl Environ Microbiol 70:954–960

    PubMed  CAS  Google Scholar 

  • Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333

    PubMed  CAS  Google Scholar 

  • Duffy BK, Défago G (1997) Zinc improves biocontrol of Fusarium crown and root rot of tomato by Pseudomonas fluorescens and represses the production of pathogen metabolites inhibitory to bacterial antibiotic synthesis. Phytopathology 87:1250–1257

    PubMed  CAS  Google Scholar 

  • Duffy B, Défago G (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65:2429–2438

    PubMed  CAS  Google Scholar 

  • Duffy B, Schouten A, Raaijmakers J (2003) Pathogen self-defence: mechanisms to counteract microbial antagonism. Annu Rev Phytopathol 41:501–538

    PubMed  CAS  Google Scholar 

  • Duijff BJ, De Kogel WJ, Bakker PAHM, Schippers B (1994) Influence of pseudobactin 358 on the iron nutrition of barley. Soil Biol Biochem 26:1681–1688

    CAS  Google Scholar 

  • Egamberdieva D, Kuchrova Z, Davranov K, Berg G, Makarova N, Azarova T, Chebotar V, Tikhonovich I, Kamilova F, Validov SZ, Lugtenberg B (2010) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biology and Fertility of Soils 47:197–205

    Google Scholar 

  • 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 in salinated soil in Uzbekistan. Environ Microbiol 10:1–9

    PubMed  CAS  Google Scholar 

  • Egamberdieva D, Berg G, Lindström K, Räsänen LA (2010) Co-inoculation of Pseudomonas spp. with Rhizobium improves growth and symbiotic performance of fodder galega (Galega orientalis Lam.). Eur J Soil Biol 46:269–272

    Google Scholar 

  • Ellenberg J, Lippincott SJ, Presley JF (1999) Dual-colour imaging with GFP variants. Trends Cell Biol 9:52–56

    PubMed  CAS  Google Scholar 

  • Fogliano V, Ballio A, Gallo M, Woo S, Scala F, Lorito M (2002) Pseudomonas lipopeptides and fungal cell wall-degrading enzymes act synergistically in biological control. Mol Plant Microbe Interact 15:323–333

    PubMed  CAS  Google Scholar 

  • Frankenberger WT, Arshad M (1995) Phytohormones in soils. Marcel Dekker, New York

    Google Scholar 

  • Fravel DR (1998) Use of Sporidesmium sclerotivorum for biocontrol of sclerotial plant pathogens. In: Boland GJ, Kuykendall LD (eds) Plant microbe interactions and biological control. Marcel Dekker, New York, pp 37–47

    Google Scholar 

  • Fravel DR, Deahl KL, Stommel JR (2005) Compatibility of the biocontrol fungus Fusarium oxysporum strain CS-20 with selected fungicides. Biol Control 34:165–169

    CAS  Google Scholar 

  • Fujishige NA, Kapadia NN, De Hoff PL, Hirsch AM (2006) Investigations of Rhizobium biofilm formations. FEMS Microbiol Ecol 56:195–206

    PubMed  CAS  Google Scholar 

  • Fulchieri M, Lucangeli C, Bottini R (1993) Inoculation with Azospirillum lipoferum affects growth and gibberellin status of corn seedling roots. Plant Cell Physiol 34:1305–1309

    CAS  Google Scholar 

  • Gaballa A, Abeysinghe PD, Urich G, Matthijs S, De Greve H, Cornelis P, Koedam N (1997) Trehalose induces antagonism towards Pythium debaryanum in Pseudomonas fluorescens ATCC 17400. Appl Environ Microbiol 63:4340–4345

    PubMed  CAS  Google Scholar 

  • Gal M, Preston GM, Massey RC, Spiers AJ, Raineys PB (2003) Genes encoding a cellulosic polymer contribute toward the ecological success of Pseudomonas fluorescens SBW25 on plant surfaces. Mol Ecol 12:3109–3121

    PubMed  CAS  Google Scholar 

  • Garbeva P, van Veen JA, van Elsas JD (2004) Assessment of the diversity, and antagonism towards Rhizoctonia solani AG3, of Pseudomonas species in soil from different agricultural regimes. FEMS Microbiol Ecol 47:51–64

    PubMed  CAS  Google Scholar 

  • García de Salome IE (2000) Direct beneficial effect of cytokinin-producing rhizobacteria on plant growth. PhD thesis. University of Saskatchewan, Saskatoon, Canada

    Google Scholar 

  • García de Salome IE, Nelson LM (2000) Effects of cytokinin-producing Pseudomonas PGPR strains on tobacco callus. Auburn University Web Site. Available http://www.ag.auburn.edu/argentina/pdfmanuscripts/garciadesalome.pdf. Cited 20 Dec 2004

  • García de Salome IE, Hynes RK, Nelson LM (2001) Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can J Microbiol 47:404–411

    Google Scholar 

  • García de Salome IE, Hynes RK, Nelson LM (2006) Role of cytokinins in plant growth promotion by rhizosphere bacteria. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilisation. Springer, Dordrecht, The Netherlands, pp 173–195

    Google Scholar 

  • Germaine K, Liu X, Cabellos G, Hogan J, Ryan D, Dowling DN (2006) Bacterial endophyte-enhanced phyto-remediation of the organochlorine herbicide 2, 4-dichlorophenoxyacetic acid. FEMS Microbiol Ecol 57:302–310

    PubMed  CAS  Google Scholar 

  • Gilbert GS, Handelsman J, Parke JL (1994) Root camouflage by disease control. Phytopathol 84:222–225

    Google Scholar 

  • Gleeson O, O’Gara F, Morrissey JP (2010) The Pseudomonas fluorescens secondary metabolite 2, 4-diacetylphloroglucinol impairs mitochondrial function in Saccharomyces cerevisiae. Antonie Leeuwenhoek 3:261–273

    Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    PubMed  CAS  Google Scholar 

  • Glick BR, Cheng Z, Czarny J, Duan J (2007a) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339

    CAS  Google Scholar 

  • Glick BR, Todorovic B, Czarny J, Cheng ZY, Duan J, McConkey B (2007b) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242

    CAS  Google Scholar 

  • Global Industry Analysts, Inc. (2008) Biopesticides. Report. GIA, USA

    Google Scholar 

  • Götz M, Gomes NCM, Dratwinski A, Costa R, Berg G, Peixoto R, Mendonça-Hagler L, Smalla K (2006) Survival of gfp-tagged antagonistic bacteria in the rhizosphere of tomato plants and their effects on the indigenous bacterial community. FEMS Microbiol Ecol 56:207–218

    PubMed  Google Scholar 

  • Gray KM, Garey JR (2001) The evolution of bacterial LuxI and LuxR quorum sensing regulators. Microbiology 147:2379–2387

    PubMed  CAS  Google Scholar 

  • Gutiérrez Manero FJ, Ramos Solano B, Probanza A, Mehouachi J, Tadeo FR, Talon M (2001) The plant growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plant 111:206–211

    Google Scholar 

  • Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319

    PubMed  CAS  Google Scholar 

  • Haas D, Keel C (2003) Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol 41:117–153

    PubMed  CAS  Google Scholar 

  • Haas D, Blumer C, Keel C (2000) Biocontrol ability of fluorescent Pseudomonas genetically dissected: importance of positive feedback regulation. Curr Opin Biotechnol 11:290–297

    PubMed  CAS  Google Scholar 

  • Hamill JD (1993) Alterations in auxin and cytokinin metabolism of higher plants due to expression of specific genes from pathogenic bacteria. Australian Journal of Plant Physiology 20:405–424

    Google Scholar 

  • Harman GE, Howel CH, Viterbo A, Chet I, Lorito M (2004) Trichoderma species – opportunistic, a virulent plant symbionts. Nat Rev Microbiol 2:43–56

    PubMed  CAS  Google Scholar 

  • Harman GE, Obregon MA, Samuels GJ, Lorito M (2010) Changing models for commercialization and implementation of biocontrol in the developing and the developed world. Plant D 94:928–939

    Google Scholar 

  • Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden DW (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269:400–403

    PubMed  CAS  Google Scholar 

  • Hiltner L (1904) Über neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter bessonderer Berücksichtigung der Gründung und Brache. Arb Dtsch Landwirtsch Ges Berl 98:59–78

    Google Scholar 

  • Hogan DA, Kolter R (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296:2229–2232

    PubMed  CAS  Google Scholar 

  • Hogan DA, Wargo MJ, Beck N (2009) Bacterial biofilms on fungal surfaces. http://www.open-access-biology.com/biofilms/biofilmsch13.pdf

  • Hoopen GM, Krauss U (2006) Biology and control of Rosellinia bunodes, Rosellinia necatrix and Rosellinia pepo: a review. Crop Prot 25:89–107

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg BJJ (2006a) Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Interact 19:250–256

    PubMed  CAS  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Makarova N, Lugtenberg BJJ (2006b) 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

    PubMed  CAS  Google Scholar 

  • Kamilova F, Leveau JHJ, Lugtenberg B (2007) Collimonas fungivorans, an unpredicted in vitro but efficient in vivo biocontrol agent for the suppression of tomato foot and root rot. Environ Microbiol 9:1597–1603

    PubMed  CAS  Google Scholar 

  • Kamilova F, Lamers G, Lugtenberg B (2008) Biocontrol strain Pseudomonas fluorescens WCS365 inhibits germination of Fusarium oxysporum spores in tomato root exudate as well as subsequent formation of new spores. Environ Microbiol 10:2455–2461

    PubMed  Google Scholar 

  • Kang JG, Shin SY, Kim MJ, Bajpai V, Maheshwari DK, Kang SC (2004) Isolation and anti-fungal activities of 2-Hydroxy-methyl-chroman-4-one produced by Burkholderia sp. MSSP. J Antibiot 57(11):726–731

    PubMed  CAS  Google Scholar 

  • Kaur R, Macleod J, Foley W, Nayudu M (2006) Gluconic acid, an antifungal agent produced by Pseudomonas species in biological control of take-all. Phytochemistry 67:595–604

    PubMed  CAS  Google Scholar 

  • Keel E, Voisard C, Berling C, Kahar H, Défago G (1989) Iron sufficiency, a prerequisite for suppression of tobacco root rot by Pseudomonas fluorescens strain CHAO under gnotobiotic conditions. Phytopathology 79:584–589

    Google Scholar 

  • Keel C, Schider U, Maurhofer M, Voisard C, Laville K, Burger U, Wirthner P, Haas D, Défago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHAO: importance of the bacterial secondary metabolite 2, 4-diacetylphloroglucinol. Mol Plant Microbe Interact 5:4–13

    CAS  Google Scholar 

  • Khalid A, Tahir S, Arshad M, Zahir ZA (2004) Relative efficiency of rhizobacteria for auxin biosynthesis in rhizosphere and non-rhizosphere soils. Aust J Soil Res 42:921–926

    CAS  Google Scholar 

  • King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44:301–307

    PubMed  CAS  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885–886

    CAS  Google Scholar 

  • Kravchenko LV, Azarova TS, Makarova NM, Tikhonovich IA (2003) The effect of tryptophan present in plant root exudates on the phytostimulating activity of rhizobacteria. Microbiol 73:156–158

    Google Scholar 

  • Kuiper I, Bloemberg GV, Noreen S, Thomas-Oates JE, Lugtenberg BJJ (2001a) Increased uptake of putrescine in the rhizosphere inhibits competitive root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact 14:1096–1104

    PubMed  CAS  Google Scholar 

  • Kuiper I, Bloemberg GV, Lugtenberg BJJ (2001b) Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol Plant Microbe Interact 14:1197–1205

    PubMed  CAS  Google Scholar 

  • Kuiper I, Kravchenko L, Bloemberg GV, Lugtenberg BJJ (2002) Pseudomonas putida strain PCL1444, selected for efficient root colonization and naphtalene degradation, efficiently utilizes root exudate components. Mol Plant Microbe Interact 15(7):734–741

    PubMed  CAS  Google Scholar 

  • Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact 17:6–15

    PubMed  CAS  Google Scholar 

  • Lagendijk EL, Validov S, Lamers GEM, De Weert S, Bloemberg GV (2010) Genetic tools tagging Gram-negative bacteria with mCherry for visualization in vitro and in natural habitats, biofilm and pathogenicity studies. FEMS Microbiol Lett 305:81–90

    PubMed  CAS  Google Scholar 

  • Lagopodi AL, Ram AFJ, Lamers GE, Punt PJ, Van den Hondel CAMJJ, Lugtenberg BJJ, Bloemberg GV (2002) Novel aspects of tomato root colonization and infection by Fusarium oxysporum f. sp. radicis-lycopersici revealed by Confocal Laser Scanning Microscopic analysis using the green fluorescent protein as a marker. Mol Plant Microbe Interact 15:172–179

    PubMed  CAS  Google Scholar 

  • Lam ST, Ellis DM, Ligon JM (1990) Genetic approaches for studying rhizosphere colonization. Plant Soil 129:11–18

    Google Scholar 

  • Larrainzar E, O’Gara F, Morrissey JP (2005) Applications of autofluorescent proteins for in situ studies in microbial ecology. Annu Rev Microbiol 59:257–277

    PubMed  CAS  Google Scholar 

  • Lavicoli A, Boutet E, Buchala A, Metraux JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact 16:851–858

    Google Scholar 

  • Laville J, Blumer C, Von Schroetter C, Gaia V, Défago G, Keel C, Hass D (1998) Characterization of the hcnABC gene cluster encoding hydrogen cyanide synthase and anaerobic regulation by ARN in the strictly aerobic biocontrol agent Pseudomonas fluorescens CHA0. J Bacteriol 180:3187–3196

    PubMed  CAS  Google Scholar 

  • Lee SW, Cooksey DA (2000) Genes expressed in Pseudomonas putida during colonisation of a plant-pathogenic fungus. Appl Environ Microbiol 66:2764–2772

    PubMed  CAS  Google Scholar 

  • Leong J (1986) Siderophores: their biochemistry and possible role in the biocontrol of plant pathogens. Annu Rev Phytopathol 24:187–209

    CAS  Google Scholar 

  • Leveau JHJ, Preston GM (2008) Bacterial mycophagy: definition and diagnosis of a unique bacterial-fungal interaction. New Phytol 177:859–876

    PubMed  Google Scholar 

  • Lipton DS, Blanchar RW, Belvins DG (1987) Citrate, malate and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiol 85:315–317

    PubMed  CAS  Google Scholar 

  • Loper JE, Buyer JS (1991) Siderophores microbial interactions plant surfaces. Mol Plant Microbe Interact 4:5–13

    CAS  Google Scholar 

  • Loper JE, Lindow SE (1997) Reporter gen systems useful in evaluating in situ gene expression by soil and plant-associated bacteria. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenbach LD, Walter MV (eds) Manual of environmental microbiology. ASM Press, Washington DC, pp 482–492

    Google Scholar 

  • Lottmann J, Heuer H, de Vries J, Mahn A, Dv;ring K, Wackernagel W, Smalla K, Berg G (2000) Establishment of introduced antagonistic bacteria in the rhizosphere of transgenic potatoes and their effect on the bacterial community. FEMS Microbiol Ecol 33:41–49

    PubMed  Google Scholar 

  • Lugtenberg BJJ, Bloemberg GV (2004) Life in the rhizosphere. In: Ramos JL (ed) Pseudomonas, vol 1, Kluwer Academic/Plenum Publishers. New York, USA, pp 403–430

    Google Scholar 

  • Lugtenberg BJJ, Dekkers LC (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ Microbiol 1:9–13

    PubMed  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting-rhizobacteria. Annu Rev Microbiol 63:541–556

    PubMed  CAS  Google Scholar 

  • Lugtenberg B, Leveau J (2007) Biocontrol of plant pathogens: principles, promises and pittfalls. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC press, Taylor and Francis Group, Boca Raton, FL, USA, pp 267–296

    Google Scholar 

  • Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490

    PubMed  CAS  Google Scholar 

  • Markowich NA, Kononova GL (2003) Lytic enzymes of Trichoderma and their role in plant defense from fungal diseases: a review. Appl Biochem Microbiol 39:341–351

    Google Scholar 

  • Matilla MA, Espinosa-Urgel M, Rodríguez-Herva JJ, Ramos JL, Ramos-González MI (2007) Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol 8:R179. doi:10.1186/gb-2007-8-9-r179

    PubMed  Google Scholar 

  • Matus A (1999) GFP in motion CD-ROM-Introduction:GFP illuminates everything. Trends Cell Biol 9:43

    Google Scholar 

  • Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, Markelov ML, Lukyanov SA (1999) Fluorescent proteins from nonbioluminiscent Anthozoa species. Nat Biotechnol 17:969–973

    PubMed  CAS  Google Scholar 

  • Mazzola M, Fujimoto DK, Thomashow LS, Cook RJ (1995) Variation in sensitivity of Gaeumannomyces graminis to antibiotics produced by fluorescent pseudomonas spp. and effect on biological control of take-all of wheat. Appl Environ Microbiol 61:2554–2559

    PubMed  CAS  Google Scholar 

  • Mazzola M, De Bruijn I, Cohen MF, Raaijmakers JM (2009) Protozoa-induced regulation of cyclic lipopeptide biosynthesis is an effectice predation defense mechanism in Pseudomonas fluorescens. Appl Environ Microbiol. doi:10.1128/AEM.01272-09

    PubMed  Google Scholar 

  • Meharg AA, Killham K (1995) Loss of exudates from the roots of perennial ryegrass inoculated with a range of microorganisms. Plant Soil 170:345–349

    CAS  Google Scholar 

  • Miernyk JA (1979) Abscisic acid inhibition of kinetin nucleotide formation in germinating lettuce seeds. Physiol Plant 45:63–66

    CAS  Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199

    PubMed  CAS  Google Scholar 

  • Milner JL, Stohl EA, Handelsman J (1996) ZwittermycinA resistance gene from Bacillus cereus. J Bacteriol 178:4266–4272

    PubMed  CAS  Google Scholar 

  • Moore FP, Barac T, Borremans B, Oeyen L, Vangronsveld J, Van der Lelie D, Campbell CD, Moore ERB (2006) Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: the characterization of isolates with potential to enhance phytoremediation. Syst Appl Microbiol 29:539–556

    PubMed  CAS  Google Scholar 

  • Neilands JB (1981) Microbial iron compounds. Annu Rev Biochem 50:715–731

    PubMed  CAS  Google Scholar 

  • Nielsen MN, Sorensen J (1999) Chitinolytic activity of Pseudomonas fluorescesn isolates from barley and sugar beet rhizosphere. FEMS Microbiol Ecol 30:217–227

    Google Scholar 

  • Normander B, Hendriksen NB, Nybroe O (1999) Green fluorescent protein-marked Pseudomonas fluorescens: localization, viability and activity in the natural barley rhizosphere. Appl Environ Microbiol 65:4646–4651

    PubMed  CAS  Google Scholar 

  • O’Sullivan LA, Weightman AJ, Jones TH, Marchbank AM, Tiedje JM, Mahenthiralinaam E (2007) Identifying the genetic basis of ecologically and biotechnologically useful functions of the bacterium Burkholderia vietnamiensis. Environ Microbiol 9:1017–1034

    PubMed  Google Scholar 

  • Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigy J-L, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090

    PubMed  CAS  Google Scholar 

  • Ordentlich AY, Elad AY, Chet I (1998) The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfssi. Phytopathology 78:84–88

    Google Scholar 

  • Oren L, Ezrati S, Cohen D, Sharon A (2003) Early events in the Fusarium verticillioides–maize interaction characterized by using a green fluorescent protein-expressing transgenic isolate. Appl Environ Microbiol 69:1695–1701

    PubMed  CAS  Google Scholar 

  • Pal KK, Gardener M (2006) Biological control of plant pathogens. The Plant Health Instructor. pp 1–25. doi:10.1094/PHI-A-2006-1117-02

    Google Scholar 

  • Palumbo JD, Yuen GY, Jochum CC, Tatum K, Kobayashi DY (2005) Mutagenesis of beta 1, 3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward Bipolaris leaf spot of tall fescue and Pythium damping-off of sugar beet. Phytopathology 95:701–707

    PubMed  CAS  Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    PubMed  CAS  Google Scholar 

  • Pérez-Jiménez RM, Zea-Bonilla T, López-Herrera CJ (2003) Studies of R. necatrix perithecia found in nature on avocado roots. J Phytopathol 151:660–664

    Google Scholar 

  • Perneel M, D’hont L, De Maeyer K, Adiobo A, Rabaey K, Höfte M (2008) Phenazines and biosurfactants interact in the biological control of soil-borne diseases caused by Pythium spp. Environ Microbiol 10:778–788

    PubMed  Google Scholar 

  • Perry LG, Alford ER, Horiuchi J, Paschke MW, Vivanco JM (2007) Chemical signals in the rhizosphere: root-root and root-microbe communication. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere. Biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC, Taylor and Francis, Boca Raton, FL, USA, pp 297–330

    Google Scholar 

  • Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894

    PubMed  CAS  Google Scholar 

  • Phillips LA, Germida JJ, Farrell RE, Greer CW (2008) Hydrocarbon degradation potential and activity of endophytic bacteria associated with prairie plants. Soil Biol Biochem 40:3054–3064

    CAS  Google Scholar 

  • Pinton R, Varanini Z, Nannipieri P (2007) The rhizosphere. Biochemistry and organic substances at the soil plant interface, 2nd edn. CRC, Taylor and Francis, Boca Raton, FL, USA

    Google Scholar 

  • Pliego C, Cazorla FM, González-Sánchez MA, Pérez-Jiménez RM, de Vicente A, Ramos C (2007) Selection for biocontrol bacteria antagonistic toward Rosellinia necatrix by enrichment of competitive avocado root tip colonizers. Res Microbiol 158:463–470

    PubMed  CAS  Google Scholar 

  • Pliego C (2008) Multitrophic interactions involved in biological control of avocado white root rot caused by Rosellinia necatrix. PhD Thesis Univ. Malaga, Spain

    Google Scholar 

  • Pliego C, De Weert S, Lamers G, De Vicente A, Bloemberg G, Cazorla FM, Ramos C (2008) Two similar enhanced root-colonizing Pseudomonas strains differ largely in their colonization strategies of avocado roots and Rosellinia neatrix hyphae. Environ Microbiol 10:3295–3304

    PubMed  Google Scholar 

  • Pliego C, Kanematsu S, Ruano-Rosa D, de Vicente A, López-Herrera C, Cazorla FM, Ramos C (2009) GFP sheds light on the infection process of avocado roots by Rosellinia necatrix. Fungal Genet Biol 46:137–145

    PubMed  CAS  Google Scholar 

  • Porteous F, Kilham K, Meharg A (2000) Use of a Lux-marked rhizobacterium as a biosensor to assess changes in rhizosphere C flow due to pollutant stress. Chemosphere 41:1549–2000

    PubMed  CAS  Google Scholar 

  • Preston GM, Bertrand N, Rainey PB (2001) Type III secretion in plant growth promoting Pseudomonas fluorescens SBW25. Mol Microbiol 41:999–1014

    PubMed  CAS  Google Scholar 

  • Raaijmakers JM, De Bruijn I, De Kock MJD (2006) Cyclic lipopeptide production by plant-associated Pseudomonas spp. diversity, activity, biosynthesis, and regulation. Mol Plant Microbe Interact 19:699–710

    PubMed  CAS  Google Scholar 

  • Rademacher W (1994) Gibberellin formation in microorganisms. Plant Growth Regul 5:303–314

    Google Scholar 

  • Rainey PB (1999) Adaption of Pseudomonas fluorescens to the plant rhizosphere. Environ Microbiol 63:881–887

    Google Scholar 

  • Rainey PB, Preston GM (2000) In vivo expression technology strategies: valuable tools for biotechnology. Curr Opin Biotechnol 11:440–444

    PubMed  CAS  Google Scholar 

  • Ramos C, Mølbak L, Molin S (2000) Bacterial activity in the rhizosphere analyzed at the single-cell level by monitoring ribosome contents and synthesis rates. Appl Environ Microbiol 66:801–809

    PubMed  CAS  Google Scholar 

  • Ramos-González MI, Campos MJ, Ramos JL (2005) Analysis of Pseudomonas putida KT2440 gene expression in the maize rhizosphere: in vitro expression technology capture and identification of root-activated promoters. J Bacteriol 187:4033–4041

    PubMed  Google Scholar 

  • Ran H, Hassett DJ, Lau GW (2003) Human targets of Pseudomonas aeruginosa pyocyanin. Proc Natl Acad Sci USA 100:14315–14320

    PubMed  CAS  Google Scholar 

  • REBECA (Regulation of biological control agents) (2008) Specific Support Action Project no. SSPE-CT-2005-022709 Deliverable 24 Cost, trade-off, and benefit analysis http://www.rebeca-net.de/?p=320

  • Rezzonico F, Défago G, Moënne-Loccoz Y (2004) Comparison of ATP-encoding type III secretion system hrcN genes in biocontrol fluorescent pseudomonas and in phytopathogenic proteobacteria. Appl Environ Microbiol 70:5119–5131

    PubMed  CAS  Google Scholar 

  • Rincón A, Ruíz-Díez B, García-Fraile S, García JA, Fernández-Pascual M, Pueyo JJ, De Felipe MR (2005) Colonisation of Pinus halepensis roots by Pseudomonas fluorescens and interaction with the ectomycorrhizal fungus Suillus granulatus. FEMS Microbiol Ecol 51:303–311

    PubMed  Google Scholar 

  • Rodríguez H, Fraga R, González T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth promoting bacteria. Plant Soil 287:15–21

    Google Scholar 

  • Rudrappa T, Czymmek KJ, Par PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556

    PubMed  CAS  Google Scholar 

  • Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wie H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth of Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932

    PubMed  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    PubMed  CAS  Google Scholar 

  • Scherwinski K, Grosch R, Berg G (2008) Effect of bacterial antagonists on lettuce: active biocontrol of Rhizoctonia solani and negligible, short-term effects on nontarget microorganism. FEMS Microbiol Ecol 64:106–116

    PubMed  CAS  Google Scholar 

  • Schirmböck M, Lorito M, Wang Y-L, Hayes CK, Arisan-Atac I, Scala F, Harman GE, Kubicek CP (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol 60:4364–4370

    PubMed  Google Scholar 

  • Schoonbeek HJ, Raaijmakers JM, De Waard MA (2002) Fungal ABC transporters and microbial interactions in natural environments. Mol Plant Microbe Interact 15:1165–1172

    PubMed  CAS  Google Scholar 

  • Schouten A, Van den Berg G, Edel-Hermann V, Steinberg C, Gautheron N, Alabouvette C, De Vos CH, Lemanceau P, Raaijmakers JM (2004) Defence responses of Fusarium oxysporum to 2, 4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by Pseudomonas fluorescens. Mol Plant Microbe Interact 17:1201–1211

    PubMed  CAS  Google Scholar 

  • Schroth MN, Hancock JG (1982) Disease-suppressive soil and root-colonizing bacteria. Science 216:1376–1381

    PubMed  CAS  Google Scholar 

  • Segura A, Rodríguez-Conde S, Ramos C, Ramos JL (2009) Bacterial responses and interactions with plants during rhizoremediation. Microb Biotechnol 2(4):452–464

    PubMed  CAS  Google Scholar 

  • Sesma A, Osbourn AE (2004) The rice leaf blast pathogen undergoes developmental processes typical of root-infecting fungi. Nature 431:582–586

    PubMed  CAS  Google Scholar 

  • Shaner NC, Campbell RE, Steinbach PA, Giepmans BNG, Palmer AE, Tsien RY (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22:1567–1572

    PubMed  CAS  Google Scholar 

  • Shea JE, Santangelo JD, Feldman RG (2000) Signature-tagged mutagenesis in the identification of virulence genes in pathogens. Curr Opin Microbiol 3:451–458

    PubMed  CAS  Google Scholar 

  • Shuhegger R, Ihring A, Gantner S, Bahnweg G, Knaooe C, Vogg G, Hutzler P, Schmid M, Van Breusegem F, Eberl L, Hartmann A, Langebartels C (2006) Induction of systemic resistance in tomato plants by N-acyl-L-homoserine lactone producing rhizosphere bacteria. Plant Cell Environ 29:909–918

    Google Scholar 

  • Simons M, Van der Bij AJ, Brand I, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1996) Gnotobiotic system for studing rhizosphere colonization by plant-growth promoting Pseudomonas bacteria. Mol Plant Microbe Interact 7:600–607

    Google Scholar 

  • Simons M, Permentier HP, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1997) Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact 10:102–106

    CAS  Google Scholar 

  • Spaepen S, Dobbelaere S, Croonenborghs A, Vanderleyden J (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312: 15–23

    CAS  Google Scholar 

  • Spaepen S, Das F, Luyten E, Michiels J, Vanderleyden J (2009) Indole-3-acetic acid- regulated genes in Rhizobium etli CNPAF512. FEMS Microbiol Lett 291:195–200

    PubMed  CAS  Google Scholar 

  • Spaink HP, Kondorosi A, Hooykaas PJJ (1998) The rhizobiaeceae. Kluwer, Dordrecht, The Netherlands

    Google Scholar 

  • Spiers AJ, Bohannon J, Gehrig S, Rainey PB (2003) Colonisation of the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50:15–27

    PubMed  CAS  Google Scholar 

  • Tamayo R, Pratt JT, Camilli A (2007) Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Ann Rev Microbiol 61:131–138

    CAS  Google Scholar 

  • Thomashow LS, Weller DM (1988) Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var Tritici. J Bacteriol 170:3499–3508

    PubMed  CAS  Google Scholar 

  • Thompson B, Chaney N, Wing JS, Gould SJ, Loper JE (1999) Characterization of the pyoluteorin biosynthetic gene cluster of Pseudomonas fluorescens Pf-5. J Bacteriol 181:2166–2174

    Google Scholar 

  • Tombolini R, Unge A, Davy ME, de Bruijn FJ, Jansson J (1997) Flow cytometric and microscopic analysis of GFP-tagged Pseudomonas fluorescens bacteria. FEMS Microbiol Ecol 22:17–28

    CAS  Google Scholar 

  • Tsien RY (1998) The green fluorescent protein. Annu Rev Biochem 67:509–544

    PubMed  CAS  Google Scholar 

  • Unge A, Jansson J (2001) Monitoring population size, activity, and distribution of gfp-luxAB-tagged Pseudomonas fluorescens SBW25 during colonisation of wheat. Microb Ecol 41:290–300

    PubMed  CAS  Google Scholar 

  • Uren NC (2007) Types, amounts, and possible function of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere. Biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 1–21

    Google Scholar 

  • Validov S, Kamilova F, Qi S, Stephan D, Wang J, Makarova N, Lugtenberg B (2007) Selection of bacteria able to control Fusarium oxysporum f.sp. radicis-lycopersici in stonewool substrate. J Appl Microbiol 102:461–471

    PubMed  CAS  Google Scholar 

  • Van Aken B, Yoon JM, Schnoor JL (2004) Biodegradation of nitro-substituted explosives 2, 4, 6-trinitrotoluene, hexahydro-1, 3, 5-trinitro-1, 3, 5-triazine, and octahydro-1, 3, 5, 7-tetranitro-1, 3, 5-tetrazocine by a phytosymbiotic Methylobacterium sp. associated with poplar tissues (Populus deltoides x nigra DN34). Appl Environ Microbiol 70:508–517

    PubMed  Google Scholar 

  • Van Bruggen AHC, Semenov AM, Zelenev VV, Semenov AV, Raaijmakers JM, Sayler RJ, De Vos O (2007) Wave-like distribution patterns of Gfp-marked Pseudomonas fluorescens along roots of wheat plants grown in two soils. Microb Ecol 55:466–475

    PubMed  Google Scholar 

  • Van Loon LC (2000) Systemic induced resistance. In: Slusarenko AJ, Franser RSS, Van Loon LC (eds) Mechanisms of resistance to plant diseases. Kluwer, Dordrecht, pp 521–574

    Google Scholar 

  • Van Loon LC (2007) Plant responses to plant growth-promoting bacteria. Eur J Plant Pathol 119:243–254

    Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    PubMed  Google Scholar 

  • Van Rij ET, Wesselink M, Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2004) Influence of environmental conditions on the production of phenazine-1-carboxamide by Pseudomonas chlororaphis PCL1391. Mol Plant Microbe Interact 17:557–566

    PubMed  Google Scholar 

  • Van Rij ET, Girard G, Lugtenberg BJJ, Bloemberg GV (2005) Influence of fusaric acid on phenazine-1-carboxamide synthesis and gene expression of Pseudomonas chlororaphis strain PCL1391. Microbiology 151:2805–2814

    PubMed  Google Scholar 

  • Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van’t Westende YAM, Hartog F, Van Loon LC (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol Plant Microbe Interact 10:716–724

    PubMed  Google Scholar 

  • Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of micro-organisms:potentials and future trends. Appl Microbiol Biotechnol 71:137–144

    PubMed  CAS  Google Scholar 

  • Villacieros M, Power B, Sánchez-Contreras M, Lloret J, Oruezabal RI, Martín M, Fernández-Piñas F, Bonilla I, Whelan C, Dowling DN, Rivilla R (2003) Colonisation behavior of Pseudomonas fluorescens and Sinorhizobium meliloti in the alfalfa (Medicago sativa) rhizosphere. Plant Soil 251:47–54

    CAS  Google Scholar 

  • Vivanco JM, Bais HP, Stermitz FR, Thelen GC, Gallaway RM (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol Lett 7:285–295

    Google Scholar 

  • Weingart H, Volksch B (1997) Ethylene production by Pseudomonas syringae pathovars in vitro and in planta. Appl Environ Microbiol 63:156–161

    PubMed  CAS  Google Scholar 

  • Weingart H, Ulrich H, Geider K, Volksch B (2001) The role of ethylene production in virulence of Pseudomonas syringae pvs. glycinea and phaseolicola. Phytopathology 91:511–518

    PubMed  CAS  Google Scholar 

  • Weller DM, Thomashow LS (1994) Current challenges in introducing beneficial microorganisms into the rhizosphere. In: O’Gara F, Dowling DN, Boesten B (eds) Molecular ecology of rhizosphere microorganisms: biotechnology and release of GMOs. VCH, New York, pp 1–18

    Google Scholar 

  • Wolk CP, Cai Y, Panoff JM (1991) Use of a transposon with luciferase as a reporter to identify environmentally responsive genes in cyanobacterium. Proc Natl Acad Sci USA 88:5355–5359

    PubMed  CAS  Google Scholar 

  • Yang TT, Sina P, Green G, Kitts PA, Chen YT, Lybarger L, Chervenak R, Patterson GH, Piston DW, Kain SR (1998) Improved fluorescence and dual color detection with enhanced blue and green variants of the green fluorescent protein. J Biol Chem 273:8212–8216

    PubMed  CAS  Google Scholar 

  • Zachow C, Pirker H, Westendorf C, Tilcher R, Berg G (2009) The Caenorhabditis elegans assay: a tool to evaluate the pathogenic potential of bacterial biocontrol agents. Eur J Plant Pathol 84:11–18

    Google Scholar 

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Acknowledgments

Clara Pliego thanks MEC, grant numbers AGL-2005-06347-C03-01, AGL2008-0543-C02-01 and Junta de Andalucia, Grupo PAI CVI264. Ben Lugtenberg thanks Leiden University, The European Commission, INTAS, the NWO departments of ALW, CW, STW as well as the Netherlands (NWO) – Russian Center of Excellence for support. All of us want to express our sincere gratitude to Prof. Fernando Pliego Alfaro for critical reading and helpful comments on the manuscript.

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Pliego, C., Kamilova, F., Lugtenberg, B. (2011). Plant Growth-Promoting Bacteria: Fundamentals and Exploitation. In: Maheshwari, D. (eds) Bacteria in Agrobiology: Crop Ecosystems. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-18357-7_11

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