Use of Plant-Associated Bacillus Strains as Biofertilizers and Biocontrol Agents in Agriculture

Abstract

Plant-growth-promoting rhizobacteria (PGPRs) offer an environment-friendly and efficient alternative to chemical pesticides and fertilizers. Among them, endospore-forming bacilli are especially attractive because their long-term stability is comparable with that of agrochemicals. Although their use is steadily increasing, exploiting of these biologicals is still limited by insufficient knowledge about the mechanisms underlying plant growth promotion and biological control. However, in recent years, some progress was made in uncovering molecular mechanisms responsible for beneficial interactions between PGP bacilli and plants. We describe here some aspects of the plant–PGP bacilli relationship in light of the genomic data recently obtained from Bacillus amyloliquefaciens, and propose to choose B. amyloliquefaciens FZB42 as a paradigm for further research on PGP bacilli.

Notes

Acknowledgments

I dedicate this article to Prof. (em.) Dr. Helmut Bochow, former chair of Plant Pathology at Humboldt University Berlin. Prof. Bochow did pioneering research with plant-growth-promoting bacilli and was one of the first who recognized importance of those bacteria in increasing crop yield and quality. I thank all the present and former members of my laboratory and the many colleagues and friends with whom I worked together in the exciting field of plant growth promotion and biocontrol during the last decade. Their trustful collaboration and innovative work made it possible to write this review.

References

  1. Arguelles-Arias A, Ongena M, Halimi B, Lara Y, Brans A, Joris B, Fickers P (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Fact 8:63PubMedCrossRefGoogle Scholar
  2. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319PubMedCrossRefGoogle Scholar
  3. Bargabus RL, Zidack NK, Sherwood JW, Jacobsen BJ (2002) Characterization of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere colonizing Bacillus mycoides, biological control agent. Physiol Mol Plant Pathol 61:289–298CrossRefGoogle Scholar
  4. Bargabus RL, Zidack NK, Sherwood JW, Jacobsen BJ (2004) Screening for the identification of potential biological control agents that induce systemic acquired resistance in sugar beet. Biol Control 30:342–350CrossRefGoogle Scholar
  5. Beatty PH, Jensen SE (2002) Paenibacillus polymyxa produces fusaricidin-type antifungal antibiotics active against Leptosphaeria maculans, the causative agent of black leg disease of canola. Can J Microbiol 48:159–169PubMedCrossRefGoogle Scholar
  6. Begon M, Townsend CA, Harper JL (2006) Ecology: from individuals to ecosystems. Blackwell, Malden, MAGoogle Scholar
  7. Bell CR, Dickie GA, Harvey WLG, Chan JWYF (1995) Endophytic bacteria in grapevine. Can J Microbiol 41:46–53CrossRefGoogle Scholar
  8. Bezzate S, Aymerich S, Chambert R, Czarnes S, Berge O, Heulin T (2000) Disruption of the Paenibacillus polymyxa levansucrase gene impairs its ability to aggregate soil in the wheat rhizosphere. Environ Microbiol 2:333–342PubMedCrossRefGoogle Scholar
  9. Bleeker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plant. Annu Rev Cell Dev Biol 16:1–18CrossRefGoogle Scholar
  10. Bloemberg GV, Lugtenberg BJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350PubMedCrossRefGoogle Scholar
  11. Bochow H (1992) Phytosanitary effects of Bacillus subtilis as a biocontrol agent. Meded Fac Landbouww Rijksuniv Gent 57(2b):387–393Google Scholar
  12. Bochow H, El-Sayed SF, Junge H, Stavropoulo A, Schmiedeknecht G (2001) Use of Bacillus subtilis as biocontrol agent. IV. Salt-stress tolerance induction by Bacillus subtilis FZB24 seed treatment in tropical vegetable field crops, and its mode of action. J Plant Dis Prot 108:21–30Google Scholar
  13. Borriss R, Bochow H, Junge H (2006) Use of Bacillus subtilis/amyloliquefaciens FZB strains for plant growth promotion and biocontrol. In: 7th international workshop on plant growth promoting rhizobacteria, Program and abstract book, Noordwijkerhout, The Netherlands, p 15Google Scholar
  14. Bothe H, Korsgen H, Lehmacher T, Hundeshagen B (1992) Differential-effects of Azospirillum, auxin and combined nitrogen on the growth of the roots of wheat. Symbiosis 13:167–179Google Scholar
  15. Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503PubMedCrossRefGoogle Scholar
  16. Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59:1229–1238PubMedCrossRefGoogle Scholar
  17. Brannen PM, Kenney DS (1997) Kodiak® – a successful biological-control product for suppression of soil-borne plant-pathogens of cotton. J Ind Microbiol Biotechnol 19:169–171CrossRefGoogle Scholar
  18. Broggini GAL, Duffy B, Holliger E, Schärer HJ, Gessler C, Patocchi A (2005) Detection of the fire blight biocontrol agent Bacillus subtilis BD170 (Biopro®) in a Swiss apple orchard. Eur J Plant Pathol 111:93–100CrossRefGoogle Scholar
  19. Burkett-Cadena M, Kokalis-Burelle N, Lawrence KS, van Santen E, Kloepper JW (2008) Suppressiveness of root-knot nematodes mediated by rhizobacteria. Biol Control 47:55–59CrossRefGoogle Scholar
  20. Butcher RA, Schroeder FC, Fischbach MA, Straight PD, Kolter R, Walsh D, Clardy J (2007) The identification of bacillaene, the product of the pksX megacomplex in Bacillus subtilis. Proc Natl Acad Sci USA 104:1506–1509PubMedCrossRefGoogle Scholar
  21. Chen XH, Vater J, Piel J, Franke P, Scholz R, Schneider K, Koumoutsi A, Hitzeroth G, Grammel N, Strittmatter AW, Gottschalk G, Süssmuth R, Borriss R (2006) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J Bacteriol 188:4024–4036PubMedCrossRefGoogle Scholar
  22. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O, Junge H, Voigt B, Jungblut PR, Vater J, Süssmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014PubMedCrossRefGoogle Scholar
  23. Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Piel J, Borriss R (2009a) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140:27–37PubMedCrossRefGoogle Scholar
  24. Chen XH, Scholz R, Borriss M, Junge H, Mögel G, Kunz S, Borriss R (2009b) Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J Biotechnol 140:38–44PubMedCrossRefGoogle Scholar
  25. Choi SK, Park SY, Kim R, Lee CH, Kim J, Park SH (2008) Identification and functional analysis of the fusaricidin biosynthetic gene of Paenibacillus polymyxa E681. Biochem Biophys Res Commun 365:89–95PubMedCrossRefGoogle Scholar
  26. Choi SK, Park SY, Kim R, Kim SB, Lee CH, Kim JF, Park SH (2009) Identification of a polymyxin synthetase gene cluster of Paenibacillus polymyxa and heterologous expression of the gene in Bacillus subtilis. J Bacteriol 191:3350–3385PubMedCrossRefGoogle Scholar
  27. Chu F, Kearns DB, Branda SS, Kolter R, Losick R (2006) Targets of the master regulator of biofilm formation in B. subtilis. Mol Microbiol 59:1216–1228PubMedCrossRefGoogle Scholar
  28. 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 71:4951–4959PubMedCrossRefGoogle Scholar
  29. Costa-Carvailhis L (2010) Transcriptional profiling of Bacillus amyloliquefaciens FZB42 in response to seed and root exudates collected under different nutrient regimes. PhD thesis, Stuttgart-HohenheimGoogle Scholar
  30. Doekel S, Marahiel MA (2001) Biosynthesis of natural products on modular peptide synthetases. Metab Eng 3:64–77PubMedCrossRefGoogle Scholar
  31. Dolej S, Bochow H (1996) Studies of the mode of action of Bacillus subtilis culture filtrates in the model pathosystem tomato seedling – Fusarium oxysporum f. sp. Radicis-lycopersici. Meded Fac Landbouww Rijksuniv Gent 61(2b):483–489Google Scholar
  32. Duitman EH, Hamoen LW, Rembold M, Venema G, Seitz H, Saenger W, Bernhard F, Reinhardt R, Schmidt M, Ullrich C, Stein T, Leenders F, Vater J (1999) The mycosubtilin synthetase of Bacillus subtilis ATCC 6633: a multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase. Proc Natl Acad Sci USA 96:13294–13299PubMedCrossRefGoogle Scholar
  33. Ehlers RE (2006) Einsatz der Biotechnologie im biologischen Pflanzenschutz. Schriftenreihe der Deutschen Phytomedizinischen Gesellschaft eV 8:17–31 (in German)Google Scholar
  34. Emmert EAB, Handelsman J (1999) Biocontrol of plant disease: a Gram-positive perspective. FEMS Microbiol Lett 171:1–9PubMedCrossRefGoogle Scholar
  35. Farag MA, Ryu CM, Sumner LW, Pare PW (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262–2268PubMedCrossRefGoogle Scholar
  36. Fritze D (2004) Taxonomy of the Genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 94:1245–1248PubMedCrossRefGoogle Scholar
  37. Fry W (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9:385–4002PubMedCrossRefGoogle Scholar
  38. Glick BR, Patten CN, Holguin B, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth promotion bacteria. Imperial College Press, London, pp 1–13CrossRefGoogle Scholar
  39. Gouvea CMCP, Souza JF, Magalhaes ACN, Martins IS (1997) NO-releasing substances that induce growth elongation in maize root segments. Plant Growth Regul 21:183–187CrossRefGoogle Scholar
  40. Grosch R, Junge H, Krebs B, Bochow H (1999) Use of Bacillus subtilis as biocontrol agent. III. Influence Bacillus subtilis fungal root diseases yield soilless culture. J Plant Dis Prot 106:568–580Google Scholar
  41. Guo JH, Liu XJ, Zhang Y, Shen JL, Han XW, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010PubMedCrossRefGoogle Scholar
  42. Gutierrez-Mañero 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 111:206–211CrossRefGoogle Scholar
  43. Gyaneshwar P, Naresh Kumar G, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93CrossRefGoogle Scholar
  44. Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent Pseudomonas. Nat Rev Microbiol 3:307–319PubMedCrossRefGoogle Scholar
  45. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108PubMedCrossRefGoogle Scholar
  46. Hamon MA, Lazazzera BA (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42:1199–1209PubMedCrossRefGoogle Scholar
  47. Hamon MA, Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2004) Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis. Mol Microbiol 52:847–860PubMedCrossRefGoogle Scholar
  48. Haverkort AJ, Boonekamp PM, Hutten R et al (2008) Social costs of late blight in potato and prospects of durable resistance through cisgenic modification. Potato Res 51:47–57CrossRefGoogle Scholar
  49. Hervas A, Landa B, Datnoff LE, Jimenez-Diaz RM (1998) Effects of commercial and indigenous microorganisms on Fusarium wilt development in chickpea. Biol Control 13:166–176CrossRefGoogle Scholar
  50. Hofemeister J, Conrad B, Adler B, Hofemeister B, Feesche J, Kucheryava N et al (2004) Genetic analysis of the biosynthesis of non-ribosomal peptide- and polyketide-like antibiotics, iron uptake and biofilm formation by Bacillus subtilis A1/3. Mol Genet Genomics 272:363–378PubMedCrossRefGoogle Scholar
  51. Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35:227–239CrossRefGoogle Scholar
  52. Idris EE, Bochow H, Ross H, Borriss R (2004) Use of Bacillus subtilis as biocontrol agent. VI. Phytohormone like action of culture filtrates prepared from plant growth-promoting Bacillus amyloliquefaciens FZB24, FZB42, FZB45 and Bacillus subtilis FZB37. J Plant Dis Prot 111:583–597Google Scholar
  53. Idris EES, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant Microbe Interact 20:619–626PubMedCrossRefGoogle Scholar
  54. Idriss EES, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Richter T, Borriss R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB 45 contributes to its plant growth-promoting effect. Microbiology 148:2097–2109PubMedGoogle Scholar
  55. Jacobsen BJ, Zidack NK, Larson BJ (2004) The role of Bacillus-based biological control agents in integrated pest management systems: plant diseases. Phytopathology 94:1272–1275PubMedCrossRefGoogle Scholar
  56. Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils – misconceptions and knowledge gaps. Plant Soil 248:31–41CrossRefGoogle Scholar
  57. Joshi R, McSpadden Gardener BB (2006) Identification and characterization of novel genetic markers associated with biological control activities in Bacillus subtilis. Phytopathology 96:145–154PubMedCrossRefGoogle Scholar
  58. Kearns DB, Chu F, Rudner R, Losick R (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55:739–749PubMedCrossRefGoogle Scholar
  59. Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39CrossRefGoogle Scholar
  60. Kevany BM, Rasko DA, Thomas M (2009) Characterization of the complete zwittermicin A biosynthesis gene cluster from Bacillus cereus. Appl Environ Microbiol 75:1144–1155PubMedCrossRefGoogle Scholar
  61. Kilian M, Steiner U, Krebs B, Junge H, Schmiedeknecht G, Hain R (2000) FZB24® Bacillus subtilis – mode of action of a microbial agent enhancing plant vitality. Pflanzenschutz Nachr Bayer 1:72–93Google Scholar
  62. Kloepper JW, Leong J, Teintze M, Schroth M (1980) Enhancing plant growth by siderophores produces by plant-growth-promoting rhizobacteria. Nature 286:885–886CrossRefGoogle Scholar
  63. Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–44CrossRefGoogle Scholar
  64. Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266PubMedCrossRefGoogle Scholar
  65. Kokalis-Burelle N, Kloepper JW, Reddy MS (2006) Plant growth-promotion rhizobacteria as transplant amendments and their effect on indigenous rhizosphere microorganisms. Appl Soil Ecol 31:91–100CrossRefGoogle Scholar
  66. Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, Franke P, Vater J, Borriss R (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186:1084–1096PubMedCrossRefGoogle Scholar
  67. Kowall M, Vater J, Kluge B, Stein T, Franke P, Ziessow D (1998) Separation and characterization of surfactin isoforms produced by Bacillus subtilis OKB 105. J Colloid Interface Sci 204:1–8PubMedCrossRefGoogle Scholar
  68. Krebs B, Höding B, Kübart S, Workie MA, Junge H, Schmiedeknecht G, Bochow H, Hevesi M (1998) Use of Bacillus subtilis as biocontrol agent. I. Activities and characterization of Bacillus subtilis strains. J Plant Dis Prot 105:181–197 (in German)Google Scholar
  69. Kumar S, Pandey P, Maheshwari DK (2009) Reduction in dose of chemical fertilizers and growth enhancement of Sesame (Sesamum indicum L.) with application of rhizospheric competent Pseudomonas aeruginosa LES4. Eur J Soil Biol 45:334–340CrossRefGoogle Scholar
  70. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessières P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Codani JJ, Connerton IF, Danchin A et al (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256PubMedCrossRefGoogle Scholar
  71. Laloi C, Apel K, Danon K (2004) Latest news in reactive oxygen species. Curr Opin Plant Biol 7:323–328PubMedCrossRefGoogle Scholar
  72. Lebuhn M, Heulin T, Hartmann A (1997) Production of auxin and other indolic and phenolic compounds by Paenibacillus polymyxa strains, isolated from different proximity to plant roots. FEMS Microbiol Ecol 22:325–334CrossRefGoogle Scholar
  73. Li X, Wu Z, Li W, Yan R, Li L, Li J, Li Y, Li M (2007) Growth promoting effect of a transgenic Bacillus mucilaginosus on tobacco planting. Appl Microbiol Biotechnol 74:1120–1125PubMedCrossRefGoogle Scholar
  74. Lin W, Okon Y, Hardy RWF (1983) Enhanced mineral uptake by Zea mays and Sorgum bicolor roots inoculated with Azospirillum brasilense. Appl Environ Microbiol 45:1775–1779PubMedGoogle Scholar
  75. Loper JE, Schroth MN (1986) Influence of bacterial sources of indole-3-acetic acid biosynthetic on root elongation of sugar beet. Phytopathology 76:386–389CrossRefGoogle Scholar
  76. Lugtenberg B, Kamilova F (2009) Plant-growth promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedCrossRefGoogle Scholar
  77. Lundberg JO (2008) Nitric oxide in the gastrointestinal tract: role of bacteria. Biosci Microflora 27:109–112Google Scholar
  78. Maheshwari DK, Kumar S, Kumar B, Pandey P (2011) Co-inoculation of urea and DAP tolerant Sinorhizobium meliloti and Pseudomonas aeruginosa as integrated approach for growth enhancement of Brassica juncea. Ind J Microbiol 50(4):425–431CrossRefGoogle Scholar
  79. Makarewicz O, Dubrac S, Msadek T, Borriss R (2006) Dual role of the PhoP P response regulator: Bacillus amyloliquefaciens FZB45 phytase gene transcription is directed by positive and negative interaction with the phyC promoter. J Bacteriol 188:6953–6965PubMedCrossRefGoogle Scholar
  80. Malakoff D (1998) Coastal ecology: death by suffocation in the Gulf of Mexico. Science 281:190–192CrossRefGoogle Scholar
  81. McInroy JA, Kloepper JW (1995) Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant Soil 173:337–342CrossRefGoogle Scholar
  82. McSpadden Gardener BB, Fravel DR (2002) Biological control of plant pathogens: research, commerzialisation, and application in the USA. Plant Health Progress. doi:10.1094/PHP-2002-0510-01-RVGoogle Scholar
  83. Mishagi IJ, Donndelinger CR (1990) Endophytic bacteria in symptom-free cotton plants. Phytopathology 9:808–811CrossRefGoogle Scholar
  84. Nicholson WL (2008) The Bacillus subtilis ydjL (bdhA) gene encodes acetoin reductase/2,3-butanediol dehydrogenase. Appl Environ Microbiol 74:6832–6838PubMedCrossRefGoogle Scholar
  85. Ortiz-Castro R, Contreras-Cornejo HA, Macias-Rodriguez L, Lopez-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712PubMedCrossRefGoogle Scholar
  86. Paulsen IT, Press CM, Ravel J, Kobayashi DY, Myers GSA, Mavrodi DV et al (2005) Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol 23:873–878PubMedCrossRefGoogle Scholar
  87. Peypoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51:553–556PubMedCrossRefGoogle Scholar
  88. Phi QT, Oh SH, Park YM, Park SH, Ryu CM, Ghim SY (2008a) Isolation and characterization of transposon-insertional mutants from Paenibacillus polymyxa E681 altering the biosynthesis of indole-3-acetic acid. Curr Microbiol 56:524–530PubMedCrossRefGoogle Scholar
  89. Phi QT, Park YM, Ryu CM, Park SH, Ghim SY (2008b) Functional identification and expression of indole-3-pyruvate decarboxylase from Paenibacillus polymyxa E681. J Microbiol Biotechnol 18:1235–1244PubMedGoogle Scholar
  90. Pleban S, Chernin L, Chet I (1997) Chitinolytic activity of an endophytic strain of Bacillus cereus. Lett Appl Microbiol 25:284–288PubMedCrossRefGoogle Scholar
  91. Ramirez CA, Kloepper JW (2009) Plant growth promotion by Bacillus amyloliquefaciens FZB45 depends on inoculum concentration and P-related soil properties. 8th International PGPR workshop. Proceedings book. Portland, Oregon, ORGoogle Scholar
  92. Ramos HC, Hoffmann T, Marino M, Nedjari H, Presecan-Siedel E, Dreesen O, Glaser P, Jahn D (2000) Fermentative metabolism of Bacillus subtilis: physiology and regulation of gene expression. J Bacteriol 182:3072–3080CrossRefGoogle Scholar
  93. Renna MC, Najimudin N, Winik R, Zahler SA (1993) Regulation of the alsS, alsD, and alsR genes involved in post-exponential-phase production of acetoin. J Bacteriol 175:3863–3875PubMedGoogle Scholar
  94. Reva O, Smirnov VV, Petterson B, Priest FG (2002) Bacillus endophyticus sp. nov., isolated from the inner tissues of cotton plants (Gossypium sp.). Int J Syst Evol Microbiol 52:101–107PubMedGoogle Scholar
  95. Reva ON, Dixelius C, Meijer J, Priest FG (2004) Taxonomic characterization and plant colonizing abilities of some bacteria related to Bacillus amyloliquefaciens and Bacillus subtilis. FEMS Microbiol Ecol 48:249–259PubMedCrossRefGoogle Scholar
  96. Roberts RJ, Wilson GA, Young FE (1977) Recognition sequence of specific endonuclease BamHI from Bacillus amyloliquefaciens H. Nature 265:82–84PubMedCrossRefGoogle Scholar
  97. Romero-Tabarez M, Jansen R, Sylla M, Lünsdorf H, Häußler S, Santosa DA, Timmis KN, Molinari G (2006) 7-O-malonyl macrolactin A, a new macrolactin antibiotic from Bacillus subtilis active against methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci and a small-colony variant of Burkholderia cepacia. Antimicrob Agents Chemother 50:1701–1709PubMedCrossRefGoogle Scholar
  98. Rudrappa T, Quinn WJ, Stanley-Wall NR, Bais HP (2007) A degradation product of the salicylic acid pathway triggers oxidative stress resulting in down-regulation of Bacillus subtilis biofilm formation on Arabidopsis thaliana roots. Planta 226:283–297PubMedCrossRefGoogle Scholar
  99. Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556PubMedCrossRefGoogle Scholar
  100. Ryu C-M, Farag MA, Hu C-H, Reddy M, Wei H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932PubMedCrossRefGoogle Scholar
  101. Ryu CM, Farag MA, Hu CH, Reddy M, Wei HX, Kloepper JW, Paré PW (2004a) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026PubMedCrossRefGoogle Scholar
  102. Ryu CM, Murphy JF, Mysore KS, Kloepper JW (2004b) Plant growth promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaicvirus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J 39:381–392PubMedCrossRefGoogle Scholar
  103. Ryu CM, Farag M, Paré PW, Kloepper JW (2005) Invisible signals from the underground: bacterial volatiles elicit plant growth promotion and induce systemic resistance. Plant Pathol J 2:7–12Google Scholar
  104. Schmiedeknecht G, Bochow H, Junge H (1998) Use of Bacillus subtilis as biocontrol agent. II. Biological control of potato diseases. J Plant Dis Prot 105:376–386Google Scholar
  105. Schmiedeknecht G, Issoufou I, Junge H, Bochow H (2001) Use of Bacillus subtilis as biocontrol agent. V. Biological control of disease on maize and sunflowers. J Plant Dis Prot 108:500–512Google Scholar
  106. Schneider K, Chen XH, Vater J, Franke P, Nicholson G, Borriss R, Süssmuth RD (2007) Macrolactin is the polyketide biosynthesis product of the pks2 cluster of Bacillus amyloliquefaciens FZB42. J Nat Prod 70:1417–1423PubMedCrossRefGoogle Scholar
  107. Seldin L, Soares Rosado A, daCruz DW, Nobrega A, vanElsas JD, Paiva E (1998) Comparison of Paenibacilus azotofixans strains isolated from rhizoplane, rhizosphere, and non-root-associated soil from maize planted in two different Brazilian soils. Appl Environ Microbiol 64:3860–3868PubMedGoogle Scholar
  108. Shishido M, Breuil C, Chanway CP (1999) Endophytic colonization of spruce by plant growth-promoting rhizobacteria. FEMS Microbiol Ecol 29:191–196CrossRefGoogle Scholar
  109. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56(4):845–857PubMedCrossRefGoogle Scholar
  110. Stein T, Vater J, Kruft V, Otto A, Wittmann-Liebold B, Franke P, Panico M, McDowell R, Morris HR (1996) The multiple carrier model of nonribosomal peptide biosynthesis at modular multienzymatic templates. J Biol Chem 271:15428–15435PubMedCrossRefGoogle Scholar
  111. Stein T, Borchert S, Conrad B, Feesche J, Hofemeister B, Hofemeister J, Entian KD (2002) Two different lantibiotic-like peptides originate from the ericin gene cluster of Bacillus subtilis A1/3. J Bacteriol 184:1703–1711PubMedCrossRefGoogle Scholar
  112. Steinmetz M (1993) Carbohydrate catabolism: enzymes, pathways, and evolution. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and other Gram-positive bacteria. ASM, Washington, DC, pp 157–170Google Scholar
  113. Timmusk S, Wagner EGH (1999) The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant Microbe Interact 12:951–959PubMedCrossRefGoogle Scholar
  114. Timmusk S, Grantcharova N, Wagner EGH (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol 71:7292–7300PubMedCrossRefGoogle Scholar
  115. Timmusk S, van West P, Gow NRA, Huffstutler RP (2009) Paenibacillus polymyxa antagonizes oomycete plant pathogens Phytophthora palmivora and Pythium aphanidermatum. J Appl Microbiol 106:1473–1481PubMedCrossRefGoogle Scholar
  116. 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, 2nd edn. CRC Press/Taylor & Francis Group, Boca Raton, FL, pp 1–21CrossRefGoogle Scholar
  117. Van Loon LC, Bakker PA, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483PubMedCrossRefGoogle Scholar
  118. Vandeputte O, Öden S, Mol A, Vereecke D, Goethals K, El Jaziri M, Prinsen E (2005) Biosynthesis of auxin by the gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infect plant tissues. Appl Environ Microbiol 71:1169–1177PubMedCrossRefGoogle Scholar
  119. Vanittanakom N, Loeffler W, Koch U, Jung G (1986) Fengycin – a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J Antibiot (Tokyo) 39:888–901CrossRefGoogle Scholar
  120. Walsh CT, Gehring AM, Weinreb PH, Quadri LEN, Flugel RS (1997) Post-translational modification of polyketide and nonribosomal peptide synthases. Curr Opin Chem Biol 1:309–315PubMedCrossRefGoogle Scholar
  121. Wolf M, Geczi A, Simon O, Borriss R (1995) Genes encoding xylan and β-glucan-hydrolysing enzymes in Bacillus subtilis: characterization, mapping and construction of strains deficient in lichenase, cellulose and xylanase. Microbiology 141:281–290PubMedCrossRefGoogle Scholar
  122. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4PubMedCrossRefGoogle Scholar
  123. Yao AV, Bochow H, Karimov S, Boturov U, Sanginboy S, Sharipov K (2006) Effect of FZB24 Bacillus subtilis as a biofertilizer on cotton yields in field tests. Arch Phytopathol Plant Prot 39:1–6CrossRefGoogle Scholar
  124. Zehnder GW, Murphy JF, Sikora EJ, Kloepper JW (2001) Application of rhizobacteria for induced resistance. Eur J Plant Pathol 107:39–50CrossRefGoogle Scholar
  125. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M et al (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851PubMedCrossRefGoogle Scholar
  126. Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant-growth promoting rhizobacteria for bioremediation. Environ Int 93:406–414CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Bacterial Genetics/Institute of BiologyHumboldt University BerlinBerlinGermany
  2. 2.ABiTEP GmbHBerlinGermany

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