Plant and Soil

, Volume 326, Issue 1–2, pp 437–452 | Cite as

Effects of genetically modified potatoes with increased zeaxanthin content on the abundance and diversity of rhizobacteria with in vitro antagonistic activity do not exceed natural variability among cultivars

  • Nicole Weinert
  • Remo Meincke
  • Christine Gottwald
  • Viviane Radl
  • Xia Dong
  • Michael Schloter
  • Gabriele Berg
  • Kornelia SmallaEmail author
Regular Article


To assess potential effects of genetically modified (GM) potatoes on the abundance and diversity of rhizobacteria with in vitro antagonistic activity in relation to natural variability among cultivars, two GM potato lines accumulating the carotenoid zeaxanthin in their tubers, the parental cultivar and four additional commercial cultivars were planted at two field sites in Germany. Rhizosphere samples were taken at three developmental stages of the plants. A total of 3,985 bacteria isolated from the rhizosphere were screened for their in vitro antagonistic activity towards Rhizoctonia solani, Verticillium dahliae and Phytophthora infestans using a dual-culture assay. Genotypic characterisation, 16S rRNA gene sequencing and antifungal metabolite analysis was performed to characterize the 595 antagonists obtained. The 16S rRNA gene-based identification of in vitro antagonists revealed strong site-dependent differences in their taxonomic composition. This study showed that the site was the overriding factor determining the proportion and diversity of antagonists from the rhizosphere of potato while the effect of the genetic modification on the proportion of antagonists obtained did not exceed natural variability among the five commercial cultivars tested.


Genetically modified potatoes In vitro antagonists BOX 16S rRNA gene 



This work was funded by grant 0313277B from the Bundesministerium für Bildung und Forschung. The authors thank U. Zimmerling, A. Büttner and G. Czeplie for valuable assistance in the lab and Dr. F. Niepold for providing the P. infestans isolate. We thank Dr. Holger Heuer and Dr. Siegfried Kropf for discussion in statistical questions. I.-M. Jungkurth is gratefully acknowledged for reading the manuscript. The authors would like to thank J. Dennert and F.X. Maidl (Technical University of Munich) for the perfect management of the experimental plots in Roggenstein and Oberviehhausen. The authors are highly thankful to G. Wenzel (Technical University of Munich) for providing the plant material of the transgenic lines.

Supplementary material

11104_2009_24_MOESM1_ESM.doc (1.3 mb)
Fig. S1 BOX-PCR fingerprints of in vitro antagonists identified as Pseudomonas fluorescens isolated from the potato rhizospheres in Roggenstein (A) and Oberviehhausen (B), respectively. ST = Standard (1 Kb Plus DNA Ladder). Strain code: cultivar/GM line (Bal = ‘Baltica’; SR47 = ‘Baltica’ co-suppression; SR48 = ‘Baltica’ antisense; Sel = ‘Selma’; Des = ‘Désirée’; Dit = ‘Ditta’; Sib = ‘Sibu’), sampling time (2 = EC60, 3 = EC90), number of replicate plot analysed (1 to 4). * of isolates that were obtained two times from the same plot and showed identical BOX patterns only one representative isolate is shown. (DOC 1,344 kb)
11104_2009_24_MOESM2_ESM.doc (1.2 mb)
Fig. S2 BOX-PCR profiles of in vitro antagonists identified as Bacillus pumilus isolated from the potato rhizospheres in Roggenstein and Oberviehhausen, respectively. (A) BOX-profiles of a subset of isolates from the potato rhizosphere in Roggenstein. (B) BOX-profiles displayed by the majority of isolates (68/80) identified as Bacillus pumilus isolated from the potato rhizosphere in Oberviehhausen. ST = Standard (1 Kb Plus DNA Ladder). Strain code: cultivar/GM line (Bal = ‘Baltica’; SR47 = ‘Baltica’ co-suppression; SR48 = ‘Baltica’ antisense; Sel = ‘Selma’; Des = ‘Désirée’; Dit = ‘Ditta’; Sib = ‘Sibu’); sampling time (2 = EC60, 3 = EC90), number of replicate plot analysed (1 to 4). * of isolates that were obtained several times from the same plot and showed identical BOX patterns only one representative isolate is shown. (DOC 1,275 kb)
11104_2009_24_MOESM3_ESM.doc (893 kb)
Fig. S3 BOX-profiles of isolates identified as Pectobacterium chrysanthemi (lanes 2–11), P. carotovorum (lanes 12–14) and P. atrosepticum (lane 15) from the potato rhizospheres in Roggenstein (R) and Oberviehhausen (O), respectively. ST = Standard (1 Kb Plus DNA Ladder). Strain code: cultivar/GM line (SR47 = ‘Baltica’ co-suppression; SR48 = ‘Baltica’ antisense; Des = ‘Désirée’; Dit = ‘Ditta’), sampling time (2 = EC60, 3 = EC90), number of replicate plot analysed (1 to 4). * of isolates that were obtained several times from the same plot and showed identical BOX patterns only one representative isolate is shown. (DOC 892 kb)
11104_2009_24_MOESM4_ESM.doc (94 kb)
Table S1 Proportions of in vitro antagonistic isolates in the potato rhizospheres of the sampling site in Roggenstein (A) and Oberviehhausen (B) towards Rhizoctonia solani AG3, Verticillium dahliae ELV25 and Phytophthora infestans as determined by dual-culture assays. (DOC 93 kb)
11104_2009_24_MOESM5_ESM.doc (1.1 mb)
Table S2 Phylogenetic affiliation of identified in vitro antagonists from both sampling sites determined by partial 16S rRNA gene sequence analysis. Numbers in parenthesis indicate the numbers of isolates that were identified based on the same BOX-fingerprint (>85% similarity). Rog = Roggenstein, Ovh = Oberviehhhausen; EC60 = flowering plants, EC90 = senescent plants; Bal = ‘Baltica’, SR47 = ‘Baltica’ co-suppression, SR48 = ‘Baltica’ antisense, Sel = ‘Selma’, Des = ‘Désirée’, Dit = ‘Ditta’, Sib = ‘Sibu’. Numbers following the cultivar/GM line indicate the plot (1 to 4). (DOC 1,098 kb)


  1. Adams PD, Kloepper JW (2002) Effect of host genotype on indigenous bacterial endophytes of cotton (Gossypium hirsutum L.). Plant Soil 240:181–198. doi: 10.1023/A:1015840224564 CrossRefGoogle Scholar
  2. Berg G, Kurze S, Buchner A, Wellington EM, Smalla K (2000) Successful strategy for the selection of new strawberry-associated rhizobacteria antagonistic to Verticillium wilt. Can J Microbiol 46:1128–1137. doi: 10.1139/cjm-46-12-1128 CrossRefPubMedGoogle Scholar
  3. Berg G, Fritze A, Roskot N, Smalla K (2001) Evaluation of potential biocontrol rhizobacteria from different host plants of Verticillium dahliae Kleb. J Appl Microbiol 91:963–971. doi: 10.1046/j.1365-2672.2001.01462.x CrossRefPubMedGoogle Scholar
  4. 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. doi: 10.1128/AEM.68.7.3328-3338.2002 CrossRefPubMedGoogle Scholar
  5. 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. doi: 10.1111/j.1574-6941.2005.00025.x CrossRefPubMedGoogle Scholar
  6. Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350Google Scholar
  7. Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12. doi: 10.1007/s002489900087 CrossRefPubMedGoogle Scholar
  8. Brimecombe MJ, de Leij FAAM, Lynch JM (2001) The effect of root exudates on rhizosphere microbial populations. In: Pinton R, Varanini R, Nannipieri P (eds) The rhizosphere. Marcel Dekker, New York, pp 95–140Google Scholar
  9. Chernin L, Chet I (2002) Microbial enzymes in biocontrol of plant pathogens and pests. In: Burns R, Dick R (eds) Enzymes in the environment: activity, ecology, and applications. Marcel Dekker, New York, pp 171–225Google Scholar
  10. Cho J-C, Tiedje JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66:5448–5456. doi: 10.1128/AEM.66.12.5448-5456.2000 CrossRefPubMedGoogle Scholar
  11. Cornelis P, Matthijs S (2002) Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ Microbiol 4:787–798. doi: 10.1046/j.1462-2920.2002.00369.x CrossRefPubMedGoogle Scholar
  12. Costa R, Falcão Salles J, Berg G, Smalla K (2006) Cultivation-independent analysis of Pseudomonas species in soil and in the rhizosphere of field-grown Verticillium dahliae host plants. Environ Microbiol 8:2136–2149. doi: 10.1111/j.1462-2920.2006.01096.x CrossRefPubMedGoogle Scholar
  13. Crecchio C, Ambrosoli R, Gelsomino A, Minati JL, Ruggiero P (2004) Functional and molecular responses of soil microbial communities under differing soil management practices. Soil Biol Biochem 36:1873–1883. doi: 10.1016/j.soilbio.2004.05.008 CrossRefGoogle Scholar
  14. De Boer M, Bom P, Kindt F, Keurentjes JJB, van der Sluis I, van Loon LC, Bakker PAHM (2003) Control of Fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms. Phytopathology 93:626–632. doi: 10.1094/PHYTO.2003.93.5.626 CrossRefPubMedGoogle Scholar
  15. Donegan KK, Palm CJ, Fieland VJ, Porteous LA, Ganio LM, Schaller DL, Bucao LQ, Seidler RJ (1995) Changes in levels, species and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. kurstaki endotoxin. Appl Soil Ecol 2:111–124. doi: 10.1016/0929-1393(94)00043-7 CrossRefGoogle Scholar
  16. Dunfield KE, Germida JJ (2001) Diversity of bacterial communities in the rhizosphere and root interior of field-grown genetically modified Brassica napus. FEMS Microbiol Ecol 38:1–9. doi: 10.1111/j.1574-6941.2001.tb00876.x CrossRefGoogle Scholar
  17. Dunfield KE, Germida JJ (2003) Seasonal changes in the rhizosphere microbial communities associated with field-grown genetically modified canola (Brassica napus). Appl Environ Microbiol 69:7310–7318. doi: 10.1128/AEM.69.12.7310-7318.2003 CrossRefPubMedGoogle Scholar
  18. Fravel DR (1988) Role of antibiosis in the biocontrol of plant diseases. Annu Rev Phytopathol 26:75–91Google Scholar
  19. Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809. doi: 10.1128/AEM.69.3.1800-1809.2003 CrossRefPubMedGoogle Scholar
  20. Griffiths BS, Geoghegan IE, Robertson WM (2000) Testing genetically engineered potato, producing the lectins GNA and ConA, on non-target soil organisms and processes. J Appl Ecol 37:159–170. doi: 10.1046/j.1365-2664.2000.00481.x CrossRefGoogle Scholar
  21. Gyamfi S, Pfeifer U, Stierschneider M, Sessitsch A (2002) Effects of transgenic glufosinate-tolerant oilseed rape (Brassica napus) and the associated herbicide application on eubacterial and Pseudomonas communities in the rhizosphere. FEMS Microbiol Ecol 41:181–190. doi: 10.1111/j.1574-6941.2002.tb00979.x CrossRefPubMedGoogle Scholar
  22. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent Pseudomonads. Nat Rev Microbiol 3:307–319. doi: 10.1038/nrmicro1129 CrossRefPubMedGoogle Scholar
  23. Hack H, Gal H, Klemke T, Klose R, Meier U, Stauß R, Witzenberger A (1993) Phänologische Entwicklungsstadien der Kartoffel (Solanum tuberosum L.). Nachrichtenbl Deut Pflanzenschutzd 45:11–19Google Scholar
  24. Hélias V, Andrivon D, Jouan B (2000) Internal colonization pathways of potato plants by Erwinia carotovora ssp. atroseptica. Plant Pathol 49:33–42. doi: 10.1046/j.1365-3059.2000.00431.x CrossRefGoogle Scholar
  25. Heuer H, Kroppenstedt RM, Lottmann J, Berg G, Smalla K (2002) Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl Environ Microbiol 68:1325–1335. doi: 10.1128/AEM.68.3.1325-1335.2002 CrossRefPubMedGoogle Scholar
  26. Hiltner L (1904) Über neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter besonderer Berücksichtigung der Gründüngung und Brache. Arb DLG 98:59–78Google Scholar
  27. Hollomon DW (1965) A medium for the direct isolation of Phytophthora infestans. Plant Pathol 14:34–35. doi: 10.1111/j.1365-3059.1965.tb00617.x CrossRefGoogle Scholar
  28. James C (2007) Global status of commercialized Biotech/GM crops: 2007. ISAAA Brief No. 37. ISAAA, Ithaca, NY.Google Scholar
  29. Juhnke ME, Mathre DE, Sands DC (1987) Identification and characterization of rhizosphere-competent bacteria of wheat. Appl Environ Microbiol 53:2793–2799PubMedGoogle Scholar
  30. Kennedy NM, Gleeson DE, Connolly J, Clipson NJW (2005) Seasonal and management influences on bacterial community structure in an upland grassland soil. FEMS Microbiol Ecol 53:329–337. doi: 10.1016/j.femsec.2005.01.013 CrossRefPubMedGoogle Scholar
  31. Kloepper JW, Ryu C-M, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266. doi: 10.1094/PHYTO.2004.94.11.1259 CrossRefPubMedGoogle Scholar
  32. Kotoujansky A (1987) Molecular genetics of pathogenesis by soft-rot Erwinias. Annu Rev Phytopathol 25:405–430. doi: 10.1146/ CrossRefGoogle Scholar
  33. Krechel A, Faupel A, Hallmann J, Ulrich A, Berg G (2002) Potato-associated bacteria and their antagonistic potential towards plant-pathogenic fungi and the plant-parasitic nematode Meloidogyne incognita (Kofoid & White) Chitwood. Can J Microbiol 48:772–786. doi: 10.1139/w02-071 CrossRefPubMedGoogle Scholar
  34. Latour X, Philippot L, Corberand T, Lemanceau P (1999) The establishment of an introduced community of fluorescent pseudomonads in the soil and in the rhizosphere is affected by the soil type. FEMS Microbiol Ecol 30:163–170. doi: 10.1111/j.1574-6941.1999.tb00645.x CrossRefPubMedGoogle Scholar
  35. Lemanceau P, Bakker PAHM, de Kogel WJ, Alabouvette C, Schippers B (1992) Effect of pseudobactin 358 production by Pseudomonas putida WCS358 on suppression of Fusarium wilt of carnations by nonpathogenic Fusarium oxysporum Fo47. Appl Environ Microbiol 58:2978–2982PubMedGoogle Scholar
  36. Leong J (1986) Siderophores: their biochemistry and possible role in the biocontrol of plant pathogens. Annu Rev Phytopathol 24:187–209. doi: 10.1146/ CrossRefGoogle Scholar
  37. Lifshitz R, Simonson C, Scher FM, Kloepper JW, Rodrick-Semple C, Zaleska I (1985) Effect of rhizobacteria on the severity of Phytophthora root rot of soybean. Can J Plant Pathol 8:102–106Google Scholar
  38. Liu X, Bimerew M, Ma Y, Müller H, Ovadis M, Eberl L, Berg G, Chernin L (2007) Quorum-sensing signaling is required for production of the antibiotic pyrrolnitrin in a rhizospheric biocontrol strain of Serratia plymuthica. FEMS Microbiol Lett 270:299–305. doi: 10.1111/j.1574-6968.2007.00681.x CrossRefPubMedGoogle Scholar
  39. Lottmann J, Berg G (2001) Phenotypic and genotypic characterization of antagonistic bacteria associated with roots of transgenic and non-transgenic potato plants. Microbiol Res 156:75–82. doi: 10.1078/0944-5013-00086 CrossRefPubMedGoogle Scholar
  40. Lottmann J, Heuer H, Smalla K, Berg G (1999) Influence of transgenic T4-lysozyme-producing potato plants on potentially beneficial plant-associated bacteria. FEMS Microbiol Ecol 29:365–377. doi: 10.1111/j.1574-6941.1999.tb00627.x CrossRefGoogle Scholar
  41. Lottmann J, Heuer H, de Vries J, Mahn A, Düring 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. doi: 10.1111/j.1574-6941.2000.tb00725.x CrossRefPubMedGoogle Scholar
  42. Lugtenberg BJJ, Dekkers LC, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490. doi: 10.1146/annurev.phyto.39.1.461 CrossRefPubMedGoogle Scholar
  43. Malajczuk N (1983) Microbial antagonism to Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (ed) Phytophthora: its biology, taxonomy, ecology, and pathology. APS Press, pp 197–218Google Scholar
  44. Marilley L, Vogt G, Blanc M, Aragno M (1998) Bacterial diversity in the bulk soil and rhizosphere fractions of Lolium perenne and Trifolium repens as revealed by PCR restriction analysis of 16S rDNA. Plant Soil 198:219–224. doi: 10.1023/A:1004309008799 CrossRefGoogle Scholar
  45. Marschner P, Yang C-H, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445. doi: 10.1016/S0038-0717(01) 00052-9 CrossRefGoogle Scholar
  46. McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GSAB, Williams P (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiol 143:3703–3711CrossRefGoogle Scholar
  47. Mercado-Blanco J, Bakker PAHM (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 92:367–389. doi: 10.1007/s10482-007-9167-1 CrossRefPubMedGoogle Scholar
  48. Meyer J-M, Geoffroy VA, Baida N, Gardan L, Izard D, Lemanceau P, Achouak W, Palleroni NJ (2002) Siderophore typing, a powerful tool for the identification of fluorescent and nonfluorescent Pseudomonads. Appl Environ Microbiol 68:2745–2753. doi: 10.1128/AEM.68.6.2745-2753.2002 CrossRefPubMedGoogle Scholar
  49. O’Sullivan D, O’Gara F (1992) Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiol Rev 56:662–676PubMedGoogle Scholar
  50. Pérombelon MCM (2002) Potato diseases caused by soft rot Erwinias: an overview of pathogenesis. Plant Pathol 51:1–12. doi: 10.1046/j.0032-0862.2001 CrossRefGoogle Scholar
  51. Picard C, Bosco M (2008) Genotypic and phenotypic diversity in populations of plant-probiotic Pseudomonas spp. colonizing roots. Naturwissenschaften 95:1–16. doi: 10.1007/s00114-007-0286-3 CrossRefPubMedGoogle Scholar
  52. Raaijmakers JM, van der Sluis I, Koster M, Bakker PAHM, Weisbeek PJ, Schippers B (1995) Utilization of heterologous siderophores and rhizosphere competence of fluorescent Pseudomonas spp. Can J Microbiol 41:126–135CrossRefGoogle Scholar
  53. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2008) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 2008. doi: 10.1007/s11104-008-9568-6
  54. Rademaker JLW, de Bruijn FJ (1997) Characterization and classification of microbes by REP-PCR genomic fingerprinting and computer-assisted pattern analysis. In: Caetano-Anollés G, Gresshoff PM (eds) DNA-markers: protocols, applications and overviews. Wiley, New York, N.Y, pp 151–171Google Scholar
  55. Rasche F, Hödl V, Poll C, Kandeler E, Gerzabek MH, van Elsas JD, Sessitsch A (2006) Rhizosphere bacteria affected by transgenic potatoes with antibacterial activities compared with the effects of soil, wild-type potatoes, vegetation stage and pathogen exposure. FEMS Microbiol Ecol 56:219–235. doi: 10.1111/j.1574-6941.2005.00027.x CrossRefPubMedGoogle Scholar
  56. Römer S, Lübeck J, Kauder F, Steiger S, Adomat C, Sandmann G (2002) Genetic engineering of zeaxanthin-rich potato by antisense inactivation and co-suppression of carotenoid epoxidation. Metab Eng 4:263–272. doi: 10.1006/mben.2002.0234 CrossRefPubMedGoogle Scholar
  57. Sari E, Etebarian HR, Roustaei A, Aminian H (2006) Biological control of Geaumannomyces graminis on wheat with Bacillus spp. J Plant Pathol 5:307–314. doi: 10.3923/ppj.2006.307.314 CrossRefGoogle Scholar
  58. Sari E, Etebarian HR, Aminian H (2007) The effects of Bacillus pumilus, isolated from wheat rhizosphere, on resistance in wheat seedling roots against the take-all fungus, Geaumannomyces graminis var. tritici. J Phytopathol 155:720–727. doi: 10.1111/j.1439-0434.2007.01306.x CrossRefGoogle Scholar
  59. Schisler DA, Slininger PJ, Behle RW, Jackson MA (2004) Formulation of Bacillus spp. for biological control of plant diseases. Phytopathology 94:1267–1271. doi: 10.1094/PHYTO.2004.94.11.1267 CrossRefPubMedGoogle Scholar
  60. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56. doi: 10.1016/0003-2697(87) 90612-9 CrossRefPubMedGoogle Scholar
  61. Sessitsch A, Weilharter A, Gerzabek MH, Kirchmann H, Kandeler E (2001) Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl Environ Microbiol 67:4215–4224. doi: 10.1128/AEM.67.9.4215-4224.2001 CrossRefPubMedGoogle Scholar
  62. Siciliano SD, Germida JJ (1999) Taxonomic diversity of bacteria associated with the roots of field-grown transgenic Brassica napus cv. Quest, compared to the non-transgenic B. napus cv. Excel and B. rapa cv. Parkland. FEMS Microbiol Ecol 29:263–272. doi: 10.1111/j.1574-6941.1999.tb00617.x CrossRefGoogle Scholar
  63. Siciliano SD, Theoret CM, de Freitas JR, Hucl PJ, Germida JJ (1998) Differences in the microbial communities associated with the roots of different cultivars of canola and wheat. Can J Microbiol 44:844–851. doi: 10.1139/cjm-44-9-844 CrossRefGoogle Scholar
  64. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751. doi: 10.1128/AEM.67.10.4742-4751.2001 CrossRefPubMedGoogle Scholar
  65. Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483. doi: 10.1146/annurev.phyto.36.1.453 CrossRefPubMedGoogle Scholar
  66. Weissburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703Google Scholar
  67. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407. doi: 10.1146/ CrossRefGoogle Scholar
  68. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511PubMedGoogle Scholar
  69. Winson KW, Swift S, Fish L, Throup JP, Jorgensen F, Chhabra SR, Bycroft BW, Williams P, Stewart GSAB (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163:185–192. doi: 10.1111/j.1574-6968.1998.tb13044.x CrossRefPubMedGoogle Scholar
  70. Yan Z, Reddy MS, Ryu C-M, McInroy JA, Wilson M, Kloepper JW (2002) Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92:1329–1333. doi: 10.1094/PHYTO. CrossRefPubMedGoogle Scholar
  71. Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microbiol 66:345–351. doi: 10.1128/AEM.66.1.345-351.2000 CrossRefPubMedGoogle Scholar
  72. Yuan WM, Crawford DL (1995) Characterization of Streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and seed rots. Appl Environ Microbiol 61:3119–3128PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Nicole Weinert
    • 1
  • Remo Meincke
    • 2
  • Christine Gottwald
    • 1
  • Viviane Radl
    • 3
  • Xia Dong
    • 4
  • Michael Schloter
    • 3
  • Gabriele Berg
    • 2
  • Kornelia Smalla
    • 1
    Email author
  1. 1.Julius Kühn-Institute - Federal Research Centre for Cultivated Plants (JKI)Institute for Epidemiology and Pathogen DiagnosticsMessewegGermany
  2. 2.Environmental BiotechnologyGraz University of TechnologyGrazAustria
  3. 3.Department for Terrestrial EcogeneticsHelmholtz Zentrum MünchenOberschleissheimGermany
  4. 4.Technical University of MunichChair for Plant BreedingFreisingGermany

Personalised recommendations