Soil type dependent rhizosphere competence and biocontrol of two bacterial inoculant strains and their effects on the rhizosphere microbial community of field-grown lettuce

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Schreiter, Susanne ^a,b   Sandmann, Martin ^b   Smalla, Kornelia ^a   Grosch, Rita ^b  

^a INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^b Inst Veg Orn Crops G Erfurt   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RIFAMPICIN; RNA 16S; BACTERIAL RNA;

16S RRNA GENE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BIOLOGICAL PEST CONTROL; COLONY FORMING UNIT; CONTROLLED STUDY; CROPPING SYSTEM; DENATURING GRADIENT GEL ELECTROPHORESIS; DISEASE SEVERITY; FUNGAL PLANT DISEASE; GENE AMPLIFICATION; LETTUCE; MICROBIAL COMMUNITY; NONHUMAN; PLANT ROOT; PSEUDOMONAS; PSEUDOMONAS JESSENII; RHIZOCTONIA SOLANI; RHIZOSPHERE BACTERIUM; SERRATIA PLYMUTHICA; SOIL INOCULATION; SOIL MICROFLORA; SOIL PROPERTY; WEATHER; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL CONSORTIUM; MICROBIOLOGY; PHYSIOLOGY; RHIZOSPHERE; SERRATIA;

DNA, BACTERIAL; LETTUCE; MICROBIAL CONSORTIA; PSEUDOMONAS; RHIZOSPHERE; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SERRATIA; SOIL MICROBIOLOGY;

EID: 84905460208     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103726     Document Type: Article

References (57)

1. Oerke EC (2006) Crop losses to pests. J Agr Sci 144: 31-43.
2. Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: the European situation. Eur J Plant Pathol 114: 329-341. (Pubitemid 43881425)
3. Leistra M, Matser AM (2004) Adsorption, transformation, and bioavailability of the fungicides carbendazim and iprodione in soil, alone and in combination. J Environ Sci Heal B 39: 1-17. (Pubitemid 38294957)
4. Wang YS, Wen CY, Chiu TC, Yen JH (2004) Effect of fungicide iprodione on soil bacterial community. Ecotox Environ Safe 59: 127-132.
5. Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40: 309-348. (Pubitemid 35235584)
6. Kazempour MN (2004) Biological control of Rhizoctonia solani, the causal agent of rice sheath blight by antagonistics bacteria in greenhouse and field conditions. Plant Pathol J 3: 88-96.
7. 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 microorganisms. FEMS Microbiol Ecol 64: 106-116. (Pubitemid 351365091)
8. Tikhonovich IA, Provorov NA (2011) Microbiology is the basis of sustainable agriculture: an opinion. Ann Appl Biol 159: 155-168.
9. Quinlan RJ, Lisansky SG (2010) North America: Biopesticides Market. CPL Business Consultants, Oxfordshire, UK.
10. Mark GL, Morrissey JP, Higgins P, O'Gara F (2006) Molecular-based strategies to exploit Pseudomonas biocontrol strains for environmental biotechnology applications. FEMS Microbiol Ecol 56: 167-177.
11. Barret M, Morrissey JP, O'Gara F (2011) Functional genomics analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence. Biol Fert Soils 47: 729-743.
12. Pierson III LS, Pierson EA (1996) Phenazine antibiotic production in Pseudomonas aureofaciens: role in rhizosphere ecology and pathogen suppression. FEMS Microbiol Lett 136: 101-108. (Pubitemid 26080356)
13. Steidle A, Allesen-Holm M, Riedel K, Berg G, Givskov M, et al. (2002) Identification and characterization of an N-acylhomoserine lactone-dependent quorum-sensing system in Pseudomonas putida strain IsoF. Appl Environ Microbiol 68: 6371-6382. (Pubitemid 36342474)
14. De Bellis P, Ercolani GL (2001) Growth interactions during bacterial colonization of seedling rootlets. Appl Environ Microbiol 67: 1945-1948. (Pubitemid 33644970)
15. Ghirardi S, Dessaint F, Mazurier S, Corberand T, Raaijmakers JM, et al. (2012) Identification of traits shared by rhizosphere-competent strains of fluorescent Pseudomonads. Microb Ecol 64: 725-737.
16. Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4: 343-350. (Pubitemid 32620718)
17. Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39: 461-493.
18. Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant-rhizobacteria interactions. Plant Cell Enviro 26: 189-199. (Pubitemid 36251203)
19. Schnider U, Keel C, Blumer C, Troxler J, Defago G, et al. (1995) Amplification of the housekeeping sigma-factor in Pseudomonas fluorescens CHA0 enhances antibiotic production and improves biocontrol abilities. J Bacteriol 177: 5387-5392.
20. Dekkers LC, Mulders IHM, Phoelich CC, Chin-A-Woeng TFC, Wijfjes AHM, et al. (2000) The sss colonization gene of the tomato-Fusarium oxysporum f. sp radicis-lycopersici biocontrol strain Pseudomonas fluorescens WCS365 can improve root colonization of other wild-type Pseudomonas spp. bacteria. Mol Plant Microbe In 13: 1177-1183.
21. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68: 3795-3801. (Pubitemid 34836687)
22. Loper JE, Hassan KA, Mavrodi DV, Davis EW, II, Lim C, et al. (2012) Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet 8: e1002784-e1002784.
23. Raaijmakers JM, Mazzola M (2012) Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu Rev Phytopathol 50: 403-424.
24. Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent Pseudomonads. Nat Rev Microbiol 3: 307-319. (Pubitemid 40443724)
25. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321: 341-361.
26. Capdevila S, Martinez-Granero FM, Sanchez-Contreras M, Rivilla R, Martin M (2004) Analysis of Pseudomonas fluorescens F113 genes implicated in flagellar filament synthesis and their role in competitive root colonization. Microbiol-Uk 150: 3889-3897. (Pubitemid 39545333)
27. Rodriguez-Navarro DN, Dardanelli MS, Ruiz-Sainz JE (2007) Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272: 127-136. (Pubitemid 47074607)
28. Mavrodi DV, Joe A, Mavrodi OV, Hassan KA, Weller DM, et al. (2011) Structural and functional analysis of the type III secretion system from Pseudomonas fluorescens q8r1-96. J Bacteriol 193: 177-189.
29. Lottmann J, Heuer H, de Vries J, Mahn A, Düring K, et al. (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. (Pubitemid 30462291)
30. Chowdhury SP, Dietel K, Randler M, Schmid M, Junge H, et al. (2013) Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community. PLoS ONE 8: e68818-e68818. doi:10.1371/journal.pone.0068818.
31. Adesina MF, Lembke A, Costa R, Speksnijder A, Smalla K (2007) Screening of bacterial isolates from various European soils for in vitro antagonistic activity towards Rhizoctonia solani and Fusarium oxysporum: Site-dependent composition and diversity revealed. Soil Biol Biochem 39: 2818-2828. (Pubitemid 47238911)
32. Grosch R, Faltin F, Lottmann J, Kofoet A, Berg G (2005) Effectiveness of 3 antagonistic bacterial isolates to control Rhizoctonia solani Kühn on lettuce and potato. Can J Microbiol 51: 345-353. (Pubitemid 41176360)
33. Wibberg D, Jelonek L, Rupp O, Hennig M, Eikmeyer F, et al. (2013) Establishment and interpretation of the genome sequence of the phytopathogenic fungus Rhizoctonia solani AG1-IB isolate 7/3/14. J Biotechnol 167: 142-155.
34. 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.
35. Berg G, Krechel A, Ditz M, Sikora RA, Ulrich A, et al. (2005) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51: 215-229. (Pubitemid 40038381)
36. Rühlmann J, Ruppel S (2005) Effects of organic amendments on soil carbon content and microbial biomass-results of the long-term box plot experiment in Grossbeeren. Arch Agron Soil Sci 51: 163-170. (Pubitemid 41674109)
37. Schreiter S, Ding G-C, Heuer H, Neumann G, Sandmann M, et al. (2014) Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front Microbiol 5: 144.
38. Gutezeit B, Herzog FN, Wenkel KO (1993) Das Beregnungsbedarfssystem für Freilandgemüse. Gemüse 29: 106-108.
39. Grosch R, Schneider JHM, Kofoet A, Feller C (2011) Impact of continuous cropping of lettuce on the disease dynamics of bottom rot and genotypic diversity of Rhizoctonia solani AG 1-IB. J Phytopathol 159: 35-44.
40. Schneider JHM, Schilder MT, Dijst G (1997) Characterization of Rhizoctonia solani AG 2 isolates causing bare patch in field grown tulips in the Netherlands. Eur J Plant Pathol 103: 265-279. (Pubitemid 27210763)
41. Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63: 3233-3241. (Pubitemid 27337820)
42. Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NCM, et al. (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microbiol 75: 3859-3865.
43. Kropf S, Heuer H, Grüning M, Smalla K (2004) Significance test for comparing complex microbial community fingerprints using pairwise similarity measures. J Microbiol Meth 57: 187-195. (Pubitemid 38446864)
44. Neumann G, Bott S, Ohler M, Mock H, Lippman R, et al. (2014) Root exudation and root development of lettuce (Lactuca sativa L. cv. Tizian) as affected by different soils. Front Microbiol 5: 2.
45. Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173: 600-610. (Pubitemid 46096096)
46. Henry S, Texier S, Hallet S, Bru D, Dambreville C, et al. (2008) Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environ Microbiol 10: 3082-3092.
47. Benizri E, Nguyen C, Piutti S, Slezack-Deschaumes S, Philippot L (2007) Additions of maize root mucilage to soil changed the structure of the bacterial community. Soil Biol Biochem 39: 1230-1233. (Pubitemid 46349212)
48. Götz M, Gomes NCM, Dratwinski A, Costa R, Berg G, et al. (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.
49. Grosch R, Dealtry S, Schreiter S, Berg G, Mendonça-Hagler L, et al. (2012) Biocontrol of Rhizoctonia solani: complex interaction of biocontrol strains, pathogen and indigenous microbial community in the rhizosphere of lettuce shown by molecular methods. Plant Soil 361: 343-357.
50. Baudoin E, Benizri E, Guckert A (2002) Impact of growth stage on the bacterial community structure along maize roots, as determined by metabolic and genetic fingerprinting. Appl Soil Ecol 19: 135-145. (Pubitemid 34122438)
51. Bull CT, Weller DM, Thomashow LS (1991) Relationship between root colonization and suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens strain 2-79. Phytopathology 81: 954-959.
52. Raaijmakers JM, Weller DM (2001) Exploiting genotypic diversity of 2,4-diacetylphloroglucinol-producing Pseudomonas spp.: Characterization of superior root-colonizing P. fluorescens strain Q8r1-96. Appl Environ Microbiol 67: 2545-2554. (Pubitemid 33639725)
53. Lemanceau P, Alabouvette C (1993) Suppression of fusarium-wilt by fluorescent pseudomonads: Mechanisms and applications. Biocontrol Sci Techn 3: 219-234.
54. Steinberg C, Edel-Hermann V, Alabouvette C, Lemanceau P (2007) Soil suppressiveness to plant diseases. Modern Soil Microbiology: 455-478.
55. Gomes NCM, Kosheleva IA, Abraham WR, Smalla K (2005) Effects of the inoculant strain Pseudomonas putida KT2442 (pNF142) and of naphthalene contamination on the soil bacterial community. FEMS Microbiol Ecol 54: 21-33. (Pubitemid 41138018)
56. Davis R, Subbarao K, Raid R, Kurtz E (1997) Compendium of Lettuce Diseases. APS Press: 15-16.
57. Heuer H, Wieland G, Schönfeld J, Schönwalder A, Gomes NCM, et al. (2001) Bacterial community profiling using DGGE or TGGE analysis; Rochelle PA, editor. 177-190 p.