Development of a real-time PCR method to quantify the PGPR strain Azospirillum lipoferum CRT1 on maize seedlings

Soil Biology and Biochemistry

Volumn 42, Issue 12, 2010, Pages 2298-2305

  Couillerot, Olivier ^a,b,c   Bouffaud, Marie Lara ^a,b,c   Baudoin, Ezékiel ^a,b,c,e   Muller, Daniel ^a,b,c   Caballero Mellado, Jesus ^d   Moënne Loccoz, Yvan ^a,b,c  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c University of Lyon   (France)

^d INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

^e LABORATOIRE DES SYMBIOSES TROPICALES ET MÉDITERRANÉENNES   (France)

Author keywords

Azospirillum; Inoculant quantification; PGPR; Real time PCR; Root colonization

Indexed keywords

DNA; SOILS;

AZOSPIRILLUM; INOCULANT QUANTIFICATION; PGPR; REAL-TIME PCR; ROOT COLONIZATION;

POLYMERASE CHAIN REACTION;

BACTERIUM; DENSITY DEPENDENCE; MAIZE; MITOCHONDRIAL DNA; NITROGEN FIXATION; POLYMERASE CHAIN REACTION; REAL TIME; RHIZOSPHERE; ROOT COLONIZATION; SEEDLING;

AZOSPIRILLUM; AZOSPIRILLUM LIPOFERUM; ZEA MAYS;

EID: 78650187269     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2010.09.003     Document Type: Article

References (53)

1. Baudoin E., Couillerot O., Spaepen S., Moënne-Loccoz Y., Nazaret S. Applicability of the 16S-23S rDNA internal spacer for PCR detection of the phytostimulatory PGPR inoculant Azospirillum lipoferum CRT1 in field soil. Journal of Applied Microbiology 2010, 108:25-38.
2. Baudoin E., Nazaret S., Mougel C., Ranjard L., Moënne-Loccoz Y. Impact of inoculation with the phytostimulatory PGPR Azospirillum lipoferum CRT1 on the genetic structure of the rhizobacterial community of field-grown maize. Soil Biology and Biochemistry 2009, 41:409-413.
3. Blaha D., Prigent-Combaret C., Mirza M.S., Moënne-Loccoz Y. Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiology Ecology 2006, 56:455-470.
4. Braid M.D., Daniels L.M., Kitts C.L. Removal of PCR inhibitors from soil DNA by chemical flocculation. Journal of Microbiological Methods 2003, 52:389-393.
5. Bruce K.D., Strike P., Ritchie D.A. DNA extraction from natural environments. Environmental Monitoring of Bacteria 1999, 97-107. Springer - Humana press, Heidelberg.
6. Charyulu P.B.B.N., Foucassie F., Barbouche A.K., Rondro Harisoa L., Omar A.M.N., Marie R., Balandreau J. Field inoculation of rice using in vitro selected bacterial and plant genotypes. Azospirillum III: Genetics, Physiology, Ecology 1985, 163-179. Springer-Verlag, Heidelberg.
7. Cook K.L., Britt J.S. Optimization of methods for detecting Mycobacterium avium subsp. paratuberculosis in environmental samples using quantitative, real-time PCR. Journal of Microbiological Method 2007, 69:154-160.
8. Couillerot O., Poirier M.-A., Prigent-Combaret C., Mavingui P., Caballero-Mellado J., Moënne-Loccoz Y. Assessment of SCAR markers to design real-time PCR primers for rhizosphere quantification of Azospirillum brasilense phytostimulatory inoculants of maize. Journal of Applied Microbiology 2010, 109:528-538.
9. Creus C.M., Graziano M., Casanovas E.M., Pereyra M.A., Simontacchi M., Puntarulo S., Barassi C.A., Lamattina L. Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 2005, 221:297-303.
10. Dandie C.E., Miller M.N., Burton D.L., Zebarth B.J., Trevors J.T., Goyer C. Nitric oxide reductase-targeted real-time PCR quantification of denitrifier populations in soil. Applied and Environmental Microbiology 2007, 73:4250-4258.
11. Dobbelaere S., Croonenborghs A., Amber T., Ptacek D., Vanderleyden J., Dutto P., Labandera-Gonzalez C., Caballero-Mellado J., Aguirre J.F., Kapulnik Y., Shimon B., Burdman S., Kadouri D., Sarig S., Okon Y. Responses of agronomically important crops to inoculation with Azospirillum. Australian Journal of Plant Physiology 2001, 28:1-9.
12. Dobbelaere S., Vanderleyden J., Okon Y. Plant growth-promoting effects of diazotrophs in the rhizosphere. Critical Review in Plant Sciences 2003, 22:107-149.
13. El Zemrany H., Cortet J., Peter Lutz M., Chabert A., Baudoin E., Haurat J., Maughan N., Felix D., Défago G., Bally R., Moënne-Loccoz Y. Field survival of the phytostimulator Azospirillum lipoferum CRT1 and functional impact on maize crop, biodegradation of crop residues, and soil faunal indicators in a context of decreasing nitrogen fertilisation. Soil Biology and Biochemistry 2006, 38:1712-1726.
14. Fages J., Mulard D. Isolement de bactéries rhizosphériques et effet de leur inoculation en pots chez Zea mays. Agronomie 1988, 8:309-314.
15. Fuentes-Ramirez L., Caballero-Mellado J. Bacterial Biofertilizers. PGPR: Biocontrol and Biofertilization 2006, 143-172. Springer-Verlag, Heidelberg.
16. Gobbin D., Rezzonico F., Gessler C. Quantification of the biocontrol agent Pseudomonas fluorescens Pf-153 in soil using a quantitative competitive PCR assay unaffected by variability in cell lysis- and DNA-extraction efficiency. Soil Biology and Biochemistry 2007, 39:1609-1619.
17. Henry S., Bru D., Stres B., Hallet S., Philippot L. Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Applied and Environmental Microbiology 2006, 72:5181-5189.
18. Jacoud C., Faure D., Wadoux P., Bally R. Development of a strain-specific probe to follow inoculated Azospirillum lipoferum CRT1 under field conditions and enhancement of maize root development by inoculation. FEMS Microbiology Ecology 1998, 27:43-51.
19. Jacoud C., Job D., Wadoux P., Bally R. Initiation of root growth stimulation by Azospirillum lipoferum CRT1 during maize seed germination. Canadian Journal of Microbiology 1999, 45:339-342.
20. James E.K. Nitrogen fixation in endophytic and associative symbiosis. Field Crops Research 2000, 65:197-209.
21. Jensen D.E., Kelly R.C., von Hippel P.H. DNA " melting" proteins. II. Effects of bacteriophage T4 gene 32-protein binding on the conformation and stability of nucleic acid structures. Journal of Biological Chemistry 1976, 251:7215-7228.
22. Johansen J.E., Binnerup S.J., Lejbolle K.B., Mascher F., Sorensen J., Keel C. Impact of biocontrol strain Pseudomonas fluorescens CHA0 on rhizosphere bacteria isolated from barley (Hordeum vulgare L.) with special reference to Cytophaga-like bacteria. Journal of Applied Microbiology 2002, 93:1065-1074.
23. Kelly R.C., Jensen D.E., von Hippel P.H. DNA " melting" proteins. IV. Fluorescence measurements of binding parameters for bacteriophage T4 gene 32-protein to mono-, oligo-, and polynucleotides. Journal of Biological Chemistry 1976, 251:7240-7250.
24. Kreader C.A. Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Applied and Environmental Microbiology 1996, 62:1102-1106.
25. Martin-Laurent F., Philippot L., Hallet S., Chaussod R., Germon J.C., Soulas G., Catroux G. DNA extraction from soils: old bias for new microbial diversity analysis methods. Applied and Environmental Microbiology 2001, 67:2354-2359.
26. Mauchline T.H., Kerry B.R., Hirsch P.R. Quantification in soil and the rhizosphere of the nematophagous fungus Verticillium chlamydosporium by competitive PCR and comparison with selective plating. Applied and Environmental Microbiology 2002, 68:1846-1853.
27. Mavrodi D.V., Mavrodi O.V., McSpadden-Gardener B.B., Landa B.B., Weller D.M., Thomashow L.S. Identification of differences in genome content among phlD-positive Pseudomonas fluorescens strains by using PCR-based subtractive hybridization. Applied and Environmental Microbiology 2002, 68:5170-5176.
28. Mavrodi O.V., Mavrodi D.V., Thomashow L.S., Weller D.M. Quantification of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens in the plant rhizosphere by real-time PCR. Applied and Environmental Microbiology 2007, 73:5531-5538.
29. Mirza M., Mehnaz S., Normand P., Prigent-Combaret C., Moënne-Loccoz Y., Bally R., Malik K. Molecular characterization and PCR detection of a nitrogen-fixing Pseudomonas strain promoting rice growth. Biology and Fertility of Soils 2006, 43:163-170.
30. Mumy K.L., Findlay R.H. Convenient determination of DNA extraction efficiency using an external DNA recovery standard and quantitative-competitive PCR. Journal of Microbiological Methods 2004, 57:259-268.
31. Nelson L.M., Knowles R. Effect of oxygen and nitrate on nitrogen fixation and denitrification by Azospirillum brasilense grown in continuous culture. Canadian Journal of Microbiology 1978, 24:1395-1403.
32. Okon Y., Kapulnik Y. Development and function of Azospirillum-inoculated roots. Plant and Soil 1986, 90:3-16.
33. Okon Y., Labandera-Gonzalez C.A. Agronomic applications of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biology and Biochemistry 1994, 26:1591-1601.
34. Park J.W., Crowley D.E. Normalization of soil DNA extraction for accurate quantification of target genes by real-time PCR and DGGE. BioTechniques 2005, 38:579-586.
35. Pedraza R.O., Bellone C.H., Carrizo de Bellone S., Boa Sorte P.M.F., Teixeira K.R.d.S. Azospirillum inoculation and nitrogen fertilization effect on grain yield and on the diversity of endophytic bacteria in the phyllosphere of rice rainfed crop. European Journal of Plant Pathology 2009, 45:36-43.
36. Pothier J.F., Wisniewski-Dyé F., Weiss-Gayet M., Moënne-Loccoz Y., Prigent-Combaret C. Promoter-trap identification of wheat seed extract induced genes in the plant-growth-promoting rhizobacterium Azospirillum brasilense Sp245. Microbiology 2007, 153:3608-3622.
37. Prigent-Combaret C., Blaha D., Pothier J.F., Vial L., Poirier M.A., Wisniewski-Dyé F., Moënne-Loccoz Y. Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. FEMS Microbiology Ecology 2008, 65:202-219.
38. Ramette A., Frapolli M., Défago G., Moënne-Loccoz Y. Phylogeny of HCN synthase-encoding hcnBC genes in biocontrol fluorescent pseudomonads and its relationship with host plant species and HCN synthesis ability. Molecular Plant-Microbe Interactions 2003, 16:525-535.
39. Revellin C., Giraud J.-J., Silva N., Wadoux P., Catroux G. Effect of some granular insecticides currently used for the treatment of maize crops (Zea mays) on the survival of inoculated Azospirillum lipoferum. Pest Management Science 2001, 57:1075-1080.
40. Rezzonico F., Binder C., Défago G., Moënne-Loccoz Y. The type III secretion system of biocontrol Pseudomonas fluorescens KD targets the phytopathogenic chromista Pythium ultimum and promotes cucumber protection. Molecular Plant-Microbe Interactions 2005, 18:991-1001.
41. Rodriguez Caceres E.A. Improved medium for isolation of Azospirilllum spp. Applied and Environmental Microbiology 1982, 44:990-991.
42. Romero D., Brom S., Martinez-Salazar J., Girard M.L., Palacios R., Davila G. Amplification and deletion of a nod-nif region in the symbiotic plasmids of Rhizobium phaseoli. Journal of Bacteriology 1991, 173:2435-2441.
43. Rosado A.S., Seldin L., Wolters A.C., van Elsas J.D. Quantitative 16S rDNA-targeted polymerase chain reaction and oligonucleotide hybridization for the detection of Paenibacillus azotofixans in soil and the wheat rhizosphere. FEMS Microbiology Ecology 1996, 19:153-164.
44. Roy N.K., Ghosh R.K., Das J. Monomeric alkaline phosphatase of Vibrio cholerae. Journal of Bacteriology 1982, 150:1033-1039.
45. Schneegurt M.A., Dore S.Y., Kulpa C.F. Direct extraction of DNA from soils for studies in microbial ecology. Current Issue in Molecular Biology 2003, 5:1-8.
46. Sørensen J., Haubjerg Nicolaisen M., Ron E., Simonet P. Molecular tools in rhizosphere microbiology - from single-cell to whole-community analysis. Plant and Soil 2009, 321:483-512.
47. Tebbe C.C., Vahjen W. Interference of humic acids and DNA extracted directly from soil in detection and transformation of recombinant DNA from bacteria and a yeast. Applied and Environmental Microbiology 1993, 59:2657-2665.
48. Tsai Y.L., Olson B.H. Rapid method for separation of bacterial DNA from humic substances in sediments for polymerase chain reaction. Applied and Environmental Microbiology 1992, 58:2292-2295.
49. Vial L., Lavire C., Mavingui P., Blaha D., Haurat J., Moënne-Loccoz Y., Bally R., Wisniewski-Dyé F. Phase variation and genomic architecture changes in Azospirillum. Journal of Bacteriology 2006, 188:5364-5373.
50. Vincent J.M. A Manual for the Practical Study of Root-Nodule Bacteria 1970, Blackwell Scientific, Oxford.
51. Von Felten A., Défago G., Maurhofer M. Quantification of Pseudomonas fluorescens strains F113, CHA0 and Pf153 in the rhizosphere of maize by strain-specific real-time PCR unaffected by the variability of DNA extraction efficiency. Journal of Microbiological Methods 2010, 81:108-115.
52. Wang C., Ramette A., Punjasamarnwong P., Zala M., Natsch A., Moënne-Loccoz Y., Défago G. Cosmopolitan distribution of phlD-containing dicotyledonous crop-associated biocontrol pseudomonads of worldwide origin. FEMS Microbiology Ecology 2001, 37:105-116.
53. Wilson I.G. Inhibition and facilitation of nucleic acid amplification. Applied and Environmental Microbiology 1997, 63:3741-3751.