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Expression on roots and contribution to maize phytostimulation of 1-aminocyclopropane-1-decarboxylate deaminase gene acdS in Pseudomonas fluorescens F113

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Abstract

Aims

The plant-beneficial bacterium Pseudomonas fluorescens F113 harbours an acdS gene, which enables deamination of 1-aminocyclopropane-1-carboxylate. The impact of abiotic and biotic factors on the expression of this gene was assessed, as well as the plant-beneficial properties of F113 under different soil moistures.

Methods

An acdS-egfp biosensor was constructed in F113, validated in vitro and used to analyse, by microscopy, its expression on roots of Zea mays comparatively to Beta vulgaris. An acdS mutant was constructed and compared with the wild-type to characterize plant-beneficial effects of F113 on maize lines EP1 and FV2, under well-watered and water deficit conditions.

Results

Different patterns of root colonization and acdS expression were observed according to plant genotype. acdS rhizoplane expression was higher on Beta vulgaris, and on maize line FV2 and hybrid PR37Y15 than on maize line EP1 and teosinte. Strain F113 but not its acdS mutant promoted root growth of EP1 under well-watered conditions and germination of FV2 under water deficit conditions.

Conclusions

Maize lines differed in their ability to induce acdS expression and to respond to P. fluorescens F113. The maize line leading to higher acdS expression, FV2, was the one benefiting from inoculation under water deficit.

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References

  • Alexeyev MF (1999) The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of Gram-negative bacteria. Biotechniques 26:824–828

    CAS  PubMed  Google Scholar 

  • Allaway D, Schofield NA, Leonard ME, Gilardoni L, Finan TM, Poole PS (2001) Use of differential fluorescence induction and optical trapping to isolate environmentally induced genes. Environ Microbiol 3:397–406

    Article  CAS  PubMed  Google Scholar 

  • Bacilio-Jimenez M, Aguilar-Flores S, Ventura-Zapata E, Perez-Campos E, Bouquelet S, Zenteno ES (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249:271–277

    Article  CAS  Google Scholar 

  • Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32

    Article  CAS  PubMed  Google Scholar 

  • Bakker PAHM, Pieterse CMJ, Van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243

    Article  PubMed  Google Scholar 

  • Barea JM, Andrade G, Bianciotto V, Dowling D, Lohrke S, Bonfante P, O’Gara F, Azcon-Aguilar C (1998) Impact on arbuscular mycorrhiza formation of Pseudomonas strains used as inoculants for biocontrol of soil-borne fungal plant pathogens. Appl Environ Microbiol 64:2304–2307

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barlow PW (2003) The root cap: cell dynamics, cell differentiation and cap function. J Plant Growth Regul 21:261–286

    Article  Google Scholar 

  • Belimov AA, Dodd IC, Safronova VI, Hontzeas N, Davies WJ (2007) Pseudomonas brassicacearum strain Am3 containing 1-aminocyclopropane-1-carboxylate deaminase can show both pathogenic and growth-promoting properties in its interaction with tomato. J Exp Bot 58:1485–1495

    Article  CAS  PubMed  Google Scholar 

  • Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol 181:413–423

    Article  CAS  PubMed  Google Scholar 

  • Blaha D, Prigent-Combaret C, Mirza MS, Moënne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470

    Article  CAS  PubMed  Google Scholar 

  • Bloemberg GV, Wijfjes AH, Lamers GE, Stuurman N, Lugtenberg BJ (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

    Article  CAS  PubMed  Google Scholar 

  • Bouffaud M-L, Kyselková M, Gouesnard B, Grundmann G, Muller D, Moënne-Loccoz Y (2012) Is diversification history of maize influencing selection of soil bacteria by roots? Mol Ecol 21:195–206

    Article  PubMed  Google Scholar 

  • Bouffaud M-L, Poirier M-A, Muller D, Moënne-Loccoz Y (2014) Root microbiome relates to plant host evolution in maize and other Poaceae. Environ Microbiol 16:2804–2814

    Article  PubMed  Google Scholar 

  • Brazelton JN, Pfeufer EE, Sweat TA, Gardener BBM, Coenen C (2008) 2,4-diacetylphloroglucinol alters plant root development. Mol Plant-Microbe Interact 21:1349–1358

    Article  CAS  PubMed  Google Scholar 

  • Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruto M, Prigent-Combaret C, Muller D, Moënne-Loccoz Y (2014) Analysis of genes contributing to plant-beneficial functions in plant growth-promoting rhizobacteria and related Proteobacteria. Sci Rep 4:6261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll H, Moënne-Loccoz Y, Dowling DN, O’Gara F (1995) Mutational disruption of the biosynthesis genes coding for the antifungal metabolite 2,4-diacetylphloroglucinol does not influence the ecological fitness of Pseudomonas fluorescens F113 in the rhizosphere of sugarbeets. Appl Environ Microbiol 61:3002–3007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chamam A, Sanguin H, Bellvert F, Meiffren G, Comte G, Wisniewski-Dyé F, Bertrand C, Prigent-Combaret C (2013) Plant secondary metabolite profiling evidences strain-dependent effect in the Azospirillum-Oryza sativa association. Phytochemistry 87:65–77

    Article  CAS  PubMed  Google Scholar 

  • Chamam A, Wisniewski-Dyé F, Comte G, Bertrand C, Prigent-Combaret C (2015) Differential responses of Oryza sativa secondary metabolism to biotic interactions with cooperative, commensal and phytopathogenic bacteria. Planta 242:1439–1452

    Article  CAS  PubMed  Google Scholar 

  • Cheng ZY, Duncker BP, McConkey BJ, Glick BR (2008) Transcriptional regulation of ACC deaminase gene expression in Pseudomonas putida UW4. Can J Microbiol 54:128–136

    Article  CAS  PubMed  Google Scholar 

  • Cheshire MV, Mundie CM (1990) Organic matter contributed to soil by plant-roots during the growth and decomposition of maize. Plant Soil 121:107–114

    Article  CAS  Google Scholar 

  • Chilton M-D, Currier TC, Farrand SK, Bendich AJ, Gordon MP, Nester EW (1974) Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc Natl Acad Sci U S A 71:3672–3676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cieslinski G, VanRees KCJ, Szmigielska AM, Huang PM (1997) Low molecular weight organic acids released from roots of durum wheat and flax into sterile nutrient solutions. J Plant Nutr 20:753–764

    Article  CAS  Google Scholar 

  • Couillerot O, Prigent-Combaret C, Caballero-Mellado J, Moënne-Loccoz Y (2009) Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Lett Appl Microbiol 48:505–512

    Article  CAS  PubMed  Google Scholar 

  • Couillerot O, Combes-Meynet E, Pothier JF, Bellvert F, Challita E, Poirier M-A, Rohr R, Comte G, Moënne-Loccoz Y, Prigent-Combaret C (2011) Role of the antimicrobial compound 2,4-diacetylphloroglucinol in the impact of biocontrol Pseudomonas fluorescens F113 on Azospirillum brasilense phytostimulators. Microbiology 157:1694–1705

    Article  CAS  PubMed  Google Scholar 

  • Cronin D, Moënne-Loccoz Y, Fenton A, Dunne C, Dowling DN, O’Gara F (1997) Ecological interaction of a biocontrol Pseudomonas fluorescens strain producing 2,4-diacetylphloroglucinol with the soft rot potato pathogen Erwinia carotovora subsp. atroseptica. FEMS Microbiol Ecol 23:95–106

    Article  CAS  Google Scholar 

  • da Silva KRA, Salles JF, Seldin L, van Elsas JD (2003) Application of a novel Paenibacillus-specific PCR-DGGE method and sequence analysis to assess the diversity of Paenibacillus spp. in the maize rhizosphere. J Microbiol Methods 54:213–231

    Article  PubMed  Google Scholar 

  • Dandie CE, Larrainzar E, Mark GL, O’Gara F, Morrissey JP (2005) Establishment of DsRed.T3_S4T as an improved autofluorescent marker for microbial ecology applications. Environ Microbiol 7:1818–1825

    Article  CAS  PubMed  Google Scholar 

  • de Lorenzo V, Timmis KN (1994) Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol 235:386–405

    Article  CAS  PubMed  Google Scholar 

  • de Werra P, Huser A, Tabacchi R, Keel C, Maurhofer M (2011) Plant- and microbe-derived compounds affect the expression of genes encoding antifungal compounds in a pseudomonad with biocontrol activity. Appl Environ Microbiol 77:2807–2812

    Article  PubMed  PubMed Central  Google Scholar 

  • Dimkpa CO, Zeng J, McLean JE, Britt DW, Zhan J, Anderson AJ (2012) Production of indole-3-acetic acid via the indole-3-acetamide pathway in the plant-beneficial bacterium Pseudomonas chlororaphis O6 is inhibited by ZnO nanoparticles but enhanced by CuO nanoparticles. Appl Environ Microbiol 78:1404–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El Zemrany H, Cortet J, Lutz MP et al (2006) 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 Biol Biochem 38:1712–1726

    Article  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    Article  CAS  PubMed  Google Scholar 

  • Glick BR, Penrose DM, Li JP (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Grichko VP, Glick BR (2000) Identification of DNA sequences that regulate the expression of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylic acid deaminase gene. Can J Microbiol 46:1159–1165

    CAS  PubMed  Google Scholar 

  • Gross H, Loper JE (2009) Genomics of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 26:1408–1446

    Article  CAS  PubMed  Google Scholar 

  • Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Wang R, Yang Z, Zhan Y, Ma Y, Ping S et al (2015) 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas stutzeri A1501 facilitates the growth of rice in the presence of salt or heavy metals. J Microbiol Biotechnol 25:1119–1128

    Article  CAS  PubMed  Google Scholar 

  • Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Z (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Annu Rev Phytopathol 36:311–327

    Article  CAS  PubMed  Google Scholar 

  • Honma S, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831

    CAS  Google Scholar 

  • Hontzeas N, Richardson AO, Belimov A, Safronova V, Abu-Omar MM, Glick BR (2005) Evidence for horizontal transfer of 1-aminocyclopropane-1-carboxylate deaminase genes. Appl Environ Microbiol 71:7556–7558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition - an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407

    Article  Google Scholar 

  • Iavicoli A, Boutet E, Buchala A, Métraux J-P (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant-Microbe Interact 16:851–885

    Article  CAS  PubMed  Google Scholar 

  • Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347

    Article  CAS  PubMed  Google Scholar 

  • Jamali F, Sharifi-Tehrani A, Lutz M, Maurhofer M (2009) Influence of host plant genotype, presence of a pathogen, and coinoculation with Pseudomonas fluorescens strains on the rhizosphere expression of hydrogen cyanide- and 2,4-diacetylphloroglucinol biosynthetic genes in P. fluorescens biocontrol strain CHA0. Microb Ecol 57:267–275

    Article  PubMed  Google Scholar 

  • Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321:5–33

    Article  CAS  Google Scholar 

  • Latz E, Eisenhauer N, Scheu S, Jousset A (2015) Plant identity drives the expression of biocontrol factors in a rhizosphere bacterium across a plant diversity gradient. Funct Ecol 29:1225–1234

    Article  Google Scholar 

  • Ma WB, Sebestianova SB, Sebestian J, Burd GI, Guinel FC, Glick BR (2003) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Anton Leeuw Int J G 83:285–291

    Article  CAS  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572

    Article  CAS  PubMed  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530

    Article  CAS  Google Scholar 

  • Melnitchouck A, Leinweber P, Eckhardt KU, Beese R (2005) Qualitative differences between day- and night-time rhizodeposition in maize (Zea mays L.) as investigated by pyrolysis-field ionization mass spectrometry. Soil Biol Biochem 37:155–162

    Article  CAS  Google Scholar 

  • Miller SH, Browne P, Prigent-Combaret C, Combes-Meynet E, Morrissey JP, O’Gara F (2009) Biochemical and genomic comparison of inorganic phosphate solubilization in Pseudomonas species. Environ Microbiol Rep 2:403–411

    Article  CAS  PubMed  Google Scholar 

  • Mrázek J, Xie S (2006) Pattern locator: a new tool for finding local sequence patterns in genomic DNA sequences. Bioinformatics 22:3099–3100

    Article  PubMed  Google Scholar 

  • Niemira BA, Safir GR, Hawes MC (1996) Arbuscular mycorrhizal colonization and border cell production: a possible correlation. Phytopathology 86:563–565

    Google Scholar 

  • Nikolic B, Schwab H, Sessitsch A (2011) Metagenomic analysis of the 1-aminocyclopropane-1-carboxylate deaminase gene (acdS) operon of an uncultured bacterial endophyte colonizing Solanum tuberosum L. Arch Microbiol 193:665–676

    Article  CAS  PubMed  Google Scholar 

  • Notz R, Maurhofer M, Schnider-Keel U, Duffy B, Haas D, Défago G (2001) Biotic factors affecting expression of the 2,4-diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology 91:873–881

    Article  CAS  PubMed  Google Scholar 

  • Penrose DM, Glick BR (2001) Levels of ACC and related compounds in exudate and extracts of canola seeds treated with ACC deaminase-containing plant growth-promoting bacteria. Can J Microbiol 47:368–372

    Article  CAS  PubMed  Google Scholar 

  • Picard C, Bosco M (2005) Maize heterosis affects the structure and dynamics of indigenous rhizospheric auxins-producing Pseudomonas populations. FEMS Microbiol Ecol 53:349–357

    Article  CAS  PubMed  Google Scholar 

  • Picard C, Frascaroli E, Bosco M (2004) Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing rhizobacteria are differentially affected by the genotype of two maize inbred lines and their hybrid. FEMS Microbiol Ecol 49:207–215

    Article  CAS  PubMed  Google Scholar 

  • Pothier JF, Wisniewski-Dye F, Weiss-Gayet M, Moënne-Loccoz Y, Prigent-Combaret C (2007) Promoter-trap identification of wheat seed extract-induced genes in the plant-growth-promoting rhizobacterium Azospirillum brasilense Sp245. Microbiology 153:3608–3622

    Article  CAS  PubMed  Google Scholar 

  • Pothier JF, Prigent-Combaret C, Haurat J, Moënne-Loccoz Y, Wisniewski-Dye F (2008) Duplication of plasmid-borne nitrite reductase gene nirK in the wheat-associated plant growth-promoting rhizobacterium Azospirillum brasilense Sp245. Mol Plant-Microbe Interact 21:831–842

    Article  CAS  PubMed  Google Scholar 

  • Prigent-Combaret C, Blaha D, Pothier JF, Vial L, Poirier MA, Wisniewski-Dye F, Moënne-Loccoz Y (2008) 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 Microbiol Ecol 65:202–219

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redondo-Nieto M, Barret M, Morrissey J, Germaine K, Martínez-Granero F, Barahona E et al (2013) Genome sequence reveals that Pseudomonas fluorescens F113 possesses a large and diverse array of systems for rhizosphere function and host interaction. BMC Genomics 14:54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rengel Z (2002) Genetic control of root exudation. Plant Soil 245:59–70

    Article  CAS  Google Scholar 

  • Rodrigues-Pousada RA, De Rycke R, Dedonder A, Van Caeneghem W, Engler G, Van Montagu M, Van Der Straeten D (1993) The Arabidopsis 1-aminocyclopropane-1-carboxylate synthase gene 1 is expressed during early development. Plant Cell 5:897–911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Shakir MA, Bano A, Arshad M (2012) Rhizosphere bacteria containing ACC-deaminase conferred drought tolerance in wheat grown under semi-arid climate. Soil Environ 31:108–112

    CAS  Google Scholar 

  • Shanahan P, O’Sullivan DJ, Simpson P, Glennon JD, O’Gara F (1992) Isolation of 2,4-diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing its production. Appl Environ Microbiol 58:353–358

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sheibani-Tezerji R, Naveed M, Jehl MA, Sessitsch A, Rattei T, Mitter B (2015) The genomes of closely related Pantoea ananatis maize seed endophytes having different effects on the host plant differ in secretion system genes and mobile genetic elements. Front Microbiol 6:440

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh RP, Shelke GM, Kumar A, Jha PN (2015) Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants. Front Microbiol 6:937

    PubMed  PubMed Central  Google Scholar 

  • Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant-Microbe Interact 13:637–648

    Article  CAS  PubMed  Google Scholar 

  • Venables WN, Smith DM (2011) The R development core team. An introduction to R. Version 2.0:04–13

  • Villacieros M, Power B, Sanchez-Contreras M et al (2003) Colonization behaviour of Pseudomonas fluorescens and Sinorhizobium meliloti in the alfalfa (Medicago sativa) rhizosphere. Plant Soil 251:47–54

    Article  CAS  Google Scholar 

  • Walker V, Bertrand C, Bellvert F, Moënne-Loccoz Y, Bally R, Comte G (2011) Host plant secondary metabolite profiling shows a complex, strain-dependent response of maize to plant growth promoting rhizobacteria of the genus Azospirillum. New Phytol 189:494–506

    Article  CAS  PubMed  Google Scholar 

  • Walker V, Couillerot O, Von Felten A, Bellvert F, Jansa J, Maurhofer M, Bally R, Moënne-Loccoz Y, Comte G (2012) Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 356:151–163

    Article  CAS  Google Scholar 

  • Wang CX, Knill E, Glick BR, Défago G (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can J Microbiol 46:898–907

    Article  CAS  PubMed  Google Scholar 

  • Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

E. Combes-Meynet and J. Vacheron were supported by Ph.D. grants from the Ministère de l’Enseignement Supérieur et de la Recherche (Paris) and Academic Research Cluster 3 of Rhône-Alpes Region, respectively. We also acknowledge funding from the ANR project SymbioMaize (ANR-12-JSV7-0014-01). This work made use of the technical platforms Serre and Centre Technologique des Microstructures at FR BioEnviS (Université Lyon 1).

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Authors and Affiliations

  1. Université de Lyon, F-69622, Lyon, France

    Jordan Vacheron, Emeline Combes-Meynet, Vincent Walker, Daniel Muller, Yvan Moënne-Loccoz & Claire Prigent-Combaret

  2. Université Lyon 1, Villeurbanne, France

    Jordan Vacheron, Emeline Combes-Meynet, Vincent Walker, Daniel Muller, Yvan Moënne-Loccoz & Claire Prigent-Combaret

  3. CNRS, UMR5557, Ecologie Microbienne, Université Lyon 1, 43 bd du 11 Novembre 1918, 69622, Villeurbanne cedex, France

    Jordan Vacheron, Emeline Combes-Meynet, Vincent Walker, Daniel Muller, Yvan Moënne-Loccoz & Claire Prigent-Combaret

  4. INRA, UMR1418, Villeurbanne, France

    Jordan Vacheron, Emeline Combes-Meynet, Vincent Walker, Daniel Muller, Yvan Moënne-Loccoz & Claire Prigent-Combaret

  5. INRA, UMR1334, AGAP, Montpellier, France

    Brigitte Gouesnard

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Vacheron, J., Combes-Meynet, E., Walker, V. et al. Expression on roots and contribution to maize phytostimulation of 1-aminocyclopropane-1-decarboxylate deaminase gene acdS in Pseudomonas fluorescens F113. Plant Soil 407, 187–202 (2016). https://doi.org/10.1007/s11104-016-2907-0

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