Skip to main content

Advertisement

SpringerLink
Log in

Contrasting colonization and plant growth promoting capacity between wild type and a gfp-derative of the endophyte Pseudomonas putida W619 in hybrid poplar

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

This study aims to investigate the colonization of poplar by the endophyte Pseudomonas putida W619 and its capacity to promote plant growth. Poplar cuttings were inoculated with P. putida W619 (wild-type or gfp-labelled). The colonization of both strains was investigated and morphological, physiological and biochemical parameters were analyzed to evaluate plant growth promotion. Inoculation with P. putida W619 (wild-type) resulted in remarkable growth promotion, decreased activities of antioxidative defence related enzymes, and reduced stomatal resistance, all indicative of improved plant health and growth in comparison with the non-inoculated cuttings. In contrast, inoculation with gfp-labelled P. putida W619 did not promote growth; it even had a negative effect on plant health and growth. Furthermore, compared to the wildtype strain, colonization by the gfp-labelled P. putida W619::gfp1 was much lower; it only colonized the rhizosphere and root cortex while the wild-type strain also colonized the root xylem vessels. Despite the strong plant growth promoting capacity of P. putida W619 (wild-type), after gfp labelling its growth promoting characteristics disappeared and its colonization capacity was strongly influenced; for these reasons gfp labelling should be applied with sufficient caution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315

    Article  CAS  Google Scholar 

  • Asghar HN, Zahir ZA, Arshad M (2004) Screening rhizobacteria for improving the growth, yield and soil content of canola (Brassica napus L.). Australian Journal of Agriculture Research 55:187–194

    Article  Google Scholar 

  • Babalola OO, Osir EO, Sanni AI, Odhiambo GD, Bulimo WD (2003) Amplification of 1-amino-cuclopropane-1-carboxylic (ACC) deaminase from plant growth promoting rhizobacteria in Striga-infected soil. Afr J Biotechnol 2:157–160

    CAS  Google Scholar 

  • Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, van der Lelie D (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583–588

    Article  PubMed  CAS  Google Scholar 

  • Barac T, Weyens N, Oeyen L, Taghavi S, van der Lelie D, Dubin D, Split M, Vangronsveld J (2009) Field note: Hydraulic containment of a BTEX plume using poplar trees. Int J Phytoremediat 11:416–424

    Article  CAS  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    Article  CAS  Google Scholar 

  • Bent E, Tuzun S, Chanway CP, Enebak S (2001) Alterations in plant growth and in root hormone levels of lodgepole pines inoculated with rhizobacteria. Can J Microbiol 47:793–800

    Article  PubMed  CAS  Google Scholar 

  • Beraha L, Wisniewski V, Garber ED (1983) Avirulence and reduced extracellular enzyme activity in Geotrichum candidum. Bot Gaz 144:461–465

    Article  CAS  Google Scholar 

  • Bergmeyer HU, Gawenn K, Grassl M (1974) Enzymes as biochemical reagents. In: Bergmeyer HU (ed) Methods in Enzymatic Analysis. Academic, NewYork, pp 425–522

    Google Scholar 

  • Bertagnolli BL, Soglio FKD, Sinclair JB (1996) Extracellular enzyme profiles of the fungal pathogen Rhizoctonia solani isolate 2B-12 and of two antagonists, Bacillus megaterium strain B153-2-2 and Trichoderma harzianum isolate Th008. I. Possible correlations with inhibition of growth and biocontrol. Physiol Mol Plant P 48:145–160

    Article  CAS  Google Scholar 

  • Bloemberg GV, Carvajal MMC (2006) Microbial interactions with plants: a hidden world. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 321–336

    Chapter  Google Scholar 

  • Buyer JS, Leong J (1986) Iron transport mediated antagonism between plant growth-promoting and plant-deleterious Pseudomonas strains. J Biol Chem 261:791–794

    PubMed  CAS  Google Scholar 

  • Cánovas D, Cases I, de Lorenzo V (2003) Heavy metal tolerance and metal homeostasis in Pseudomonas putida as revealed by complete genome analysis. Environ Microbiol 5:1242–1256

    Article  PubMed  Google Scholar 

  • Cassman KG, Liska AJ (2007) Food and fuel for all: realistic or foolish? Biofuels Bioprod Bioref 1:18–23

    Article  CAS  Google Scholar 

  • Coombs JT, Franco CMM (2003) Visualization of an endophytic Streptomyces species in wheat seed. Appl Environ Microb 69:4260–4262

    Article  CAS  Google Scholar 

  • Cunningham J, Kuiack C (1992) Production of citric and oxalic acids and solubilization of calcium phosphate by Penicillium bilaii. Appl Environ Microbiol 58(5):1451–1458

    PubMed  CAS  Google Scholar 

  • Dell’Amico E, Cavalca L, Andreoni V (2005) Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS Microbiol Lett 52:153–162

    Article  Google Scholar 

  • de Salamone IEG, Hynes RK, Nelson LM (2001) Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can J Microbiol 47:404–411

    Article  Google Scholar 

  • Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333

    Article  PubMed  CAS  Google Scholar 

  • Dowling DN, O’Gara F (1994) Metabolites of Pseudomonas involved in the biocontrol of plant disease. Trends Biotechnol 12:133–141

    Article  CAS  Google Scholar 

  • Gao Q, Peng SL, Zhao P, Zeng XP, Cai X, Yu M, Shen WJ, Liu YH (2003) Explanation of vegetation succession in subtropical southern China based on ecophysiological characteristics of plant species. Tree Physiol 23:641–648

    Article  PubMed  Google Scholar 

  • Germaine K, Keogh E, Borremans B, van der Lelie D, Barac T, Oeyen L, Vangronsveld J, Porteus Moore F, Moore ERB, Campbel CD, Ryan D, Dowling D (2004) Colonisation of poplar trees by gfp expressing endophytes. FEMS Microbiol Ecol 48:109–118

    Article  PubMed  CAS  Google Scholar 

  • Haberl H, Beringer T, Bhattacharya SC, Erb K-H, Hoogwijk M (2010) The global technical potential of bio-energy in 2050 considering sustainable constraints. Current opinion in Environmental Sustainability 2:394–403

    Article  Google Scholar 

  • Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. P Natl Acad Sci USA 94:2122–2127

    Article  CAS  Google Scholar 

  • Hurek T, Reinhold-Hurek B, Van Montagu M, Kellenberger E (1994) Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J Bacteriol 176:1913–1923

    PubMed  CAS  Google Scholar 

  • James EK (2000) Nitrogen fixation in endophytic and associative symbiosis. Field crop res 65:197–209

    Article  Google Scholar 

  • James EK, Reis VM, Olivares FL, Baldani JI, Döbereiner J (1994) Infection of sugar cane by the nitrogen fixing bacterium Acetobacter diazotrophicus. J Exp Bot 45:757–766

    Article  CAS  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  PubMed  CAS  Google Scholar 

  • Krechel A, Faupal A, Hallmann J, Ulrich A, Berg G (2002) Potato-associated bacteria and their antogonistic potential towards plant-pathogenic fungi and the plant-parasitic nematode Meloidogyne incognita (Kofoid and White) Chitwood. Can J Microbiol 48:772–786

    Article  PubMed  CAS  Google Scholar 

  • Lamb TG, Tonkyn DW, Kluepfel DA (1996) Movement of Pseudomonas aureofaciens from the rhizosphere to aerial plant tissue. Can J Microbiol 42:1112–1120

    Article  CAS  Google Scholar 

  • Mahaffee WF, Kloepper JW, Van Vuurde JWL, Van der Wolf JM, Van den Brink M (1997) Endophytic colonization of Phaseolus vulgaris by Pseudomonas fluorescens strain 89B-27 and Enterobacter asburiae strain JM22. In: Ryder MHR, Stevens PM, Bowen GD (eds) Improving plant productivity in rhizosphere bacteria. CSIRO, Melbourne, p 180

    Google Scholar 

  • Mastretta C, Barac T, Vangronsveld J, Newman L, Taghavi S, van der Lelie D (2006) Endophytic bacteria and their potential application to improve the phytoremediation of contaminated environments. Biotechnol Genet Eng Rev 23:175–207

    PubMed  CAS  Google Scholar 

  • Mayer AM (1958) Determination of Indole Acetic Acid by the Salkowsky Reaction. Nature 182:1670–1671

    Article  PubMed  CAS  Google Scholar 

  • McCord J, Fridovich I (1969) Superoxide dismutase: an enzymatic function for erythrocuperein (hemocuprein). J Biol Chem 244:6049–6055

    PubMed  CAS  Google Scholar 

  • Merckx R, van Ginkel JH, Sinnaeve J, Cremers A (1986) Plant induced changes in the rhizosphere of maize and wheat. Plant Soil 96:85–93

    Article  Google Scholar 

  • Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, Van Gijsegem F (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334

    PubMed  CAS  Google Scholar 

  • Newman KL, Almeida RPP, Purcell AH, Lindow SE (2003) Use of a green fluorescent strain for analysis of Xylella fastidiosa colonization of Vitis vinifera. Appl Environ Microb 69:7319–7327

    Article  CAS  Google Scholar 

  • O’Sullivan DJ, O’Gara F (1992) Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiology Reviews 56:662–676

    Google Scholar 

  • Patten C, Glick B (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68(8):3795–3801

    Article  PubMed  CAS  Google Scholar 

  • Petri C, Wang H, Alburquerque N, Faize M, Burgos L (2008) Agrobacterium-mediated transformation of apricot (Prunus armeniaca L.) leaf explants. Plant Cell Rep 27:1317–1324

    Article  PubMed  CAS  Google Scholar 

  • Porteous Moore F, Barac T, Borremans B, Oeyen L, Vangronsveld J, van der Lelie D, Campbell CD, Moore ERB (2006) Endophytic bacterial diversity in Poplar trees growing on a BTEX-contaminated site: The characterisation of isolates with potential to enhance phytoremediation. Syst Appl Microbiol 29:539–556

    Article  Google Scholar 

  • Prinsen E, Van Dongen W, Esmans E, Van Onckelen H (1997) HPLC Linked electrospray tandem mass spectrometry: a rapid and reliable method to analyze indole-3-acetic acid metabolism in bacteria. J Mass Spectrom 32:12–22

    Article  CAS  Google Scholar 

  • Quadt-Hallmann A, Kloepper JW (1996) Immunological detection and localization of the cotton endophyte Enterobacter asburiae JM22 in different plant species. Can J Microbiol 42:1144–1154

    Article  CAS  Google Scholar 

  • Quadt-Hallmann A, Benhamou N, Kloepper JW (1997) Bacterial endophytes in cotton: mechanisms entering the plant. Can J Microbiol 43:577–582

    Article  CAS  Google Scholar 

  • Ramos-Gonzalez MI, Campos MJ, Ramos JL (2005) Analysis of Pseudomonas putida KT2440 gene expression in maize rhizosphere: in vitro expression technology capture and indentification of root-activated promoters. J Bacteriol 187:4033–4041

    Article  PubMed  CAS  Google Scholar 

  • Redig P, Shaul O, Inzé D, Van Montagu M, Van Onckelen H (1996) Levels of endogenous cytokinins, indole-3-acetic acid and abscisic acid during the cell cycle of synchronized tobacco BY-2 cells. FEBS Lett 391:175–180

    Article  PubMed  CAS  Google Scholar 

  • Spiertz H (2010) Food production, crops and sustainability: restoring confidence in science and technology. Current opinion in Environmental Sustainability 2:439–443

    Article  Google Scholar 

  • Sprent JI, de Faria SM (1988) Mechanisms of infection of plants by nitrogen fixing organisms. Plant Soil 110:157–165

    Article  Google Scholar 

  • Schwyn B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160(1):47–56

    Article  PubMed  CAS  Google Scholar 

  • Taghavi S, Barac T, Greenberg B, Borremans B, Vangronsveld J, van der Lelie D (2005) Horizontal gene transfer to endogenous endophytic bacteria from Poplar improves phytoremediation of toluene. Appl Environ Microb 71:8500–8505

    Article  CAS  Google Scholar 

  • Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar. Appl Environ Microb 75:748–757

    Article  CAS  Google Scholar 

  • Tanimoto E (2007) Regulation of plant growth by plant hormones – Roles for Auxin and Gibberelin. Crit Rev Plant Sci 24:249–265

    Article  Google Scholar 

  • van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    Article  PubMed  Google Scholar 

  • Verbeke G, Molenberghs G (2000) Linear mixed models for longitudinal data. Springer Series in Statistics. Springer, New York

    Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Vangronsveld J, Clijsters H (1994) Toxic effects of metals. In: Farago M (ed) Plants and the chemical elements. VCH Verlagsgesellschaft, Germany, pp 149–177

    Chapter  Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009a) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotech 20:248–254

    Article  PubMed  CAS  Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009b) Exploiting plant–microbe partnerships for improving biomass production and remediation. Trends Biotechnol 27:591–598

    Article  PubMed  CAS  Google Scholar 

  • Weyens N, Taghavi S, Barac T, van der Lelie D, Boulet J, Artois T, Vangronsveld J (2009c) Bacterial diversity associated with English Oak and Common Ash growing on a TCE-contaminated site: characterization of strains with potential to improve phytoremediation. Environ Sci Pollut R 16:830–843

    Article  CAS  Google Scholar 

  • Weyens N, van der Lelie D, Artois T, Smeets K, Taghavi S, Newman L, Carleer R, Vangronsveld J (2009d) Bioaugmentation with engineered endophytic bacteria improves contaminant fate in phytoremediation. Environ Sci Technol 43:9413–9418

    Article  PubMed  CAS  Google Scholar 

  • Weyens N, Truyens S, Dupae J, Newman L, van der Lelie D, Carleer R, Vangronsveld J (2010) Potential of Pseudomonas putida W619-TCE to reduce TCE phytotoxicity and evapotranspiration in poplar cuttings. Environ Pollut 158:2915–2919

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen) for N.W. and by the Fund for Scientific Research Flanders (FWO-Vlaanderen), Ph.D. grant for J.B. The project was further supported by the UHasselt Methusalem project 08 M03 VGRJ. Work by S.T. was funded by Laboratory Directed Research and Development funds (LDRD05-063 and LDRD09-005) at the Brookhaven National Laboratory under contract with the U.S. Department of Energy.

Author information

Authors and Affiliations

  1. Environmental Biology, Hasselt University, Agoralaan Building D, B-3590, Diepenbeek, Belgium

    Nele Weyens, Jana Boulet & Jaco Vangronsveld

  2. Laboratory of Cell Biology & Histology, Department of Veterinary Sciences, Antwerp University, Groenenborgerlaan 171, 2020, Antwerp, Belgium

    Dirk Adriaensen & Jean-Pierre Timmermans

  3. Department of Biology, Groenenborgercampus, Antwerp University, Groenenborgerlaan 171, 2020, Antwerp, Belgium

    Els Prinsen & Sandra Van Oevelen

  4. Institute for Materials Research, Hasselt University, Wetenschapspark 1, B-3590, Diepenbeek, Belgium

    Jan D’Haen

  5. Biodiversity, Phylogeny & Population Studies, Hasselt University, Agoralaan Building D, B-3590, Diepenbeek, Belgium

    Karen Smeets

  6. Research Triangle Institute (RTI), International 3040 Cornwallis Road, Research Triangle Park, NC, 27709-2194, USA

    Daniel van der Lelie

  7. Brookhaven National Laboratory (BNL), Biology Department, Building 463, Upton, NY, 11973, USA

    Safiyh Taghavi

Authors
  1. Nele Weyens
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jana Boulet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dirk Adriaensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jean-Pierre Timmermans
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Els Prinsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sandra Van Oevelen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jan D’Haen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Karen Smeets
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Daniel van der Lelie
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Safiyh Taghavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jaco Vangronsveld
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nele Weyens.

Additional information

Responsible Editor: Euan K. James.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weyens, N., Boulet, J., Adriaensen, D. et al. Contrasting colonization and plant growth promoting capacity between wild type and a gfp-derative of the endophyte Pseudomonas putida W619 in hybrid poplar. Plant Soil 356, 217–230 (2012). https://doi.org/10.1007/s11104-011-0831-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-011-0831-x

Keywords

Search

Navigation