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Interactions of bacterial cytokinins and IAA in the rhizosphere may alter phytostimulatory efficiency of rhizobacteria

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Abstract

Phytohormones from rhizobacterial origin have been linked to their phytostimulation potential. However, while studying the efficacy of plant growth promoting bacteria, focus has always been on a single hormone. The role of plant hormones often overlay and they mutually modulate their effect. In current study focus was on the role of two hormones (cytokinins and indole acetic acid) in phytostimulation by rhizobacteria. Endogenous rhizosphere bacteria were isolated and screened for the presence of phytohormones. Bacterial strains from three different genera (Pseudomonas, Bacillus and Azospirillum) were screened positive for cytokinins and IAA. Phytohormones were simultaneously determined in SPE purified bacterial extract by ultra performance liquid chromatography (UPLC) coupled to a tandem mass spectrometer through electrospray interface. Cytokinins and IAA were determined in positive and negative mode, respectively with MRM scan. Zeatin, zeatin riboside and dihydrozeatin riboside were detected and quantified in the selected strains. Significant positive correlation between cytokinins and IAA in bacterial culture and plant endogenous hormones (r = 0.933 and r = 0.983; P = 0.01, respectively) was observed. However, strains with high IAA to cytokinins ratio could hardly enhance in-planta cytokinins, indicating antagonistic relation between the two hormones. Significant correlation of cytokinin with shoot length (r = 0.797; P = 0.01), fresh weight (r = 0.685; P = 0.01) and dry weight (r = 0.704; P = 0.01) was reported under axenic conditions. Bacterial IAA was correlated negatively to root length (r = 0.853; P = 0.01) and positively correlated to the number of roots (r = 0.964; P = 0.01). In natural conditions maximum increase in spike length (33%), number of tillers (71%) and weight of seeds (39%) was documented at final harvest in bacterially inoculated plants.

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References

  • Akiyoshi DE, Regier DA, Gordon MP (1987) Cytokinin production by Agrobacterium and Pseudomonas spp. J Bacteriol 169:4242–4248

    CAS  Google Scholar 

  • Ali B, Sabri AN, Ljung K, Hasnain S (2009a) Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L. Lett Appl Microbiol 48:542–547

    Article  CAS  Google Scholar 

  • Ali B, Sabri AN, Ljung K, Hasnain S (2009b) Quantification of indole-3-acetic acid from plant associated Bacillus spp. and their phytostimulatory effect on Vigna radiata (L.). World J Microbiol Biotechnol 25:519–526

    Article  CAS  Google Scholar 

  • Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57–67

    Article  CAS  Google Scholar 

  • Arkhipova T, Melentiev A, Veselov S, Kudoyarova G (2004) Effect of cytokinin-producing microorganisms on resistance of lettuce plant to drought and toxic metal. Acta Physiol Plantarum 26:275

    Google Scholar 

  • Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272:201–209

    Article  CAS  Google Scholar 

  • Arkhipova TN, Veselov SY, Melent’ev AI, Martynenko EV, Kudoyarova GR (2006) Comparison of effects of bacterial strains differing in their ability to synthesize cytokinins on growth and cytokinin content in wheat plants. Russ J Plant Physiol 53:507–513

    Article  CAS  Google Scholar 

  • 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 

  • Aslantas R, Cakmakci R, Sahin F (2007) Effect of plant growth promoting rhizobacteria on young apple tree growth and fruit yield under orchard conditions. Sci Hortic 111:371–377

    Article  Google Scholar 

  • Barazani OZ, Friedman J (1999) Is IAA the major root growth factor secreted from plant-growth-mediating bacteria? J Chem Ecol 25:2397–2406

    Article  CAS  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  Google Scholar 

  • Benizri E, Courtade A, Picard C, Guckert A (1998) Role of maize root exudates in the production of auxins by Pseudomonas fluorescens M. 3.1. Soil Biol Biochem 30:1481–1484

    Article  CAS  Google Scholar 

  • Carabelli M et al (2007) Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev 21:1863–1868

    Article  CAS  Google Scholar 

  • Dworkin M, Foster JW (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–603

    CAS  Google Scholar 

  • Fischer SE, Fischer SI, Magris S, Mori GB (2007) Isolation and characterization of bacteria from the rhizosphere of wheat. World J Microbiol Biotechnol 23:895–903

    Article  CAS  Google Scholar 

  • Ghosh S, Sengupta C, Maiti TK, Basu PS (2008) Production of 3-indolylacetic acid in root nodules and culture by a Rhizobium species isolated from root nodules of the leguminous pulse Phaseolus mungo. Folia Microbiol 53:351–355

    Article  CAS  Google Scholar 

  • Hasnain S, Thomas CM (1996) Two related rolling circle replication plasmids from salt-tolerant bacteria. Plasmid 36:191–199

    Article  CAS  Google Scholar 

  • Hussain A, Hasnain S (2009) Cytokinin production by some bacteria: its impact on cell division in cucumber cotyledons. Afr J Microbiol Res 3:704–712

    CAS  Google Scholar 

  • Hussain A, Hasnain S (2010) Phytostimulation and biofertilization in wheat by cyanobacteria. J Ind Microbiol Biotechnol 38:85–92

    Article  Google Scholar 

  • Hussain A, Krischke M, Roitsch T, Hasnain S (2010) Rapid determination of cytokinins and auxin in Cyanobacteria. Curr Microbiol 61:361–369

    Article  CAS  Google Scholar 

  • Idris ESE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant Microbe Int 20:619–626

    Article  CAS  Google Scholar 

  • Johnson BJ (1994) Influence of plant-growth regulators and mowing on 2 bermuda grasses. Agron J 86:805–810

    Article  Google Scholar 

  • Joo GJ, Kim YM, Lee IJ, Song KS, Rhee IK (2004) Growth promotion of red pepper plug seedlings and the production of gibberellins by Bacillus cereus, Bacillus macroides and Bacillus pumilus. Biotechnol Lett 26:487–491

    Article  CAS  Google Scholar 

  • Karadeniz A, Topcuoglu SF, Inan S (2006) Auxin, gibberellin, cytokinin and abscisic acid production in some bacteria. World J Microbiol Biotechnol 22:1061–1064

    Article  CAS  Google Scholar 

  • Karthikeyan N, Prasanna R, Sood A, Jaiswal P, Nayak S, Kaushik BD (2009) Physiological characterization and electron microscopic investigation of cyanobacteria associated with wheat rhizosphere. Folia Microbiol 54:43–51

    Article  CAS  Google Scholar 

  • Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480

    Article  CAS  Google Scholar 

  • Lata H, Li XC, Silva B, Moraes RM, Halda-Alija L (2006) Identification of IAA-producing endophytic bacteria from micropropagated Echinacea plants using 16S rRNA sequencing. Plant Cell Tissue Org 85:353–359

    Article  CAS  Google Scholar 

  • Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS ONE 3:e2702

    Article  Google Scholar 

  • McLellan CA, Turbyville TJ, Wijeratne EM, Kerschen A, Vierling E, Queitsch C, Whitesell L, Gunatilaka AA (2007) A rhizosphere fungus enhances Arabidopsis thermotolerance through production of an HSP90 inhibitor. Plant Physiol 145:174–182

    Article  CAS  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plantarum 118:10–15

    Article  CAS  Google Scholar 

  • Pérez-Miranda S, Cabirol N, George-Téllez R, Zamudio-Rivera LS, Fernández FJ (2007) O-CAS, a fast and universal method for siderophore detection. Microbiol Methods 70:127–131

    Article  Google Scholar 

  • Pertry I et al (2009) Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc Natl Acad Sci 106:929–934

    Article  CAS  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Microbiol 17:362–370

    CAS  Google Scholar 

  • Ramos B, Garcia JAL, Probanza A, Barrientos ML, Manero FJG (2003) Alterations in the rhizobacterial community associated with European alder growth when inoculated with PGPR strain Bacillus licheniformis. Environ Exp Bot 49:61–68

    Article  Google Scholar 

  • Remans R et al (2008) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161

    Article  CAS  Google Scholar 

  • Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285–292

    Article  CAS  Google Scholar 

  • Spaepen S, Dobbelaere S, Croonenborghs A, Vanderleyden J (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312:15–23

    Article  CAS  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signaling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  CAS  Google Scholar 

  • Tien TM, Gaskins MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl Environ Microbiol 37:1016–1024

    CAS  Google Scholar 

  • Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:117–126

    Article  CAS  Google Scholar 

  • Tzfira T, Jensen CS, Wang WX, Zuker A, Vinocur B, Altman A, Vainstein A (1997) Transgenic Populus tremula: a step-by-step protocol for its Agrobacterium-mediated transformation. Plant Mol Biol Rep 15:219–235

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Higher Education commission of Pakistan is acknowledged for providing financial support to the visit of Mr. Anwar Hussain to Wurzburg University Germany. Prof. Dr. Thomas Roitsch and Dr. Markus Krischke, Department of Pharmaceutical Biology, Wurzburg University, Germany, are acknowledged for providing the laboratory facilities and help in phytohormones determination.

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Correspondence to Shahida Hasnain.

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Hussain, A., Hasnain, S. Interactions of bacterial cytokinins and IAA in the rhizosphere may alter phytostimulatory efficiency of rhizobacteria. World J Microbiol Biotechnol 27, 2645–2654 (2011). https://doi.org/10.1007/s11274-011-0738-y

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  • DOI: https://doi.org/10.1007/s11274-011-0738-y

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