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Inoculation of seed-borne fungus in the rhizosphere of Festuca arundinacea promotes hydrocarbon removal and pyrene accumulation in roots

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Abstract

Background and aims

The selective inoculation of specific hydrocarbon-degrading microbes into the plant rhizosphere offers a useful means for remediating hydrocarbon-contaminated soils. The effect of inoculating a seed-borne filamentous fungus (Lewia sp.) on hydrocarbon removal by Festuca arundinacea and its growth was studied on perlite (model soil) and soil, both spiked with hydrocarbons.

Methods

A hydrocarbon mixture (1,500 mg kg−1) of two polycyclic aromatic hydrocarbons (PAH), phenanthrene and pyrene, blended with hexadecane (1.0:0.5:0.5 weight) was used. Greenhouse experiments were carried out for 45 days. Inoculated and non-inoculated plants were grown in dark cylindrical glass pots containing perlite or soil.

Results

Inoculation with Lewia sp. stimulated (100 %) root growth in spiked perlite. Inoculated plants showed higher phenanthrene removal (100 %) compared to non-inoculated plants in perlite and soil. Pyrene removal by inoculated plants was 37-fold higher than that by non-inoculated plants in perlite; in soil, pyrene removal by inoculated plants (97.9 %) differed significantly from that of non-inoculated plants (91.4 %). Accumulation of pyrene in roots (530.9 mg kg−1 of dry roots) was promoted in perlite.

Conclusions

Our results demonstrate that Lewia sp. (endophytic fungus) improved the efficiency of PAH removal by F. arundinacea, on both perlite and soil, stimulating pyrene accumulation in roots.

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References

  • Acevedo F, Pizzul L, Castillo MP, Cuevas R, Diez MC (2011) Degradation of polycyclic aromatic hydrocarbons by the Chilean white-rot fungus Anthracophyllum discolor. J Hazard Mater 185:212–219

    Article  PubMed  CAS  Google Scholar 

  • Cerniglia CE, Sutherland JB (2010) Degradation of polycyclic aromatic hydrocarbons by fungi. In: Timmis KN (ed) Handbook of Hydrocarbon and Lipid Microbiology. Springer-Verlag, Berlin Heidelberg, pp 2079–2110

    Chapter  Google Scholar 

  • Chaudhry Q, Blom-Zandstra M, Gupta S, Joner EJ (2005) Utilising the synergy between plants and rhizosphere microorganisms to enhance breakdown of organic pollutants in the environment. Environ Sci Pollut Res Int 12:34–48

    Article  PubMed  CAS  Google Scholar 

  • Cheema SA, Khan MI, Tang X, Zhang C, Shen C, Malik Z, Ali S, Yang J, Shen K, Chen X, Chen Y (2009) Enhancement of phenanthrene and pyrene degradation in rhizosphere of tall fescue (Festuca arundinacea). J Hazard Mater 166:1226–1231

    Article  PubMed  CAS  Google Scholar 

  • Chiapusio G, Pujol S, Toussaint ML, Badot PM, Binet P (2007) Phenanthrene toxicity and dissipation in rhizosphere of grassland plants (Lolium perenne L. and Trifolium pratense L.) in three spiked soils. Plant Soil 294:103–112

    Article  CAS  Google Scholar 

  • Dugay A, Herrenknecht C, Czok M, Guyon F, Pages N (2002) New procedure for selective extraction of polycyclic aromatic hydrocarbons in plants for gas chromatographic–mass spectrometric analysis. J Chromatogr A 958:1–7

    Article  PubMed  CAS  Google Scholar 

  • Escalante-Espinosa E, Gallegos-Martínez ME, Favela-Torres E, Gutiérrez-Rojas M (2005) Improvement of the hydrocarbon phytoremediation rate by Cyperus laxus Lam. inoculated with a microbial consortium in a model system. Chemosphere 59:405–413

    Article  PubMed  CAS  Google Scholar 

  • Gan S, Lau EV, Ng HK (2009) Remediation of soil contaminated with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater 172:532–549

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Ling W (2006) Comparison for plant uptake of phenanthrene and pyrene from soil and water. Biol Fertil Soils 42:387–394

    Article  CAS  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  PubMed  CAS  Google Scholar 

  • Gawronski SW, Gawrosnska H (2007) Plant taxonomy for phytoremediation. In: Samotokin B, Marmiroli M, Marmiroli N (eds) Advanced science and technology for biological decontamination of sites affected by chemical and radiological nuclear agents. Springer, Netherlands, pp 79–88

    Chapter  Google Scholar 

  • Karthikeyan R, Kulakow PA (2003) Soil plant microbe interactions in phytoremediation. In: Scheper T (ed) Advances in Biochemical Engineering/Biotechnology. Springer-Verlag, Berlin Heidelberg, pp 51–74

    Google Scholar 

  • Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact 17:6–15

    Article  PubMed  CAS  Google Scholar 

  • Kwasna H, Kiosak B (2003) Lewia avenicola sp. nov. and its Alternaria anamorph from oat grain, with a key to the species of Lewia. Mycol Res 107:371–376

    Article  PubMed  Google Scholar 

  • Kwasna H, Ward E, Kosiak B (2006) Lewia hordeicola sp. nov. from barley grain. Mycol 98:662–668

    Article  Google Scholar 

  • Larena I, Salazar O, González V, Julián MC, Rubio V (1999) Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. J Biotechnol 75:187–194

    Article  PubMed  CAS  Google Scholar 

  • Lazcano EA, Guerrero-Zuñiga LA, Rodriguez-Tovar A, Rodriguez-Dorantes A, Vasquez-Murrieta MS (2010) Rhizospheric plant-microbe interactions that enhance the remediation of contaminated soil. In: Méndez-Vilas A (ed) Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. Microbiology Book Series, Formatex Research Center, Spain, pp 251–256

    Google Scholar 

  • Lugtenberg BJJ, Chin-A-Woeng TF, Bloemberg GV (2002) Microbe–plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383

    Article  PubMed  CAS  Google Scholar 

  • Martínez DA, Landini AM, Svartz H, Vence L, Bottini L, Mascarini L, Orden S, Vilella F (2006) Physical and hydraulic properties of perlites used in rose cultures and their dependency on time. Ci Suelo 24:177–182

    Google Scholar 

  • Mohsenzadeh F, Nasseri S, Mesdaghinia A, Nabizadeh R, Zafari D, Khodakaramian G, Chehregani A (2010) Phytoremediation of petroleum-polluted soil: application of Polygonum aviculare and its root-associated (penetrated) fungal strains for bioremediation of petroleum-polluted soils. Ecotoxicol Environ Saf 73:613–619

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Ndimele PE (2010) A review on the phytoremediation of petroleum hydrocarbons. Pak J Biol Sci 13:715–722

    Article  PubMed  CAS  Google Scholar 

  • Paparu P, Dubois T, Coyne D, Viljoen A (2007) Defense-related gene expression in susceptible and tolerant bananas (Musa spp.) following inoculation with non-pathogenic Fusarium oxysporum endophytes and challenge with Radopholus similis. Physiol Mol Plant Pathol 71:149–157

    Article  CAS  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  PubMed  CAS  Google Scholar 

  • Reynoso-Cuevas L, Gallegos-Martínez ME, Cruz-Sosa F, Gutiérrez-Rojas M (2011) Phytoremediation and removal mechanisms in Bouteloua curtipendula growing in sterile hydrocarbon spiked cultures. Int J Phytoremediat 13:613–625

    Article  CAS  Google Scholar 

  • Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340

    Article  PubMed  CAS  Google Scholar 

  • Sinha RK, Herat S, Tandon PK (2007) Phytoremediation: role of plant in contaminated site management. In: Signh SN, Tripathi RD (eds) Environmental bioremediation technologies. Springer, Berlin, pp 315–330

    Chapter  Google Scholar 

  • Soleimani M, Afyuni M, Hajabbasi MA, Nourbakhsh F, Sabzalian MR, Christensen JH (2010) Phytoremediation of an aged petroleum contaminated soil using endophyte infected and non-infected grasses. Chemosphere 81:1084–1090

    Article  PubMed  CAS  Google Scholar 

  • Srogi K (2007) Monitoring of environmental exposure to polycyclic aromatic hydrocarbons: a review. Environ Chem Lett 5:169–195

    Article  CAS  Google Scholar 

  • Su Y, Yang X, Chiou CT (2008) Effect of rhizosphere on soil microbial community and in-situ pyrene biodegradation. Front Environ Sci Engin China 2:468–474

    Article  Google Scholar 

  • Sudip SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20:243–248

    Article  Google Scholar 

  • Tarkka M, Schrey S, Hampp R (2008) Plant associated soil micro-organisms. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Berlin, pp 3–51

    Chapter  Google Scholar 

  • Thomas SE, Crozier J, Catherine Aime M, Evans HC, Holmes KA (2008) Molecular characterisation of fungal endophytic morphospecies associated with the indigenous forest tree, Theobroma gileri, in Ecuador. Mycol Res 112:852–860

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

A. Cruz-Hernández received a fellowship from the Consejo Nacional de Ciencia y Tecnología (CONACyT). This research was partially supported by Petróleos Mexicanos (PEMEX)-Refinación.

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Authors and Affiliations

  1. Departamento de Biotecnología, Universidad Autónoma Metropolitana-Iztapalapa, Av. San Rafael Atlixco No. 186. Col. Vicentina, Iztapalapa, Mexico, D. F. C.P. 09340, Mexico

    A. Cruz-Hernández, A. Tomasini-Campocosio, F. J. Fernández-Perrino & M. Gutiérrez-Rojas

  2. Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana-Iztapalapa, Av. San Rafael Atlixco No. 186. Col. Vicentina, Iztapalapa, Mexico, D. F. C.P. 09340, Mexico

    L. J. Pérez-Flores

Authors
  1. A. Cruz-Hernández
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  2. A. Tomasini-Campocosio
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  3. L. J. Pérez-Flores
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  4. F. J. Fernández-Perrino
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  5. M. Gutiérrez-Rojas
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Corresponding author

Correspondence to M. Gutiérrez-Rojas.

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Responsible Editor: Bernard Glick.

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Cruz-Hernández, A., Tomasini-Campocosio, A., Pérez-Flores, L.J. et al. Inoculation of seed-borne fungus in the rhizosphere of Festuca arundinacea promotes hydrocarbon removal and pyrene accumulation in roots. Plant Soil 362, 261–270 (2013). https://doi.org/10.1007/s11104-012-1292-6

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  • DOI: https://doi.org/10.1007/s11104-012-1292-6

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