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Improved growth and control of oxidative stress in plants of Festuca arundinacea exposed to hydrocarbons by the endophytic fungus Lewia sp.

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Abstract

Aims

The protective role of fungal endophytes in plants under stress by hydrocarbons is yet poorly understood. The influence of the endophytic fungus Lewia sp. on growth and oxidative stress control in plants of Festuca arundinacea exposed to a hydrocarbon mixture (HCM) was evaluated.

Methods

Plants of F. arundinacea were inoculated or not with Lewia sp. to establish endophytic association. After 15 days, the plant growth, oxidative stress, and activity of antioxidant enzymes were analyzed in associated and unassociated plants. Then, both groups of plants were exposed for 7 days to a HCM (800 mg kg−1) in a model soil. The effect of the HCM was assessed in the plants through the same variables as mentioned above.

Results

Endophytic association was established after 15 days. The fungus enhanced plant growth, as well as H2O2 and malondialdehyde concentration, and decreased glutathione S-transferase (GST) activity. Lewia sp. decreased the H2O2 concentration in plants exposed to the HCM and increased the activity of superoxide dismutase and peroxidases, while significantly decreasing GST activity.

Conclusions

This study demonstrates the positive role of Lewia sp. in promoting growth and alleviating oxidative stress in F. arundinacea exposed to hydrocarbons.

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References

  • Abdellatif L, Bouzid S, Kaminskyj S, Vujanovic V (2009) Endophytic hyphal compartmentalization is required for successful symbiotic Ascomycota association with root cells. Mycol Res 113:782–791

    Article  PubMed  Google Scholar 

  • Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. S Afr J Bot 77:36–44

    Article  CAS  Google Scholar 

  • Alkio M, Tabuchi TM, Wang X, Colớn-Carmona A (2005) Stress responses to polycyclic aromatic hydrocarbons in Arabidopsis include growth inhibition and hypersensitive response-like symptoms. J Exp Bot 56:2983–2994

    Article  CAS  PubMed  Google Scholar 

  • Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J, Samuels GJ, Choi I-Y, Holmes KA (2006) Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224:1449–1464

    Article  CAS  PubMed  Google Scholar 

  • Balasubramanlyam A, Chapman MM, Harvey JP (2015) Responses of tall fescue (Festuca arundinacea) to growth in naphthalene-contaminated sand: xenobiotic stress versus water stress. Environ Sci Pollut Res 22:7495–7507

    Article  Google Scholar 

  • Baptista P, Martins A, Pais MS, Tavares RM, Lino-Neto T (2007) Involvement of reactive oxygen species during early stages of ectomycorrhizal establishment between Castanea sativa and Pisolithus tictorius. Mycorrhiza 17:185–193

    Article  CAS  PubMed  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2013) ROS as key players in plant stress signaling. J Exp Bot. doi:10.1093/jbx/ert375

    PubMed  Google Scholar 

  • Becerra-Castro C, Prieto-Fernández Á, Kidd SP, Weyens N, Rodrígruez-Garrido B, Touceda-González M, Acea MJ, Vangronsveld J (2013) Improving performance of Cytisus striatus on substrates contaminated with hexachlorocyclohexane (HCH) isomers using bacterial inoculants: developing a phytoremediation strategy. Plant Soil 362:247–260

    Article  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  PubMed  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775

    Article  Google Scholar 

  • Cheeseman JM (2006) Hydrogen peroxide concentration in leaves under natural conditions. J Exp Bot 57:2435–2444

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Hernández A, Tomasini-Campocosio A, Pérez-Flores LJ, Fernández-Perrino FJ, Gutiérrez-Rojas M (2013) Inoculation of seed-borne fungus in the rhizosphere of Festuca arundinacea promotes hydrocarbon removal and pyrene accumulation in roots. Plant Soil 362:261–270

    Article  Google Scholar 

  • Cvjetko P, Tolić S, Šikić S, Balen B, Tkalec M, Vidaković-Cifrek Ž, Pavlica M (2010) Effect of copper on the toxicity and genotoxicity of cadmium in duckweed (Lemna minor L.). Arh Hig Rada Toksikol 61:287–296

    CAS  PubMed  Google Scholar 

  • Debiane D, Garçon G, Verdin A, Fontaine J, Durand R, Grandmougin-Ferjani A, Shirali P, Sahraoui AL-H (2008) In vitro evaluation of the oxidative stress and genotoxic potentials of anthracene on mycorrhizal chicory roots. Environ Exp Bot 64:120–127

    Article  CAS  Google Scholar 

  • Debiane D, Garçon G, Verdin A, Fontaine J, Durand R, Shirali P, Grandmougin-Ferjani A, Sahraoui AL-H (2009) Mycorrhization alleviates benzo[a]pyrene-induced oxidative stress in an in vitro chicory root model. Phytochemistry 70:1421–1427

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. In: Jacoby WB (ed) Method Enzymol 77: 398–405

  • Hu Z, Xie Y, Jin G, Fu J, Li H (2015) Growth responses of two tall fescue cultivars to Pb stress and their metal accumulation characteristics. Ecotoxicology 24:563–572

    Article  CAS  PubMed  Google Scholar 

  • Juszczuk IM, Tybura A, Rychter AM (2008) Protein oxidation in leaves and roots of cucumber plants (Cucumis sativus L.) mutant MSC16 and wild type. J Plant Physiol 165:355–365

    Article  CAS  PubMed  Google Scholar 

  • Kawaoka A, Matsunaga E, Endo S, Kondo S, Yoshida K, Shinmyo A, Ebinuma H (2003) Ectopic expression of a horseradish peroxidase enhances growth rate and increases oxidative stress resistance in hybrid aspen. Plant Physiol 132:1177–1185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khalmuratova I, Kim H, Nam Y-J, Oh Y, Jeong M-J, Choi H-R, You Y-H, Choo Y-S, Lee I-J, Shin J-H, Yoon H, Kim J-G (2015) Diversity and plant growth promoting capacity of endophytic fungi associated with halophytic plants from the west coast of Korea. Mycobiology 43:373–383

    Article  PubMed  PubMed Central  Google Scholar 

  • Kreslavski VD, Lankin AV, Vasilyeva GK, Luybimov VY, Semenova GN, Schmitt F-J, Friedrich T, Allakhverdiev SI (2014) Effects of polyaromatic hydrocarbons on photosystem II activity in pea leaves. Plant Physiol Biochem 81:135–142

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Hasan AM, Chkrabrty D, Deo TR, Shanker DR, Kumar TP (2013) Differential expression of rice Lambda class GST gene family members during plant growth, development, and response to stress conditions. Plant Mol Biol Report 31:569–580

    Article  CAS  Google Scholar 

  • Kvesitadze E, Sadunishvili T, Kvesitadze GK (2009) Mechanisms of organic contaminants uptake and degradation in plants. World Acad Sci Eng Technol 55:458–468

    Google Scholar 

  • Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume host. Plant Physiol 137:1319–1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Weisman D, Ye Y, Cui B, Huang Y, Colón-Carmona A, Wang Z (2009) An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana. Plant Sci 176:375–382

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrhough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–273

    CAS  PubMed  Google Scholar 

  • Mei C, Flinn BS (2010) The use of beneficial microbial endophytes for plant biomass and stress tolerance improvement. Recent Pat Biotechnol 4:81–95

    Article  CAS  PubMed  Google Scholar 

  • Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61:4197–4220

    Article  CAS  PubMed  Google Scholar 

  • Mirzahosseini Z, Shabani L, Sabzalian MR, Sharifi-Tehrani M (2014) Neotyphodium endophytes may increase tolerance to Ni in tall fescue. Eur J Soil Biol 63:33–40

    Article  CAS  Google Scholar 

  • Mirzahosseini Z, Shabani L, Sabzalian MR, Sharifi-Tehrani M (2015) ABC transporter and metallothionein expression affected by NI and Epichloe endophyte infection in tall fescue. Ecotoxicol Environ Saf 120:13–19

    Article  Google Scholar 

  • Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Vitam Horm 72:155–202

    Article  CAS  PubMed  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 

  • Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J Integr Plant Biol 52:195–204

    Article  CAS  PubMed  Google Scholar 

  • Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315

    Article  CAS  PubMed  Google Scholar 

  • Pryor WA, Castle L (1984) Chemical methods for the detection of lipid hydroperoxides. Methods Enzymol 105:293–299

    Article  CAS  PubMed  Google Scholar 

  • Rojas-Loria CC, Favela-Torres E, González-Márquez H, Volke-Sepúlveda TL (2014) Role of glutathione and glutathione S-transferase in lead tolerance and bioaccumulation by Dodonea viscosa (L.) Jacq. Acta Physiol Plant 36:2501–2510

    Article  CAS  Google Scholar 

  • Shahrtash M (2013) Plant glutathione S-transferases function during environmental stresses: a review article. Rom J Biol 58:19–25

    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  CAS  PubMed  Google Scholar 

  • Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari S, Lata C, Singh CP, Shekhar NC (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117

    Article  CAS  PubMed  Google Scholar 

  • Tomar RS, Jajoo A (2015) Photomodified fluoranthene exerts more harmful effects as compared to intact fluoranthene by inhibiting growth and photosynthetic processes in wheat. Ecotoxicol Environ Saf 122:31–36

    Article  CAS  PubMed  Google Scholar 

  • White JF Jr, Torres SM (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440–446

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Fan X, Li C, Nan Z (2010) Effects of cadmium stress and seed germination, seedling growth and antioxidative enzymes in Achnatherum inebrians plants infected with a Neotyphodium endophyte. Plant Growth Regul 60:91–97

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was partially supported by Consejo Nacional de Ciencia y Tecnologia (CONACyT), Mexico. The authors acknowledge Dr. David M. Diaz-Pontones for the support in confocal microscopy analysis. C. Mendarte-Alquisira thanks CONACyT for the financial support (grant number 35330).

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Correspondence to Tania Volke-Sepúlveda.

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Responsible Editor: Alain Pierret.

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Mendarte-Alquisira, C., Gutiérrez-Rojas, M., González-Márquez, H. et al. Improved growth and control of oxidative stress in plants of Festuca arundinacea exposed to hydrocarbons by the endophytic fungus Lewia sp.. Plant Soil 411, 347–358 (2017). https://doi.org/10.1007/s11104-016-3035-6

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