Skip to main content
SpringerLink
Log in

Microbial Consortium-Induced Changes in Oxidative Stress Markers in Pea Plants Challenged with Sclerotinia sclerotiorum

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The ability for rhizobacteria and fungus to act as bioprotectants via induced systemic resistance has been demonstrated, and considerable progress has been made in elucidating the mechanisms of plant–biocontrol agent–pathogen interactions. Pseudomonas aeruginosa PJHU15, Trichoderma harzianum TNHU27, and Bacillus subtilis BHHU100 from rhizospheric soils were used singly and in consortium and assessed on the basis of their ability to provide disease protection by relating changes in ascorbic acid and hydrogen peroxide (H2O2) production, lipid peroxidation, and antioxidant enzymes in pea under the challenge of Sclerotinia sclerotiorum. Increased production of H2O2 24 h after pathogen challenge was observed and was 254.4 and 231.7–287.7 % higher in the triple consortium and singly treated plants, respectively, when compared to untreated challenged control plants. A similar increase in ascorbic acid content and ascorbate peroxidase activity was observed 24 and 48 h after pathogen challenge, respectively, whereas increased activities of catalase, guaiacol peroxidase, and glutathione peroxidase were observed 72 h after pathogen challenge. Similarly, lipid peroxidation reached a maximum at 72 h of pathogen challenge and was 61.2 and 11.2–32.1 % less in the triple consortium and singly treated plants, respectively, when compared to untreated challenged control plants. These findings suggest that the interaction of microorganisms in the rhizosphere enhanced protection from oxidative stress generated by pathogen attack through induction of antioxidant enzymes and improved reactive oxygen species management.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  • Akhtar MS, Siddiqui ZA (2008) Biocontrol of root-rot disease complex of chickpea by Glomus intraradices, Rhizobium sp. and Pseudomonas striata. Crop Prot 27:410–417

    Article  Google Scholar 

  • Anderson ME (1996) Glutathione. In: Punchard NA, Kelly FJ (eds) Free radicals: a practical approach. Oxford University Press, Oxford, pp 213–226

    Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ et al (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287

    Google Scholar 

  • Bestwick CS, Brown IR, Benneth MHR, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9:209–221

    PubMed  CAS  Google Scholar 

  • Cessna SG, Sears VE, Dickman MB, Low PS (2000) Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum suppresses the oxidative burst of the host plant. Plant Cell 12:2191–2200

    PubMed  CAS  Google Scholar 

  • Conklin PL, Barth C (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environ 27:959–970

    Article  CAS  Google Scholar 

  • de Boer M, Bom P, Kindt F, Keurentjes JJB, van der Sluis I, van Loon LC, Bakker PAHM (2003) Control of Fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms. Biol Control 93:626–632

    Google Scholar 

  • El-Zahaby HB, Gullner G, Király Z (1995) Effects of powdery mildew infection of barley on the ascorbate–glutathione cycle and other antioxidants in different host-pathogen interactions. Biochem Cell Biol 85(10):1225–1230

    CAS  Google Scholar 

  • Jain A, Singh S, Sarma BK, Singh HB (2012) Microbial consortium mediated reprogramming of defense network in pea to enhance tolerance against Sclerotinia sclerotiorum. J Appl Microbiol 112(3):537–550

    Article  PubMed  CAS  Google Scholar 

  • Jetiyanon K (2007) Defensive-related enzyme response in plants treated with a mixture of Bacillus strains (IN937a and IN937b) against different pathogens. Biol Control 42:178–185

    Article  Google Scholar 

  • Kang KM, Saltveit ME (2002) Chilling tolerance of corn, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576

    Article  PubMed  CAS  Google Scholar 

  • Keller T, Schwager H (1977) Air pollution and ascorbic acid. Eur J Plant Pathol 7:338–350

    Article  CAS  Google Scholar 

  • Kuźniak E, Urbanek H (2000) The involvement of hydrogen peroxide in plant responses to stresses. Acta Physiol Plant 22(2):195–203

    Article  Google Scholar 

  • Lee KP, Kim C, Landgraf F, Apel K (2007) EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 104:10270–10275

    Article  PubMed  CAS  Google Scholar 

  • Lowry OH, Rosenbrough JJ, Farr AL, Randall RJ (1951) Estimation of protein with the folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Lu H, Higgins VJ (1999) The effect of hydrogen peroxide on the viability of tomato cells and of the pathogen Cladosporium fulvum. Physiol Mol Plant Pathol 54:131–143

    Article  CAS  Google Scholar 

  • Malenčić D, Kiprovski B, Popović M, Prvulović D, Miladinović J, Djordjević V (2010) Changes in antioxidant systems in soybean as affected by Sclerotinia sclerotiorum (Lib.) de Bary. Plant Physiol Biochem 48(10–11):903–908

    PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Murgia I, Tarantino D, Vannini C, Bracale M, Carrabvieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–995

    Article  PubMed  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nizamuddin A (1987) NADPH-dependent and O2-dependent lipid peroxidation. Biochem Educ 15(2):58–62

    Article  Google Scholar 

  • Noctor G, Foyer C (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:51–58

    Article  Google Scholar 

  • Philosoph-Hadas S, Meir S, Akiri B, Kanner J (1994) Oxidative defense systems in leaves of three edible herb species in relation to their senescence rates. J Agric Food Chem 42(11):2376–2381

    Article  CAS  Google Scholar 

  • Salin ML (1988) Toxic oxygen species and protective systems of the chloroplast. Physiol Plant 72:681–689

    Article  CAS  Google Scholar 

  • Sarma BK, Ameer Basha S, Singh DP, Singh UP (2007) Use of nonconventional chemicals as an alternative approach to protect chickpea (Cicer arietinum) from Sclerotinia stem rot. Crop Prot 26:1042–1048

    Article  CAS  Google Scholar 

  • Singh BN, Singh A, Singh SP, Singh HB (2011) Trichoderma harzianum-mediated reprogramming of oxidative stress response in root apoplast of sunflower enhances defence against Rhizoctonia solani. Eur J Plant Pathol 131:121–134

    Article  CAS  Google Scholar 

  • Srivastava R, Khalid A, Singh US, Sharma AK (2010) Evaluation of arbuscular mycorrhizal fungus, fluorescent Pseudomonas and Trichoderma harzianum formulation against Fusarium oxysporum f. sp. lycopersici for the management of tomato wilt. Biol Control 53:24–31

    Article  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Vallad GE, Goodman RM (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44:1920–1934

    Article  Google Scholar 

  • Velikova V (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Walz A, Sell IZ, Theisen S, Kortekamp A (2008) Reactive oxygen intermediates and oxalic acid in the pathogenesis of the necrotrophic fungus Sclerotinia sclerotiorum. Eur J Plant Pathol 120(4):317–330

    Article  CAS  Google Scholar 

  • Willets HJ, Wong JAL (1980) The biology of Sclerotinia sclerotiorum, S. trifoliorum and S. minor with emphasis on species nomenclature. Bot Rev 46:101–165

    Article  Google Scholar 

  • Williams R, Rohr AM, Wang WT, Choi IY, Lee P, Berman NEJ, Lynch SG, LeVine SM (2011) Iron deposition is independent of cellular inflammation in a cerebral model of multiple sclerosis. BMC Neurosci 12:59

    Article  PubMed  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–692

    PubMed  CAS  Google Scholar 

  • Xu X, Qin G, Tian S (2008) Effect of microbial biocontrol agents on alleviating oxidative damage of peach fruit subjected to fungal pathogen. Int J Food Microbiol 126:153–158

    Article  PubMed  CAS  Google Scholar 

  • Zheng X, Van Huystee RB (1992) Peroxide-regulated elongation of segments from peanuts hypocotyls. Plant Sci 81:47–56

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Akansha Jain is grateful to Department of Science and Technology, Government of India, New Delhi, for financial assistance under AORC scheme as INSPIRE-JRF.

Author information

Authors and Affiliations

  1. Department of Botany, Banaras Hindu University, Varanasi, Uttar Pradesh, India

    Akansha Jain, Akanksha Singh & Surendra Singh

  2. Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, 221005, India

    Harikesh Bahadur Singh

Authors
  1. Akansha Jain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akanksha Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Surendra Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harikesh Bahadur Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harikesh Bahadur Singh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jain, A., Singh, A., Singh, S. et al. Microbial Consortium-Induced Changes in Oxidative Stress Markers in Pea Plants Challenged with Sclerotinia sclerotiorum . J Plant Growth Regul 32, 388–398 (2013). https://doi.org/10.1007/s00344-012-9307-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-012-9307-3

Keywords

Search

Navigation