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Physiological and biochemical changes in tomato cultivar PT-3 with dual inoculation of mycorrhiza and PGPR against root-knot nematode

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Abstract

Arbuscular mycorrhizal fungi (AMF) and plant growth promoting rhizobacteria (PGPR) have potential to control soil-borne diseases including plant-parasitic nematodes. First, the effects of dual inoculation of mycorrhiza (Rhizophagus irregularis) and two stains of pseudomonads (Pseudomonas jessenii strain R62 and Pseudomonas synxantha strain R81) on tomato (Solanum lycopersicum cv. PT-3) growth were tested. Further, the physiological and biochemical changes caused by these beneficial organisms during infection by the root-knot nematode Meloidogyne incognita were studied. The experiment was conducted under glass house conditions and carried out up to one month after nematode inoculation. Plants treated with dual or individual inoculation of AMF and PGPR showed significantly enhanced plant growth and reduced nematode infection. In addition, they exhibited potent activity of phenolics (28 %) and defensive enzymes i.e. peroxidase (PO; 1.26 fold), polyphenyloxidase (PPO; 1.35 fold) and superoxide dismutase (SOD; 1.09 fold) while a significant reduction in malondialdehyde (MDA; 1.63 fold) and hydrogen peroxide (H2O2; 1.30 fold) content was recorded when compared to the nematode-infected plants. These findings indicate the feasibility of AMF and PGPR individually or in combinations as potential biocontrol agents for the management of root-knot nematodes.

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References

  • Ahmed N, Abbasi MW, Shaukat SS, Zaki MJ (2009) Physiological changes in leaves of mungbean plants infected with Meloidogyne javanica. Phytopathol Mediterr 48:262–268

    Google Scholar 

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

    Article  Google Scholar 

  • Al-Askar AA, Rashad YM (2010) Arbuscular mycorrhizal fungi: a biocontrol agent against common bean fusarium root rot disease. Plant Pathol J 9:31–38

    Article  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Anita B, Samiyappan R (2012) Induction of systemic resistance in rice by Pseudomonas fluorescens against rice root knot nematode Meloidogyne graminicola. J Biopest 5:53–59

    CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplast polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashraf MY, Akhtar K, Sarwar G, Ashraf M (2005) Role of rooting system in salt tolerance potential of different guar accessions. Agron Sustain Dev 25:243–249

    Article  Google Scholar 

  • Banuelos J, Alarcon A, Larsen JS, Cruz-Sánchez TD (2014) Interactions between arbuscular mycorrhizal fungi and Meloidogyne incognita in the ornamental plant Impatiens balsamina. J Soil Sci Plant Nutr 14(1):63–74

    Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:246–254

    Article  Google Scholar 

  • Bybd DW, Kirkpatrick JRT, Barker KR (1983) An improved technique for clearing and staining plant tissues for detection of nematodes. J Nematol 15:142–143

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carlsen SCK, Understrup A, Fomsgaard AG, Mortensen S, Ravnskov C (2008) Flavonoids in roots of white clover: interaction of arbuscular mycorrhizal fungi and a pathogenic fungus. Plant Soil 302(1–2):33–43

    Article  CAS  Google Scholar 

  • Claussen W (2005) Proline as a measure of stress in tomato plants. Plant Sci 168:241–248

    Article  CAS  Google Scholar 

  • Dai M, Wang HX, Yin YY, Wu X, Liu RJ (2008) Effects and mechanisms of interactions between arbuscular mycorrrhizal fungi and plant growth promoting rhizobacteria. Acta Ecol Sin 28:2854–2860

    Google Scholar 

  • Daudi A, Cheng Z, O’Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP (2012) The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • dos Anjos ECT, Cavalcante UMT, Gonçalves DMC, Pedrosa EMR, dos Santos VF, Maia LC (2010) Interactions between an arbuscular mycorrhizal fungus (Scutellospora heterogama) and the root-knot nematode (Meloidogyne incognita) on sweet passion fruit (Passiflora alata). Braz Arch Biol Technol 53:801–809

    Article  Google Scholar 

  • Duponnois R, Plenchette C (2003) A mycorrhiza helper bacterium enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian acacia species. Mycorrhiza 13:85–91

    Article  CAS  PubMed  Google Scholar 

  • El-Beltagi HS, Farahat AA, Alsayed A, Alsayed AA, Mahfoud NA (2012) Response of antioxidant substances and enzymes activities as a defense mechanism against root-knot nematode infection. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 40(1):132–142

    CAS  Google Scholar 

  • Elsen A, Gervacio D, Swennen R, Waele DD (2008) AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18:251–256

    Article  CAS  PubMed  Google Scholar 

  • Farahat AA, Alsayed AA, El-Beltagi HS, Mahfoud NM (2012) Impact of organic and inorganic fertilizers on nematode reproduction and biochemical alterations on tomato. Notulae Scientia Biologicae 4:58–66

    Google Scholar 

  • Flor-Peregrin E, Azcon R, Salmeron T, Talavera M (2012) Biological protection conferred by Glomus spp. and Bacillus megaterium against Meloidogyne incognita in tomato and pepper. IOBC-WPRS Bulletin 83:215–218

    Google Scholar 

  • Gaur R, Shani N, Kawaljeet K, Johri BN, Rossi P, Aragno M (2004) Diacetylphloroglucinol-producing pseudomonads do not influence AM fungi in wheat rhizosphere. Curr Sci 86:453–457

    CAS  Google Scholar 

  • Goswami J, Pandey RK, Tewari JP, Goswami BK (2008) Management of root knot nematode on tomato through application of fungal antagonists, Acremonium strictum and Trichoderma harzianum. J Environ Sci Health 43:237–240

    Article  CAS  Google Scholar 

  • Gurmani AR, Bano A, Salim M (2007) Effect of abscisic acid and 6-benzyladenine on growth and ion accumulation of wheat under salinity stress. Pak J Bot 39:141–149

    Google Scholar 

  • Hammerschmidt R, Nuckles EM, Kuae J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletorichum lagenarium. Physiol Plant Pathol 20:73–82

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agr Expt Sta 347:1–32

    Google Scholar 

  • Hol GWH, Cook R (2005) An overview of arbuscular mycorrhizal fungi–nematode interactions. Basic Appl Ecol 6:489–503

    Article  Google Scholar 

  • Hooper DJ, Hallman J, Subbotin S (2005) Methods for extraction, processing and detection of plant and soil nematodes. In: Luc M, Sikora R, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. CABI Publishing, Wallingford, pp. 53–86

    Chapter  Google Scholar 

  • Hyoe AT, Davoren JE, Wipf P, Fink MP, Kagan VE (2008) Targeting mitochondria. Acc Chem Res 41:87–97

    Article  Google Scholar 

  • Jaizme-Vega MC, Rodriguez-Romero AS, Nunez LAB (2006) Effect of the combined inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria on papaya (Carica papaya L.) infected with the root-knot nematode Meloidogyne incognita. Fruits 61:1–7

    Article  Google Scholar 

  • Jin D, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Mol 15:7313–7352

    Article  Google Scholar 

  • Kesba HH, El-Beltagi HES (2012) Biochemical changes in grape rootstocks resulted from humic acid treatments in relation to nematode infection. Asian Pac J Trop Biomed 2:287–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiewnick S, Sikora RA (2006) Biological control of the root-knot nematode Meloidogyne incognita by Paecilomyces lilacinus strain 251. Biol Control 38:179–187

    Article  Google Scholar 

  • Kokalis-Burelle N, Vavrina CS, Rosskopf EN, Shelby RA (2002) Field evaluation of plant growth-promoting Rhizobacteria amended transplant mixes and soil solarization for tomato and pepper production in Florida. Plant Soil 238:257–266

    Article  CAS  Google Scholar 

  • Korayem AM, El-Bassiouny HMS, El-Monem AA, Mohamed MMM (2012) Physiological and biochemical changes in different sugar beet genotypes infected with root-knot nematode. Acta Physiol Plant 34:1847–1861

    Article  CAS  Google Scholar 

  • Kotchoni SO, Gachomo EW (2006) The reactive oxygen species network pathways: an essential prerequisite for perception of pathogen attack and the acquired disease resistance in plants. J Biosci 31:389–404

    Article  CAS  PubMed  Google Scholar 

  • Kuniak E, Sklodowska M (2001) Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. Plant Sci 160:723–731

    Article  Google Scholar 

  • Leng P, Su S, Wei F, Yu F, Duan Y (2009) Correlation between browning, total phenolic content, polyphenol oxidase and several antioxidation enzymes during pistachio tissue culture. Acta Hortic 829:127–132

    Article  CAS  Google Scholar 

  • Liu R, Dai M, Wu X, Li M, Liu X (2012) Suppression of the root-knot nematode [Meloidogyne incognita (Kofoid & White) Chitwood] on tomato by dual inoculation with arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria. Mycorrhiza 22:289–296

    Article  PubMed  Google Scholar 

  • Mader P, Kaiser F, Adholeya A, Singh R, Uppal HS, Sharma AK, Srivastava R, Sahai V, Aragno M, Wiemken A, Johri BN, Fried PM (2011) Inoculation of root microorganisms for sustainable wheat rice and wheat black gram rotations in India. Soil Biol Biochem 43:609–619

    Article  CAS  Google Scholar 

  • Mayer AM, Harel E, Shaul RB (1965) Assay of catechol oxidase - a critical comparison of methods. Phytochem 5:783–789

    Article  Google Scholar 

  • Meena B, Radhajeyalakshmi R, Marimuthu T, Vidhyasekaran P, Doraiswamy S, Velazhahan R (2000) Induction of pathogenesis related proteins, phenolics and phenylalanine ammonia lyase in groundnut by Pseudomonas fluorescens. Z PflKrankh PflSchutz 107:514–527

    CAS  Google Scholar 

  • Melakeberhan H, Brook RC, Webster JM (1986) Relationship between physiological response of French beans of different age to Meloidogyne incognita and subsequent yield loss. Plant Pathol 35:203–213

    Article  Google Scholar 

  • Mishra CD, Mohanty KC (2007) Role of phenolics and enzymes in imparting resistance to rice plants against root-knot nematode, Meloidogyne graminicola. Ind J Nematol 37(2):131–134

    CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Nandakumar R, Babu S, Viswanathan R, Raghuchander T, Swamiappan R (2001) Induction of systemic resistance in rice against sheath blight disease by Pseudomonas fluorescens. Soil Biol Biochem 33:603–612

    Article  CAS  Google Scholar 

  • Padgham JL, Sikora RA (2007) Biological control potential and modes of action of Bacillus megaterium against Meloidogyne graminicola on rice. Crop Prot 26:971–977

    Article  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pnueli L, Liang H, Rozenberg M, Mittler R (2003) Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1) - deficient Arabidopsis plants. Plant J 34(2):187–203

    Article  CAS  PubMed  Google Scholar 

  • Rajendran L, Samiyappan R, Raguchander T, Saravanakumar D (2007) Endophytic bacteria mediated plant resistance against cotton bollworm. J Plant Interact 2:1–10

    Article  CAS  Google Scholar 

  • Ramamoorthy V, Viswanathan R, Raguchandar J, Prakasham T, Samiyappan R (2001) Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pest and diseases. Crop Prot 20:1–11

    Article  CAS  Google Scholar 

  • Roesti D, Gaur R, Johri BN, Imfeld G, Sharma S, Kawaljeet K, Aragno M (2006) Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields. Soil Biol Biochem 38:1111–1120

    Article  CAS  Google Scholar 

  • Sarma MVRK, Sahai V, Bisaria VS (2009) Genetic algorithm based medium optimization for enhanced production of fluorescent pseudomonad R81 and siderophores. Biochem Eng J 47:100–108

    Article  CAS  Google Scholar 

  • Sharma IP, Sharma AK (2015a) Application of arbuscular mycorrhiza for managing root-knot disease in tomato (Lycopersicon esculentum) under glass-house conditions in Pantnagar, India. Afr J Microbiol Res 9:463–468

    Article  Google Scholar 

  • Sharma IP, Sharma AK (2015b) Root–knot nematodes (Meloidogyne incognita) suppression through pre-colonized arbuscular mycorrhiza (Glomus intraradices) in tomato-PT3. Sci Agric 12:52–57

    Google Scholar 

  • Siddiqui ZA, Akhtar MS (2009) Effects of antagonistic fungi, plant growth-promoting rhizobacteria, and arbuscular mycorrhizal fungi alone and in combination on the reproduction of Meloidogyne incognita and growth of tomato. J Gen Plant Pathol 75:144–153

    Article  Google Scholar 

  • Siddiqui IA, Haque ES (2000) Use of Pseudomonas aerugiosa (Schroeter) Migula in the control of root rot-root knot disease complex on tomato. Nematol Mediterr 28:189–192

    Google Scholar 

  • Singh HB, Singh BN, Singh SP, Nautiyal CS (2010) Solid-state cultivation of Trichoderma harzianum NBRI-1055 for modulating natural antioxidants in soy-bean seed matrix. Bioresour Technol 101:6444–7253

    Article  CAS  PubMed  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 defense against Rhizoctonia solani. Eur J Plant Pathol 131:121–134

    Article  CAS  Google Scholar 

  • Singh A, Sarmab BK, Upadhyaya RS, Singh HB (2013) Compatible rhizosphere microbes mediated alleviation of biotic stress in chickpea through enhanced antioxidant and phenylpropanoid activities. Microbiol Res 168:33–40

    Article  CAS  PubMed  Google Scholar 

  • Sohrabi M, Mohammadi H, Mohammadi AH (2015) Influence of AM fungi, Glomus mosseae and Glomus intraradices on Chickpea Growth and Root-Rot Disease Caused by Fusarium solani f sp pisi under Greenhouse Conditions. J Agr Sci Tech 17:1919–1929

    Google Scholar 

  • Soriano M, Blanco A, Diaz P, Pastor FI (2000) An unusual pectate lyase from a Bacillus sp. with high activity on pectin: cloning and characterization. Microbiol 146:89–95

    Article  CAS  Google Scholar 

  • Swain B, Prasad JS (1988) Chlorophyll content in rice as influenced by the root-knot nematode, Meloidogyne graminicola infection. Curr Sci 57:895–896

    CAS  Google Scholar 

  • Tufail A, Arfan M, Gurmani AR, Khan A, Bano A (2013) Salicylic acid induced salinity tolerance in maize (Zea mays). Pak J Bot 45:75–82

    CAS  Google Scholar 

  • Vierheilig H, Steinkellner S, Khaosaad T, Garcia-Garrido JM (2008) The biocontrol effect of mycorrhization on soil-borne fungal pathogens and the autoregulation of the AM symbiosis: one mechanism, two effects? In: Varma A (ed) Mycorrhiza: genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer, Heidelberg, pp. 307–320

    Chapter  Google Scholar 

  • Vos C, Geerinckx K, Mkandawire R, Panis B, De Waele D, Elsen A (2012a) Arbuscular mycorrhizal fungi affect both penetration and further life stage development of root-knot nematodes in tomato. Mycorrhiza 22:157–163

    Article  PubMed  Google Scholar 

  • Vos CM, Tesfahuna AM, Panis B, De Waele D, Elsen A (2012b) Arbuscular mycorrhizal fungi induce systemic resistance in tomato against the sedentary nematode Meloidogyne incognita and the migratory nematode Pratylenchus penetrans. Appl Soil Ecol 61:1–6

    Article  Google Scholar 

  • Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panis B, Gianinazzi-Pearson V (2013) Mycorrhiza-induced resistance against the root–knot nematode Meloidogyne Incognita involves priming of defense gene responses in tomato. Soil Biol Biochem 60:45–54

    Article  CAS  Google Scholar 

  • Waceke JW, Waudo SW, Sikora R (2001) Suppression of Meloidogyne hapla by arbuscular mycorrhiza fungi (AMF) on pyrethrum in Kenya. Int J Pest Manage 47(2):135–140

    Article  Google Scholar 

  • Wani AH, Bhat MY (2012) Control of root-knot nematode, Meloidogyne incognita by urea coated with Nimin or other natural oils on mung. Vigna radiata (L) R Wilczek J Biopest 5:255–258

    Google Scholar 

  • Wijngaard HH, Roble C, Brunton N (2009) A survey of Irish fruit and vegetable waste and byproducts as a source of polyphenolic antioxidants. Food Chem 116:202–207

    Article  CAS  Google Scholar 

  • Wrzaczek M, Brosche M, Kangasjarvi J (2013) ROS signaling loops—production, perception, regulation. Curr Opin Plant Biol 16:575–582

    Article  CAS  PubMed  Google Scholar 

  • Xu XM, Xu K, Yu Q, Zhang-Xiaoyan (2008) The relationship between resistance to Meloidogyne incognita and phenylpropanes metabolism in roots of eggplant root-stock. Acta Phys Sin 35:43–46

    CAS  Google Scholar 

  • Zhang S, White TL, Martinez MC, McInroy JA, Kloepper JW, Klassen W (2010) Evaluation of plant growth-promoting rhizobacteria for control of Phytophthora blight on squash under greenhouse conditions. Biol Control 53:129–135

    Article  Google Scholar 

  • Zieslin N, Ben-Zaken R (1993) Peroxidase activity and presence of phenolic substances in peduncles of rose flowers. Plant Physiol Biochem 31:333–339

    CAS  Google Scholar 

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Acknowledgments

The authors wish to thanks all the members of Rhizosphere Biology Lab, CBSH, GBPUAT, Pantnagar who support, help and encourage the research works.

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  1. Department of Biological Sciences, College of Basic Sciences and Humanities, G.B. Pant University of Agriculture & Technology, Pantnagar – 263 145, U.S, Nagar, Uttarakhand, India

    Ishwar Prakash Sharma & A. K. Sharma

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Sharma, I.P., Sharma, A.K. Physiological and biochemical changes in tomato cultivar PT-3 with dual inoculation of mycorrhiza and PGPR against root-knot nematode. Symbiosis 71, 175–183 (2017). https://doi.org/10.1007/s13199-016-0423-x

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