Advertisement

Role of plant growth promoting Bacteria (PGPRs) as biocontrol agents of Meloidogyne incognita through improved plant defense of Lycopersicon esculentum

  • Kanika Khanna
  • Vijay Lakshmi Jamwal
  • Sukhmeen Kaur Kohli
  • Sumit G. Gandhi
  • Puja Ohri
  • Renu BhardwajEmail author
  • Leonard Wijaya
  • Mohammed Nasser Alyemeni
  • Parvaiz AhmadEmail author
Regular Article
  • 97 Downloads

Abstract

Background and aims

Root-knot nematodes are major constraints among different pathogens with wide host range and cause severe agricultural loss worldwide. The present study was designed to understand the role of plant growth promoting bacteria (Pseudomonas aeruginosa & Burkholderia gladioli) on growth and antioxidative potential in nematode infected Lycopersicon esculentum seedlings.

Methods

An experiment was conducted to assess the levels of superoxide anions, H2O2 and MDA contents generated during nematode infection. Moreover, the contribution of antioxidative enzymes, non-enzymatic antioxidants, total antioxidants and gene expression profiling was also carried out in nematode infected Lycopersicon esculentum seedlings.

Results

The results of present study revealed that nematode infection reduced the growth of seedlings which upon inoculation of microbes was improved. Moreover, number of galls were reduced upon supplementation of these strains. Nematode infection also caused accumulation of superoxide anion, H2O2, and malondialdehyde contents along with nuclear damage and loss of cell viability which was reduced upon supplementation of microbes. The oxidative burst generated enhanced various antioxidant enzymes such as SOD (30.6%), POD (3.6%), CAT (18.1%), GPOX (65.9%), APOX (24.8%), GST (5.6%), DHAR (13.9%), GR (11%) and PPO (2.5%) which were further elevated upon application of P. aeruginosa (23.9%, 7.2%, 7%, 66%, 28.9%, 71.3%, 14.5%, 10.6% and 38.3%) and B. gladioli (5.1%, 30.6%, 16.2%, 92.1%, 78.5%, 97.5%, 15.5%, 65.7% and 23.2%). The non-enzymatic antioxidants (glutathione, ascorbic acid and tocopherol) and total antioxidants contents (both water soluble and lipid soluble) were also enhanced upon inoculation of microbes. Confocal microscopy revealed the improvement in nuclear damage and cell viability in microbe inoculated roots. Gene expression profiling revealed the enhanced expression levels of SOD, POD, CAT, GR, GPOX, APOX, PPOgenes in P.aeruginosa inoculated nematode infected seedlings by 53%, 2.7%, 64.1%, 10.4%,19.7%, 29.2%, 38.4% and B. gladioli inoculated seedlings by 18.3%,144%, 67%, 43%, 308%, 151% respectively.

Conclusions

The results therefore suggest the favourable aspects of micro-organisms in modulating growth characteristics and antioxidative defense expression of Lycopersicon esculentum to encounter oxidative stress generated under nematode infection.

Keywords

Root-knot nematodes Oxidative stress Plant growth promoting rhizobacteria Antioxidative defense Gene expression studies 

Abbreviations

MDA

Malondialdehyde

H2O2

Hydrogen peroxide

CAT

Catalase

GST

Glutathione-S-transferase

GPOX

Glutathione peroxidase

APOX

Ascorbate peroxidase

DHAR

Dehydroascorbate peroxidase

GR

Glutathione reductase

SOD

Superoxide dismutase

POD

Guaiacol peroxidase

PPO

Polyphenol oxidase

WSA

Water soluble Antioxidants

LSA

Lipid soluble Antioxidants

ASA

Ascorbic acid

GSH

Glutathione

ROS

Reactive oxygen species

PPB

Phosphate buffer

PI

Potassium Iodide

TCA

Trichloroacetic acid

CLSM

Confocal laser scanning microscope

BSA

Bovine serum albumin

Notes

Acknowledgments

The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for its funding to the Research Group number (RGP-199).

Author contribution

Renu Bhardwaj, Kanika Khanna and Parvaiz Ahmad designed the experimental work. Kanika Khanna, Sukhmeen Kaur Kohli and Vijay Laxmi Jamwal performed the work. Sumit Gandhi, Leonard Wijaya and Mohammed Nasser Alyemeni analyzed the data. Puja Ohri, Mohammed Nasser Alyemeni, Parvaiz Ahmad and Renu Bhardwaj revised the manuscript to the present form.

Compliance with ethical standards

Conflict of interest

Authors declare no conflict of interest exists.

References

  1. Abad P, Favery B, Rosso MN, Castagnone-Sereno P (2003) Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Mol Plant Pathol 4:217–224Google Scholar
  2. Abdel-Salam MS, Ameen HH, Soliman GM, Elkelany US, Asar AM (2018) Improving the nematicidal potential of Bacillus amyloliquefaciens and Lysinibacillus sphaericus against the root-knot nematode Meloidogyne incognita using protoplast fusion technique. Egypt J Biol Pest Co 28(1):31Google Scholar
  3. Adam M, Heuer H, Hallmann J (2014) Bacterial antagonists of fungal pathogen also control root-knot nematodes by induced systemic resistance of tomato plants. PLOS One 9(2):e90402Google Scholar
  4. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126Google Scholar
  5. Afify AEMMR, Farahat AA, Al-Sayed AA, Mahfoud NAM (2014) Antioxidant enzymes as well as oxidant activities involved in defense mechanisms against the root-knot, reniform and citrus nematodes in their host plants. Int J Biotecnol Food Sci 2(6):102–111Google Scholar
  6. Ahmed N, Abbasi MW, Shaukat SS, Zaki MJ (2009) Physiological changes in leaves of mungbean plants infected with Meloidogyne javanica. Phytopathol Mediterr 48:262–268Google Scholar
  7. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Biol 53:1331–1341Google Scholar
  8. Asada K (1992) Ascorbate peroxidase–a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85(2):235–241Google Scholar
  9. Awasthi P, Mahajan V, Rather IA, Gupta AP, Rasool S, Bedi YS et al (2015) Plant omics: isolation, identification, and expression analysis of cytochrome P450 gene sequences from Coleusforskohlii. Omics 19:782–792Google Scholar
  10. Awasthi P, Mahajan V, Jamwal VL, Kapoor N, Rasool S, Bedi YS, Gandhi SG (2016) Cloning and expression analysis of chalcone synthase gene fromColeus forskohlii. J Genet 95:647–657.  https://doi.org/10.1007/s12041-016-0680-8 Google Scholar
  11. Azhagumurugan C, Rajan MK (2014) Efficacy of root knot nematode (Meloidogyne incognita) on the growth characteristics of black gram (Vigna mungo) treated with leaf extract of Magilam (Mimusops elengi). Am-Euras J Sci Res 9:175–181Google Scholar
  12. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interaction with plants and other organisms. Plant Biol 57:233–266Google Scholar
  13. Borah B, Ahmed R, Hussain M, Phukon P, Wann SB, Sarmah DK, Bhau BS (2018) Suppression of root-knot disease in Pogostemoncablin caused by Meloidogyne incognita in a rhizobacteria mediated activation of phenylpropanoid pathway. Biol Control 119:43–50Google Scholar
  14. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Google Scholar
  15. Burkett-Cadena M, Kokalis-Burelle N, Lawrence KS, van Santen E, Kloepper JW (2008) Suppressiveness of root-knot nematodes mediated by rhizobacteria. Biol Control 47:55–59Google Scholar
  16. Callard D, Axelos M, Mazzolini L (1996) Novel molecular markers for the late phase of the growth cycle of Arabidopsis thaliana cell suspension cultures are expressed during organ senescence. Plant Physiol 112:705–715Google Scholar
  17. Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475–5480Google Scholar
  18. Cepulyte R, Danquah WB, Bruening G, Williamson VM (2018) Potent attractant for root-knot nematodes in exudates from seedling root tips of two host species. Sci Rep 8(1):10847Google Scholar
  19. Cetintas R, Kusek M, Fateh SA (2018) Effect of some plant growth-promoting rhizobacteria strains on root-knot nematode, Meloidogyne incognita, on tomatoes. Egypt J Biol Pest Co 28(1):7Google Scholar
  20. Chen F, Wang M, Zheng Y, Luo J, Yang X, Wang X (2010) Quantitative changes of plant defense enzymes and Phytohormone in biocontrol of cucumber Fusarium wilt by Bacillus subtilis B579. World J Microbiol Biotechnol 26:675–684Google Scholar
  21. Chen L, Jiang H, Cheng Q, Chen J, Wu G, Kumar A, Sun M, Liu Z (2015) Enhanced nematicidal potential of the chitinase pachi from Pseudomonas aeruginosa in association with Cry21Aa. Sci Rep 5:14395Google Scholar
  22. Choudhary DK, Prakash A, Johri BN (2007) Induced systemic resistance (ISR) in plants: mechanism of action. Indian J Microbiol 47:289–297Google Scholar
  23. Claussen W (2005) Proline as a measure of stress in tomato plants. Plant Sci 168(1):241–248Google Scholar
  24. Collange B, Navarrete M, Peyre G, Mateille T, Tchamitchian M (2011) Root-knot nematode (Meloidogyne) management in vegetable crop production: the challenge of an agronomic system analysis. Crop Prot 30:1251–1262Google Scholar
  25. Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci 83:3811–3815Google Scholar
  26. Dong LQ, Zhang KQ (2006) Microbial control of plant-parasitic nematodes: a five-party interaction. Plant Soil 288(1–2):31–45Google Scholar
  27. Elhady A, Adss S, Hallmann J, Heuer H (2018) Rhizosphere microbiomes modulated by pre-crops assisted plants in defense against plant-parasitic nematodes. Front Microbiol 9:1133.  https://doi.org/10.3389/fmicb.2018.01133 Google Scholar
  28. Flohe L, Gunzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–121Google Scholar
  29. Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523Google Scholar
  30. Gilbert GA, Knight JD, Vance CP, Allan DL (1999) Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ 22:801–810Google Scholar
  31. Goellner M, Wang X, Davis EL (2001) Endo-beta-1,4-glucanase expression in compatible plant-nematode interactions. Plant Cell 13:2241–2255Google Scholar
  32. Goyal D, Pandey J, Prakash O (2017) Role of plant growth-promoting Rhizobacteria (PGPR) in degradation of xenobiotic compounds and Allelochemicals. Advances in PGPR Research, 330Google Scholar
  33. Gupta R, Saikia SK, Pandey R (2015) Bioconsortia augments antioxidant and yield in Matricaria recutita L. Against Meloidogyne incognita (Kofoid and white) Chitwood infestation. Proc Natl Acad Sci Ind Sect B: Biol Sci 87:335–342.  https://doi.org/10.1007/s40011-015-0621-y Google Scholar
  34. Gupta R, Singh A, Srivastava M, Gupta MM, Pandey R (2016) Augmentation of systemic resistance and secondary metabolites by chitinolytic microbes in Withania somnifera against Meloidogyne incognita. Biocontrol Sci Tech 26:1626–1642.  https://doi.org/10.1080/09583157.2016.1230729 Google Scholar
  35. Gupta G, Snehi SK, Singh V (2017a) Role of PGPR in biofilm formations and its importance in plant health. Biofilms in Plant and Soil Health, 27Google Scholar
  36. Gupta R, Singh A, Ajayakumar PV, Pandey R (2017b) Microbial interference mitigates Meloidogyne incognita mediated oxidative stress and augments bacoside content in Bacopa monnieri L. Microbiol Res 199:67–78Google Scholar
  37. Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405Google Scholar
  38. Hallmann J, Quadt-Hallmann A, Miller WG, Sikora RA, Lindow SE (2001) Endophytic colonization of plants by the biocontrol agent Rhizobium etli G12 in relation to Meloidogyne incognita infection. Phytopathology 91:415–422Google Scholar
  39. Hasky-Gunther K, Hoffmann-Hergarten S, Sikora RA (1998) Resistance against the potato cyst nematode Globodera pallida systemically induced by the rhizobacteria Agrobacterium radiobacter (G12) and Bacillus sphaericus (B43). Fundam Appl Nematol 21:511–517Google Scholar
  40. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198.  https://doi.org/10.1016/0003-9861(68)90654-1
  41. Hirsch PR, Miller AJ, Dennis PG (2013) Do root exudates exert more influence on rhizosphere bacterial community structure than other rhizodeposition? In: Bruijn FJ (ed) Molecular Microbial Ecology of the Rhizosphere, John Wiley & Sons, Inc., pp 229–242Google Scholar
  42. Jang JY, Le Dang Q, Choi YH, Choi GJ, Jang KS, Cha B, Luu NH, Kim JC (2014) Nematicidal activities of 4-quinolone alkaloids isolated from the aerial part of Triumfetta grandidens against Meloidogyne incognita. J Agric Food Chem 63:68–74Google Scholar
  43. Jayakumar J, Ramakrishnan S, Rajendran G (2002) Bio-control of reniform nematode, Rotylenchulus reniformis through fluorescent Pseudomonas. Pesttol 26:45–46Google Scholar
  44. Jimenez A, Hernandez JA, del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284Google Scholar
  45. Jung SJ, An KN, Jin YL, Park RD, Kim KY, Shon BK, Kim TH (2002) Effect of chitinase-producing Paenibacillus illinoisensis KJA-424 on egg hatching of root-knot nematode (Meloidogyne incognita). J Microbiol Biotechnol 12(6):865–871Google Scholar
  46. Karczmarek A, Overmars H, Helder J, Goverse A (2004) Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Mol Plant Pathol 5(4):343–346Google Scholar
  47. 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 2:287–293Google Scholar
  48. Khan Z, Kim SG, Jeon YH, Khan HU, Son SH, Kim YH (2008) A plant growth promoting rhizobacterium, Paenibacillus polymyxa strain GBR-1, suppression of root-knot nematode. Bioresour Technol 99:3016–3023Google Scholar
  49. Kono Y (1978) Generation of superoxide radical during autooxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys 186:189–195Google Scholar
  50. 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 34:1847–1861Google Scholar
  51. Korayem A, Mohamed M, El-Ashry S (2016) Yield and oil quality of sunflower infected with the root-knot nematode, Meloidogyne arenaria. Int J Chem Tech Res 3:207–2014Google Scholar
  52. Kumar KB, Khan PA (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine coracana cv. PR 202) leaves during senescence. Indian J Exp Biol 20:412–416Google Scholar
  53. Kuniak E, Sklodowska M (2001) Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. Plant Sci 160:723–731Google Scholar
  54. Lambert KN (1995). Isolation of genes induced early in the resistance response to Meloidogyne javanica in Lycopersicon esculentum. [PhD Dissertation]: University of California-Davis, Davis, CAGoogle Scholar
  55. Li Y, Yang R, Zhang A, Wang S (2014) The distribution of dissolved lead in the coastal waters of the East China Sea. Mar Pollut Bull 85:700–709Google Scholar
  56. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408Google Scholar
  57. Mahalik J, Routray B (2010) Changes in growth traits in blackgram mutant lines induced by different mutagenic treatments towards root knot nematode infection. Assam University. J Sci Technol 4:56–60Google Scholar
  58. Ma YY, Li YL, Lai HX, Guo Q, Xue QH (2017) Effects of two strains of Streptomyces on root-zone microbes and nematodes for biocontrol of root-knot nematode disease in tomato. Appl Soil Ecol 112:34–41Google Scholar
  59. Manju P, Subramanian S (2016) Induction of defense related enzymes and phenols ted enzymes and phenols in Gerbera jamesonii by Bacillus spp. against root knot nematode, Meloidogyne incognita. Bioscan 11(1):159–163Google Scholar
  60. Martinek RG (1964) Method for the determination of vitamin E (total tocopherols) in serum. Clin Chem 10:1078–1086Google Scholar
  61. Mehmood U, Inam-ul-Haq M, Saeed M, Altaf A, Azam F (2018) A brief review on plant growth promoting Rhizobacteria (PGPR): a key role in plant growth promotion. Plant Prot 2(2):77–82Google Scholar
  62. Mekete T, Hallmann J, Kiewnick S, Sikora R (2009) Endophytic bacteria from Ethiopian coffee plants and their potential to antagonise Meloidogyne incognita. Nematology 11(1):117–127Google Scholar
  63. Meyer AJ, May MJ, Fricker M (2001) Quantitative in vivo measurement of glutathione in Arabidopsis cells. Plant J 27(1):67–78Google Scholar
  64. Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MNV (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44(1):25–37Google Scholar
  65. Mollavali M, Bolandnazar SA, Schwarz D, Rohn S, Riehle P, Nahandi FZ (2016) Flavonol glucoside and antioxidant enzyme biosynthesis affected by mycorrhizal fungi in various cultivars of onion (Allium cepa L.). J Agri Food Chem 64(1):71–77Google Scholar
  66. Mostafanezhad H, Sahebani N, Nourinejhad-Zarghani S (2014) Control of root-knot nematode (Meloidogyne javanica) with combination of Arthrobotrys oligospora and salicylic acid and study of some plant defense responses. Biocontrol Sci Tech 24(2):203–215Google Scholar
  67. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific-peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880Google Scholar
  68. Niebel A, Heungens K, Barthels N, Inze D, Van MM, Gheysen G (1995) Characterization of a pathogen-induced potato catalase and its systemic expression upon nematode and bacterial infection. Mol Plant-Microbe Interact 8(3):371–378Google Scholar
  69. Nikoo FS, Sahebani N, Aminian H, Mokhtarnejad L, Ghaderi R (2014) Induction of systemic resistance and defense-related enzymes in tomato plants using Pseudomonas fluorescens CHAO and salicylic acid against root-knot nematode Meloidogyne javanica. J Plant Prot Res 54(4):383–389Google Scholar
  70. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49(1):249–279Google Scholar
  71. Oostendorp M, Sikora RA (1990) In-vitro interrelationships between rhizosphere bacteria and Heterodera schachtii. Rev Nematol 13:269–274Google Scholar
  72. Prasad M, Srinivasan R, Chaudhary M, Choudhary M, Jat LK (2019) Plant Growth Promoting Rhizobacteria (PGPR) for Sustainable Agriculture: Perspectives and Challenges. In: PGPR Amelioration in Sustainable Agriculture (pp. 129–157). Woodhead PublishingGoogle Scholar
  73. Putter J. (1974). Peroxidases. In:methods of enzymatic analysis(second edition),2:685–690Google Scholar
  74. Radwan MA, Farrag SAA, Abu-Elamayem MM, Ahmed NS (2012) Biological control of the root-knot nematode, Meloidogyne incognita on tomato using bioproducts of microbial origin. Appl Soil Ecol 56:58–62Google Scholar
  75. Rather IA, Awasthi P, Mahajan V, Bedi YS, Vishwakarma RA, Gandhi SG (2015) Molecular cloning and functional characterization of an antifungal PR-5 protein from Ocimum basilicum. Gene 558:143–151Google Scholar
  76. Ray S, Singh S, Singh S, Sarma BK, Singh HB (2016) Biochemical and histochemical analyses revealing endophytic Alcaligenes faecalis mediated suppression of oxidative stress in Abelmoschus esculentus challenged with Sclerotium rolfsii. Plant Physiol Biochem 109:430–441Google Scholar
  77. Razavi BS, Hoang DTT, Blagodatskaya E, Kuzyakov Y (2017) Mapping the footprint of nematodes in the rhizosphere: cluster root formation and spatial distribution of enzyme activities. Soil Biol Biochem 115:213–220Google Scholar
  78. Roe JH, Kuether CA (1943) The determination of ascorbic acid in whole blood and urine through the 2,4-dinitrophenyl hydrazine derivative of dehydroascorbic acid. J Biol Chem 147:399–407Google Scholar
  79. Saed-Moucheshi A, Pakniyat H, Pirasteh-Anosheh H, Azooz MM (2014) Role of ROS as signaling molecules in plants. In: Ahmad P (ed) Oxidative damage to plants antioxidant networks and signaling. Elsevier, OxfordGoogle Scholar
  80. Sahebani N, Hadavi N (2009) Induction of H2O2 and related enzymes in tomato roots infected with root knot nematode (M. javanica) by several chemical and microbial elicitors. Biocontrol Sci Tech 19:301–313.  https://doi.org/10.1080/09583150902752012 Google Scholar
  81. Sedlak J, Lindsay RH (1968) Estimation of total, protein bound, and non-protein sulfhydryl groups in tissue with Ellman's reagent. Anal Chem 25:192–205.  https://doi.org/10.1016/0003-2697(68)90092-4 Google Scholar
  82. Seid A, Fininsa C, Mekete T, Decraemer W, Wesemael WML (2015) Tomato (Solanum lycopersicum) and root-knot nematodes (Meloidogyne spp.) – a century-old battle. Nematol 17:995–1009Google Scholar
  83. Seinhorst JT (1961) Plant-nematode inter-relationships. Annu Rev Microbiol 15(1):177–196Google Scholar
  84. Shane MW, Lambers H (2005) Systemic suppression of cluster-root formation and net P-uptake rates in Grevillea crithmifolia at elevated P supply: a proteacean with resistance for developing symptoms of ‘P toxicity. J Exp Bot 57(2):413–423Google Scholar
  85. Sharma IP, Sharma AK (2016) Physiological and biochemical changes in tomato cultivar PT-3 with dual inoculation of mycorrhiza and PGPR against root-knot nematode. Symbiosis 71(3):175–183Google Scholar
  86. Sharma IP, Sharma AK (2017) Co-inoculation of tomato with an arbuscular mycorrhizal fungus improvesplant immunity and reduces root-knot nematode infection. Rhizosphere 4:25–28Google Scholar
  87. Siddique S, Matera C, Radakovic ZS, Hasan MS, Gutbrod P, Rozanska E, Grundler FM (2014) Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Sci Signal 7(320):ra33–ra33Google Scholar
  88. Siddiqui ZA, Mahmood I (1999) Role of bacteria in the management of plant parasitic nematodes: a review. Bioresource Technol 69:167–179Google Scholar
  89. Siddiqui IA, Shaukat SS (2002) Rhizobacteria-mediated induction of systemic resistance (ISR) in tomato against Meloidogyne javanica. J Phytopathol 150:469–473Google Scholar
  90. Siddiqui IA, Haas D, Heeb S (2005) Extracellular protease of Pseudomonas fluorescensCHA0, a biocontrol factor with activity against the root-knot nematode Meloidogyne incognita. Appl Environ Microbiol 71:5646–5649Google Scholar
  91. Sidhu, H. S. (2018). Potential of plant growth-promoting rhizobacteria in the management of nematodes: a reviewGoogle Scholar
  92. Sikora RA, Hoffmann-Hergarten S (1993) Biological control of plant parasitic nematodes with plant-health promoting rhizobacteria. In: Lumsden PD, Vaugh JL (eds) Biologically based technology. ACS Symposium series, USA, pp 166–172Google Scholar
  93. Sikora RA, Schafer K, Dababat AA (2007) Modes of action associated with microbially induced in planta suppression of plant-parasitic nematodes. Australas Plant Pathol 36(2):124–134Google Scholar
  94. 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 168:33–40Google Scholar
  95. Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Plant Sci 19:267–290Google Scholar
  96. Sohrabi F, Sheikholeslami M, Heydari R, Rezaee S, Sharifi R (2018) Evaluation of four rhizobacteria on tomato growth and suppression of root-knot nematode, Meloidogyne javanica under greenhouse conditions, a pilot study. Egypt J Biol Pest Co 28(1):56Google Scholar
  97. 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(6):1187–1194Google Scholar
  98. Tian B, Yang J, Zhang KQ (2007) Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol Ecol 61(2):197–213Google Scholar
  99. Timmusk S, Grantcharova N, Wagner EGH (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol 71(11):7292–7300Google Scholar
  100. Tiwari S, Pandey S, Chauhan PS, Pandey R (2017) Biocontrol agents in co-inoculation manages root knot nematode [Meloidogyne incognita (Kofoid & White) Chitwood] and enhances essential oil content in Ocimum basilicum L. Ind Crop Prod 97:292–301Google Scholar
  101. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer 3—new capabilities and interfaces. Nucleic Acids Res 40:e115Google Scholar
  102. Van Peer R, Niemann GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728–734Google Scholar
  103. Vanderspool MC, Kaplan DT, McCollum TG, Wodzinski RJ (1994) Partial characterization of cytosolic superoxide dismutase activity in the interaction of Meloidogyne incognita with two cultivars of Glycine max. J Nematol 26(4):422Google Scholar
  104. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66.  https://doi.org/10.1016/S0168-9452(99)00197-1 Google Scholar
  105. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164(4):645–655Google Scholar
  106. Verma RK, Sachan M, Vishwakarma K, Upadhyay N, Mishra RK, Tripathi DK, Sharma S (2018) Role of PGPR in sustainable agriculture: molecular approach toward disease suppression and growth promotion. In: Role of Rhizospheric microbes in soil. Springer, Singapore, pp 259–290Google Scholar
  107. Vidhyasekaran P (2002) Bacterial disease resistance in plants. Molecular biology and biotechnological applications. Binghamton, New York: The Haworth PressGoogle Scholar
  108. Vos C, Schouteden N, Van Tuinen D, Chatagnier O, Elsen A, De Waele D et al (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.  https://doi.org/10.1016/j.soilbio.2013.01.013 Google Scholar
  109. Wang C, Hu HJ, Li X, Wang YF, Tang YY, Chen SL, Yan SZ (2018) Effects of varying environmental factors on the biological control of Meloidogyne incognita in tomato by Bacillus cereus strain BCM2. Biocontrol Sci Technol 28(4):359–376.  https://doi.org/10.1080/09583157.2018.1450489 Google Scholar
  110. Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745Google Scholar
  111. Williamson VM, Roberts PA (2009) Mechanisms and genetics of resistance. In: Perry RN, Moens M, Starr JL (eds) Root-knot nematodes. CAB International, Wallingford, pp 301–325Google Scholar
  112. Wu GL, Cui J, Tao L, Yang H (2010) Fluroxypyr triggers oxidative damage by producing superoxide and hydrogen peroxide in rice (Oryza sativa). Ecotoxicol 19:124–132.  https://doi.org/10.1007/s10646-009-0396-0 Google Scholar
  113. Xiang N, Lawrence KS, Donald PA (2018) Biological control potential of plant growth-promoting rhizobacteria suppression of Meloidogyne incognita on cotton and Heterodera glycines on soybean: a review. J Phytopathol 166:449–458Google Scholar
  114. Zacheo G, Pricolo G, Bleve-Zacheo T (1988) Effect of temperature on resistance and biochemical changes in tomato inoculated with Meloidogyne incognita. Nematol Mediterr 16(1)Google Scholar
  115. Zaied KA, Kawther S, Kash S, Ibrahim A, Tawfik TM (2009) Improving nematocidial activity of bacteria via protoplast fusion. Aust J Basic Appl Sci 3(2):1412–1427Google Scholar
  116. Zeynadini-Riseh A, Mahdikhani-Moghadam E, Rouhani H, Moradi M, Saberi-Riseh R, Mohammadi A (2018) Effect of some Probiotic Bacteria as Biocontrol Agents of Meloidogyne incognita and Evaluation of Biochemical Changes of Plant Defense Enzymes on Two Cultivars of Pistachio. J Agri Sci and Tech 20(1):179–191Google Scholar
  117. Zhai Y, Shao Z, Cai M, Zheng L, Li G, Huang D, Cheng W, Thomashow LS, Weller DM, Yu Z, Zhang J (2018) Multiple modes of nematode control by volatiles of Pseudomonas putida 1A00316 from Antarctic soil against Meloidogyne incognita. Front Microbiol 9:253Google Scholar
  118. Zhou J, Jia F, Shao S, Zhang H, Li G, Xia X, Zhou Y, Yu J, Shi K (2015) Involvement of nitric oxide in the jasmonate- dependent basal defense against root-knot nematode in tomato plants. Front Plant Sci 6:193Google Scholar
  119. Zhou L, Yuen G, Wang Y, Wei L, Ji G (2016) Evaluation of bacterial biological control agents for control of root knot nematode disease on tomato. Crop Prot 84:8–13Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Kanika Khanna
    • 1
  • Vijay Lakshmi Jamwal
    • 2
  • Sukhmeen Kaur Kohli
    • 1
  • Sumit G. Gandhi
    • 2
  • Puja Ohri
    • 3
  • Renu Bhardwaj
    • 1
  • Leonard Wijaya
    • 4
  • Mohammed Nasser Alyemeni
  • Parvaiz Ahmad
    • 4
    • 5
  1. 1.Department of Botanical and Environmental SciencesGuru Nanak Dev UniversityAmritsarIndia
  2. 2.Council of Scientific and Industrial ResearchIndian Institute of Integrative Medicine (CSIR-IIIM)JammuIndia
  3. 3.Department of ZoologyGuru Nanak Dev UniversityAmritsarIndia
  4. 4.Botany and Microbiology Department, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  5. 5.Department of Botany, S.P. CollegeSrinagarIndia

Personalised recommendations