Skip to main content
SpringerLink
Log in

Soil application of entomopathogenic nematodes suppresses the root-knot nematode Meloidogyne javanica in cucumber

  • Original Article
  • Published:
Journal of Plant Diseases and Protection Aims and scope Submit manuscript

Abstract

Cucumber (Cucumis sativus) cultivation in commercial greenhouses occupies an important section of vegetable production in Iran. Root-knot nematode Meloidogyne javanica considered the most destructive soil-borne pathogen in cucumber growing greenhouses. In this study, biocontrol activity of three species of entomopathogenic nematodes (EPNs, i.e., Steinernema carpocapsae, S. feltiae and Heterorhabditis bacteriophora) was determined on M. javanica infecting cucumber under growth chamber and greenhouse conditions. The aqueous suspension of infective juveniles (IJs) was used in five different inoculation times (i.e., 1 or 2 weeks pre-inoculation, simultaneously, and 1 or 2 weeks post-inoculation of the pathogenic nematode into the cucumber soil). Results showed that S. carpocapsae and H. bacteriophora were capable of decreasing all the pathogenicity indices (number of galls, eggs and egg masses) of M. javanica in growth chamber, as well as greenhouse conditions. The best application time for EPNs was determined as 1 week after post-inoculation of M. javanica into the soil. Although EPNs showed significant inhibition in 25 IJ/cm2 (3.8 IJ/cm3) of soil, the best biocontrol activity was observed in 125 IJ/cm2 (19.1 IJ/cm3). Furthermore, the highest reduction in pathogenicity indices was observed when EPNs-colonized cadavers were used as carrier of biocontrol agents. Significant increase in plant growth indices (e.g., fresh/dry weight of shoots/roots) was recorded for all treatments except S. feltiae. Altogether, our results provide a novel insight into the applicability of EPNs against the root-knot nematode M. javanica on cucumber. Further investigations are warranted to evaluate the commercial usability of the agents in cucumber growing greenhouses in Iran.

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

Similar content being viewed by others

References

  • Akhyani A, Modjtahedi H, Naderi A (1984) Species and physiological races of root-knot nematodes in Iran. Iran J Plant Pathol 20:57–70

    Google Scholar 

  • Bi Y, Gao C, Yu Z (2018) Rhabdopeptides from Xenorhabdus budapestensis SN84 and their nematicidal activities against Meloidogyne incognita. J Agric Food Chem 66(15):3833–3839. https://doi.org/10.1021/acs.jafc.8b00253

    Article  CAS  PubMed  Google Scholar 

  • Bird AF, Bird J (1986) Observations on the use of insect parasitic nematodes as a means of biological control of root-knot nematodes. Int J Parasitol 16(5):511–516. https://doi.org/10.1016/0020-7519(86)90086-X

    Article  Google Scholar 

  • Caccia M, Lax P, Doucet M (2013) Effect of entomopathogenic nematodes on the plant-parasitic nematode Nacobbus aberrans. Biol Fertil Soils 49(1):105–109. https://doi.org/10.1007/s00374-012-0724-z

    Article  CAS  Google Scholar 

  • Cao Y, Zhenhua Z, Ning L, Yujuan Y, Xinyan Z, Biao S, Qirong S (2011) Bacillus Subtilis Sqr 9 can control Fusarium wilt in cucumber by colonizing plant roots. Biol Fertil Soils 47(5):495–506. https://doi.org/10.1007/s00374-011-0556-2

    Article  CAS  Google Scholar 

  • Daykin ME, Hussey RS (1985) Staining and histopathological techniques in nematology. In: Baker KR, Carter CC, Sasser JN (eds) An advanced treatise on Meloidogyne. Methodology, vol II. North Carolina State University Graphics, Raleigh, pp 39–48

    Google Scholar 

  • Del Valle EE, Lax P, Rondan Dueñas J, Doucet ME (2013) Effects of insect cadavers infected by Heterorhabditis bacteriophora and Steinernema diaprepesi on Meloidogyne incognita parasitism in pepper and summer squash plants. Ciencia e investigación agraria 40(1):109–118. https://doi.org/10.7764/rcia.v40i1.456

    Article  Google Scholar 

  • Dong K, Dean RA, Fortnum BA, Lewis SA (2001) Development of PCR primer to identify species of root knot nematode: Meloidogyne arenaria, M. hapla, M. incognita and M. javanica. Nematropica 31:273–282

    Google Scholar 

  • Eischen FA, Dietz A (1990) Improved culture techniques for mass rearing Galleria mellonella (Lepidoptera: Pyralidae). Entomol News 101(2):123–128

    Google Scholar 

  • Esmaili-Shirazi E, Banihashemi Z (2008) The Role of Phytophthora melonis and P. drechsleri in Cucurbit Root Rot in Iran. Iran J Plant Pathol 44:54–72

    Google Scholar 

  • Fallon DJ, Kaya HK, Gaugler R, Sipes BS (2002) Effects of etomopathiogenic nematodes on Meloidogyne javanica on tomatoes and soybeans. J Nematol 34(3):239–245

    PubMed  PubMed Central  Google Scholar 

  • Fallon DJ, Kaya HK, Gaugler R, Sipes BS (2004) Effect of Steinernema feltiae-Xenorhabdus bovienii insect pathogen complex on Meloidogyne javanica. Nematology 6(5):671–680. https://doi.org/10.1163/1568541042843496

    Article  Google Scholar 

  • FAOSTAT (2017) Food and Agriculture Organization of the United Nations. FAOSTAT database. http://faostat.fao.org/

  • Grewal P, Martin W, Miller R, Lewis E (1997) Suppression of plant-parasitic nematode populations in turfgrass by application of entomopathogenic nematodes. Biocontrol Sci Tech 7(3):393–400. https://doi.org/10.1080/09583159730802

    Article  Google Scholar 

  • Grewal PS, Lewis EE, Venkatachari S (1999) Allelopathy: a possible mechanism of suppression of plant-parasitic nematodes by entomopathogenic nematodes. Nematology 1(7):735–743. https://doi.org/10.1163/156854199508766

    Article  Google Scholar 

  • Hu K, Li J, Webster J (1999) Nematicidal metabolites produced by Photorhabdus Luminescens (Enterobacteriaceae), bacterial symbiont of entomopathogenic nematodes. Nematology 1(5):457–469. https://doi.org/10.1163/156854199508469

    Article  CAS  Google Scholar 

  • Huang X, Nan Z, Xiaoyu Y, Xingming Y, Qirong S (2012) Biocontrol of Rhizoctonia solani damping-off disease in cucumber with Bacillus pumilus Sqr-N43. Microbiol Res 167(3):135–143. https://doi.org/10.1016/j.micres.2011.06.002

    Article  CAS  PubMed  Google Scholar 

  • Hunt DJ, Handoo ZA (2009) Taxonomy, identification and principal species. In: Perry RN, Moens M, Starr JL (eds) Root-knot nematodes. CABI Publishing, London, pp 55–88

    Chapter  Google Scholar 

  • Jagdale GB, Grewal PS (2008) Influence of the entomopathogenic nematode Steinernema carpocapsae infected host cadavers or their extracts on the foliar nematode Aphelenchoides fragariae on Hosta in the greenhouse and laboratory. Biol Control 44(1):13–23. https://doi.org/10.1016/j.biocontrol.2007.07.001

    Article  Google Scholar 

  • Jagdale GB, Somasekhar N, Grewal PS, Klein MG (2002) Suppression of plant-parasitic nematodes by application of live and dead infective juveniles of an entomopathogenic nematode, Steinernema carpocapsae, on Boxwood (Buxus Spp.). Biol Control 24(1):42–49. https://doi.org/10.1016/S1049-9644(02)00004-X

    Article  Google Scholar 

  • Jagdale G, Kamoun S, Grewal P (2009) Entomopathogenic nematodes induce components of systemic resistance in plants: biochemical and molecular evidence. Biol Control 51(1):102–109. https://doi.org/10.1016/j.biocontrol.2009.06.009

    Article  CAS  Google Scholar 

  • Kaya HK, Stock SP (1997) Techniques in insect nematology. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic Press, London, pp 281–324

    Chapter  Google Scholar 

  • Kepenekci I, Hazir S, Lewis EE (2016) Evaluation of entomopathogenic nematodes and the supernatants of the in vitro culture medium of their mutualistic bacteria for the control of the root-knot nematodes Meloidogyne incognita and M. arenaria. Pest Manag Sci 72(2):327–334. https://doi.org/10.1002/ps.3998

    Article  CAS  PubMed  Google Scholar 

  • Koppenhöfer AM, Baur ME, Stock SP, Choo HY, Chinnasri B, Kaya HK (1997) Survival of entomopathogenic nematodes within host cadavers in dry soil. Appl Soil Ecol 6(3):231–240. https://doi.org/10.1016/S0929-1393(97)00018-8

    Article  Google Scholar 

  • Marull J, Pinochet J (1991) Host suitability of Prunus rootstocks to Meloidogyne species and Pratylenchus vulnus in Spain. Nematropica 21(2):185–195

    Google Scholar 

  • Molina JP, Dolinski C, Souza RM, Lewis EE (2007) Effect of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) on Meloidogyne mayaguensis Rammah and Hirschmann (Tylenchida: Meloidoginidae) infection in tomato plants. J Nematol 39(4):338–342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nyczepir AP, Shapiro-Ilan DI, Lewis EE, Handoo ZA (2004) Effect of entomopathogenic nematodes on Mesocriconema Xenoplax populations in peach and pecan. J Nematol 36(2):181–185

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez EE, Lewis EE (2002) Use of entomopathogenic nematodes to suppress Meloidogyne incognita on greenhouse tomatoes. J Nematol 34(2):171–174

    PubMed  PubMed Central  Google Scholar 

  • Pérez EE, Lewis EE (2004) Suppression of Meloidogyne incognita and Meloidogyne hapla with entomopathogenic nematodes on greenhouse peanuts and tomatoes. Biol Control 30(2):336–341. https://doi.org/10.1016/j.biocontrol.2004.01.001

    Article  Google Scholar 

  • Robinson A (1995) Optimal release rates for attracting Meloidogyne incognita, Rotylenchulus reniformis, and other nematodes to carbon dioxide in sand. J Nematol 27(1):42–50

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sayedain FS, Olia M, Jaimand K (2013) Effect of initial density of Meloidogyne javanica on Salvia officinalis. J Med Plants By-Prod 2(1):13–16

    Google Scholar 

  • Sayedain FS, Ahmadzadeh M, Talaei-Hasanlouei R, Olia M, Bode HB (2019) Nematicidal effect of cell-free culture filtrates of EPN-symbiotic bacteria on Meloidogyne javanica. Biol Control Pests Plant Dis 8(1):17–26. https://doi.org/10.22059/jbioc.2018.244323.212

    Article  Google Scholar 

  • Sedighian N, Shams-Bakhsh M, Osdaghi E, Khodaygan P (2014) Etiology and host range of bacterial leaf blight and necrosis of squash and muskmelon in Iran. J Plant Pathol 96:507–514. https://doi.org/10.4454/jpp.v96i3.3201

    Article  Google Scholar 

  • Shapiro DI, Lewis EE (1999) Comparison of entomopathogenic nematode infectivity from infected hosts versus aqueous suspension. Environ Entomol 28(5):907–911. https://doi.org/10.1093/ee/28.5.907

    Article  Google Scholar 

  • Shapiro-Ilan DI, Nyczepir AP, Lewis EE (2006) Entomopathogenic nematodes and bacteria applications for control of the pecan root-knot nematode, Meloidogyne partityla, in the greenhouse. J Nematol 38(4):449–454

    PubMed  PubMed Central  Google Scholar 

  • Silva AT, Penna JCV, Goular LR, Santos MA, Arantes NE (2000) Genetic variability among and within races of Heterodera glycines ichinohe assessed by RAPD markers. Genet Mol Biol 23:323–329. https://doi.org/10.1590/S1415-47572000000200014

    Article  Google Scholar 

  • Smitley D, Warner F, Bird G (1992) Influence of irrigation and Heterorhabditis bacteriophora on plant-parasitic nematodes in turf. J Nematol 24(4S):637–641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Somasekhar N, Grewal PS, De Nardo EA, Stinner BR (2002) Non-target effects of entomopathogenic nematodes on the soil nematode community. J Appl Ecol 39(5):735–744

    Article  Google Scholar 

  • Tsai BY, Yeh HL (1995) Effect of Steinernema carpocapsae Weiser on the infectivity of Pratylenchus coffeae (Zimmermann) Filipjev & Schuurmans Stekhoven and Meloidogyne javanica (Treub) Chitwood. Plant Pathol Bull 4(3):106–110

    Google Scholar 

  • Webster JM, Chen G, Hu K, Li J (2002) Bacterial metabolites. In: Gaugler R (ed) Entomopathogenic nematology. CABI, Wallingford, pp 99–114

    Chapter  Google Scholar 

Download references

Acknowledgements

Financial support for this study was provided by the University of Tehran. Also the authors would like to thank Gyah corporation for help at the beginning of this project.

Author information

Authors and Affiliations

  1. Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

    Fatemeh Sadat Sayedain & Masoud Ahmadzadeh

  2. Boyce Thompson Institute, Cornell University, Ithaca, NY, USA

    Somayeh Fattah-Hosseini

  3. Molekulare Biotechnologie, Fachbereich Biowissenschaften and Buchmann Institute for Molecular Life Sciences (BMLS), Goethe Universität Frankfurt, Frankfurt am Main, Germany

    Helge B. Bode

Authors
  1. Fatemeh Sadat Sayedain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masoud Ahmadzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Somayeh Fattah-Hosseini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helge B. Bode
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fatemeh Sadat Sayedain.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Human and animal rights

This article does not contain any studies with human or animal subjects.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sayedain, F.S., Ahmadzadeh, M., Fattah-Hosseini, S. et al. Soil application of entomopathogenic nematodes suppresses the root-knot nematode Meloidogyne javanica in cucumber. J Plant Dis Prot 128, 215–223 (2021). https://doi.org/10.1007/s41348-020-00367-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41348-020-00367-1

Keywords

Search

Navigation