Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal (AM) fungi and plant growth-promoting rhizobacteria (PGPR) have potential for the biocontrol of soil-borne diseases. The objectives of this study were to quantify the interactions between AM fungi [Glomus versiforme (Karsten) Berch and Glomus mosseae (Nicol. & Gerd.) Gerdemann & Trappe] and PGPR [Bacillus polymyxa (Prazmowski) Mace and Bacillus sp.] during colonization of roots and rhizosphere of tomato (Lycopersicon esculentum Mill) plants (cultivar Jinguan), and to determine their combined effects on the root-knot nematode, Meloidogyne incognita, and on tomato growth. Three greenhouse experiments were conducted. PGPR increased colonization of roots by AM fungi, and AM fungi increased numbers of PGPR in the rhizosphere. Dual inoculations of AM fungi plus PGPR provided greater control of M. incognita and greater promotion of plant growth than single inoculations, and the best combination was G. mosseae plus Bacillus sp. The results indicate that specific AM fungi and PGPR can stimulate each other and that specific combinations of AM fungi and PGPR can interact to suppress M. incognita and disease development.

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

Similar content being viewed by others

References

  • Ahmed SH, Abdelgani ME, Yassin AM (2009) Effects of interaction between vesicular-arbuscular mycorrhizal (VAM) fungi and root-knot nematodes on Dolichos bean (Lablab niger Medik.) plants. AEJSA 3:678–683

    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 Protect 27:410–417

    Article  Google Scholar 

  • Attia M, Awad NM (2003) Assessment the impact of certain growth promoting rhizobacteria strains on symbiotic effectiveness of arbuscular mycorrhizal fungi. Egypt J Microbiol 38:75–88

    Google Scholar 

  • Barea JM, Toro M, Orozco MO, Campos E, Azcón R (2002) The application of isotopic 32P and 15N-dilution techniques to evaluate the interactive effect of phosphate-solubilizing rhizobacteria, mycorrhizal fungi and Rhizobium to improve the agronomic efficiency of rock phosphate for legume crops. Nutr Cycl Agroecosyst 63:35–42

    Article  CAS  Google Scholar 

  • Bashan Y, Holguin G (1998) Proposal for the division of plant growth-promoting rhizobacteria into classifications: Biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biol Biochem 30:1225–1228

    Article  CAS  Google Scholar 

  • Bashan Y, Holguin G, Lifshitz R (1993) Isolation and characterization of plant growth-promoting rhizobacteria. In: Glick BR, Thompson JE (eds) Methods in plant molecular biology and biotechnology. CRC Press, Boca Raton, pp 331–345

    Google Scholar 

  • Becker JO, Zavaleta-Mejia E, Colbert SF, Schroth MN, Weinhold AR, Hancock JG, Van Gundy SD (1988) Effects of rhizobacteria on root-knot nematodes and gall formation. Phytopathology 78:1466–1469

    Article  Google Scholar 

  • Biermann B, Linderman RG (1981) Quantifying vercular-arbuscular mycorrhizas: a proposed method towards standardization. New Phytol 87:63–67

    Article  Google Scholar 

  • Biró B, Koves-Pechy K, Vörös I, Takács T, Eggenberger P, Strasser RJ (2000) Interrelations between azospirillum and rhizobium nitrogen-fixers and arbuscular mycorrhizal fungi in the rhizosphere of alfalfa in sterile, AMF-free or normal soil conditions. Appl Soil Ecol 15:159–168

    Article  Google Scholar 

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

    Google Scholar 

  • Caroli L, Glazer I, Gaugler R (1996) Entomopathogenic nematode infectivity assay: comparison of penetration rate into different hosts. Biocontrol Sci Technol 6:227–233

    Article  Google Scholar 

  • Cooper KM, Grandisons GS (1986) Interaction of vesicular-arbuscular mycorrhizal fungi and root-knot nematode on cultivars of tomato and white clover susceptible to Meloidogyne hapla. Annu Appl Biol 108:555–565

    Article  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 Ecologica Sinica 28:2854–2860 (In Chinese with English abstract)

    Google Scholar 

  • de la Peña E, Echeverría SR, van der Putten WH, Moens FHM (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829–840

    Article  PubMed  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 

  • Dwivedi D, Johri BN, Ineichen K, Wray V, Wiemken A (2009) Impact of antifungals producing rhizobacteria on the performance of Vigna radiata in the presence of arbuscular mycorrhizal fungi. Mycorrhiza 19:559–570

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Elsheikh EAE, Mirghani AMO (1997) Interaction of VA mycorrhiza and root-knot nematode on tomato plants—effects of nematode inoculum density, soil texture and soil sterilization. Jonares 1:1–6

    Google Scholar 

  • Fan YL, Zhang WG, Lu SH, Gao XY, Liu LK (2009) Identification of the root-knot nematode from vegetables in greenhouses in Shandong. Acta Agriculturae Boreali-Sinica 24(Suppl):262–264 (In Chinese with English abstract)

    Google Scholar 

  • Fang ZD (1998) Research methods of plant pathology (in Chinese), 3rd edn. China Agri Press, Beijing, pp p11–p12

    Google Scholar 

  • Gryndler M (2000) Interactions of arbuscular mycorrhizal fungi with other soil organisms. In: Kapulnik Y, Douds DD Jr (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 239–262

    Google Scholar 

  • Hu JL, Lin XG, Wang JH, Shen WH, Wu S, Peng SP, Mao TT (2010) Arbuscular mycorrhizal fungal inoculation enhances suppression of cucumber Fusarium wilt in greenhouse soils. Pedosphere 20:586–593

    Article  CAS  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 (Caria papaya L.) infected with root-knot nematode Meloidogyne incognita. Fruits 61:151–162

    Article  Google Scholar 

  • Li JX, Liu RJ (2007) Potential of mycorrhizal fungal agents on controlling soil-borne plant diseases. Acta Phytopathologica Sinica 37:1–8 (In Chinese with English abstract)

    Google Scholar 

  • Li M, Liu RJ, Li XL (2004) Influences of arbuscular mycorrhizal fungi on growth and Fusarium-wilt disease of watermelon in field. Acta Phytopathologica Sinica 34:472–473 (in Chinese with English abstract)

    Google Scholar 

  • Linderman RG (1988) Mycorrhizal intercations with the rhizopshere microflora: the mycorrhizosphere effect. Phytopathology 78:366–371

    Google Scholar 

  • Liu WZ (1995) Research techniques of plant nematology (in Chinese). Liaoning Science Technol Press, Shenyang, pp 1–242

    Google Scholar 

  • Liu RJ, Chen YL (2007) Mycorrhizaology (in Chinese). Science Press, Beijing, pp 208–209

    Google Scholar 

  • Meyer JR, Linderman RG (1986) Response of subterranean clover to dual inoculation with vesicular- arbuscular mycorrhizal fungi and a plant growth-promoting bacterium Pseudomonas putida. Soil Biol Biochem 18:185–190

    Article  CAS  Google Scholar 

  • Miroslav V, Milan G (2000) Response of micropropagated potatoes transplanted to peat media to post-vitro inoculation with arbuscular mycorrhizal fungi and soil bacteria. Appl Soil Ecol 15:145–152

    Article  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 

  • Powell JR, Campbell RG, Dunfield KE, Gulden RH, Hart MM, Levy-Booth DJ, Klironomos JN, Pauls KP, Swanton CJ, Trevors JT, Antunes PM (2009) Effect of glyphosate on the tripartite symbiosis formed by Glomus intraradices, Bradyrhizobium japonicum, and genetically modified soybean. Appl Soil Ecol 41:128–136

    Article  Google Scholar 

  • Preston GM (2004) Plant perceptions of plant growth-promoting Pseudomonas. Philos Trans R Soc Lond B Biol Sci 359:907–918

    Article  PubMed  CAS  Google Scholar 

  • Serfoji P, Rajeshkumar S, Selvaraj T (2010) Management of root-knot nematode, Meloidogyne incognita on tomato cv Pusa Ruby. by using vermicompost, AM fungus, Glomus aggregatum and mycorrhiza helper bacterium, Bacillus coagulans. J Agric Technol 6:37–45

    Google Scholar 

  • Shi LB, Wang ZH, Wu HY, Liu J (2010) Influence of continuous tomato-cropping on second-stage juveniles of root-knot nematode and free-living nematodes from rhizosphere soil in plastic greenhouse. Acta Phytopathologica Sinica 40:81–89 (In Chinese with English abstract)

    Google Scholar 

  • Shreenivasa KR, Krishnappa K, Ravichandra NG (2007a) Interaction effects of arbuscular mycorrhizal fungus Glomus fasciculatum and root–knot nematode, Meloidogyne incognita on growth and phosphorous uptake of tomato. Karnataka J Agric Sci 20:57–61

    Google Scholar 

  • Shreenivasa KR, Krishnappa K, Ravichandra NG (2007b) Survival and penetration of Meloidogyne incognita larvae in tomato roots in presence of arbuscular mycorrhizal fungus, Glomus fasciculatum. Karnataka J Agric Sci 20:166–16

    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 

  • Smith GS, Rongadori RW, Hussey RS (1986) Interaction of endomycorrhizal fungi, superphosphate, and Meloidogyne incognita on cotton in microplot and field studies. J Nematol 18:208–216

    PubMed  CAS  Google Scholar 

  • Srivastava R, Roseti D, Sharma AK (2007) The evaluation of microbial diversity in a vegetable based cropping system under organic farming practices. Appl Soil Ecol 36:116–123

    Article  Google Scholar 

  • Tchabi A, Coyne D, Hountondji F, Lawouin L, Wiemken A, Oehl F (2010) Efficacy of indigenous arbuscular mycorrhizal fungi for promoting white yam (Dioscorea rotundata) growth in West Africa. Appl Soil Ecol 45:92–100

    Article  Google Scholar 

  • Tian H, Robert DR (2000) Effects of rhizobacteria on soybean cyst nematode, Heterodera glycines. J Nematol 32:377–388

    PubMed  CAS  Google Scholar 

  • Vestberg A, Kukkonen S, Saari K, Parikka P, Huttunen J, Tainio L, Devos D, Weekers F, Kevers C, Thonart P, Lemoine MC, Cordier C, Alabouvette C, Gianinazzi S (2004) Microbial inoculation for improving the growth and health of micropropagated strawberry. Appl Soil Ecol 27:243–258

    Article  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

    Google Scholar 

  • Wang YL, Hu ZJ (2000) Effect of VA mycorrhiza on nematodiasis of tomato. J Huazhong Agric Uni 19:25–28 (In Chinese with English abstract)

    Google Scholar 

  • Weller DM (1988) Biological control of soil-borne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:397–407

    Article  Google Scholar 

  • Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227

    Article  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 

  • Zhao B, He SJ (2002) Microbiology experiments (in Chinese). Science Press, Beijing, pp 23–54

    Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (30871737) and the Sub-project in Industry Program of Ministry of Agriculture (nyyzx 07-050-5).

Author information

Authors and Affiliations

  1. Institute of Mycorrhizal Biotechnology, Qingdao Agricultural University, Qingdao, 266109, China

    Runjin Liu, Mei Dai, Xia Wu & Min Li

  2. Key Laboratory of Systematic Mycology and Lichenology, Institute of Microbiology, Chinese Academy of Sciences, No 3, No 1 Beichen West Road, Chaoyang District, Beijing, 100101, China

    Xingzhong Liu

Authors
  1. Runjin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mei Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xia Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Min Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xingzhong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xingzhong Liu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, R., Dai, M., Wu, X. et al. 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 (2012). https://doi.org/10.1007/s00572-011-0397-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-011-0397-8

Keywords

Search

Navigation