Antagonistic role of the microbiome from a Meloidogyne hapla-suppressive soil against species of plant-parasitic nematodes with different life strategies

In: Nematology
View More View Less
  • 1 Institute of Epidemiology and Pathogen Diagnostics, Braunschweig, Germany
  • 2 Department of Crop Protection, Geisenheim, Germany
  • 3 Department of Vegetable Crops, Geisenheim, Germany

Summary

In certain soils populations of plant-parasitic nematodes (PPN) decline. Understanding this effect may open up environmentally friendly management options. We identified such a suppressive soil containing virtually no PPN. Inoculated Meloidogyne hapla declined in this soil more than in a control soil and reproduction on tomato was reduced. The extracted soil microbiome alone decreased root invasion of second-stage juveniles (J2) and progeny as well as the native soil. We tested the antagonistic potential against PPN that differ in life strategies. The microbiome was most suppressive against two populations of M. hapla and one population of Pratylenchus neglectus, and least suppressive against M. incognita and the ectoparasite Hemicycliophora conida. In a split-root system with M. hapla, plant-mediated but not direct effects of the microbiome significantly reduced root invasion of J2, while direct exposure of M. hapla to the microbiome significantly affected reproduction. Overall, both plant-mediated and direct effects of the microbiome were responsible for the soil suppressiveness against M. hapla.

  • Adam, M., Heuer, H. & Hallmann, J. (2014a). Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS ONE 9, e90402. DOI: 10.1371/journal.pone.0090402

    • Search Google Scholar
    • Export Citation
  • Adam, M., Westphal, A., Hallmann, J. & Heuer, H. (2014b). Specific microbial attachment to root knot nematodes in suppressive soil. Applied and Environmental Microbiology 80, 2679-2686. DOI: 10.1128/AEM.03905-13

    • Search Google Scholar
    • Export Citation
  • Berg, G. & Smalla, K. (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology 68, 1-13. DOI: 10.1111/j.1574-6941.2009.00654.x

    • Search Google Scholar
    • Export Citation
  • Bernard, G.C., Egnin, M. & Bonsi, C. (2017). The impact of plant-parasitic nematodes on agriculture and methods of control. In: Shah, M.M. & Mahamood, M. (Eds). Nematology – concepts, diagnosis and control. InTech OpenAccess. DOI: 10.5772/intechopen.68958

    • Search Google Scholar
    • Export Citation
  • Bird, A.F. & Zuckerman, B.M. (1989). Studies on the surface coat (glycocalyx) of the dauer larva of Anguina agrostis. International Journal for Parasitology 19, 235-240. DOI: 10.1016/0020-7519(89)90134-3

    • Search Google Scholar
    • Export Citation
  • Castillo, J.D., Vivanco, J.M. & Manter, D.K. (2017). Bacterial microbiome and nematode occurrence in different potato agricultural soils. Microbial Ecology 74, 888-900. DOI: 10.1007/s00248-017-0990-2

    • Search Google Scholar
    • Export Citation
  • Chapman, R.A. & Turner, D.R. (1975). Effect of Meloidogyne incognita on reproduction of Pratylenchus penetrans in red clover and alfalfa. Journal of Nematology 7, 6-9.

    • Search Google Scholar
    • Export Citation
  • Chen, S.-Y., Dickson, D.W. & Mitchell, D.J. (1996). Population development of Heterodera glycines in response to mycoflora in soil from Florida. Biological Control 6, 226-231.

    • Search Google Scholar
    • Export Citation
  • Cook, R.J. (1984). Biological control of plant pathogens: theory to application. Phytopathology 75, 25-29.

  • Crump, D.H. & Kerry, B.R. (1987). Studies on the population dynamics and fungal parasitism of Heterodera schachtii in soil from a sugar-beet monoculture. Crop Protection 6, 49-55. DOI: 10.1016/0261-2194(87)90028-7

    • Search Google Scholar
    • Export Citation
  • Dababat, A.A. & Sikora, R.A. (2007). Induced resistance by the mutualistic endophyte, Fusarium oxysporum strain 162, toward Meloidogyne incognita on tomato. Biocontrol Science and Technology 17, 969-975. DOI: 10.1080/09583150701582057

    • Search Google Scholar
    • Export Citation
  • Duffy, B.K., Ownley, B.H. & Weller, D.M. (1997). Soil chemical and physical properties associated with suppression of take-all of wheat by Trichoderma koningii. Phytopathology 87, 1118-1124. DOI: 10.1094/PHYTO.1997.87.11.1118

    • Search Google Scholar
    • Export Citation
  • Elhady, A., Giné, A., Topalović, O., Jacquiod, S., Sørensen, S.J., Sorribas, F.J. & Heuer, H. (2017). Microbiomes associated with infective stages of root-knot and lesion nematodes in soil. PLoS ONE 12, e0177145. DOI: 10.1371/journal.pone.0177145

    • Search Google Scholar
    • Export Citation
  • Gair, R., Mathias, P.L. & Harvey, P.N. (1969). Studies of cereal nematode populations and cereal yields under continuous or intensive culture. Annals of Applied Biology 63, 503-512. DOI: 10.1111/j.1744-7348.1969.tb02846.x

    • Search Google Scholar
    • Export Citation
  • Hooper, D.J., Hallmann, J. & Subbotin, S.A. (2005). Methods for extraction, processing and detection of plant and soil nematodes. In: Luc, M., Sikora, R.A. & Bridge, J. (Eds). Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edition. Wallingford, UK, CAB International, pp. 53-85. DOI: 10.1079/9780851997278.0000

    • Search Google Scholar
    • Export Citation
  • Hornby, D. (1983). Suppressive soils. Annual Review of Phytopathology 21, 65-85. DOI: 10.1146/annurev.py.21.090183.000433

  • Hu, L., Robert, C.A.M., Cadot, S., Zhang, X., Ye, M., Li, B., Manzo, D., Chervet, N., Steinger, T., van der Heijden, M.G.A. et al. (2018). Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nature Communications 9, 2738. DOI: 10.1038/s41467-018-05122-7

    • Search Google Scholar
    • Export Citation
  • Jones, J.T., Haegeman, A., Danchin, E.G.J., Gaur, H.S., Helder, J., Jones, M.G.K., Kikuchi, T., Manzanilla-López, R., Palomares-Rius, J.E., Wesemael, W.M.L. et al. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14, 946-961. DOI: 10.1111/mpp.12057

    • Search Google Scholar
    • Export Citation
  • Kerry, B.R. (1975). Fungi and the decrease of cereal cyst-nematode populations in cereal monoculture. EPPO Bulletin 5, 353-361.

  • Kerry, B.R. (1982). The decline of Heterodera avenae populations. EPPO Bulletin 12, 491-496.

  • Kerry, B.R. (1988). Fungal parasites of cyst nematodes. Agriculture, Ecosystems and Environment 24, 293-305. DOI: 10.1016/0167-8809(88)90073-4

    • Search Google Scholar
    • Export Citation
  • Kluepfel, D.A., McInnis, T.M. & Zehr, E.I. (1993). Involvement of root-colonizing bacteria in peach orchard soils suppressive of the nematode Criconemella xenoplax. Phytopathology 83, 1240-1245.

    • Search Google Scholar
    • Export Citation
  • Mankau, R. (1975). Bacillus penetrans n. comb. causing a virulent disease of plant-parasitic nematodes. Journal of Invertebrate Pathology 26, 333-339. DOI: 10.1016/0022-2011(75)90231-1

    • Search Google Scholar
    • Export Citation
  • Martínez-Medina, A., Fernández, I., Lok, G.B., Pozo, M.J., Pieterse, C.M.J. & Van Wees, S.C.M. (2017). Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytologist 213, 1363-1377. DOI: 10.1111/nph.14251

    • Search Google Scholar
    • Export Citation
  • Mazzola, M. (2002). Mechanisms of natural soil suppressiveness to soilborne diseases. Antonie Van Leeuwenhoek 81, 557-564.

  • Mendy, B., Wang’ombe, M.W., Radakovic, Z.S., Holbein, J., Ilyas, M., Chopra, D., Holton, N., Zipfel, C., Grundler, F.M.W. & Siddique, S. (2017). Arabidopsis leucine-rich repeat receptor-like kinase NILR1 is required for induction of innate immunity to parasitic nematodes. PLoS Pathogens 13, e1006284. DOI: 10.1371/journal.ppat.1006284

    • Search Google Scholar
    • Export Citation
  • Nicol, J.M., Turner, S.J., Coyne, D.L., den Nijs, L., Hockland, S. & Maafi, Z.T. (2011). Current nematode threats to world agriculture. In: Jones, J., Gheysen, G. & Fenoll, C. (Eds). Genomics and molecular genetics of plant-nematode interactions. Dordrecht, The Netherlands, Springer, pp. 21-43. DOI: 10.1007/978-94-007-0434-3

    • Search Google Scholar
    • Export Citation
  • Piśkiewicz, A.M., Duyts, H. & van der Putten, W.H. (2008). Multiple species-specific controls of root-feeding nematodes in natural soils. Soil Biology and Biochemistry 40, 2729-2735. DOI: 10.1016/j.soilbio.2008.07.006

    • Search Google Scholar
    • Export Citation
  • Pyrowolakis, A., Westphal, A., Sikora, R.A. & Becker, J.O. (2002). Identification of root-knot nematode suppressive soils. Applied Soil Ecology 19, 51-56. DOI: 10.1016/S0929-1393(01)00170-6

    • Search Google Scholar
    • Export Citation
  • Rimé, D., Nazaret, S., Gourbière, F., Cadet, P. & Moënne-Loccoz, Y. (2003). Comparison of sandy soils suppressive or conducive to ectoparasitic nematode damage on sugarcane. Phytopathology 93, 1437-1444. DOI: 10.1094/PHYTO.2003.93.11.1437

    • Search Google Scholar
    • Export Citation
  • Sasser, J.N. (1977). Worldwide dissemination and importance of root-knot nematodes, Meloidogyne spp. Journal of Nematology 9, 26-29.

  • Selim, M.E., Mahdy, M.E., Sorial, M.E., Dababat, A.A. & Sikora, R.A. (2014). Biological and chemical dependent systemic resistance and their significance for the control of root-knot nematodes. Nematology 16, 917-927. DOI: 10.1163/15685411-00002818

    • Search Google Scholar
    • Export Citation
  • Shane, W.W. & Barker, K.R. (1986). Effects of temperature, plant age, soil texture, and Meloidogyne incognita on early growth of soybean. Journal of Nematology 18, 320-326.

    • Search Google Scholar
    • Export Citation
  • Siddiqui, I.A. & Shaukat, S.S. (2004). Systemic resistance in tomato induced by biocontrol bacteria against the root-knot nematode, Meloidogyne javanica is independent of salicylic acid production. Journal of Phytopathology 152, 48-54. DOI: 10.1046/j.1439-0434.2003.00800.x

    • Search Google Scholar
    • Export Citation
  • Stirling, G.R. (2011). Suppressive biological factors influence populations of root lesion nematode (Pratylenchus thornei) on wheat in vertosols from the northern grain-growing region of Australia. Australasian Plant Pathology 40, 416-429. DOI: 10.1007/s13313-011-0059-5

    • Search Google Scholar
    • Export Citation
  • Stirling, G.R. & Mankau, R. (1979). Mode of parasitism of Meloidogyne and other nematode eggs by Dactylella oviparasitica. Journal of Nematology 11, 282-288.

    • Search Google Scholar
    • Export Citation
  • Stirling, G.R., Rames, E., Stirling, A.M. & Hamill, S. (2011). Factors associated with the suppressiveness of sugarcane soils to plant-parasitic nematodes. Journal of Nematology 43, 135-148.

    • Search Google Scholar
    • Export Citation
  • Topalović, O. & Heuer, H. (2019). Plant-nematode interactions assisted by microbes in the rhizosphere. Current Issues in Molecular Biology 30, 75-88. DOI: 10.21775/cimb.030.075

    • Search Google Scholar
    • Export Citation
  • Umesh, K.C., Ferris, H. & Bayer, D.E. (1994). Competition between the plant-parasitic nematodes Pratylenchus neglectus and Meloidogyne chitwoodi. Journal of Nematology 26, 286-295.

    • Search Google Scholar
    • Export Citation
  • Wallace, H.R. (1966). Factors influencing the infectivity of plant parasitic nematodes. Proceedings of the Royal Society of London. Series B. Biological Sciences 164, 592-614. DOI: 10.1098/rspb.1966.0050

    • Search Google Scholar
    • Export Citation
  • Westphal, A. (2005). Detection and description of soils with specific nematode suppressiveness. Journal of Nematology 37, 121-130.

  • Westphal, A. & Becker, J.O. (1999). Biological suppression and natural population decline of Heterodera schachtii in a California field. Phytopathology 89, 434-440. DOI: 10.1094/PHYTO.1999.89.5.434

    • Search Google Scholar
    • Export Citation
  • Westphal, A. & Becker, J.O. (2000). Transfer of biological soil suppressiveness against Heterodera schachtii. Phytopathology 90, 401-406. DOI: 10.1094/PHYTO.2000.90.4.401

    • Search Google Scholar
    • Export Citation
  • Westphal, A. & Becker, J.O. (2001a). Components of soil suppressiveness against Heterodera schachtii. Soil Biology and Biochemistry 33, 9-16. DOI: 10.1016/S0038-0717(00)00108-5

    • Search Google Scholar
    • Export Citation
  • Westphal, A. & Becker, J.O. (2001b). Soil suppressiveness to Heterodera schachtii under different cropping sequences. Nematology 3, 55-558. DOI: 10.1163/156854101753389167

    • Search Google Scholar
    • Export Citation
  • Westphal, A., Pyrowolakis, A., Sikora, R.A. & Becker, J.O. (2011). Soil suppressiveness against Heterodera schachtii in California cropping areas. Nematropica 41, 161-171.

    • Search Google Scholar
    • Export Citation
  • Zhou, D., Feng, H., Schuelke, T., de Santiago, A., Zhang, Q., Zhang, J., Luo, C. & Wei, L. (2019). Rhizosphere microbiomes from root knot nematode non-infested plants suppress nematode infection. Microbial Ecology. DOI: 10.1007/s00248-019-01319-5

    • Search Google Scholar
    • Export Citation

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 274 274 47
Full Text Views 38 38 1
PDF Downloads 20 20 1