Antagonistic role of the microbiome from a Meloidogyne hapla-suppressive soil against species of plant-parasitic nematodes with different life strategies
In: NematologySearch for other papers by Olivera Topalović in
Current site
Google Scholar
Search for other papers by Holger Heuer in
Current site
Google Scholar
Search for other papers by Annette Reineke in
Current site
Google Scholar
Search for other papers by Jana Zinkernagel in
Current site
Google Scholar
Search for other papers by Johannes Hallmann in
Current site
Google Scholar
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.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
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
-
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
-
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
-
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
-
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
-
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
-
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.
-
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.
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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.
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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.
-
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
-
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
-
Stirling, G.R. & Mankau, R. (1979). Mode of parasitism of Meloidogyne and other nematode eggs by Dactylella oviparasitica. Journal of Nematology 11, 282-288.
-
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.
-
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
-
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.
-
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
-
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
-
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
-
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
-
Westphal, A. & Becker, J.O. (2001b). Soil suppressiveness to Heterodera schachtii under different cropping sequences. Nematology 3, 55-558. DOI: 10.1163/156854101753389167
-
Westphal, A., Pyrowolakis, A., Sikora, R.A. & Becker, J.O. (2011). Soil suppressiveness against Heterodera schachtii in California cropping areas. Nematropica 41, 161-171.
-
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
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2178 | 413 | 84 |
| Full Text Views | 571 | 30 | 1 |
| PDF Views & Downloads | 317 | 41 | 1 |
Antagonistic role of the microbiome from a Meloidogyne hapla-suppressive soil against species of plant-parasitic nematodes with different life strategies
In: NematologySearch for other papers by Olivera Topalović in
Current site
Google Scholar
PubMed
Search for other papers by Holger Heuer in
Current site
Google Scholar
PubMed
Search for other papers by Annette Reineke in
Current site
Google Scholar
PubMed
Search for other papers by Jana Zinkernagel in
Current site
Google Scholar
PubMed
Search for other papers by Johannes Hallmann in
Current site
Google Scholar
PubMed
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.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2178 | 413 | 84 |
| Full Text Views | 571 | 30 | 1 |
| PDF Views & Downloads | 317 | 41 | 1 |
