Skip to main content
SpringerLink
Log in

Impact of the genetic diversity of three cyst nematodes on the effectiveness of root exudates to induce hatching

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Cyst nematodes are sedentary endoparasites of plants which cause important economic losses worldwide. New nematode control measures are needed since the removal of effective chemical nematicides from the market due to their negative impact on environment and human health. Induced hatching of second-stage juveniles in the absence of host plant using root exudates, also named “suicide hatching”, could be a sustainable alternative method to reduce nematode population densities in infested soils. Unfortunately, biocontrol methods are often less effective in agricultural fields than in laboratory or greenhouse and this could be due to, among other reasons, a different susceptibility of nematode populations to root exudate stimulation. Testing this intra-specific variability would help to anticipate any drop in the efficiency of this new biocontrol strategy. A selection of root exudates from different plant species, maximizing the hatching level highlighted in a previous study, was tested on the hatching of representative populations of the genetic diversity for Globodera pallida, Heterodera schachtii and Heterodera carotae. Results showed significant differences between populations for given nematode species but not correlated with the genetic structure. Overall, root exudates tested provide a high level of hatching of these three nematode species. Surprisingly, the root exudate from broccoli induces hatching of European populations of the potato cyst nematode G. pallida.

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

  • Aires, A., Carvalho, R., Barbosa, M. D. C., & Rosa, E. (2009). Suppressing potato cyst nematode, Globodera rostochiensis, with extracts of Brassicacea plants. American Journal of Potato Research, 86(4), 327–333.

    Article  Google Scholar 

  • Ali, A., Haider, M. S., Hanif, S., & Akhtar, N. (2014). Assessment of the antibacterial activity of Cuscuta pedicellata Ledeb. African Journal of Biotechnology, 13(3), 430–433.

    Article  Google Scholar 

  • Aubert, V. (1986). Contribution à l'étude de la biologie d'un parasite de la carotte Université de Neuchâtel].

    Google Scholar 

  • Balendres, M. A., Nichols, D. S., Tegg, R. S., & Wilson, C. R. (2016). Metabolomes of potato root exudates: Compounds that stimulate resting spore germination of the soil-borne pathogen Spongospora subterranea. Journal of Agricultural and Food Chemistry, 64(40), 7466–7474.

    Article  CAS  Google Scholar 

  • Baranski, R., Maksylewicz-Kaul, A., Nothnagel, T., Cavagnaro, P. F., Simon, P. W., & Grzebelus, D. (2012). Genetic diversity of carrot (Daucus carota L.) cultivars revealed by analysis of SSR loci. Genetic Resources and Crop Evolution, 59(2), 163–170.

    Article  Google Scholar 

  • Bardin, M., Schmitt, A., & Nicot, P. C. (2013). Diversity in the effect of an extract from Fallopia sachalinensis on isolates of cucurbit powdery mildews grown on melon. IOBC-WPRS Bull, 88, 93–97.

    Google Scholar 

  • Bones, A. M., & Rossiter, J. T. (2006). The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry, 67(11), 1053–1067.

    Article  CAS  Google Scholar 

  • Devine, K., & Jones, P. (2000). Response of Globodera rostochiensis to exogenously applied hatching factors in soil. Annals of Applied Biology, 137(1), 21–29.

    Article  Google Scholar 

  • Fahey, J. W., Zalcmann, A. T., & Talalay, P. (2001). The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 56(1), 5–51.

    Article  CAS  Google Scholar 

  • Fournet, S., Pellan, L., Porte, C., Piriou, C., Grenier, E., & Montarry, J. (2018). Populations of the beet cyst nematode Heterodera schachtii exhibit strong differences in their life-history traits across changing thermal conditions. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2018.02801.

  • Gautier, C., Esquibet, M., Fournet, S., Piriou, C., Yvin, J.-C., Nguema-Ona, E., Grenier, E., & Montarry, J. (2019). Microsatellite markers reveal two genetic groups in European populations of the carrot cyst nematode Heterodera carotae. Infection, Genetics and Evolution, 73, 81–92.

    Article  Google Scholar 

  • Grenier, E., Anthoine, G., Fournet, S., & Petit, E. (2010). A cyst nematode ‘species factory’ called the Andes. Nematology, 12(2), 163–169.

  • Grzebelus, D., Iorizzo, M., Senalik, D., Ellison, S., Cavagnaro, P., Macko-Podgorni, A., Heller-Uszynska, K., Kilian, A., Nothnagel, T., & Allender, C. (2014). Diversity, genetic mapping, and signatures of domestication in the carrot (Daucus carota L.) genome, as revealed by diversity arrays technology (DArT) markers. Molecular Breeding, 33(3), 625–637.

    Article  CAS  Google Scholar 

  • Hockland, S., Niere, B., Grenier, E., Blok, V., Phillips, M., den Nijs, L., Anthoine, G., Pickup, J., & Viaene, N. (2012). An evaluation of the implications of virulence in non-European populations of Globodera pallida and G. rostochiensis for potato cultivation in Europe. Nematology, 14(1), 1–13.

  • Iorizzo, M., Senalik, D. A., Ellison, S. L., Grzebelus, D., Cavagnaro, P. F., Allender, C., Brunet, J., Spooner, D. M., Van Deynze, A., & Simon, P. W. (2013). Genetic structure and domestication of carrot (Daucus carota subsp. sativus)(Apiaceae). American Journal of Botany, 100(5), 930–938.

    Article  Google Scholar 

  • Kaczmarek, A., Mackenzie, K., Kettle, H., & Biok, V. C. (2014). Influence of soil temperature on Globodera rostochiensis and Globodera pallida. Phytopathologia Mediterranea, 53(3), 396–405.

    CAS  Google Scholar 

  • Le Mire, G., Nguyen, M., Fassotte, B., du Jardin, P., Verheggen, F., Delaplace, P., & Jijakli, H. (2016). Implementing biostimulants and biocontrol strategies in the agroecological management of cultivated ecosystems. Société et Environnement: Biotechnologie, Agronomie.

    Google Scholar 

  • Lettice, E. P., & Jones, P. W. (2015). Evaluation of rhizobacterial colonisation and the ability to induce Globodera pallida hatch. Nematology, 17(2), 203–212.

    Article  Google Scholar 

  • Lord, J. S., Lazzeri, L., Atkinson, H. J., & Urwin, P. E. (2011). Biofumigation for control of pale potato cyst nematodes: Activity of brassica leaf extracts and green manures on Globodera pallida in vitro and in soil. Journal of Agricultural and Food Chemistry, 59(14), 7882–7890.

    Article  CAS  Google Scholar 

  • Masamune, T., Anetai, M., Takasugi, M., & Katsui, N. (1982). Isolation of a natural hatching stimulus, glycinoeclepin a, for the soybean cyst nematode. Nature, 297(5866), 495–496.

    Article  CAS  Google Scholar 

  • Masler, E., & Perry, R. (2018). Hatch, survival and sensory perception (pp. 44–73). Cyst nematodes. Wallingford, UK: CAB International.

    Google Scholar 

  • Molinari, S. (2011). Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides. Plant Cell Reports, 30(3), 311–323.

    Article  CAS  Google Scholar 

  • Mugniery, D., & Bossis, M. (1988). Heterodera carotae Jones, 1950. 1. Gamme d’hôtes, vitesse de développement, cycle. Revue de nématologie, 11(3), 307–313.

    Google Scholar 

  • Ngala, B. M., Haydock, P. P., Woods, S., & Back, M. A. (2015). Biofumigation with Brassica juncea, Raphanus sativus and Eruca sativa for the management of field populations of the potato cyst nematode Globodera pallida. Pest Management Science, 71(5), 759–769.

    Article  CAS  Google Scholar 

  • Ngala, B., Mariette, N., Ianszen, M., Dewaegeneire, P., Denis, M. C., Porte, C., Piriou, C., Robilliard, E., Couetil, A., Nguema-Ona, E., Yvin, J. C., Gobert, V., Beury, A., Le Roux, A. C., Montarry, J., & Fournet, S. (2021). Hatching induction of cyst nematodes in bare soils drenched with root exudates under controlled conditions. Frontiers in Plant Science, 11, 602825.

    Article  Google Scholar 

  • Nicot, P. C., Alabouvette, C., Bardin, M., Blum, B., Köhl, J., & Ruocco, M. (2012). Review of factors influencing the success or failure of biocontrol: Technical, industrial and socio-economic perspectives. IOBC-WPRS Bull, 78, 95–98.

    Google Scholar 

  • Parnell, J. J., Berka, R., Young, H. A., Sturino, J. M., Kang, Y., Barnhart, D., & DiLeo, M. V. (2016). From the lab to the farm: An industrial perspective of plant beneficial microorganisms. Frontiers in Plant Science, 7, 1110.

    Article  Google Scholar 

  • Perry, R. N., Moens, M., & Jones, J. T. (2018). Cyst nematodes. CABI.

  • Picard, D., Sempere, T., & Plantard, O. (2007). A northward colonisation of the Andes by the potato cyst nematode during geological times suggests multiple host-shifts from wild to cultivated potatoes. Molecular Phylogenetics and Evolution, 42(2), 308–316.

    Article  CAS  Google Scholar 

  • Plantard, O., Picard, D., Valette, S., Scurrah, M., Grenier, E., & Mugniéry, D. (2008). Origin and genetic diversity of Western European populations of the potato cyst nematode (Globodera pallida) inferred from mitochondrial sequences and microsatellite loci. Molecular Ecology, 17(9), 2208–2218.

    Article  CAS  Google Scholar 

  • Development Core Team, R. (2019). R: A language and environment for statistical computing. Vienna, Austria: The R Foundation for Statistical Computing Available at http://www.R-project.org/.

    Google Scholar 

  • Rashid, A., Ahmed, H., Xiao, Q., Hwang, S., & Strelkov, S. (2013). Effects of root exudates and pH on Plasmodiophora brassicae resting spore germination and infection of canola (Brassica napus L.) root hairs. Crop Protection, 48, 16–23.

    Article  CAS  Google Scholar 

  • Schenk, H., Driessen, R. A., de Gelder, R., Goubitz, K., Nieboer, H., Brüggemann-Rotgans, I. E., & Diepenhorst, P. (1999). Elucidation of the structure of Solanoeclepin a, a natural hatching factor of potato and tomato cyst nematodes, by single-crystal x-ray diffraction. Croatica Chemica Acta, 72(2–3), 593–606.

    CAS  Google Scholar 

  • Sullivan, M., Inserra, R., Franco, J., Moreno-Leheudé, I., & Greco, N. (2007). Potato cyst nematodes: Plant host status and their regulatory impact. Nematropica, 37(2), 193–202.

    Google Scholar 

  • Tanino, K., Takahashi, M., Tomata, Y., Tokura, H., Uehara, T., Narabu, T., & Miyashita, M. (2011). Total synthesis of solanoeclepin a. Nature Chemistry, 3(6), 484–488.

    Article  CAS  Google Scholar 

  • Turner, S. J., & Subbotin, S. A. (2013). Cyst nematodes. In R. N. Perry & M. Moens (Eds.), Plant Nematology,2nd edn. Wallingford, UK: CAB International.

    Google Scholar 

  • Zwanenburg, B., Mwakaboko, A. S., & Kannan, C. (2016). Suicidal germination for parasitic weed control. Pest Management Science, 72(11), 2016–2025.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge FN3PT/RD3PT who produced potato root exudates, SILEBAN who produced carrot root exudates and Nicolas Mariette and Marie-Christine Denis from INRAE IGEPP who produced tomato, broccoli, brown mustard and sugar beet root exudates.

Funding

This work was funded by ADEME (Agence de l’Environnement et de la Maîtrise de l’Energie) through the PIA-BIODERA project (n.1682C0290). Camille Gautier is supported by a PhD grant from Centre Mondial de l’Innovation Roullier and ANRT (Association Nationale Recherche Technologie).

Author information

Authors and Affiliations

  1. INRAE, UMR1349 IGEPP, Institute of Genetic Environment and Plant Protection, F35650, Le Rheu, France

    Camille Gautier, Josselin Montarry, Christophe Piriou, Lionel Renault, Catherine Porte & Sylvain Fournet

  2. Laboratoire de Nutrition Végétale - Pôle Stress Biotique, Centre Mondial de l’Innovation-Roullier, F35400, Saint Malo, France

    Camille Gautier, Jean-Claude Yvin & Eric Nguema-Ona

Authors
  1. Camille Gautier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Josselin Montarry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christophe Piriou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lionel Renault
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Catherine Porte
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jean-Claude Yvin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eric Nguema-Ona
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sylvain Fournet
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CG and CP conducted the experiments according to a protocol elaborated by CG, JM, JCY, ENO and SF. LR, CP and SF multiplied nematode populations used in this study. CG, JM and SF analysed the data, realized the figures and wrote the text. All authors edited the paper and approved the current version.

Corresponding author

Correspondence to Sylvain Fournet.

Ethics declarations

Conflict of interest/competing interests

The authors declare that they have no conflict of interest.

Ethics approval

The authors bear all the ethical responsibilities of this manuscript.

Consent for publication

All authors have consented for this research to be published.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gautier, C., Montarry, J., Piriou, C. et al. Impact of the genetic diversity of three cyst nematodes on the effectiveness of root exudates to induce hatching. Eur J Plant Pathol 161, 553–563 (2021). https://doi.org/10.1007/s10658-021-02341-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-021-02341-5

Keywords

Search

Navigation