Skip to main content
SpringerLink
Log in

Highly Potent Extracts from Pea (Pisum sativum) and Maize (Zea mays) Roots Can Be Used to Induce Quiescence in Entomopathogenic Nematodes

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Root exudates can play an important role in plant-nematode interactions. Recent studies have shown that the root cap exudates obtained from several plant species trigger a state of dormancy or quiescence in various genera of nematodes. This phenomenon is not only of fundamental ecological interest, but also has application potential if the plant-produced compound(s) could be used to control harmful nematodes or help to prolong the shelf-life of beneficial entomopathogenic nematodes (EPNs). The identification of the compound(s) involved in quiescence induction has proven to be a major challenge and requires large amounts of active material. Here, we present a high-throughput method to obtain bioactive root extracts from flash-frozen root caps of green pea and maize. The root cap extract obtained via this method was considerably more potent in inducing quiescence than exudate obtained by a previously used method, and consistently induced quiescence in the EPN Heterorhabditis megidis, even after a 30-fold dilution. Extracts obtained from the rest of the root were equally effective in inducing quiescence. Infective juveniles (IJs) of H. megidis exposed to these extracts readily recovered from their quiescent state as soon as they were placed in moist soil, and they were at least as infectious as the IJs that had been stored in water. Excessive exposure of IJs to air interfered with the triggering of quiescence. The implications of these results and the next steps towards identification of the quiescence-inducing compound(s) are discussed from the perspective of applying EPN against soil-dwelling insect pests.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams B, Nguyen K (2002) Taxonomy and systematics. In: Gaugler R (ed) Entomopathogenic nematology. CABI, New York, pp 1–34

    Chapter  Google Scholar 

  • Ali JG, Alborn HT, Stelinski LL (2010) Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. J Chem Ecol 36:361–368. doi:10.1007/s10886-010-9773-7

    Article  CAS  PubMed  Google Scholar 

  • Ali JG, Alborn HT, Campos-Herrera R, Kaplan F, Duncan LW, Rodriguez-Saona C, Koppenhöfer M, Stellinski LL (2012) Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats. PLoS ONE 7:1–8. doi:10.1371/journal.pone.0038146

    CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. doi:10.1146/annurev.arplant.57.032905.105159

    Article  CAS  PubMed  Google Scholar 

  • Barber BYDA, Martin JK, June I (1976) The release of organic substances by cereal roots into soil. New Phytol 76:69–80

    Article  CAS  Google Scholar 

  • Barrett J (1991) Anhydrobiotic nematodes. In: Evans K (ed) Agricultural zoological reviews. Vol. 4. Intercept, Andover, pp 161–176

    Google Scholar 

  • Chen S, Glazer I (2005) A novel method for long-term storage of the entomopathogenic nematode Steinernema feltiae at room temperature. Biol Control 32:104–110. doi:10.1016/j.biocontrol.2004.08.006

    Article  CAS  Google Scholar 

  • Curtis RHC, Robinson AF, Perry RN (2009) Hatch and host location. In: Perry R, Moen M, Starr J (eds) Root-knot nematodes. CABI Publ, Wallingford, pp 139–162

    Chapter  Google Scholar 

  • Den Nijs LJMF, Lock CAM (1992) Differential hatching of the potato cyst nematodes Globodera rostochiensis and G. pallida in root diffusates and water of differing ionic composition. Neth J Plant Pathol 98:117–128. doi:10.1007/BF01996324

    Article  Google Scholar 

  • Dillman AR, Chaston JM, Adams BJ, Ciche TA, Goodrich-Blair H, Stock SP, Sternberg PW (2012) An entomopathogenic nematode by any other name. PLoS Pathog 8:8–11. doi:10.1371/journal.ppat.1002527

    Article  Google Scholar 

  • Forst S, Clarke D (2002) Bacteria-nematode symbiosis. In: Gaugler R (ed) Entomopathogenic nematology. CABI Publishing, New York, pp 57–77

    Chapter  Google Scholar 

  • Gaur HS, Beane J, Perry RN (2000) The influence of root diffusate, host age and water regimes on hatching of the root-knot nematode, Meloidogyne triticoryzae. Nematology 2:191–199

    Article  Google Scholar 

  • Georgis R, Koppenhöfer M, Lacey LA, Bélair G, Duncam LW, Grewal PS, Samish M, Tan L, Torr P, van Tol RWHM (2006) Successes and failures in the use of parasitic nematodes for pest control. Biol Control 38:103–123. doi:10.1016/j.biocontrol.2005.11.005

  • Grewal PS (2002) Formulation and application technology. In: Gaugler R (ed) Entomopathogenic nematology. CABI Publishing, New York, pp 265–287

    Chapter  Google Scholar 

  • Grewal PS, Peters A (2005) Formulation and quality control of entomopathogenic nematodes. In: Grewal PS, Ehlers RU, Shapiro-Ilan D (eds) Nematodes as biocontrol agents. CABI Publishing, Wallingford, pp 79–90

    Chapter  Google Scholar 

  • Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846. doi:10.1016/j.phytochem.09.017

    Article  CAS  PubMed  Google Scholar 

  • Hiltpold I, Turlings TCJ (2012) Manipulation of chemically mediated interactions in agricultural soils to enhance the control of crop pests and to improve crop yield. J Chem Ecol 38:641–650. doi:10.1007/s10886-012-0131-9

    Article  CAS  PubMed  Google Scholar 

  • Hiltpold I, Erb M, Robert CAM, Turlings TCJ (2011) Systemic root signalling in a belowground, volatile-mediated tritrophic interaction. Plant Cell Environ 34:1267–1275. doi:10.1111/j.1365-3040.2011.02327.x

    Article  CAS  PubMed  Google Scholar 

  • Hiltpold I, Hibbard BE, French BW, Turlings TCJ (2012) Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the western corn rootworm. Plant Soil 358:11–25. doi:10.1007/s11104-012-1253-0

    Article  CAS  Google Scholar 

  • Hiltpold I, Jaffuel G, Turlings TCJ (2014) The dual effects of root-cap exudates on nematodes: from quiescence in plant-parasitic nematodes to frenzy in entomopathogenic nematodes. J Exp Bot. doi:10.1093/jxb/eru345

    PubMed Central  PubMed  Google Scholar 

  • Hubbard JE, Flores-Lara Y, Schmitt M, McCLure MA, Stock SP, Hawes MC (2005) Increased penetration of host roots by nematodes after recovery from quiescence induced by root cap exudate. Nematology 7:321–331

    Article  Google Scholar 

  • Kaya HK, Gaugler R (1993) Entomopathogenic nematodes. Annu Rev Entomol 38:181–206. doi:10.1146/annurev.en.38.010193.001145

    Article  Google Scholar 

  • Khokon MAR, Okuma E, Rahman T, Wesemael WML, Murata Y, Moens M (2009) Quantitative analysis of the effects of diffusates from plant roots on the hatching of Meloidogyne chitwoodi from young and senescing host plants. Biosci Biotechnol Biochem 73:2345–2347. doi:10.1271/bbb.90392

    Article  CAS  PubMed  Google Scholar 

  • Köhler HR, Triebskorn R (2013) Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341:759–765. doi:10.1126/science.1237591

    Article  PubMed  Google Scholar 

  • Kumar R, Pandey S, Pandey A (2006) Plant roots and carbon sequestration. Curr Sci 91:885–890

    CAS  Google Scholar 

  • Lello ER, Patel MN, Matthews G, Wright DJ (1996) Application technology for entomopathogenic nematodes against foliar pests. Crop Prot 15:567–574. doi:10.1016/0261-2194(96)00026-9

    Article  Google Scholar 

  • Lewis EE, Campbell J, Griffin C, Kaya H, Peters A (2006) Behavioral ecology of entomopathogenic nematodes. Biol Control 38:66–79. doi:10.1016/j.biocontrol.2005.11.007

    Article  Google Scholar 

  • Prot J (1980) Migration of plant-parasitic nematodes towards plant roots. Rev Nemtology 3(2): 305–318

  • Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenton J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737. doi:10.1038/nature03451

    Article  CAS  PubMed  Google Scholar 

  • Rasmann S, Hiltpold I, Ali J (2012) The role of root-produced volatile secondary metabolites in mediating soil interactions. In: Montanaro G, Cichio B (eds) Advances in selected plant physiology aspects. InTech Open Access Publisher, Croatia, pp 269–290

    Google Scholar 

  • Reynolds AM, Dutta TK, Curtis RHC, Powers SJ, Gaur HS, Kerry BR (2011) Chemotaxis can take plant-parasitic nematodes to the source of a chemo-attractant via the shortest possible routes. J R Soc Interface 8:568–577. doi:10.1098/rsif.2010.0417

    Article  PubMed Central  PubMed  Google Scholar 

  • Rolfe RN, Barrett J, Perry ARN (2000) Analysis of chemosensory responses of second stage juveniles of Globodera rostochiensis using electrophysiological techniques. Nematology 2:523–533

    Article  CAS  Google Scholar 

  • Shapiro-Ilan DI, Gouge DH, Piggott SJ, Fife JP (2006) Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biol Control 38:124–133. doi:10.1016/j.biocontrol.2005.09.005

    Article  Google Scholar 

  • Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:51–60. doi:10.1007/s11104-012-1295-3

    Article  CAS  Google Scholar 

  • Van Dam NM (2009) Belowground herbivory and plant defenses. Annu Rev Ecol Evol Syst 40:373–391. doi:10.1146/annurev.ecolsys.110308.120314

    Article  Google Scholar 

  • Van Tol RWHM, Van der Sommen ATC, Boff MIC, Van Bezooijen J, Sabelis MW, Smits PH (2001) Plants protect their roots by alerting the ennemies of grubs. Ecol Lett 4:292–294. doi:10.1046/j.1461-0248.2001.00227.x

    Article  Google Scholar 

  • Vining LC (1990) Functions of secondary metabolites. Annu Rev Microbiol 44:395–427. doi:10.1146/annurev.mi.44.100190.002143

    Article  CAS  PubMed  Google Scholar 

  • White GF (1927) A method for obtaining infective nematode larvae from cultures. Science 66:302–303

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Schmitt M, Hawes MC (2000) Species-dependent effects of border cell and root tip exudates on nematode behavior. Phytopathology 90:1239–1245. doi:10.1094/PHYTO.2000.90.11.1239

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the members of the FARCE laboratory for their frequent assistance and relevant discussion. We especially thank Drs. Jinwon Kim and Raquel Campos Herrera for fruitful discussions and their helpful comments on an earlier version of the manuscript. We also thank Andermatt Biocontrol SA (Switzerland), and DSP SA (Switzerland) for providing EPNs and seeds, respectively. This work was supported by an economic stimulus grant from the Swiss National Science Foundation.

Author information

Authors and Affiliations

  1. FARCE Laboratory, Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, 2000, Neuchâtel, Switzerland

    Geoffrey Jaffuel & Ted C. J. Turlings

  2. Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bag 1797, Penrith, NSW, 2751, Australia

    Ivan Hiltpold

Authors
  1. Geoffrey Jaffuel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivan Hiltpold
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ted C. J. Turlings
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ted C. J. Turlings.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaffuel, G., Hiltpold, I. & Turlings, T.C.J. Highly Potent Extracts from Pea (Pisum sativum) and Maize (Zea mays) Roots Can Be Used to Induce Quiescence in Entomopathogenic Nematodes. J Chem Ecol 41, 793–800 (2015). https://doi.org/10.1007/s10886-015-0623-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-015-0623-5

Keywords

Search

Navigation