Cookies Policy

This site uses cookies. By continuing to browse the site you are agreeing to our use of cookies.

I accept this policy

Find out more here

Phenotyping dauer juvenile oxidative stress tolerance, longevity and persistence within wild type and inbred lines of the entomopathogenic nematode Heterorhabditis bacteriophora

No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.
The full text of this article is not currently available.

Brill’s MyBook program is exclusively available on BrillOnline Books and Journals. Students and scholars affiliated with an institution that has purchased a Brill E-Book on the BrillOnline platform automatically have access to the MyBook option for the title(s) acquired by the Library. Brill MyBook is a print-on-demand paperback copy which is sold at a favorably uniform low price.

Access this article

+ Tax (if applicable)
Add to Favorites
You must be logged in to use this functionality

For more content, see Nematologica.

The commercial use of the entomopathogenic nematode Heterorhabditis bacteriophora as a biocontrol agent against noxious insects is limited due to its relatively short shelf-life. Longevity of dauer juveniles (DJ) during storage and in transit to end users is considerably restricted by environmental stresses. As a derivative stress triggered by environmental factors, oxidative stress causes a strong internal metabolic imbalance leading to lifespan reduction. In this study, the relation between DJ oxidative stress tolerance and longevity in H. bacteriophora was investigated at 25 and 7°C. A strong and significant correlation between DJ oxidative stress tolerance and longevity during storage in Ringer’s solution (R=0.802 at 7°C; R=0.604 at 25°C) was recorded. Phenotyping of these traits was performed for 40 H. bacteriophora wild type strain and inbred line collections. At 25°C, the mean time survived in Ringer’s by 50% of the DJ (MTS50) ranged from 21 to 57 days, whereas under oxidative stress, survival was from 3 to 22 days. At 7°C, a maximum MTS50 of 94 days was assessed when DJ were stored in Ringer’s, while the maximum MTS50 was only 25 days with oxidative stress induction. The heritability of DJ tolerance to oxidative stress, determined by using homozygous inbred lines, is high (h2>0.9), an indication of a high probability for successful selective breeding. In a subset of preselected H. bacteriophora inbred lines, DJ oxidative stress tolerance correlated with the DJ survival (persistence) after application to sand (R=0.719). The study provides fundamental data required for a genetic breeding programme to produce hybrids with improved stress tolerance and prolonged shelf-life and soil persistence.

Affiliations: 1: 1Faculty of Agricultural and Nutritional Sciences, Christian-Albrechts-University Kiel, Hermann-Rodewald-Strasse 4, 24118 Kiel, Germany ; 2: 2e-nema GmbH, Klausdorfer Strasse 28-36, 24223 Schwentinental, Germany ; 3: 3Department of Biology, Ghent University, K.L. Ledeganckstraat 35, B-9000 Ghent, Belgium

*Corresponding author, e-mail:

Full text loading...


Data & Media loading...

1. Aan G.J., Zainudin M.S.A., Karim N.A., Ngah W.Z.W. (2013). "Effect of the tocotrienol-rich fraction on the lifespan and oxidative biomarkers in Caenorhabditis elegans under oxidative stress". Clinics Vol 68, 599-604. DOI: 10.6061/clinics/2013(05)04 [Crossref]
2. Addis T., Demissie S., Strauch O., Ehlers R.-U. (2016). "Influence of bacterial density and mating on life history traits of Heterorhabditis bacteriophora". Nematology Vol 18, 963-972. DOI: 10.1163/15685411-00002966 [Crossref]
3. Anbesse S., Sumaya N.H., Dörfler A.V., Strauch O., Ehlers R.-U. (2013a). "Stabilisation of heat tolerance traits in Heterorhabditis bacteriophora through selective breeding and creation of inbred lines in liquid culture". BioControl Vol 58, 85-93. DOI: 10.1007/s10526-012-9467-x [Crossref]
4. Anbesse S., Sumaya N.H., Dörfler A.V., Strauch O., Ehlers R.-U. (2013b). "Selective breeding for desiccation tolerance in liquid culture provides genetically stable inbred lines of the entomopathogenic nematode Heterorhabditis bacteriophora". Applied Microbiology and Biotechnology Vol 97, 731-739. DOI: 10.1007/s00253-012-4227-5 [Crossref]
5. Andaló V., Moino A., Maximiniano C., Campos V.P., Mendonca L.A. (2011). "Influence of temperature and duration of storage on the lipid reserves of entomopathogenic nematodes". Revista Colombiana de Entomología Vol 37, 203-209.
6. Berner M., Ehlers R.-U., Schnetter W. (2001). Genetic variability and discrimination of isolates, inbred lines and hybrids of Heterorhabditis bacteriophora via RAPD-PCR. In: 34th Annual Meeting of the Society for Invertebrate Pathology. Noordwijkerhout, The Netherlands, August 25-30, p. 7.
7. Brooks A., Johnson T.E. (1991). "Genetic specification of life span and self-fertility in recombinant-inbred strains of Caenorhabditis elegans". Heredity Vol 67, 19-28. DOI: 10.1038/hdy.1991.60 [Crossref]
8. Charlesworth B. (1987). "The heritability of fitness". In: Bradbury J.W., Andersson M.B. (Eds). Sexual selection: testing the alternatives. Chichester, UK, Wiley, pp.  21-40.
9. Cobb N.A. (1918). Estimating the nematode population of soil, with special reference to the sugar-beet and root-gall nematodes, Heterodera schachtii Schmidt and Heterodera radicicola (Greef) Müller and with a description of Tylencholaimus aequalis n. sp. Washington, DC, USA, Government Printing Office.
10. Crichton R.R., Wilmet S., Legssyer R., Ward R.J. (2002). "Molecular and cellular mechanisms of iron homeostasis and toxicity in mammalian cells". Journal of Inorganic Biochemistry Vol 91, 9-18. DOI: 10.1016/S0162-0134(02)00461-0 [Crossref]
11. Cypser J.R., Johnson T.E. (2002). "Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity". The Journals of Gerontology Series A: Biological Sciences and Medical Sciences Vol 57, B109-B114. DOI: 10.1093/gerona/57.3.B109 [Crossref]
12. Ehlers R.-U., Lunau S., Krasomil-Osterfeld K., Osterfeld K.H. (1998). "Liquid culture of the entomopathogenic nematode-bacterium-complex Heterorhabditis megidis/P. luminescens". BioControl Vol 43, 77-86. DOI: 10.1023/A:1009965922794 [Crossref]
13. Ehlers R.-U., Oestergaard J., Hollmer S., Wingen M., Strauch O. (2005). "Genetic selection for heat tolerance and low temperature activity of the entomopathogenic nematode-bacterium-complex Heterorhabditis bacteriophora-Photorhabdus luminescens". Biocontrol Vol 50, 699-716. DOI: 10.1007/s10526-005-5079-z [Crossref]
14. Falconer D.S. (1989). Introduction to quantitative genetics, 3rd edition. New York, NY, USA, Longman Scientific and Technical.
15. Falconer D.S., Mackay T.F.C. (1996). Introduction to quantitative genetics, 4th edition. Harlow, UK, Longman.
16. Fan X., Hominick W.M. (1991). "Effects of low storage temperature on survival and infectivity of two Steinernema species (Nematoda: Steinernematidae)". Revue de Nématologie Vol 14, 407-412.
17. Finkel T., Holbrook N.J. (2000). "Oxidants, oxidative stress and the biology of ageing". Nature Vol 408, 239-247. DOI: 10.1038/35041687 [Crossref]
18. Finney D.J. (1952). "Probit analysis". Journal of the Institute of Actuaries Vol 78, 388-390.
19. Fisher R.A. (1930). The genetical theory of natural selection: a complete variorum edition. Oxford, UK, Oxford University Press.
20. Fitters P.F., Griffin C.T. (2006). "Survival, starvation, and activity in Heterorhabditis megidis (Nematoda: Heterorhabditidae)". Biological Control Vol 37, 82-88. DOI: 10.1016/j.biocontrol.2005.08.005 [Crossref]
21. Georgis R., Kaya H.K. (1998). "Formulation of entomopathogenic nematodes". In: Burges H.D. (Ed.). Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments. Dordrecht, The Netherlands, Kluwer Academic Publishers, pp.  289-308. DOI: 10.1007/978-94-011-4926-6 [Crossref]
22. Glazer I. (2002). "Survival biology". In: Gaugler R. (Ed.). Entomopathogenic nematology. Wallingford, UK, CAB International, pp.  169-187. [Crossref]
23. Grewal P.S., Peters A. (2005). "Formulation and quality control of entomopathogenic nematodes". In: Grewal P.S., Ehlers R.-U., Shapiro-Ilan D. (Eds). Nematodes as biocontrol agents. Wallingford, UK, CAB International, pp.  79-90. DOI: 10.1079/9780851990170.0079 [Crossref]
24. Grewal P.S., Wang X., Taylor R.A.J. (2002). "Dauer juvenile longevity and stress tolerance in natural populations of entomopathogenic nematodes: is there a relationship?" International Journal for Parasitology Vol 32, 717-725. DOI: 10.1016/S0020-7519(02)00029-2 [Crossref]
25. Grewal P.S., Ehlers R.-U., Shapiro-Ilan D.I. (Eds) (2005). Nematodes as biocontrol agents. Wallingford, UK, CAB International. DOI: 10.1079/9780851990170.0000
26. Grewal P.S., Bai X., Jagdale G.B. (2011). "Longevity and stress tolerance". In: Perry R.N., Wharton D.A. (Eds). Molecular and physiological basis of nematode survival. Wallingford, UK, CAB International, pp.  157-181. DOI: 10.1079/9781845936877.0157 [Crossref]
27. Gustafsson L. (1986). "Lifetime reproductive success and heritability: empirical support for Fisher’s fundamental theorem". The American Naturalist Vol 128, 761-764. [Crossref]
28. Harman D. (1956). "Aging: a theory based on free radical and radiation chemistry". Journal of Gerontology Vol 11, 298-300. DOI: 10.1093/geronj/11.3.298 [Crossref]
29. Hartl D.L., Clark A.G., Clark A.G. (1989). Principles of population genetics, 2nd edition. Sunderland, MA, USA, Sinauer Associates.
30. Hass B., Downes M., Griffin C. (2002). "Persistence of four Heterorhabditis spp. isolates in soil: role of lipid reserves". Journal of Nematology Vol 34, 151-158.
31. Hominick W.M. (2002). "Biogeography". In: Gaugler R. (Ed.). Entomopathogenic nematology. Wallingford, UK, CAB International, pp.  115-143. [Crossref]
32. Honda Y., Honda S. (1999). "The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans". FASEB Journal Vol 13, 1385-1393.
33. Johnigk S.A., Ehlers R.-U. (1999a). "Juvenile development and life cycle of Heterorhabditis bacteriophora and H. indica (Nematoda: Heterorhabditidae)". Nematology Vol 1, 251-260. DOI: 10.1163/156854199508234 [Crossref]
34. Johnigk S.A., Ehlers R.-U. (1999b). "Endotokia matricida in hermaphrodites of Heterorhabditis spp. and the effect of the food supply". Nematology Vol 1, 717-726. DOI: 10.1163/156854199508748 [Crossref]
35. Johnigk S.A., Hollmer S., Strauch O., Wyss U., Ehlers R.-U. (2002). "Heritability of the liquid culture mass production potential of the entomopathogenic nematode Heterorhabditis bacteriophora". Biocontrol Science and Technology Vol 12, 267-276. DOI: 10.1080/09583150120124504 [Crossref]
36. Johnson T.E., Wood W.B. (1982). "Genetic analysis of life-span in Caenorhabditis elegans". Proceedings of the National Academy of Sciences of the United States of America Vol 79, 6603-6607. [Crossref]
37. Johnson T.E., de Castro E., de Castro S.H., Cypser J.R., Henderson S., Tedesco P.M. (2001). "Relationship between increased longevity and stress resistance as assessed through gerontogene mutations in Caenorhabditis elegans". Experimental Gerontology Vol 36, 1609-1617. [Crossref]
38. Johnson T.E., Henderson S., Murakami S., de Castro E., de Castro S.H., Cypser J., Rikke B., Tedesco P., Link C. (2002). "Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease". Journal of Inherited Metabolic Disease Vol 25, 197-206. DOI: 10.1023/A:1015677828407 [Crossref]
39. Jung K. (1996). "Storage of entomopathogenic nematodes of the genus Heterorhabditis at two temperatures. Effect on infectivity, energy reserve and number of bacteria". IOBC/WPRS Bulletin Vol 19, 103-106.
40. Knoefler D., Thamsen M., Koniczek M., Niemuth N.J., Diederich A.K., Jakob U. (2012). "Quantitative in vivo redox sensors uncover oxidative stress as an early event in life". Molecular Cell Vol 47, 767-776. DOI: 10.1016/j.molcel.2012.06.016 [Crossref]
41. Kumsta C., Thamsen M., Jakob U. (2011). "Effects of oxidative stress on behavior, physiology, and the redox thiol proteome of Caenorhabditis elegans". Antioxidants & Redox Signaling Vol 14, 1023-1037. DOI: 10.1089/ars.2010.3203 [Crossref]
42. Kurtz B., Toepfer S., Ehlers R.-U., Kuhlmann U. (2007). "Assessment of establishment and persistence of entomopathogenic nematodes for biological control of western corn rootworm". Journal of Applied Entomology Vol 131, 420-425. DOI: 10.1111/j.1439-0418.2007.01202.x [Crossref]
43. Larsen P.L. (1993). "Aging and resistance to oxidative damage in Caenorhabditis elegans". Proceedings of the National Academy of Sciencesof the United States of America Vol 90, 8905-8909. [Crossref]
44. Lee D.L., Atkinson H.J. (1976). Physiology of nematodes. London, UK, Macmillan. [Crossref]
45. Lewis E., Selvan S., Campbell J., Gaugler R. (1995). "Changes in foraging behaviour during the infective stage of entomopathogenic nematodes". Parasitology Vol 110, 583-590. DOI: 10.1017/S0031182000065306 [Crossref]
46. Menti H., Patel M.N., Wright D.J., Perry R.N. (2003). "Lipid utilisation during storage of the entomopathogenic nematodes Steinernema feltiae and Heterorhabditis megidis from Greece and the UK". Nematology Vol 5, 31-37. DOI: 10.1163/156854102765216669 [Crossref]
47. Mukuka J., Strauch O., Waeyenberge L., Viaene N., Moens M., Ehlers R.-U. (2010a). "Heat tolerance among different strains of the entomopathogenic nematode Heterorhabditis bacteriophora". BioControl Vol 55, 423-434. DOI: 10.1007/s10526-009-9255-4 [Crossref]
48. Mukuka J., Strauch O., Ehlers R.-U. (2010b). "Variability in desiccation tolerance among different strains of the entomopathogenic nematode Heterorhabditis bacteriophora". Nematology Vol 12, 711-720. DOI: 10.1163/138855409X12607871174454 [Crossref]
49. Muñoz M.J., Riddle D.L. (2003). "Positive selection of Caenorhabditis elegans mutants with increased stress resistance and longevity". Genetics Vol 163, 171-180.
50. Murakami S., Johnson T.E. (1996). "A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans". Genetics Vol 143, 1207-1218.
51. Murphy C.T., McCarroll S.A., Bargmann C.I., Fraser A., Kamath R.S., Ahringer J., Li H., Kenyon C. (2003). "Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans". Nature Vol 424, 277-283. DOI: 10.1038/nature01789 [Crossref]
52. Muschiol D., Traunspurger W. (2007). "Life cycle and calculation of the intrinsic rate of natural increase of two bacterivorous nematodes, Panagrolaimus sp. and Poikilolaimus sp. from chemoautotrophic Movile Cave, Romania". Nematology Vol 9, 271-284. DOI: 10.1163/156854107780739117 [Crossref]
53. Nimkingrat P., Khanam S., Strauch O., Ehlers R.-U. (2013). "Hybridisation and selective breeding for improvement of low temperature activity of the entomopathogenic nematode Steinernema feltiae". BioControl Vol 58, 417-426. DOI: 10.1080/09583157.2012.758238 [Crossref]
54. Olahova M., Taylor S.R., Khazaipoul S., Wang J., Morgan B.A., Matsumoto K., Blackwell T.K., Veal E.A. (2008). "A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance". Proceedings of the National Academy of Sciences of the United States of America Vol 105, 19839-19844. DOI: 10.1073/pnas.0805507105 [Crossref]
55. Patel M.N., Stolinski M., Wright D.J. (1997). "Neutral lipids and the assessment of infectivity in entomopathogenic nematodes: observations on four Steinernema species". Parasitology Vol 114, 489-496. [Crossref]
56. Petriv I., Rachubinski R.A. (2004). "Lack of peroxisomal catalase causes a progeric phenotype in Caenorhabditis elegans". Journal of Biological Chemistry Vol 279, 19996-20001. DOI: 10.1074/jbc.M400207200 [Crossref]
57. Pilz C., Toepfer S., Knuth P., Strimitzer T., Heimbach U., Grabenweger G. (2014). "Persistence of the entomoparasitic nematode Heterorhabditis bacteriophora in maize fields". Journal of Applied Entomology Vol 138, 202-212. DOI: 10.1111/j.1439-0418.2012.01743.x [Crossref]
58. Price G.R. (1972). "Fisher’s ‘fundamental theorem’ made clear". Annals of Human Genetics Vol 36, 129-140. DOI: 10.1111/j.1469-1809.1972.tb00764.x [Crossref]
59. Price T., Schluter D. (1991). "On the low heritability of life-history traits". Evolution Vol 45, 853-861. DOI: 10.1111/j.1558-5646.1991.tb04354.x [Crossref]
60. Reynolds R.M., Phillips P.C. (2013). "Natural variation for lifespan and stress response in the nematode Caenorhabditis remanei". PLoS ONE Vol 8, e58212. DOI: 10.1371/journal.pone.0058212
61. Rhee S.G., Yang K.S., Kang S.W., Woo H.A., Chang T.S. (2005). "Controlled elimination of intracellular H2O2: regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification". Antioxidants & Redox Signaling Vol 7, 619-626. DOI: 10.1089/ars.2005.7.619 [Crossref]
62. Selvan S., Gaugler R., Lewis E.E. (1993). "Biochemical energy reserves of entomopathogenic nematodes". Journal of Parasitology Vol 79, 167-172. DOI: 10.2307/3283503 [Crossref]
63. Ślesak I., Libik M., Karpinska B., Karpinski S., Miszalski Z. (2007). "The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses". Acta Biochimica Polonica – English Edition Vol 54, 39-50.
64. Strauch O., Niemann I., Neumann A., Schmidt A., Peters A., Ehlers R.-U. (2000). "Storage and formulation of the entomopathogenic nematodes Heterorhabditis indica and H. bacteriophora". BioControl Vol 45, 483-500. DOI: 10.1023/A:1026528727365 [Crossref]
65. Strauch O., Oestergaard J., Hollmer S., Ehlers R.-U. (2004). "Genetic improvement of the desiccation tolerance of the entomopathogenic nematode Heterorhabditis bacteriophora through selective breeding". BioControl Vol 31, 218-226. DOI: 10.1016/j.biocontrol.2004.03.009
66. Susurluk A., Ehlers R.-U. (2008). "Field persistence of the entomopathogenic nematode Heterorhabditis bacteriophora in different crops". BioControl Vol 53, 627-641. DOI: 10.1007/s10526-007-9104-2 [Crossref]
67. Thamsen M. (2011). The role of oxidative stress in C. elegans aging. Ph.D. Thesis, Johannes Gutenberg-University Mainz, Germany.
68. Toepfer S., Burger R., Ehlers R.-U., Peters A., Kuhlmann U. (2010). "Controlling Western Corn Rootworm larvae with entomopathogenic nematodes: effect of application techniques on plant-scale efficacy". Journal of Applied Entomology Vol 134, 467-480. DOI: 10.1111/j.1439-0418.2009.01469.x [Crossref]
69. Wright S. (1931). "Evolution in Mendelian populations". Genetics Vol 16, 97-159.
70. Yanase S., Yasuda K., Ishii N. (2002). "Adaptive responses to oxidative damage in three mutants of Caenorhabditis elegans (age-1, mev-1 and daf-16) that affect life span". Mechanisms of Ageing and Development Vol 123, 1579-1587. DOI: 10.1016/S0047-6374(02)00093-3 [Crossref]

Article metrics loading...



Can't access your account?
  • Tools

  • Add to Favorites
  • Printable version
  • Email this page
  • Subscribe to ToC alert
  • Get permissions
  • Recommend to your library

    You must fill out fields marked with: *

    Librarian details
    Your details
    Why are you recommending this title?
    Select reason:
    Nematology — Recommend this title to your library
  • Export citations
  • Key

  • Full access
  • Open Access
  • Partial/No accessInformation