Abstract
Quality of biological control products based on entomopathogenic nematodes can be severely damaged due to exposure to high temperature surpassing 40°C. The study screened 36 natural populations and 18 hybrid or inbred strains of Heterorhabditis bacteriophora for their response to high temperature. Nematodes were tested with or without prior adaptation to heat at 35°C for 3 h. Five strains of H. indica and one of H. megidis were also included. Molecular identification using nuclear ribosomal DNA sequences confirmed the designation to the three Heterorhabditis spp. The mean tolerated temperature ranged from 33.3°C to 40.1°C for non-adapted and from 34.8°C to 39.2°C for adapted strain populations. H. indica was the most tolerant, followed by H. bacteriophora and H. megidis. No correlation was recorded between tolerance assessed with and without adaptation to heat, implying that different genes are involved. Correlation between heat tolerance and mean annual temperature at place of origin of the strains was weak. A high variability in tolerance among strains and the relatively high heritability (h² = 0.68) for the adapted heat tolerance recorded for H. bacteriophora provide an excellent foundation for future selective breeding with the objective to enhance heat tolerance of H. bacteriophora.
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References
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 of invertebrate pathology. Noordwijkerhout, p 7
Ciche T (2007) The biology and genome of Heterorhabditis bacteriophora. In: WormBook (ed) The C. elegans research community. http://www.wormbook.org/chapters/www_genomesHbacteriophora/genomesHbacteriophora.html
Ciche TA, Darby C, Ehlers R-U, Forst S, Goodrich-Blair H (2006) Dangerous liaisons: the symbiosis of entomopathogenic nematodes and bacteria. Biol Control 38:22–46
Curran J, Gilbert C, Butler K (1992) Routine cryopreservation of Steinernema and Heterorhabditis spp. J Nematol 24:1–3
Dowds BCA, Peters A (2002) Virulence mechanisms. In: Gaugler R (ed) Entomopathogenic nematology. CABI Publishing, UK, pp 79–98
Dutky SR, Thompson JV, Cantwell GE (1962) A technique for mass rearing the greater wax moth (Lepidopera: Galleriidae). Proc Ent Soc Wash 64:56–58
Ehlers R-U (2001) Mass production of entomopathogenic nematodes for plant protection. Appl Microbiol Biotechnol 56:623–633
Ehlers R-U (2003) Biocontrol nematodes. In: Hokkanen HMT, Hajek AE (eds) Environmental impacts of microbial insecticides. Kluwer Academic Publishers, The Netherlands, pp 177–220
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 50:699–716
Glazer I (2002) Survival biology. In: Gaugler R (ed) Entomopathogenic nematology. CABI Publishing, UK, pp 169–187
Glazer I, Gaugler R, Segal D (1991) Genetics of the entomopathogenic nematode Heterorhabditis bacteriophora (strain HP88): the diversity of beneficial traits. J Nematol 23:324–333
Grewal PS, Gaugler R, Kaya HK, Wusaty M (1993) Infectivity of the entomopathogenic nematode Steinernema scapterisci (Nematoda: Steinernamatidae). J Invertebr Pathol 62:22–28
Grewal PS, Selvan S, Gaugler R (1994) Thermal adaptation of entomopathogenic nematodes: Niche breadth for infection, establishment and reproduction. J Thermal Biol 19:245–253
Grewal PS, Wang X, Taylor RAJ (2002) Dauer juvenile longevity and stress tolerance in natural populations of entomopathogenic nematodes: is there a relationship? Int J Parasitol 32:717–725
Grewal PS, Ehlers R-U, Shapiro-Ilan DI (2005) Nematodes as biocontrol agents. CABI International, UK
Grewal PS, Bornstein-Forst S, Burnell AM, Glazer I, Jagdale GB (2006) Physiological, genetic, and molecular mechanisms of chemoreception, thermobiosis, and anhydrobiosis in entomopathogenic nematodes. Biol Contr 38:54–65
Griffin CR, Downes MJ (1991) Low temperature activity in Heterorhabditis sp. (Nematoda: Heterorhabditidae). Nematologica 37:83–91
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows95/98/NT. Nucl Acids Symp Ser 41:95–98
Han R, Ehlers R-U (2000) Pathogenicity, development and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. J Invertebr Pathol 75:55–58
Hashmi GS, Hashmi S, Selvan S, Grewal PS, Gaugler R (1997) Polymorphism in heat shock protein gene (hsp70) in entomopathogenic nematodes (Rhabditida). J Therm Biol 22:143–149
Jagdale GB, Grewal PS, Salminen SO (2005) Both heat-shock and cold-shock influence trehalose metabolism in an entomopathogenic nematode. J Parasitol 91:988–994
Johnigk SA, 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 Sci Technol 12:267–276
Joyce SA, Burnell AM, Powers TO (1994) Characterization of Heterorhabditis isolates by PCR amplification of segments of mtDNA and rDNA genes. J Nematol 26:260–270
Koppenhöfer AM (2000) Nematodes. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology. Kluwer Academic Press, The Netherlands, pp 283–301
Kung SP, Gaugler R, Kaya HK (1991) Effects of soil temperature, moisture and relative humidity on entomopathogenic nematode persistence. J Invertebr Pathol 57:242–249
Molyneux AS (1986) Heterorhabditis spp. and Steinernema (=Neoaplectana) spp.: temperature and aspects of behaviour and infectivity. Exp Parasit 62:169–180
Nguyen KB (2007) Methodology, morphology and identification. In: Nguyen KB, Hunt DJ (eds) Entomopathogenic nematodes: systematics, phylogeny and bacterial symbionts. Hunt DJ, Perry RN (Series eds) Nematology monographs and perspectives, Brill NV, The Netherlands, pp 59–119
Nguyen KB, Hunt DJ (2007) Entomopathogenic nematodes: systematics, phylogeny and bacterial symbionts. Hunt DJ, Perry RN (Series eds) Nematology monographs and perspectives, Brill NV, The Netherlands
Selvan S, Grewal PS, Leustek T, Gaugler R (1996) Heat shock enhances thermotolerance of infective juvenile insect-parasitic nematodes Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae). Experientia 52:727–730
Somasekhar N, Grewal PS, Klein MG (2002) Genetic variability in stress tolerance and fitness among natural populations of Steinernema carpocapsae. Biol Control 23:303–310
Strauch O, Niemann I, Neumann A, Schmidt AJ, Peters A, Ehlers R-U (2000) Storage and formulation of the entomopathogenic nematodes Heterorhabditis indica and H. bacteriophora. BioControl 45:483–500
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. Biol Control 31:218–226
Susurluk A, Ehlers R-U (2008) Field persistence of the entomopathogenic nematode Heterorhabditis bacteriophora in different crops. BioControl 53:627–641
Swofford DL (1998) PAUP, phylogenetic analysis using parsimony and other methods. Version 4. Sinauer Associates, Sunderland, MA, p 128
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows inference: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acid Res 24:4876–4882
White F (1927) A method for obtaining infective juveniles from cultures. Science 66:1666–1670
Wright PJ (1992) Cool temperature reproduction of steinernematid and heterorhabditid nematodes. J Invertebr Pathol 60:148–151
Wright DJ, Peters A, Schroer S, Fife JP (2005) Application technology. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI Publishing, UK, pp 91–106
Acknowledgments
Thanks are due to all colleagues, who kindly provided nematode strains and to Berhanu Hunegnaw Kassahun for technical support with the molecular identification. The scholarship to the first author by the German Academic Exchange Service (http://www.daad.de) is highly appreciated.
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Mukuka, J., Strauch, O., Waeyenberge, L. et al. Heat tolerance among different strains of the entomopathogenic nematode Heterorhabditis bacteriophora . BioControl 55, 423–434 (2010). https://doi.org/10.1007/s10526-009-9255-4
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DOI: https://doi.org/10.1007/s10526-009-9255-4