Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T14:52:42.726Z Has data issue: false hasContentIssue false
  • English
  • Français

Cross-stress tolerance and expression of stress-related proteins in osmotically desiccated entomopathogenic Steinernema feltiae IS-6

Published online by Cambridge University Press:  06 July 2005

S. CHEN ,
N. GOLLOP  and
I. GLAZER
S. CHEN
Affiliation:
Department of Nematology, ARO, The Volcani Center, Bet Dagan 50250, Israel
N. GOLLOP
Affiliation:
Department of Food Science, ARO, The Volcani Center, Bet Dagan 50250, Israel
I. GLAZER
Affiliation:
Department of Nematology, ARO, The Volcani Center, Bet Dagan 50250, Israel
Get access Rights & Permissions [Opens in a new window]

Abstract

Infective juveniles (IJs) of the entomopathogenic nematode (EPN) Steinernema feltiae IS-6 can survive exposure to 24% glycerol solution by entering an osmotically desiccated state. Exposure of osmotically desiccated nematodes to extreme temperature assays (40 °C for 10 h and −20 °C for 360 h) resulted in gradual reduction in survival, whereas non-desiccated IJs died within a short exposure to the assay conditions. Through SDS-PAGE, a stress-related protein UNC-87 was found in osmotically desiccated IJs exposed to 40 °C for 3, 6, and 8 h, whose survival rates were 98·9±1·43, 78·5±5·87 and 20·9±4·93%, respectively. The protein was not found in IJs following exposure of osmotically desiccated individuals to 40 °C for 10 h, in which none of the IJs survived. After exposure to −20 °C for 360 h, the survival of osmotically desiccated EPNs with a weak band of UNC-87 was 13·0±3·32%. To identify other responsive proteins that are required for osmotic stress, we used 2-dimensional electrophoresis to analyse the proteins in osmotically desiccated EPNs. The results revealed that 10 novel protein spots and 10 up-regulated protein spots in osmotically desiccated IJs were detected by digital image analysis. Mass spectrometry analysis of 7 significant spots indicated that osmotic stress in desiccated IJs was associated with the induction of actin, Proteasome regulatory particle (ATPase-like), GroEL chaperonin, GroES co-chaperonin and transposase family member. It seems to show actin, UNC-87 and Proteasome regulatory particle may play distinct roles in specific aspects of organization of macromolecular structures under desiccation stress. GroEL and GroES are members of the Hsp60 family of chaperons.

Keywords

Sternernema feltiae IS-6osmotic desiccationstress tolerance2-dimensional electrophoresisstress-related proteins
Type
Research Article
Information
Parasitology , Volume 131 , Issue 5 , November 2005 , pp. 695 - 703
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abu-Hatab, M., Gaugler, R. and Ehlers, R. U. ( 1998). Influence of culture method on Steinernema glaseri lipids. Journal of Parasitology 84, 215–221.CrossRefGoogle Scholar
Beer, I., Barnea, E., Ziv, T. and Admon, A. ( 2004). Improving large-scale proteomics by clustering of mass spectrometry data. Proteomics 4, 950–960.CrossRefGoogle Scholar
Blum, H., Beier, H. and Gross, H. J. ( 1987). Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8, 93–99.CrossRefGoogle Scholar
Browne, J. A., Dolan, K. M., Tyson, T., Goyal, K., Tunnacliffe, A. and Burnell, A. M. ( 2004). Dehydration-Specific Induction of Hydrophilic Protein Genes in the Anhydrobiotic Nematode Aphelenchus avenae. Eukaryotic Cell 3, 966–975.CrossRefGoogle Scholar
Browne, J., Tunnacliffe, A. and Burnell, A. ( 2002). Anhydrobiosis: plant desiccation gene found in a nematode. Nature 416, 38.CrossRefGoogle Scholar
Chen, S. and Glazer I. ( 2004). Effect of rapid and gradual Increase of osmotic stress on survival of entomopathogenic nematodes. Phytoparasitica 32, 486–497.CrossRefGoogle Scholar
Chen, S. and Glazer, I. ( 2005). A novel method for long-term storage of the entomopathogenic nematode Steinernema feltiae at room temperature. Biological Control 32, 104–110.CrossRefGoogle Scholar
Chen, S., Yang, H. and Jiang, S. ( 2001). Morphology and oxygen consumption of entomopathogenic nematode Steinernema carpocapsae BJ in anhydrobiosis. Acta Entomologica Sinica 44, 62–66.Google Scholar
Chen, S., Yang, H. and Jiang, S. ( 2000). Studies on the biochemical characters of Steinernema carpocapsae BJ in anhydrobiosis. Acta Parasitologica et Medica Entomologica Sinica 7, 30–34.Google Scholar
Close, T. J., Kortt, A. A. and Chandler, P. M. ( 1989). A c-DNA based comparison of dehydration induced proteins (dehydrins) in barley and corn. Plant Molecular Biology 13, 95–108.CrossRefGoogle Scholar
Crowe, J. H. and Crowe, L. M. ( 1992). Preservation of liposomes by freeze drying. In Liposome Technology ( ed. Gregoriadis, G.), pp. 229–252. CRC Press, Boca Raton, FL, USA.
Davy, A., Bello, P., Thierry-Mieg, N., Vaglio, P., Hitti, J., Doucette-Stamm, L., Thierry-Mieg, D., Reboul, J., Boulton, S., Walhout, A. J. M., Coux, O. and Vidal, M. ( 2001). A protein-protein interaction map of the Caenorhabditis elegans 26S proteasome. EMBO Reports 2, 821–828.CrossRefGoogle Scholar
Demeure, Y. and Freckman, D. W. ( 1981). Recent advances in the study of anhydrobiotic nematodes. In Plant Parasitic Nematodes ( ed. Zuckerman, B. M. and Rohde, R. A.), pp. 205–226. Academic Press, New York.CrossRef
Dhaubhadel, S., Browning, K. S., Gallie, D. R. and Krishna, P. ( 2002). Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. The Plant Journal 29, 681–691.CrossRefGoogle Scholar
Dowds, B. C. A. and Peters, A. ( 2002). Virulence mechanisms. In Entomopathogenic Nematology ( ed. Gaugler. R.), pp. 79–98. CABI Publishing, Wallingford, UK.CrossRef
Dunphy, G. B. and Thurston, G. S. ( 1990). Insect inmunity. In Entomopathogenic Nematodes in Biological Control ( ed. Gaugler, R. and Kaya, H. K.), pp. 301–323. CRC Press, Boca Raton, FL, USA.
Frost, S., Dowds, B., Boemare, N. and Stackebrandt, E. ( 1997). Xenorhabdus and Photorhabdus spp.: Bugs that kill bugs. Annual Review of Microbiology 51, 47–72.Google Scholar
Gabai, V. L. and Sherman, M. Y. ( 2002). Invited review: interplay between molecular chaperones and signaling pathways in survival of heat shock. Journal of Applied Physiology 92, 1743–1748.CrossRefGoogle Scholar
Gal, T. Z., Glazer, I. and Koltai, H. ( 2003). Differential gene expression during desiccation stress in Insect-killing nematode Steinernema feltiae IS-6. Journal of Parasitology 89, 761–766.CrossRefGoogle Scholar
Gaugler, R. and Han, R. ( 2002). Production Technology. In Entomopathogenic Nematology ( ed. Gaugler. R.), pp. 289–310. CABI Publishing, Wallingford, UK.CrossRef
Georgis, R. and Manweiler, S. A. ( 1994). Entomopathogenic nematodes: a developing biological control technology. Agricultural Zoology Reviews 6, 63–94.Google Scholar
Gimona, M. and Mital, R. ( 1998). The single CH domain of calponin is neither sufficient nor necessary for F-actin binding. Journal Cell Science 111, 1813–1821.Google Scholar
Glazer, I. and Salame, L. ( 2000). Osmotic survival of the entomopathogenic nematode Steinernema carpocapsae. Biological Control 18, 251–257.CrossRefGoogle Scholar
Glazer, I. ( 2002). Survival biology. In Entomopathogenic Nematology ( ed. Gaugler. R.), pp. 169–187. CABI Publishing, Wallingford, UK.CrossRef
Gonczy, P., Echeverri, C., Oegema, K., Coulson, A., Jones, S. J. M., Copley, R. R., Duperon, J., Oegema, J., Brehm, M., Cassin, E., Hannak, E., Kirkham, M., Pichler, S., Flohrs, K., Goessen, A., Leidel, S., Alleaume, A. M., Martin, C., Özlü, N., Bork, P. and Hyman, A. A. ( 2000). Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature, London 408, 331–336.Google Scholar
Grewal, P. S. ( 2002). Formulation and application technology. In Entomopathogenic Nematology ( ed. Gaugler, R.), pp. 265–287. CABI Publishing, Wallingford, UK.CrossRef
Grewal, P. S. and Jagdale, G. B. ( 2002). Enhanced trehalose accumulation and desiccation survival of entomopathogenic nematodes through cold preacclimation. Biocontrol Science and Technology 12, 533–545.CrossRefGoogle Scholar
Grewal, P. S. ( 2000). Anhydrobiotic potential and long-term storage of entomopathogenic nematodes (Rhabditida: Steinernematidae). International Journal for Parasitology 30, 995–1000.CrossRefGoogle Scholar
Guchte, M. V. D., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S. D. and Maguin, E. ( 2002). Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 82, 187–216.CrossRefGoogle Scholar
Hennequin, C., Collignon, A. and Karjalainen, T. ( 2001). Analysis of expression of GroEL (Hsp60) of Clostridium difficile in response to stress. Microbial Pathogenesis 31, 255–260.CrossRefGoogle Scholar
Hennequin, C., Porcheray, F., Waligora-Dupriet, A. J., Collignon, A., Barc, M. C., Bourlioux, P. and Karjalainen, T. ( 2001). GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology 147, 87–96.CrossRefGoogle Scholar
Hill, R. D., Hladun, L. S., Scherer, S. and Potts, M. ( 1994). Water stress proteins of Nostoc commune (Cyanobacteria) are secreted with UV-A/B-absorbing pigments and associated with 1,4-β-D-Xylanxylanohydrolase activity. Journal of Biological Chemistry 269, 7726–7734.Google Scholar
Jagdale, G. B. and Grewal, P. S. ( 2003). Acclimation of entomopathogenic nematodes to novel temperatures: trehalose accumulation and the acquisition of thermotolerance. International Journal for Parasitology 33, 145–152.CrossRefGoogle Scholar
Kaya, H. K. and Gaugler, R. ( 1993). Entomopathogenic nematodes. Annual Review of Entomology 38, 181–206.CrossRefGoogle Scholar
Kaya, H. K. and Stock, S. P. ( 1997). Techniques in insect nematology. In Manual of Techniques in Insect Pathology ( ed. Lacey, L.), pp. 281–324. Academic Press, San Diego, CA, USA.CrossRef
Kilstrup, M., Jacobsen, S., Hammer, K. and Vogensen, F. K. ( 1997). Induction of heat shock proteins Dnak, GroEL, and GroES by salt stress in Lactococcus lactis. Applied and Environmental Microbiology 63, 1826–1837.Google Scholar
Kim, S. T., Cho, K. S., Jang, Y. S. and Kang, K. Y. ( 2001). Two-dimensional electrophoretic analysis of rice proteins by polyethylene glycol fractionation for protein arrays. Electrophoresis 22, 2103–2109.3.0.CO;2-W>CrossRefGoogle Scholar
Kranewitter, W. J., Ylanne, J. and Gimona M. ( 2001). UNC-87 Is an Actin-bundling Protein. The Journal of Biological Chemistry 276, 6306–6312.CrossRefGoogle Scholar
Laemmli, U. K. ( 1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680–685.CrossRefGoogle Scholar
Leinweber, B., Tang, J. X., Stafford, W. F., III and Chalovich, J. M. ( 1999). Calponin interaction with (alpha-actinin-actin): Evidence for a structural role for calponin. Biophysical Journal 77, 3208–3217.CrossRefGoogle Scholar
Lodish, H., Berk, A., Zipursky, S. L., Matsudaira, P., Baltimore, D. and Darnell, J. ( 2000). Cell motility and shape II: microtubules and intermediate filaments. In Molecular Cell Biology, pp. 751–794. New York.
Pena, P. and Garesse, R. ( 1993). The beta subunit of the Drosophila melanogaster ATP synthase: cDNA cloning, amino acid analysis and identification of the protein in adult flies. Biochemical and Biophysical Research Communications 195, 785–791.CrossRefGoogle Scholar
Perry, R. N. ( 1998). Survival of terrestrial organisms. In Survival of Entomopathogenic Nematodes (ed. Glazer, I., Richardson, P., Boemare, N. and Coudert, F.), pp. 7–13. European Commission Press, UK.
Ritossa, F. ( 1962). A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18, 571–573.CrossRefGoogle Scholar
Ritossa, F. ( 1996). Discovery of the heat shock response. Cell Stress Chaperones 1, 97–98.2.3.CO;2>CrossRefGoogle Scholar
SAS ( 1988). SAS/STAT User's Guide, release 6.12. SAS Institute Inc., Cary, NC, USA.
Solomon, A., Salomon, R., Paperna, I. and Glazer, I. ( 2000). Desiccation stress of entomopathogenic nematodes induces the accumulation of a novel heat-stable protein. Parasitology 121, 409–416.CrossRefGoogle Scholar
Solomon, A., Paperna, I. and Glazer, I. ( 1999). Desiccation survival of the entomopathogenic nematode Steinernema feltiae: Induction of anhydrobiosis. Nematology 1, 61–68.CrossRefGoogle Scholar
Tang, J. X., Szymanki, P. T., Janmey, P. A. and Tao, T. ( 1997). Electrostatic effects of smooth muscle calponin on actin assembly. European Journal of Biochemistry 247, 432–440.CrossRefGoogle Scholar
Thomashow, M. F. ( 1998). Role of cold-responsive genes in plant freezing tolerance. Plant Physiology 118, 1–7.CrossRefGoogle Scholar
Tissieres, A., Mitchell, H. K. and Tracy, U. M. ( 1974). Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. Journal of Molecular Biology 85, 389–398.CrossRefGoogle Scholar
Womersley, C. Z., Wharton, D. A. and Higa, L. M. ( 1998). Survival biology. In The Physiology and Biochemistry of Free-Living and Plant-Parasitic Nematodes ( ed. Perry, R. N. and Wright, D. J.), pp. 271–302. CABI Publishing, London.
Zugel, U. and Kaufmann, S. H. ( 1999). Role of heat shock proteins in protection from and pathogenesis of infectious diseases. Clinical Microbiology Reviews 12, 19–39.Google Scholar