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Activation of hatching in diapaused and quiescent Globodera pallida

Published online by Cambridge University Press:  20 December 2012

JUAN E. PALOMARES-RIUS ,
JOHN T. JONES ,
PETER J. COCK ,
PABLO CASTILLO  and
VIVIAN C. BLOK
JUAN E. PALOMARES-RIUS*
Affiliation:
Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
JOHN T. JONES
Affiliation:
Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
PETER J. COCK
Affiliation:
Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
PABLO CASTILLO
Affiliation:
Department of Plant Protection, Institute for Sustainable Agriculture (IAS-CSIC), Cordoba, 14080, Cordoba, Campus de Excelencia Internacional Agroalimentario, ceiA3, Spain
VIVIAN C. BLOK
Affiliation:
Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
*
*Corresponding author: Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK. E-mail: [email protected]
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Summary

The potato cyst nematodes (PCN) Globodera pallida and G. rostochiensis are major pests of potatoes. The G. pallida (and G. rostochiensis) life cycle includes both diapause and quiescent stages. Nematodes in dormancy (diapause or quiescent) are adapted for long-term survival and are more resistant to nematicides. This study analysed the mechanisms underlying diapause and quiescence. The effects of several compounds (8Br-cGMP, oxotremorine and atropine) on the activation of hatching were studied. The measurements of some morphometric parameters in diapaused and quiescent eggs after exposure to PRD revealed differences in dorsal gland length, subventral gland length and dorsal gland nucleolus. In addition, the expression of 2 effectors (IVg9 and cellulase) was not induced in diapaused eggs in water or PRD, while expression was slightly induced in quiescent eggs. Finally, we performed a comparative study to identify orthologues of C. elegans diapause related genes in plant-parasitic nematodes (G. pallida, Meloidogyne incognita, M. hapla and Bursaphelenchus xylophilus). This analysis suggested that it was not possible to identify G. pallida orthologues of the majority of C. elegans genes involved in the control of dauer formation. All these data suggest that G. pallida may use different mechanisms to C. elegans in regulating the survival stage.

Keywords

hatchingcGMPmuscarinic pathwaypotato cyst nematodesroot diffusate
Type
Research Article
Information
Parasitology , Volume 140 , Issue 4 , April 2013 , pp. 445 - 454
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Altschul, S. F, Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool . Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Atkinson, H. J., Taylor, J. D. and Fowler, M. (1987). Changes in the second stage juveniles of Globodera rostochiensis prior to hatching in response to potato root diffusate. Annals of Applied Biology 110, 105–114.CrossRefGoogle Scholar
Banyer, R. J. and Fisher, J. M. (1971). Seasonal variation in hatching of eggs of Heterodera avenae. Nematologica 17, 225–236.CrossRefGoogle Scholar
Bird, A. F. and Buttrose, M. S. (1974). Ultrastructural changes in the nematode Anguina tritici associated with anhydrobiosis. Journal of Ultrastructural Research 48, 177–189.CrossRefGoogle ScholarPubMed
Blair, L., Perry, R. N., Oparka, K. and Jones, J. (1999). Activation of transcription during the hatching process of the potato cyst nematode Globodera rostochiensis. Nematology 1, 103–111.CrossRefGoogle Scholar
Brand, A. and Hawdon, J. M. (2004). Phosphoinositide-3-OH-kinase inhibitor LY294002 prevents activation of Ancylostoma caninum and Ancylostoma ceylanicum third-stage infective larvae. International Journal for Parasitology 34, 909–914.CrossRefGoogle ScholarPubMed
Campbell, C. L. and Madden, L. (1990). Introduction to Plant Disease Epidemiology. John Wiley & Sons, New York, USA.Google Scholar
Clarke, A. J., Perry, R. N. and Hennessy, J. (1978). Osmotic stress and the hatching of Globodera rostochiensis. Nematologica 24, 384–392.Google Scholar
Ellenby, C. and Perry, R. N. (1976). The influence of the hatching factor on the water uptake of the second stage larva of the potato cyst nematode Heterodera rostochiensis. Journal of Experimental Biology 64, 141–147.CrossRefGoogle Scholar
Elling, A. A., Mitreva, M., Recknor, J., Gai, X., Martin, J., Maier, T. R., McDermott, J. P., Hewezi, T., McK Bird, D., Davis, E. L., Hussey, R. S., Nettleton, D., McCarter, J. P. and Baum, T. J. (2007). Divergent evolution of arrested development in the dauer stage of Caenorhabditis elegans and the infective stage of Heterodera glycines. Genome Biology 8, R211. doi: 10.1186/gb-2007–8–10-r211.CrossRefGoogle ScholarPubMed
Fielenbach, N. and Antebi, A. (2008). C. elegans dauer formation and the molecular basis of plasticity. Genes and Development 22, 2149–2165 doi:10.1101/gad.1701508.CrossRefGoogle ScholarPubMed
Goecks, J., Nekrutenko, A., Taylor, J. and The Galaxy Team. (2010). Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biology 25,11: R86.CrossRefGoogle Scholar
Gomez, K. A. and Gomez, A. A. (1984). Statistical Procedures for Agricultural Research, 2nd Edn. John Wiley & Sons. New York, USA.Google Scholar
Hawdon, J. M. and Datu, B. (2003). The second messenger cyclic GMP mediates activation in Ancylostoma caninum infective larvae. International Journal for Parasitology 33, 787–793.CrossRefGoogle ScholarPubMed
Hawdon, J. M. and Schad, G. A. (1993). Ancylostoma caninum: Glutathione stimulates feeding in third stage larvae by a sulfhydryl independent mechanism. Experimental Parasitology 77, 489–491.CrossRefGoogle ScholarPubMed
Holterman, M., van der Wurff, A., van den Elsen, S., van Megen, H., Bongers, T., Holovachov, O., Bakker, J. and Helder, J. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23, 1792–1800.CrossRefGoogle ScholarPubMed
Hominick, W. M., Forrest, J. M. S. and Evans, A. A. F. (1985). Diapause in Globodera rostochiensis and variability in hatching trials. Nematologica 31, 159–170.Google Scholar
Hu, P. J. (2007). Dauer. In WormBook (ed. Riddle, L. R.), doi/10.1895/wormbook.1.144.1, http://www.wormbook.org.Google Scholar
Huang, S. C., Chan, D. T. Y., Smyth, D. J., Ball, G., Gounaris, K. and Selkirk, M. E. (2010). Activation of Nippostrongylus brasiliensis infective larvae is regulated by a pathway distinct from the hookworm Ancylostoma caninum. International Journal for Parasitology 40, 1619–1628.CrossRefGoogle ScholarPubMed
Jiménez-Pérez, N.Crozzoli, R. and Greco, N. (2009). Life-cycle and emergence of second stage juveniles from cysts of Globodera rostochiensis in Venezuela. Nematologia Mediterranea 37: 155–160.Google Scholar
Jones, J. T., Kumar, A., Pylypenko, L. A., Thirugnanasambandam, A., Castelli, L., Chapman, S., Cock, P. J., Grenier, E., Lilley, C. J., Phillips, M. S. and Blok, V. C. (2009). Identification and functional characterisation of effectors in Expressed Sequence Tags from various life cycle stages of the potato cyst nematode Globodera pallida. Molecular Plant Pathology 10, 815–828.CrossRefGoogle ScholarPubMed
Kikuchi, T., Cotton, J. A., Dalzell, J. J., Hasegawa, K., Kanzaki, N., McVeigh, P., Takanashi, T., Tsai, I. J., Assefa, S. A., Cock, P. J. A., Dan Otto, T., Hunt, M., Reid, A. J., Sanchez-Flores, A., Tsuchihara, K., Yokoi, T., Larsson, M. C., Miwa, J., Maule, A. G., Sahashi, N., Jones, J. T. and Berriman, M. (2011). Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathogens 7, e1002219.CrossRefGoogle ScholarPubMed
Langeslag, M., Mugniery, D. and Fayet, G. (1982). Développement embryonnaire de Globodera rostochiensis et G. pallida en fonction de la température, en conditions contrôlées et naturelles. Revue Nématologie 5, 103–109.Google Scholar
Miller, R. E. (1981). Pancreatic neuroendocrinology: peripheral neural mechanisms in the regulation of the Islets of Langerhans. Endocrine Reviews 2, 471–494.CrossRefGoogle ScholarPubMed
Muhammad, Z. (1994). Diapause in the nematode G. pallida. European Journal of Plant Pathology 100, 413–423.CrossRefGoogle Scholar
Opperman, C. H., Bird, D. M., Williamson, V. M., Rokhsar, D. S., Burke, M., Cohn, J., Cromer, J., Diener, S., Gajan, J., Graham, S., Houfek, T. D., Liu, Q., Mitros, T., Schaff, J., Schaffer, R., Scholl, E., Sosinski, B. R., Thomas, V. P. and Windham, E. (2008). Sequence and genetic map of Meloidogyne hapla: A compact nematode genome fro plant parasitism. Proceedings of the National Academy of Sciences, USA 105, 14802–14807.CrossRefGoogle Scholar
Perry, R. N. (1989). Dormancy and hatching of nematode eggs. Parasitology Today 5, 377–383.CrossRefGoogle ScholarPubMed
Perry, R. N. (1998). The physiology and sensory perception of potato cyst nematodes, Globodera species. In Potato Cyst Nematodes: Biology, Distribution and Control (ed. Marks, R. J. and Brodie, B. B.), pp. 27–49. CABI Publishing, Wallingford, UK.Google Scholar
Perry, R. N. and Beane, J. (1982). The effect of brief exposure to potato root diffusate on the hatching of Globodera rostochiensis. Revue de Nematologie 5, 221–224.Google Scholar
Perrry, R. N. and Gaur, H. S. (1996). Host plant influences on the hatching of cyst nematodes. Fundamental and Applied Nematology 19, 505–510.Google Scholar
Perry, R. N. and Moens (2011). Survival of parasitic nematodes outside the host. In Molecular and Physiological Basis of Nematode Survival (ed. Perry, R. N. and Wharton, D. A.), pp. 1–27. CABI Publishing, Wallingford, UK.CrossRefGoogle Scholar
Perry, R. N., Wharton, D. A. and Clarke, A. J. (1982). The structure of the egg-shell of Globodera rostochiensis (Nematoda: Tylenchida). International Journal for Parasitology 12, 481–485.CrossRefGoogle Scholar
Pylypenko, L. A., Uehara, T., Phillips, M. S., Sigareva, D. D. and Blok, V. C. (2005). Identification of Globodera rostochiensis and G. pallida in the Ukraine by PCR. European Journal of Plant Pathology 111, 39–46.CrossRefGoogle Scholar
Rozen, S. and Skaletsky, H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology (ed. Krawetz, S. and Misener, S.), pp. 365–368. Humana Press, Totowa, NJ, USA.Google Scholar
Spears, J. F. (1968). The golden nematode handbook: survey, laboratory, control, and quarantine procedures. USDA Agriculture Handbook. No. 353.Google Scholar
Tissembaum, H. A., Hawdon, J., Perregaux, M., Hotez, P., Guarente, L. and Ruvkun, G. (2000). A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. Proceedings of the National Academy of Sciences, USA 97, 460–465.CrossRefGoogle Scholar