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Parasitism by Cotesia flavipes alters the haemocyte population and phenoloxidase activity of the sugarcane borer, Diatraea saccharalis

Published online by Cambridge University Press:  18 May 2012

A.M.A. Mahmoud ,
E.J. De Luna-Santillana ,
X. Guo  and
Mario A. Rodríguez-Pérez
A.M.A. Mahmoud*
Affiliation:
Zoology Department, Assiut University, 71515 Assiut, Egypt Centro de Biotecnología Genómica (CBG), Instituto Politécnico Nacional (IPN), Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas 88710, México
E.J. De Luna-Santillana
Affiliation:
Centro de Biotecnología Genómica (CBG), Instituto Politécnico Nacional (IPN), Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas 88710, México
X. Guo
Affiliation:
Centro de Biotecnología Genómica (CBG), Instituto Politécnico Nacional (IPN), Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas 88710, México
Mario A. Rodríguez-Pérez
Affiliation:
Centro de Biotecnología Genómica (CBG), Instituto Politécnico Nacional (IPN), Blvd. del Maestro esq. Elías Piña, Col. Narciso Mendoza, Reynosa, Tamaulipas 88710, México
*
1Corresponding author (e-mail: alialimh@yahoo.com).
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Abstract

Parasitism of Diatraea saccharalis (Fabricius) (Lepidoptera: Crambidae) larvae by Cotesia flavipes Cameron (Hymenoptera: Braconidae) or injection of C. flavipes polydnavirus causes numerous alterations in host physiology including developmental arrest, abrogation of host immunity, and biochemical changes in proteins, carbohydrates, glycogen, and lipids. This study focused on changes in haemocyte composition occurring in the cellular immune system of parasitised D. saccharalis larvae. We also analysed the effects of parasitisation by C. flavipes on humoral immunity in terms of phenoloxidase (PO) activity in the host. In nonparasitised D. saccharalis larvae, granular cells represented the main haemocyte type (39%) and plasmatocytes were also present at around 35% among the total haemocytes. The percentages of these two major haemocytes decreased significantly in parasitised larvae after 6 days of parasitoid oviposition and the total haemocyte counts exhibited a significant reduction in parasitised larvae 3 and 6 days following parasitisation. The parasitised larvae also showed a significant decrease in humoral immune capacity as evidenced by reduction of PO activity. Moreover, the plasma had more PO activity than the haemocytes and the parasitised larvae showed less PO activity than the control larvae. This research demonstrates that the parasitism of C. flavipes adversely affects the total haemocyte populations and PO activity of D. saccharalis larvae, which would contribute to host immunosuppression.

Résumé

Le parasitisme des larves de Diatraea saccharalis (Fabricius) (Lepidoptera: Crambidae) par Cotesia flavipes Cameron (Hymenoptera: Braconidae) ou une injection du virus polyADN C. flavipes cause de nombreuses modifications de la physiologie de l'hôte, y compris un arrêt du développement, la suppression de l'immunité de l'hôte, ainsi que des changements biochimiques dans les protéines, les hydrates de carbone, le glycogène et les lipides. Notre étude examine les changements dans la composition des hémocytes qui se produisent dans le système immunitaire cellulaire des larves parasitées de D. saccharalis. Nous analysons aussi les effets du parasitisme par C. flavipes sur l'immunité humorale reflétée par l'activité de la phénoloxydase (PO) de l'hôte. Chez les larves non parasitées de D. saccharalis, les cellules granulaires représentent le type principal (39%) d'hémocytes et les plasmocytes font environ 35% de l'ensemble des hémocytes. Les pourcentages de ces deux principaux hémocytes diminuent significativement chez les larves parasitées 6 jours après la ponte du parasitoïde et les nombres totaux d'hémocytes connaissent une réduction significative chez les larves parasitées 3 et 6 jours après le début du parasitisme. Les larves parasitées montrent aussi une réduction significative de leur capacité immunitaire humorale comme l'indique la diminution de l'activité de la phénoloxydase. De plus, le plasma a une activité de la PO plus importante que les hémocytes et les larves parasitées ont une activité de la PO inférieure à celle des larves témoins. Notre recherche démontre que le parasitisme par C. flavipes affecte négativement la population totale d'hémocytes et l'activité de la PO chez les larves de D. saccharalis, ce qui contribue à l'immunosuppression chez l'hôte.

Type
Original Article
Information
The Canadian Entomologist , Volume 144 , Issue 4 , 03 August 2012 , pp. 599 - 608
Copyright
Copyright © Entomological Society of Canada 2012

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References

Amaya, K., Asgari, S., Jung, R., Hongskula, M., Beckage, N.E. 2005. Parasitization of Manduca sexta by the parasitoid wasp Cotesia congregata induces an impaired host immune response. Journal of Insect Physiology, 51: 505–512.CrossRefGoogle ScholarPubMed
Ashida, M.Brey, P.T. 1995. Role of the integument in insect defense: pro-phenol oxidase cascade in the cuticular matrix. Proceedings of the National Academy of Sciences of the United States of America, 92: 10698–10702.CrossRefGoogle ScholarPubMed
Ashida, M.Brey, P. 1998. Recent advances in research on the insect prophenoloxidase cascade. In Mechanisms of immune responses in insects. Edited by P. Brey and D. Hultmark. Chapman and Hall, London. pp. 135–172.Google Scholar
Bae, S.Kim, Y. 2004. Host physiological changes due to parasitism of a braconid wasp, Cotesia plutellae, on diamondback moth, Plutella xylostella. Journal of Comparative Biochemistry and Physiology, 138A: 39–44.CrossRefGoogle Scholar
Baldwin, M.R.Barbieri, J.T. 2005. The type III cytotoxins of Yersinia and Pseudomonas aeruginosa that modulate the actin cytoskeleton. Current Topics in Microbiology and Immunology, 291: 147–166.Google ScholarPubMed
Beck, M.Strand, M.R. 2005. Glc1.8 from Microplitis demolitor bracovirus induces a loss of adhesion and phagocytosis in insect High Five and S2 cells. Journal of Virology, 79: 1861–1870.CrossRefGoogle ScholarPubMed
Beckage, N.E., Metcalf, J.S., Nesbit, D.J., Schleifer, K.W., Zetlan, S.R., DeBuron, I. 1990. Host hemolymph monophenoloxidase activation in parasitized Manduca sexta larvae and evidence of inhibition by the wasp polydnavirus. Journal of Insect Biochemistry, 20: 285–294.CrossRefGoogle Scholar
Bogdan, C., Rollinghoff, M., Diefenbach, A. 2000. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Current Opinion in Immunology, 12: 64–76.CrossRefGoogle ScholarPubMed
Doucet, D.Cusson, M. 1996. Role of calyx fluid in alterations of immunity in Choristoneura fumiferana larvae parasitized by Tranosema rostrale. Journal of Comparative Biochemistry and Physiology, 114A: 311–317.CrossRefGoogle Scholar
Gardiner, E.M.M.Strand, M.R. 1999. Monoclonal antibodies bind distinct classes of hemocytes in the moth, Pseudoplusia includens. Journal of Insect Physiology, 45: 113–126.CrossRefGoogle ScholarPubMed
Glatz, R.V., Asgari, S., Schmidt, O. 2004. Evolution of polydnaviruses as insect immune suppressors. Trends in Microbiology, 12: 545–554.CrossRefGoogle ScholarPubMed
Gupta, A.P. 1991. Immunology of insects and other arthropods. CRC Press, Boca Raton, Florida, United States of America.Google Scholar
Hilgarth, R.S. 1997. Effects of Campoletis sonorensis calyx fluid on tyrosine, lysozyme and protein in the host Heliothis virescens. M.S. thesis. Kansas State University, Kansas, United States of America.Google Scholar
Huxham, I.M.Lackie, A.M. 1988. Behaviour in vitro of separated hemocytes from the locust, Schistocerca gregaria. Cell Tissue Research, 251: 677–684.CrossRefGoogle Scholar
Hu, J., Xiong, X., Wen, Z., Fu, J. 2003. Passive evasion of encapsulation in Macrocentrus cingulum Brischke (Hymenoptera: Braconidae), a polyembryonic parasitoid of Ostrinia furnacalis Guenée (Lepidoptera: Pyralidae). Journal of Insect Physiology, 49: 367–375.CrossRefGoogle ScholarPubMed
Ibrahim, A.M.A.Kim, Y. 2006. Parasitism by Cotesia plutellae alters the hemocyte population and immunological function of the diamondback moth Plutella xylostella. Journal of Insect Physiology, 52: 943–950.CrossRefGoogle ScholarPubMed
Kanost, M.R., Jiang, H., Yu, X.Q. 2004. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunological Reviews, 198: 97–105.CrossRefGoogle ScholarPubMed
Kim, K., Park, Y., Kim, Y., Lee, Y. 2001. Study on the inoculation augmentation of Paecilomyces japonicus to the silkworm, Bombyx mori, using dexamethasone. Korean Journal of Applied Entomology, 40: 51–58.Google Scholar
Kim, Y., Basio, N.A., Ibrahim, A.M.A., Bae, S. 2006. Gene structure of Cotesia plutellae bracovirus (CpBV)–IκB and its expression pattern in diamondback moth, Plutella xylostella, parasitized by Cotesia plutellae. Korean Journal of Applied Entomology, 45: 1–10.Google Scholar
Lavine, M.D.Beckage, N.E. 1995. Polydnaviruses: potent mediators of host insect immune dysfunction. Parasitology Today, 11: 368–378.CrossRefGoogle ScholarPubMed
Lavine, M.D.Strand, M.R. 2002. Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32: 1295–1309.CrossRefGoogle ScholarPubMed
Ling, E.Yu, X.Q. 2005. Prophenoloxidase binds to the surface of hemocytes and is involved in hemocyte melaniztion in Manduca sexta. Insect Biochemistry and Molecular Biology, 35: 1356–1366.CrossRefGoogle Scholar
Lowenberger, C. 2001. Innate immune response of Aedes aegypti. Insect Biochemistry and Molecular Biology, 31: 219–229.CrossRefGoogle ScholarPubMed
Mahmoud, A.M.A., De Luna-Santillana, E.J., Rodríguez-Pérez, M.A. 2011. Parasitism by the endoparasitoid wasp Cotesia flavipes induces cellular immunosuppression and enhances the susceptibility of Diatraea saccharalis to Bacillus thuringenisis. Journal of Insect Science, 11: 1–15, article 119. Available from http://www.insectscience.org/11.119/i1536-2442-11-119.pdf [accessed 28 January 2012].CrossRefGoogle Scholar
Mavrouli, M.D., Tsakas, S., Theodorou, G.L., Lampropoulou, M., Marmaras, V.J. 2005. MAP kinases mediate phagocytosis and melanization via prophenoloxidase activation in medfly hemocytes. Biochimica et Biophysica Acta, 17 (44), 145–156.CrossRefGoogle Scholar
Nakahara, Y., Kanamori, Y., Kiuchi, M., Kamimura, M. 2003. In vitro studies of hematopoiesis in the silkworm: cell proliferation in and hemocyte discharge from the hematopoietic organ. Journal of Insect Physiology, 49: 907–916.CrossRefGoogle ScholarPubMed
Pennacchio, F.Strand, M.R. 2006. Evolution of developmental strategies in parasitic Hymenoptera. Annual Review of Entomology, 51: 233–258.CrossRefGoogle ScholarPubMed
Pruissjers, A.J., Falabella, P., Eum, J.H., Pennacchio, F., Brown, M.R., Strand, M.R. 2009. Infection by a symbiotic polydnavirus induces wasting and inhibits metamorphosis of the moth Pseudoplusia includens. Journal of Experimental Biology, 212: 2998–3006.CrossRefGoogle Scholar
Richards, E.H.Edwards, J.P. 2000. Parasitism of Lacanobia oleracea (Lepidoptera) by the ectoparasitoid, Eulophus pennicornis, is associated with a reduction in host hemolymph phenoloxidase activity. Comparative Biochemistry and Physiology, 127: 289–298.CrossRefGoogle Scholar
Schmidt, O., Theopold, M., Strand, M.R. 2001. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays, 23: 344–351.CrossRefGoogle ScholarPubMed
Shelby, K.S., Ade yeye., O.A., Okot-Kotber., B.M., Webb., B.A. 2000. Parasitism-linked block of host plasma melanization. Journal of Invertebrate Pathology, 75: 218–225.CrossRefGoogle ScholarPubMed
Shelby, K.S.Webb, B.A. 1999. Polydnavirus-mediated suppression of insect immunity. Journal of Insect Physiology, 45: 507–514.CrossRefGoogle ScholarPubMed
Statistical Package for the Social Sciences (SPSS). 2001. SPSS 11.0 syntax reference guide, Vol. 1. Prentice Hall, Upper Saddle River, New Jersey, United States of America.Google Scholar
Stoltz, D.B. 1993. The polydnavirus life cycle. In Parasites and pathogens of insects. Edited by N.E. Beckage, S.N. Thompson and B.A. Federici. Academic Press, San Diego. pp. 167–187.CrossRefGoogle Scholar
Stoltz, D.B.Cook, D. 1983. Inhibition of host phenoloxidase activity by parasitoid Hymenoptera. Experientia, 39: 1022–1024.CrossRefGoogle Scholar
Stoltz, D.B.Guzo, D. 1986. Apparent haemocytic transformations associated with parasitoid-induced inhibition of immunity in Malacosoma disstria larvae. Journal of Insect Physiology, 32: 377–388.CrossRefGoogle Scholar
Strand, M.R.Pech, L.L. 1995. Microplitis demolitor polydnavirus induces apoptosis of a specific hemocyte morphotype in Pseudoplusia includens. Journal of General Virology, 76: 283–291.CrossRefGoogle ScholarPubMed
Tanaka, K., Matsumoto, H., Hayakawa, I. 2002. Detailed characterization of polydnavirus immunoevasive proteins in an endoparasitoid wasp. European Journal of Biochemistry, 269: 2557–2566.CrossRefGoogle Scholar
Teramoto, T.Tanaka, T. 2004. Mechanism of reduction in the number of the circulating hemocytes in the Pseudaletia separata host parasitized by Cotesia kariyai. Journal of Insect Physiology, 50: 1103–1111.CrossRefGoogle ScholarPubMed
Walzer, T., Galibert, L., De Smedt, T. 2005. Poxvirus semaphoring A39R inhibits phagocytosis by dendritic cells and neutrophils. European Journal of Immunology, 35: 391–398.CrossRefGoogle Scholar
Webb, B.A., Beckage, N.E., Hayakawa, Y., Krell, P.J., Lanzrein, B., Strand, M.R., et al. . 2000. Polydnaviridae. In Virus taxonomy: seventh report of the International Committee on Taxonomy of Virurses. Edited by M.H.V. Regenmortel, C.M. Fauquet, D.H.L. Bishop, E.B. Carstens, M.K. Estes, S.M. Lemon, J. Maniloff, M.A. Mayo, D.J. McGeoch, C.R. Pringle and R.B. Wichner. Academic Press, San Diego. pp. 253–259.Google Scholar
Webb, B.A.Strand, M.R. 2005. The biology and genomes of polydnaviruses. In Comprehensive molecular insect science, Vol. 6. Edited by L.I. Gilbert, K. Iatrou and S.S. Gill. Elsevier, New York. pp. 323–360.CrossRefGoogle Scholar
Wyler, T.Lanzrein, B. 2003. Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. II. Ultrastructural analysis of calyx cell development, virion formation and release. Journal of General Virology, 84: 1151–1163.CrossRefGoogle ScholarPubMed
Yu, R., Chen, Y., Chen, X., Huang, F., Lou, Y., Liu, S. 2007. Effects of venom/calyx fluid from the endoparasitic wasp Cotesia plutellae on the hemocytes of its host Plutella xylostella in vitro. Journal of Insect Physiology, 53: 22–29.CrossRefGoogle ScholarPubMed