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Immune response of Chilo suppressalis Walker (Lepidoptera: Crambidae) larvae to different entomopathogenic fungi

Published online by Cambridge University Press:  09 January 2014

A. Zibaee  and
D. Malagoli
A. Zibaee*
Affiliation:
Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran
D. Malagoli
Affiliation:
Department of Life Sciences, University of Modena and Reggio Emilia, Modena 41125, Italy
*
*Author for correspondence Phone: +98 0131 6690264 Fax: +98 131 6690281 E-mail: arash.zibaee@gmx.com and arash.zibaee@guilan.ac.ir
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Abstract

The current study reports mortality and effects on cellular immune response of several entomopathogenic fungi including isoleates BB1, BB2 and BB3 of Beauveria bassiana, Metarhizium anisopliae, Isaria fumosoroseus and Lecanicilium lecanii against larvae of Chilo suppressalis. Prohemocytes, granulocytes, plasmatocytes and oenocytoids were identified as the main circulating hemocytes in the hemolymph of larvae using Giemsa staining solution. Entomopathogenic fungi caused differential mortality on larvae: BB1, BB3, M. anisopliae lead to the highest mortality on larvae and L. lecanii caused the lowest mortality. The highest numbers of total hemocytes were observed 3 h post-injection of B. bassiana isolates and 6 h for the other treatments. The highest numbers of plasmatocytes were observed 3 h post-injection of BB1 and Tween 80, whereas BB2, BB3, M. anisopliae, I.fumosoroseus and L. lecani caused plasmatocyte increase 6 h post-injection. Similar results were obtained in case of granulocytes but only Tween 80 showed the highest number of hemocytes 3 h post-injection. The highest numbers of nodules were found at various time intervals after injection of fungal isolates and latex bead. The highest activities of phenoloxidase were observed 12 h post-injection by BbB1, BbB3, M. anisopliae and latex bead; 3–6 h post-injection by BbB2, 6 h post-injection by I. fumosoroseus and 3–6 h post-injection by L. lecanii. Our data demonstrate the possibility of utilizing different fungal extracts in the field to help reduce the risk of resistance evolution in C. suppressalis and encourage experimentations aimed to increase the number of biological control agent for insect pests such as the striped rice stem borer C. suppressalis.

Keywords

immunityrice striped stem borerentomopathogenic fungi
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 2 , April 2014 , pp. 155 - 163
Copyright
Copyright © Cambridge University Press 2014 

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References

Azambuja, P., Garcia, E.S. & Ratcliffe, N.A. (1991) Aspects of classification of hemiptera hemocytes from six triatomine species. Memórias do Instituto Oswaldo Cruz 86, 1–10.CrossRefGoogle ScholarPubMed
Bandani, A. (2005) Effects of Tolypocladium cylindrosporum and its secondary metabolites, efrapeptins, on the immune system of Galleria mellonella larvae. Biocontrol Science and Technology 15, 67–79.CrossRefGoogle Scholar
Bidochka, M.J. & Khachatourians, G.G. (1987) Haemocytic defense responses to the entomopathogenic fungus Beauveria bassiana in the migratory grasshopper, Melanoplus sanguinipes . Entomologia Experimentalis et Applicata 45, 151–156.CrossRefGoogle Scholar
Borges, A.R., Santos, P.N., Furtado, A.F. & Figueiredo, R.C.B. (2008) Phagocytosis of latex beads and bacteria by hemocytes of the triatomine bug Rhodnius prolixus (Hemiptera: Reduvidae). Micron 39, 486–494.Google Scholar
Brayner, F.A., Araujo, H.R.C., Cavalcanti, M.G., Alves, L.C. & Peixoto, C.A. (2005) Ultrastructural characterization of the hemocytes of Culex quinquefasciatus (Diptera: Culicidae). Micron 36, 359–367.CrossRefGoogle ScholarPubMed
Chen, C.C. & Chen, C.S. (1995) Brugia pahangi: effects of melanization on the uptake of nutrients by microfilariae in vitro . Experimental Parasitology 81, 72–78.Google Scholar
Chouvenc, T., Su, N.Y. & Robert, A. (2009) Cellular encapsulation in the eastern subterranean termite, Reticulitermes flavipes (Isoptera), against infection by the entomopathogenic fungus Metarhizium anisopliae . Journal of Invertebrate Pathology 101, 234–241.CrossRefGoogle ScholarPubMed
Christensen, B.M., Li, J., Chen, C.C. & Nappi, A.J. (2005) Melanization immune responses in mosquito vectors. Trends in Parasitology 21, 192–199.Google Scholar
Dularay, B. & Lackie, A.M. (1985) Haemocytic encapsulation and the prophenoloxidaseactivaion pathway in the locust Schistocerca gregaria . Journal of Insect Physiology 15, 827–834.Google Scholar
Eleftherianos, I., Marokhazi, J., Millichap, P.J., Hodgkinson, A.J., Sriboonlert, A., ffrench-Constant, R.H. & Reynolds, S.E. (2006) Prior infection of Manduca sexta with non-pathogenic Escherichia coli elicits immunity to pathogenic Photorhabdus luminescens: roles of immune-related proteins shown by RNA interference. Insect Biochemistry and Molecular Biology 36, 517–525.Google Scholar
Franssens, V., Smagghe, G., Simonet, G., Claeys, I., Breugelmans, B., DeLoof, A. & Vanden Broeck, J. (2006) 20-Hydroxy ecdysone and juvenile hormone regulate the laminarin-induced nodulation reaction in larvae of the fleshfly, Neobellieria bullata . Developmental and Comparative Immunology 30, 735–740.CrossRefGoogle Scholar
Gillespie, J.P., Kanost, M.R. & Trenczek, T. (1997) Biological mediators of insect immunity. Annual Review of Entomology 42, 611–643.Google Scholar
Gillespie, J.P., Burnett, C. & Charnley, A.K. (2000) The immune response of the desert locust Schistocerca gregaria during mycosis of the entomopathogenic fungus, Metarhizium anisopliae var acridum . Journal of Insect Physiology 46, 429–437.Google Scholar
Gorman, M.J., Schwartz, A.M. & Paskewitz, S.M. (1998) The role of surface characteristics in eliciting humoral encapsulation of foreign bodies in Plasmodium-refractory and susceptible strains of Anopheles gambiae . Journal of Insect Physiology 44, 947–954.Google Scholar
Gorman, M.J., An, C. & Kanost, M.R. (2007) Characterization of tyrosine hydroxylase from Manduca sexta . Insect Biochemistry and Molecular Biology 37, 1327–1337.Google Scholar
Gunnarsson, S.G.S. & Lackie, A.M. (1985) Haemocytic aggregation in Schistocerca gregaria and Periplaneta americana as a response to injected substances of microbial origin. Journal of Invertebrate Pathology 46, 312–319.CrossRefGoogle Scholar
Haine, E.R., Moret, Y., Siva-Jothy, M.T. & Rolff, J. (2008) Antimicrobial defense and persistent infection in insects. Science 322, 1257–1259.Google Scholar
Hajek, A.E. & St. Leger, R.J. (1994) Interactions between fungal pathogens and insect hosts. Annual Review of Entomology 39, 293–322.CrossRefGoogle Scholar
Hung, S.Y. & Boucias, D.G. (1992) Influence of Beauveria bassiana on the cellular defense response of the beet armyworm, Spodoptera exigua . Journal of Invertebrate Pathology 60, 152–158.CrossRefGoogle Scholar
Huxham, I.M., Lackie, A.M. & McCorkindale, N.J. (1989) Inhibitory effects of cyclodepsipeptides, destruxins, from the fungus Metarhizium anisopliae, on cellular immunity in insects. Journal of Insect Physiology 35, 97–105.Google Scholar
Iwama, R. & Ashida, M. (1986) Biosynthesis of prophenoloxidase in hemocytes of larval hemolymph of the silkworm, Bombyx mori. Insect Biochem 16, 547–555.Google Scholar
Kanost, M.R. & Gorman, M.J. (2008) Phenoloxidases in insect immunity. pp. 69–96 in Beckage, N.E. (Ed.) Insect Immunology. San Diego, USA, Academic Press.Google Scholar
Khanjani, M. (2006) Crop Pests of Iran. Hamadan, Iran, Boali Sina University Press.Google Scholar
Laughton, A.M., Garcia, J.R., Altincicek, B., Strand, M.R. & Gerardo, N.M. (2011) Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum . Journal of Insect Physiology 57, 830–839.Google Scholar
Lavine, M.D. & Strand, M.R. (2001) Surface characteristics of foreign targets that elicit an encapsulation response by the moth Pseudoplusia includens . Journal of Insect Physiology 47, 965–974.CrossRefGoogle ScholarPubMed
Lavine, M.D. & Strand, M.R. (2002) Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 32, 1295–1309.Google Scholar
Leonard, C., Kenneth, S. & Ratcliffe, N.A. (1985) Studies on prophenoloxidase and protease activity of Blaberua craniifer haemocytes. Insect Biochemistry 15, 803–810.Google Scholar
Ling, E. & Yu, X.Q. (2006) Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta . Developmental and Comparative Immunology 30, 289–299.Google Scholar
Majidi-Shilsar, F. (2002) Determination of ecological location and pathogenicity of Beauveria bassiana on Chilo suppressalis and its laboratory rearing. PhD Dissertation, Islamic Azad University, Branch of Science and Research, Tehran. p. 165.Google Scholar
Majidi-Shilsar, F., Alinia, F. & Ershad, J. (2008) Pathogenocity of Beauveria Bassiana on Rice Striped Stem Borer in Field Condition. Hamedan, 18th Iranian Plant Protection Congress. p. 31.Google Scholar
Mazet, I., Hung, S.Y. & Boucias, D.G. (1994) Detection of toxic metabolites in the hemolymph of Beauveria bassiana infected Spodoptera exigua larvae. Experentia 50, 142–147.Google Scholar
Michel, K. & Kafatos, F.C. (2005) Mosquito immunity against Plasmodium . Insect Biochemistry Molecular Biology 35, 677–689.Google Scholar
Nakahara, Y., Shimura, S., Ueno, C., Kanamori, Y., Mita, K., Kiuchi, M. & Kamimura, M. (2009) Purification and characterization of silkworm hemocytes by flow cytometry. Developmental and Comparative Immunology 33, 439–448.Google Scholar
Nappi, A.J. & Christensen, B.M. (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry Molecular Biology 35, 443–459.Google Scholar
Pech, L.L. & Strand, M.R. (1996) Granular cells are required for encapsulation of foreign targets by insect haemocytes. Journal of Cell Science 109, 2053–2060.Google Scholar
Ruoslahti, E. (1996) RGD and other recognition sequences for integrins. Annual Review of Cell Development and Biology 12, 697–715.CrossRefGoogle ScholarPubMed
Samuels, R.I., Charnley, A.K. & Reynolds, S.E. (1988) The role of destruxins in the pathogenicity of 3 strains of Metarhizium anisopliae for the tobacco hornworm Manduca sexta . Mycopathology 104, 51–58.Google Scholar
SAS institute (1997) SAS/STAT User's Guide for Personal Computers. Cary, Nc, SAS Institute.Google Scholar
Schmid-Hempel, P. (2005) Evolutionary ecology of insect immune defenses. Annual Review of Entomology 50, 529–551.Google Scholar
Sewify, G.H. & Hashem, M.Y. (2001) Effect of the entomopathogenic fungus Metarhizium anisopliae (Metsch.) Sorokin on cellular defence response and oxygen uptake of the wax moth Galleria mellonella L. (Lep., Pyralidae). Journal of Applied Entomology 125, 533–536.Google Scholar
Soderhall, K. & Cerenius, L. (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 23–28.Google Scholar
Solter, L.F. & Maddox, J.V. (1998) Physiological host specificity of microsporidia as an indicator of ecological host specificity. Journal of Invertebrate Pathology 71, 207–216.CrossRefGoogle ScholarPubMed
Solter, L.F., Maddox, J.V. & McManus, M.L. (1997) Host specificity of microsporidia (Protista: Microspora) from European populations of Lymantria dispar (Lepidoptera: Lymantriidae) to indigenous North American lepidoptera. Journal of Invertebrate Pathology 69, 135–150.CrossRefGoogle ScholarPubMed
Vakili, A. (1998) Appendix in 13th Iranian plant protection congress, Karaj. Plant protection organization. p. 13.Google Scholar
Wago, H. (1991). Phagocytic recognition in Bombyx mori. In: Gupta, A.P. (Ed.). Immunology of insects and other arthropods. Boca Raton: CRC Press.Google Scholar
Yamashita, M. & Iwabuchi, K. (2001) Bombyx mori prohemocyte division and differentiation in individual microcultures. J Insect Physiol 47, 325–331.Google Scholar
Ye, Y.H., Chenoweth, S.F. & McGraw, E. (2009) Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster . PLoS Pathogens 5, e1000385.Google Scholar
Zibaee, A., Sendi, J.J., Alinia, F., Ghadamyari, M. & Etebari, K. (2009) Diazinon resistance in different selected strains of Chilo suppressalis Walker (Lepidoptera: Pyralidae), rice striped stem borer, in the north of Iran. Journal of Economic Entomology 102, 1189–1196.Google Scholar
Zibaee, A., Bandani, A.R., Talaei-Hassanlouei, R. & Malagoli, D. (2011) Cellular immune reactions of Eurygaster integriceps, to the entomopathogenic fungus, Beauveria bassiana and its secondary metabolites. Journal of Insect Science 11, 138.Google Scholar
Zibaee, A., Hoda, H. & Fazeli-Dinan, M. (2012) Role of proteases in extra-oral digestion of a predatory bug, A. spinidens . Journal of Insect Science 12, 51. Available online at http://insectscience.org/12.51.CrossRefGoogle Scholar