Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-17T17:08:38.677Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of Artemisia annua L. (Asteracea) on the digestive enzymatic profiles and the cellular immune reactions of the Sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae), against Beauveria bassiana

Published online by Cambridge University Press:  12 June 2009

A. Zibaee  and
A.R. Bandani
A. Zibaee
Affiliation:
Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, 31584, Iran
A.R. Bandani*
Affiliation:
Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, 31584, Iran
*
*Author for correspondence Fax: +98-0261-2238529 E-mail: abandani@ut.ac.ir
Get access Rights & Permissions [Opens in a new window]

Abstract

Plant extracts are currently studied more and more because of the possibility of their usage in plant protection. Many of the natural plant compounds which are used in the control of pests are known to affect the digestion and immune functions of insects. In this study, effects of Artemisia annua extract on the digestive enzymatic profiles and the cellular immune reactions of Eurygaster integriceps were investigated to reach a better understanding of its role in the control of this pest as the most destructive one in the production of wheat in the Near and Middle East, eastern and southern Europe and North Africa. Feeding and injection methods were used to study the plant extract effects on digestive enzymes and cellular immunity, respectively. When adult E. integriceps fed on food and water containing plant extracts, activity of the digestive enzymes, including α-amylase, α- and β-glucosidases, protease and lipase, in addition to cellular immune reactions (total and differentiate hemocyte numbers, phagocytosis, nodule formation and phenoloxidase activity) against Beauveria bassiana were affected and significantly decreased in comparison with controls, in that the clear dose-response relationships were established with respect to enzyme activities and immune reactions. A. annua extract had a significant effect on kinetic parameters (Vmax and Km) of digestive enzymes and phenoloxidase activity so that the presence of the plant extract decreased the value of Vmax and increased Km, causing the reduction of enzyme affinity to the substrate, overall velocity of the reaction and finally interfering with the rate of breakdown of the enzyme-substrate complex. The understanding of fungal-induced immune responses and identification of factors regarding fungal virulence could be important in accelerating host death in a biological control scenario. Hence, the combination of botanical pesticides and microbes to control insect pest populations would be a safe and possibly rapid method to decrease their damage and environmental risk due to the use of chemical pesticides.

Keywords

Eurygaster integricepsBeauveria bassianadigestive enzymescellular immune reactions
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 100 , Issue 2 , April 2010 , pp. 185 - 196
Copyright
Copyright © Cambridge University Press 2009

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

Abudulai, M., Shepard, B.M. & Mitchell, P.L. (2001) Parasitism and predation on eggs of Leptoglossus phyllopus (L.) (Hemiptera: Coreidae) in Cowpea: Impact of Endosulfan Sprays. Journal of Agricultural and Urban Entomology 18, 105–115.Google Scholar
Akhtar, Y. & Isman, M.B. (2004) Comparative growth inhibitory and antifeedant effects of plant extract and pure allelochemicals on some phytophagous insect species, Journal of Applied Entomology 128, 32–38.CrossRefGoogle Scholar
Anggraeni, T. & Ratcliffe, N.A. (1991) Studies on cell-cell cooperation during phagocytosis by purified haemocyte populations of the wax moth, Galleria mellonella. Journal of Insect Physiology 37, 453–460.CrossRefGoogle Scholar
Ascher, K.R.S. & Ishaaya, I. (2004) Antifeeding and protease and amylase inhibiting activity of phentin acetate in Spodoptera littoralis larvae, Pesticide Biochemistry and Physiology 75, 326–336.Google Scholar
Azambuja, P., Garcia, E.S. & Ratcliffe, N.A. (1991a) Aspects of classification of hemiptera hemocytes from six triatomine species. Memo′rias do Instituto Oswaldo Cruz 86, 1–10.CrossRefGoogle ScholarPubMed
Azambuja, P., Garcia, E.S., Ratcliffe, N.A. & Warthen, J.D. Jr. (1991b) Immune-depression in Rhodnius prolixus induced by the growth inhibitor, azadirachtin. Journal of Insect Physiology 37, 771–777.CrossRefGoogle Scholar
Bernfeld, P. (1955) Amylases, α and β. Methods in Enzymology 1, 149–158.Google Scholar
Bhakuni, R.S., Sharma, R.P. & Kumar, S. (2001) Secondary metabolites of Artemisia annua and their biological activity. Current Science 80, 35–49.Google Scholar
Boyd, D.W., Cohen, A.C. & Alverson, D.R. (2002) Digestive enzymes and stylet morphology of Deraeocoris nebulosus (Hemiptera: Miridae), a predacious plant bug. Annals of Entomological Society of America 95, 395–401.Google Scholar
Bradford, M. (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Broadway, R.M. (1989) Characterization and ecological implication of midgut proteolytic activity in Pieris rapae and Trichoplusia ni. Journal of Chemical Ecology 15, 2101–2113.Google Scholar
Broadway, R.M. & Duffey, S.S. (1988) The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. Journal of Insect Physiology 34, 1111–1117.CrossRefGoogle Scholar
Chapman, R.F. (1985) Structure of the digestive systems. pp. 165–211 in Kerkut, G.A., Gilbert, L.I. (Eds) Comprehensive Insect Physiology Biochemistry and Pharmacology. vol. 4. Oxford, Pergamon Press.Google Scholar
Cohen, A.C. (1993) Organization of digestion and preliminary characterization of salivary trypsin like enzymes in a predaceous Heteropteran, Zelus renadii. Journal of Insect Physiology 39, 823–829.Google Scholar
Dularay, B. & Lackie, A.M. (1985) Haemocytic encapsulation and the prophenoloxidase-activaion pathway in the locust Schistocerca gregaria. Journal of Insect Physiology 15, 827–834.Google Scholar
Elpidina, E.N., Vinokurov, K.S., Gromenko, V.A., Rudenskaya, Y.A., Dunaevsky, Y.E. & Zhuzhikov, D.P. (2001) Compartmentalization of proteinases and amylases in Nauphoeta cinerea midgut. Archives of Insect Biochemistry and Physiology 48, 206–216.Google Scholar
Etebari, K., Mirhoseini, S.Z. & Matindoost, L. (2005) A study on intraspecific biodiversity of eight groups of silkworm (Bombyx mori) by biochemical markers. Insect Science. 12, 87–94.Google Scholar
Feng, M.G., Johnson, J.B. & Kish, L.P. (1990) Virulence of Verticillium lecanii and an aphid-derived isolate of Beauveria bassiana (Fungi: Hyphomycetes) for six species of cereal aphids (Homoptera: Aphididae). Environmental Entomology 19, 815–820.CrossRefGoogle Scholar
Ferreira, C. & Terra, W.R. (1983) Physical and kinetic properties of a plasma-membrane-bound P-Dglucosidase (cellobiase) from midgut cells of an insect (Rhynchosciara americana larva). Biochemistry Journal 213, 43–51.Google Scholar
Figueiredo, M.B., Castroa, D.P., Nogueirab, N.F.S., Garciaa, E.S. & Azambuja, P. (2006) Cellular immune response in Rhodnius prolixus: Role of ecdysone in hemocyte phagocytosis. Journal of Insect Physiology 52, 711–716.CrossRefGoogle ScholarPubMed
Franssens, V., Smagghe, G., Simonet, G., Claeys, I., Breugelmans, B., De Loof, A. & Broeck, J.V. (2006) 20-hydroxyecdyson and juvenile hormone regulate the laminarin-induced nodulation reaction in larvae of the flesh fly, Neobellieria bullata. Developmental and Comparative Immunology 30, 735–740.Google Scholar
Greenberg, S. & Silverstein, S.C. (1993) Phagocytosis. pp. 941–965 in Paul, W.E. (Ed.) Fundamental of Immunology. New York, Raven Press.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.Google Scholar
Hatting, J.L., Wraight, S.P. & Miller, R.M. (2004) Efficacy of Beauveria bassiana (Hyphomycetes) for control of Russian wheat aphid (Homoptera: Aphididae) on resistant wheat under field conditions. Biocontrol Science and Technology 14, 459–473.CrossRefGoogle Scholar
Hemmingi, J.D.C. & Lindroth, R.L. (1999) Effects of light and nutrient availability on aspen: growth, phytochemistry and insect performance. Journal of Chemical Ecology 26, 1687–1714.CrossRefGoogle Scholar
Hemmingi, J.D.C. & Lindroth, R.L. (2000) Effects of phenolic glycosides and protein on Gypsy Moth (Lepidoptera: Lymantriidae) and Forest tent caterpillar (Lepidoptera: Lasiocampidae) performance and detoxication activities. Environmental Entomology 29, 1108–1115.Google Scholar
Hori, K. (1969) Effect of various activators on the salivary amylase of the bug Lygus disponsi. Journal of Insect Physiology 15, 2305–2317.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
Isman, M.B. (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology 51, 45–66.CrossRefGoogle Scholar
Johnson, D.E., Brookhart, G.L., Kramer, K.J., Barnett, B.D. & McGaughey, W.H. (1990) Resistance to Bacillus thuringiensis by the Indian meal moth Plodia interpunctella: Comparison of midgut proteinase from susceptible and resistant larvae. Journal of Invertebrate Pathology 55, 235–244.Google Scholar
Kazzazi, M., Bandani, A.R. & Hoszeinkhani, S. (2005) Biochemical characterization of α-amylase of the Sunn pest, Eurygaster integriceps. Entomological Science 8, 371–377.Google Scholar
Lackie, A.M. & Vasta, G.R. (1988) The role of a galactosyl-binding lectin in the cellular immune response of the cockroach Periplaneta americana (Dictyoptera). Immunity 64, 353–357.Google Scholar
Lee, H.R., Kim, J.W. & Lee, I. (1994) Studies on the toxicity of insect growth regulators against the fall armyworm (Hyphantaria cunea Drury) and the rice stem borer (Chilo suppressalis Walker) comparisonsa in enzyme activitiesa. Korean Journal of Applied Entomology 33, 88–95.Google Scholar
Leonard, C., Kenneth, S. & Ratcliffe, N.A. (1985) Studies on prophenoloxidase and protease activity of Blaberua craniifer hemocytes. Insect Biochemistry 15, 803–810.CrossRefGoogle Scholar
LeOra Software (1987) POLO-PC: A user guide to probit or logit analysis. LeOra software, Berkeley, California.Google Scholar
Morris, J.G. (1978) A Biologist's Physical Chemistry. 2nd edn. 390 pp. London, Edward Arnold Publishing.Google Scholar
Nayar, J.K., & Knight, J.W. (1997) Hemagglutinind in Anopheles quadrimaculatus strains susceptible and refractory to Brugia malayi and their role in the immune response to filarial parasites. Comparative Biochemistry and Physiology 116B, 109–117.Google Scholar
Oliveira, M.A. & De Souza, W. (2003) Further morphological studies on the behavior of Trypanosoma rangeli in the hemocytes of Rhodnius prolixus. Parasitology International 52, 299–307.Google Scholar
Paulian, F. & Popov, C. (1980) Sunn pest or cereal bug. pp. 69–74 in Wheat Technical Monograph. Basel, Switzerland, Ciba-Geigy.Google Scholar
Popov, C., Barbulescu, A. & Vonica, I. (1996) Population dynamics and management of Sunn pest in Romania. FAO Plant Production and Protection 138, 47–59.Google Scholar
Rabinovitch, M. (1967) The dissociation of the attachment and ingestion phases of phagocytosis by macrophages. Experimental Cell Research 46, 19–32.Google Scholar
Ratcliffe, N.A., & Rowley, A.F. (1987) Insect response to parasites and other pathogens. pp. 271–332 in Soulsby, E.J.L. (Ed.) Immunology, Immunoprophylaxis and Immunotherapy of Parasitic Infections. Boca Raton, FL, USA, CRC Press.Google Scholar
Ratcliffe, N.A., Leonard, C. & Rowley, A.F. (1984) Prophenoloxidase activation nonself recognition and cell cooperation in insect immunity. Science 226, 557–559.Google Scholar
Robertson, J.L., Preisler, H.K. & Russell, R.M. (2007) PoloPlus: Probit and logit analysis user's guide. LeOra Software, Petaluna, CA, USA.Google Scholar
Rohloff, L.H., Wiesner, A. & Gotz, P. (1994) A fluorescence assay demonstrating stimulation of phagocytosis by haemolymph molecules of Galleria mellonella. Journal of Insect Physiology 40, 1045–1049.Google Scholar
Saleem, M.A. & Shakoori, A.R. (1987) Point effects of Dimilin and Ambush on enzyme activies of Tribolium castaneum larvae. Pesticide Biochemistry and Physiology 29, 127–137.CrossRefGoogle Scholar
SAS Institute (1997) SAS/STAT User's Guide for Personal Computers. SAS Institute, Cary, NC.Google Scholar
Schmutterer, H. (1990) Properties and potential of natural pesticides from the neem tree, Azadirachta indica. Annual Review of Entomology 35, 271–297.CrossRefGoogle ScholarPubMed
Senthil Nathan, S. & Kalaivani, K. (2005) Efficacy of nucleopolyhedrovirus (NPV) and azadirachtin on Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Biological Control 34, 93–98.Google Scholar
Senthil Nathan, S., Chunga, P.G. & Muruganb, K. (2006) Combined effect of biopesticides on the digestive enzymatic profiles of Cnaphalocrocis medinalis (Guenee) (the rice leaffolder) (Insecta: Lepidoptera: Pyralidae). Ecotoxicology and Environmental Safety 64, 382–389.Google Scholar
Senthil Nathan, S., Choia, M.Y., Seoa, H.Y., Paika, C.H., Kalaivania, K. & Kim, J.D. (2008) Effect of azadirachtin on acetylcholinesterase (AChE) activity and histology of the brown planthopper Nilaparvata lugens. Ecotoxicology and Environmental Safety 70, 244–250.CrossRefGoogle ScholarPubMed
Shekari, M., Jalali Sendi, J., Etenbari, K., Zibaee, A. & Shadparvar, A. (2008) Effects of Artemisia annua L. (Asteracea) on nutritional physiology and enzyme activities of elm leaf beetle, Xanthogaleruca luteola Mull. (Coleoptera: Chrysomellidae). Pesticide Biochemistry and Physiology 91, 66–74.CrossRefGoogle Scholar
Sibley, R.M. (1981) Strategies of digestion and defaecation. pp. 109–136in Townsend, C.R. & Calew, P. (Eds) Physiological Ecology and Evolutionary Approach to Resource use. Oxford, Blackwell Publishers.Google Scholar
Smith, V.J., Soderall, K. & Hamilton, M. (1984) β-1,3-Glucan induced cellular defence reaction in the shore-crab Carcinus means. Comparative Biochemistry and Physiology 77, 635–639.CrossRefGoogle Scholar
Stryer, L. (1995) Biochemistry. 1514 pp. New York, W.H. Freeman and Company.Google Scholar
Talaei, R. & Kharazzi Pakdel, A. (2002) Evaluation of Sunn Pest, Eurygaster integriceps Susceptibility in Different Developmental Stages to Beauvaria bassiana. pp. 588–592 in 2nd International Conference on Alternative Methods against Plant Pests and Disease Control. 4–7 March 2002, Lille, France.Google Scholar
Tsujita, T., Ninomiya, H. & Okuda, H. (1989) p-nitrophenyl butyrate hydrolyzing activity of hormone-sensitive lipase from bovine adipose tissue. Journal of Lipid Research 30, 997–1004.Google Scholar
Vey, A., Matha, V. & Dumas, C. (2002) Effects of the peptide mycotoxin destruxin E on insect haemocytes and on dynamics and efficiency of the multicellular immune reaction. Journal of Invertebrate Pathology 80, 177–187.Google Scholar
Weinzierl, R. & Henn, T. (1991) Alternatives in insect management: biological and biorational approaches. Cooperative Extension Service, University of Illinois at Urbana-Champaign, North Central Regional Extension Publication 401, 73 pp.Google Scholar
Wilson, K. & Goulding, K.H. (Eds) (1986) Principle and Techniques of Practical Biochemistry. 3rd edn. 299 pp. London, Edward Arnold Publishing.Google Scholar
Wraight, S.P., Carruthers, R.I., Bradleg, C.A., Jaronski, S.T., Lacey, L.A., Wood, P. & Galaini-Wroigh, S. (1998) Pathogenicity of the entomopathogenic fungi paecilomyces spp. and Beauveria bassiana against the Silverleaf whitefly, Bemesia argentifolii. Journal of Invertebrate Pathology 71, 217–226.CrossRefGoogle Scholar
Zibaee, A., Jalali Sendi, J., Etebari, K., Alinia, F. & Ghadamyari, M. (2008a) The effect of diazinon on some biochemical characteristics of Chilo suppressalis Walker (Lepidoptera: Pyralidae), rice striped stem borer. Munis Entomology and Zoology 3, 255–264.Google Scholar
Zibaee, A., Sendi, J., Alinia, F. & Etebari, J. (2008b) A study on biochemical differences among five different groups of rice striped stem borer Chilo suppressalis Walker (Lepidoptera: Pyralidae). Invertebrate Survival Journal 5, 20–29.Google Scholar