Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T09:31:17.794Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphology and preliminary enzyme characterization of the salivary glands from the predatory bug Podisus nigrispinus (Heteroptera: Pentatomidae)

Published online by Cambridge University Press:  09 March 2007

J.A. Oliveira ,
M.G.A. Oliveira ,
R.N.C. Guedes  and
M.J. Soares
J.A. Oliveira
Affiliation:
Departamento de Biologia Animal, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil
M.G.A. Oliveira*
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Instituto de Biotecnologia Aplicada a Agropecuária (BIOAGRO), Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil
R.N.C. Guedes
Affiliation:
Departamento de Biologia Animal, Universidade Federal de Viçosa, Viçosa, MG 36571-000, Brazil
M.J. Soares
Affiliation:
Departamento de Ultraestrutura e Biologia Celular, Fundação Instituto Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, RJ 21040-900, Brazil
*
*Fax (+55)(31)3899 4012 Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Podisus nigrispinus (Dallas) is a common predator in agricultural and natural systems in Neotropical America. Its feeding strategy involves extra-oral digestion and to better understand this process its salivary glands were extracted and subjected to morphological and preliminary enzyme characterization. The salivary glands of P. nigrispinus are formed by a pair of main and accessory gland complexes. The main salivary glands are further divided into an anterior and a posterior lobe. The compartmentalization of the salivary gland complex is likely to be important for the production, activation and release of the digestive enzymes used in the extra-oral digestion of prey items. Proteases and lipase, important digestive enzymes involved in zoophagy, were detected in the salivary glands of P. nigrispinus. The prevailing trypsin-like protease activity was characterized by using the serine-protease substrate N-α-benzoyl-L-Arg-p-nitroanilidine (L-BApNA) and the trypsin inhibitors tosyl-L-lysine chloromethyl ketone (TLCK) and benzamidine. The KM value obtained for trypsin-like activity was 1.57 mm and the different peaks of optimum pH and temperature activity suggest the presence of multiple forms of this enzyme in P. nigrispinus. Detection of amylase activity in the salivary glands of this predator suggests its ability to digest starch and obtain nutrients from plants, which may have adaptative value under prey scarcity.

Keywords

amylaselipasetrypsin-like proteaseHeteropteraPentatomidaeAsopinaeextra-oral digestionspined soldier bug
Type
Review Article
Information
Bulletin of Entomological Research , Volume 96 , Issue 3 , June 2006 , pp. 251 - 258
Copyright
Copyright © Cambridge University Press 2006

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

Agusti, N. & Cohen, A.C. (2000) Lygus hesperus and L. lineolares (Hemiptera: Miridae), phytophages, zoophages, or omnivores: evidence of feeding adaptations suggested by the salivary and midgut digestive enzymes. Journal of Entomological Science 25, 176–186.Google Scholar
Baptist, B.A. (1941) The morphology and physiology of the salivary glands of Hemiptera-Heteroptera. Quarterly Journal of Microscopical Science 83, 91–139.Google Scholar
Bell, H.A., Down, R.E., Edwards, J.P., Gatehouse, J.A. & Gatehouse, A.M.R. (2005) Digestive proteolytic activity in the gut and salivary glands of the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae); effect of proteinase inhibitors. European Journal of Entomology 102, 139–145.CrossRefGoogle Scholar
Beynon, R.J. & Bond, J.S. (2001) Proteolytic enzymes: a practical approach 2nd Oxford IRL.Google Scholar
Boyd, D.W. Jr. (2003) Digestive enzymes and stylet morphology of Deraeocoris nigritulus (Uhler) (Hemiptera: Miridae) reflect adaptations for predatory habits. Annals of the Entomological Society of America 96, 667–671.CrossRefGoogle Scholar
Boyd, D.W., Jr., Cohen & A.C., Alverson D.R. (2002) Digestive enzymes and stylet morphology of Deraeocoris nebulosus (Hemiptera: Miridae), a predaceous plant bug. Annals of the Entomological Society of America 95, 395–401.CrossRefGoogle Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Caraway, W.T. (1959) A stable starch substrate for the determination of amylase in serum and other body fluids. American Journal of Clinical Pathology 32, 97–99.Google Scholar
Cherry, I.S. & Crandall, L.A. (1932) The specificity of pancreatic lipase: its appearance in the blood after pancreatic injury. American Journal of Physiology 100, 266–270.Google Scholar
Cohen, A.C. (1990) Feeding adaptations of some predacious Heteroptera. Annals of the Entomological Society of America 83, 1215–1223.Google Scholar
Cohen, A.C. (1993) Organization of digestion and preliminary characterization of salivary trypsin-like enzymes in a predaceous heteropteran, Zelus renardii. Journal of Insect Physiology 39, 823–829.Google Scholar
Cohen, A.C. (1995) Extra-oral digestion in predaceous terrestrial Arthropoda. Annual Review of Entomology 40, 85–103.Google Scholar
Cohen, A.C. (1996) Plant feeding by predatory Heteroptera: evolutionary and adaptational aspects of trophic switching Zoophytophagous Heteroptera: implications for life history and integrated pest management 1 – 17 Alomar O. Wiedenmann R.N. Lanham Thomas Say Publications in Entomology, Entomological Society of AmericaGoogle Scholar
Cohen, A.C. (1998a) Solid-to-liquid feeding: the inside(s) story of extra-oral digestion in predaceous Arthropoda. American Entomologist 44, 103–117.Google Scholar
Cohen, A.C. (1998b) Biochemical and morphological dynamics and predatory feeding habits in terrestrial Heteroptera Predatory Heteroptera: their ecology and use in biological control 21 – 32 Coll M. Ruberson J.R. Lanham Proceedings of the Thomas Say Publications in Entomology, Entomological Society of AmericaGoogle Scholar
De Clercq, P. (2000) Predaceous stinkbugs (Heteroptera: Asopinae) Heteroptera of economic importance 737 – 789 Schaefer C.W. Panizzi A.R. Cambridge Cambridge University PressGoogle Scholar
De Clercq, P. & Degheele, D. (1992) Plant feeding by two species of predatory bugs of the genus Podisus (Heteroptera: Pentatomidae). Mededelingen van de Faculteit Landbouwwetenschappen Universiteit Gent 57, 591–596.Google Scholar
Erlanger, B.F. & Kokowsky, N., Cohen, W. (1961) The preparation and properties of two new chromogenic substrates of trypsin. Archives of Biochemistry and Biophysics 95, 271–278.Google Scholar
Goodchild, A.J.P. (1966) Evolution of the alimentary canal in the Hemiptera. Biological Reviews 41, 97–140.Google Scholar
Habibi, J., Backus, E.A., Coudron, T.A. & Brandt, S.L. (2001) Effect of different host substrates on hemipteran salivary protein profiles. Entomologia Experimentalis et Applicata 98, 369–375.CrossRefGoogle Scholar
Hori, K. (1970) Some variations in the activities of salivary amylase and protease of Lygus disponsi Linnavnori (Hemiptera: Miridae). Applied Entomology and Zoology 5, 51–61.Google Scholar
Lacombe, D. (1999) Anatomia e histologia das glândulas salivares nos triatomínios. Memórias do Instituto Oswaldo Cruz 94, 411–416.Google Scholar
Laurema, A., Varis, L. & Miettinen, H. (1985) Studies on enzymes in the salivary glands of Lygus rugulipennis (Hemiptera: Miridae). Insect Biochemistry 15, 211–224.Google Scholar
Miles, P.W. (1967) The physiological division of labor in the salivary glands of Oncopeltus fasciatus (Dall.) (Heteroptera: Lygaeidae). Australian Journal of Biological Sciences 20, 785–797.Google Scholar
Miles, P.W. (1972) The saliva of Hemiptera. Advances in Insect Physiology 9, 183–255.Google Scholar
Oliveira, M.G.A., Rogana, E., Rosa, J.C., Reinhold, B.B., Andrade, M.H., Greene, L.J. & Mares-Guia, A.M. (1993) Tyrosine 151 is part of the substrate activation binding site. Journal of Biological Chemistry 268, 26893–26903.Google Scholar
Oliveira, M.G.A., De Simone, S.G., Xavier, L.P. & Guedes, R.N.C. (2005) Partial purification and characterization of digestive trypsin-like proteases from the velvet bean caterpillar, Anticarsia gemmatalis. Comparative Biochemistry and Physiology B140, 369–380.Google Scholar
Saini, E.D. (1994) Aspectos morfologicos y biologicos de Podisus connexivus Bergroth (Heteroptera: Pentatomidae). Revista da Sociedade Entomologica Argentina 53, 35–42.Google Scholar
Schaefer, C.W. & Panizzi, A.R. (2000) Economic importance of Heteroptera: a general view Heteroptera of economic importance 3 – 8 Schaefer C.W. Panizzi A.R. Cambridge Cambridge University PressGoogle Scholar
Stamopoulos, D.C., Diamantidis, G. & Chloridis, A. (1993) Activités enzymatiques du tube digestif du prédateur Podisus maculiventris (Hem.: Pentatomidae). Entomophaga 38, 493–499.Google Scholar
Swart, C.C. & Felgenhauer, B.E. (2003) Structure and function of the mouthparts and salivary gland complex of the giant waterbug, Belostoma lutarium (Stål) (Hemiptera: Belostomatidae). Annals of the Entomological Society of America 96, 870–882.Google Scholar
Xavier, L.P., Oliveira, M.G.A., Guedes, R.N.C., Santos, A.V. & De Simone, S.G. (2005) Trypsin-like activity of membrane-bound midgut proteases from Anticarsia gemmatalis (Lepidoptera: Noctuidae). European Journal of Entomology 102, 147–153.Google Scholar
Zanuncio, J.C., Ferreira, A.T., Zanuncio, T.V. & Garcia, J.F. (1993) Influence of feeding on Eucalyptus urophylla seedlings on the development of the predatory bug Podisus connexivus (Hemiptera: Pentatomidae). Mededelingen van de Faculteit Landbouwwetenschappen Universiteit Gent 58, 469–475.Google Scholar
Zanuncio, J.C., Zanuncio, T.V., Guedes, R.N.C. & Ramalho, F.S. (2000) Effect of feeding on three Eucalyptus species on the development of Brontocoris tabidus (Heteroptera: Pentatomidae) fed with Tenebrio molitor (Col.: Tenebrionidae). Biocontrol Science and Technology 10, 443–450.Google Scholar
Zanuncio, J.C., Guedes, R.N.C., Oliveira, H.N. & Zanuncio, T.V. (2002) Uma década de estudos com percevejos predadores: conquistas e desafios. pp. 495–510 in Parra, J.R.P., Botelho, P.S.M., Corrêa-Ferreira, B.S. & Bento, J.M.S. (eds) Controle biológico no Brasil: parasitóides e predadores. São Paulo, Manole.Google Scholar
Zeng, F. & Cohen, A.C. (2000a) Comparison of alpha-amylase and protease activities of a zoophytophagous and two phytozoophagous Heteroptera. Comparative Biochemistry and Physiology A126, 101–106.Google Scholar
Zeng, F. & Cohen, A.C. (2000b) Demonstration of amylase from the zoophytophagous anthocorid Orius insidiosus. Archives of Insect Biochemistry and Physiology 44, 136–139.Google Scholar