Eur. J. Entomol. 103 (3): 515-522, 2006 | DOI: 10.14411/eje.2006.067

Activity of endo-polygalacturonases in mirid bugs (Heteroptera: Miridae) and their inhibition by plant cell wall proteins (PGIPs)

Francesca FRATI1,3, Roberta GALLETTI2, Giulia DE LORENZO2, Gianandrea SALERNO1, Eric CONTI*,1
1 Dipartimento di Scienze Agrarie e Ambientali - Entomologia, UniversitL di Perugia, Borgo XX Giugno 74, 06121 Perugia, Italy
2 Dipartimento di Biologia vegetale, UniversitL di Roma "La Sapienza", Piazzale Aldo Moro 5, 00185 Roma, Italy
3 Dipartimento di Biologia e Difesa Agro-Forestale - Entomologia, University of Basilicata, Campus di Macchia Romana, 85100 Potenza, Italy


Endo-polygalacturonases (PGs) are hydrolytic enzymes involved in the degradation of pectin, one of the major components of plant cell wall. While PGs from fungi, bacteria and plants have been extensively studied, PGs from insects are much less known, although they are likely to play an important role in insect-plant interactions. Presence of PGs has been reported for both piercing-sucking and chewing insect species, and possibly more commonly in mirid bugs (Heteroptera: Miridae). A screening of some common mirid species and other insects, belonging to different orders and families, was conducted using agarose diffusion assays run at different pHs. All the mirid species tested [Lygus rugulipennis Popp., L. pratensis (L.), Orthops kalmi (L.), Adelphocoris lineolatus (Goeze) and Closterotomus norwegicus (Gmelin)] showed PG activity, mainly at pH 7-8, whereas no activity was recorded for the other insect species, except Sitophilus sp. (Coleoptera: Curculionidae). PG activity in females of L. pratensis was significantly higher than in males, whereas there were no differences between the sexes in the other species. In all these species, PGs were present both in the salivary glands and the gut, with a higher activity in the salivary glands, confirming the role of these enzymes in the feeding behaviour of mirid bugs. Inhibition of mirid PGs by polygalacturonase-inhibiting proteins (PGIPs) from different plant sources was analysed at pH 7. PGIPs are extracellular plant proteins known for their ability to inhibit fungal PGs and restrict fungal colonization. Two PGIPs from Phaseolus vulgaris (PvPGIP3 and PvPGIP4) inhibited PGs of all the mirid bugs tested. This information may be helpful for the development of innovative insect-resistant plant varieties, for use in low-impact IPM.

Keywords: Miridae, Heteroptera, Curculionidae, Coleoptera, endo-polygalacturonase, PG, polygalacturonase-inhibiting proteins (PGIP), plant cell wall proteins, plant induced plant defence, direct defence, saliva

Received: September 9, 2005; Revised: December 12, 2005; Accepted: December 12, 2005; Published: July 3, 2006  Show citation

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FRATI, F., GALLETTI, R., DE LORENZO, G., SALERNO, G., & CONTI, E. (2006). Activity of endo-polygalacturonases in mirid bugs (Heteroptera: Miridae) and their inhibition by plant cell wall proteins (PGIPs). EJE, 103(3), 515-522. doi: 10.14411/eje.2006.067
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    References

    1. ADAMS J.B. & MCALLAN J.W. 1956: Pectinase in the saliva of Myzus persicae (Sulz.) (Homoptera: Aphididae). Can. J. Zool. 34: 541-543 Go to original source...
    2. AGBLOR A., HENDERSON H.M. & MADRID F.J. 1994: Characterisation of alpha-amylase and polygalacturonase from Lygus spp. (Heteroptera: Miridae). Food Res. Int. 27: 321-326 Go to original source...
    3. AGUSTI N. & COHEN A. 2000: Lygus hesperus and L. lineolaris (Hemiptera: Miridae): the salivary and midgut enzymes. J. Entom. Sci. 35: 176-182 Go to original source...
    4. BELLINCAMPI D., CAMARDELLA L., DELCOUR J.A., DESSEAUX V., D'OVIDIO R., DURAND A., ELLIOT G., GEBRUERS K., GIOVANE A., JUGE N., SY J.F., SVENSSON B. & VAIRO D. 2004: Potential physiological role of plant glycosidase inhibitors. Biochim. Biophy. Acta 1696: 265-274 Go to original source...
    5. BOYD D.W. JR. 2003: Digestive enzymes and stylet morphology of Deraeocoris nigritulus (Uhler) (Hemiptera: Miridae) reflect adaptations for predatory habits. Ann. Entomol. Soc. Am. 96: 667-671 Go to original source...
    6. BOYD D.W. JR., COHEN A.C. & ALVERSON D.R. 2002: Digestive enzymes and stylet morphology of Deraeocoris nebulosus (Hemiptera: Miridae), a predacious plant bug. Ann. Entomol. Soc. Am. 95: 395-401 Go to original source...
    7. BRADFORD M.M. 1976: A rapid sensitive method for the quantisation of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem. 72: 248-254 Go to original source...
    8. CAMPBELL B.C. & DREYER D.L. 1985: Host-plant resistance of sorghum: differential hydrolysis of sorghum pectic substances by polysaccharases of greenbug biotypes (Schizaphis graminum, Homoptera: Aphididae). Arch. Insect Biochem. 2: 203-215. Go to original source...
    9. CHERQUI A. & TJALLINGII W.F. 2000: Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. J. Insect Physiol. 46: 1177-1186 Go to original source...
    10. COHEN A.C. 1998: Solid-to-liquid feeding: the inside(s) story of extra-oral digestion in predaceous Arthropoda. Am. Entomol. 44: 103-117 Go to original source...
    11. COHEN A.C. & TANG R. 1997: Relative prey weight influences handling time and biomass extraction in Sinea confusa and Zelus renardii (Heteroptera: Reduviidae). Environ. Entomol. 26: 559-565 Go to original source...
    12. COHEN A.C. & WHEELER A.G. JR. 1998: Role of saliva in the highly destructive fourlined plant bug (Hemiptera: Miridae: Mirinae). Ann. Entomol. Soc. Am. 91: 94-100 Go to original source...
    13. CONTI E. & BIN F. 2001: Native Lygus spp. (Heteroptera: Miridae) damaging introduced Hibiscus cannabinus in Italy. J. Econ. Entomol. 94: 648-657 Go to original source...
    14. CONTI E., SALERNO G. & BIN F. 2002: Oviposition strategies of Lygus rugulipennis (Hemiptera: Miridae). ESA Annual Meeting, Fort Lauderdale, Florida, USA, 2002. p. 38 (abstract, http://esa.confex.com/esa/2002/techprogram/paper_7534.htm)
    15. CONTI E., FRATI F., GALLETTI R., SALERNO G., BIN F. & DE LORENZO G. 2004: Mirid bug polygalacturonases (PGs) are inhibited by cell wall proteins (PGIPs), indicating potential for induced resistance in plants. 12th International Symposium on Insect-Plant Relationships, 2004, Berlin, Germany. (Abstract) p. 130
    16. DE LORENZO G. & FERRARI S. 2002: Polygalacturonase inhibiting proteins in defence against phytopathogenic fungi. Curr. Opin. Plant Biol. 5: 295-299 Go to original source...
    17. DE LORENZO G., CASTORIA R., BELLINCAMPI D. & CERVONE F. 1997: Fungal invasion enzymes and their inhibition. In Carroll G. & Tudzynski P. (eds): The Mycota. Springer, Berlin, pp. 61-83 Go to original source...
    18. DE LORENZO G., D'OVIDIO R. & CERVONE F. 2001: The role of polygalacturonase-inhibiting proteins (PGIPs) in defence against pathogenic fungi. Annu. Rev. Phytopathol. 39: 313-335 Go to original source...
    19. DICKE M., GOLS R., LUDEKING D. & POSTHUMUS M.A. 1999: Jasmonic acid and herbivory differentially induces carnivoreattracting plant volatiles in lima bean plants. J. Chem. Ecol. 25: 1907-1922 Go to original source...
    20. DICKE M. & VAN LOON J.J.A. 2000: Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl. 97: 237-249 Go to original source...
    21. DOOSTDAR H., MC COLLUM T.G. & MAYER R.T. 1997: Purification and characterization of an endo-polygalacturonase from the gut of West Indies sugarcane rootstalk borer weevil (Diaprepes abbreviatus L.) larvae. Comp. Biochem. Phys. (B) 118: 861-867 Go to original source...
    22. D'OVIDIO R., RAIOLA A., CAPODICASA C., DEVOTO A., PONTIGGIA D., ROBERTI S., GALLETTI R., CONTI E., O'SULLIVAN D., DE LORENZO G. 2004: Characterization of the complex locus of Phaseolus vulgaris encoding polygalacturonase-inhibiting proteins (PGIPs) reveals sub-functionalization for defence against fungi and insects. Plant Physiol. 135: 2424-2435 Go to original source...
    23. FERRARI S., VAIRO D., AUSUBEL F.M., CERVONE F. & DE LORENZO G. 2003: Tandemly duplicated Arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal trasduction pathways in response to fungal infection. Plant Cell 15: 93-106 Go to original source...
    24. FERRY N., EDWARDS M.G., GATEHOUSE J.A. & GATEHOUSE A.M.R. 2004: Plant-insect interactions: molecular approaches to insect resistance. Curr. Opin. Biotech. 15: 155-161 Go to original source...
    25. GIACOMETTI R. 1995: Rearing of Sesamia nonagrioides Lefebvre on a meridic diet (Lepidoptera: Noctuidae). Redia 78: 19-27
    26. GIRARD C. & JOUANIN L. 1999: Molecular cloning of cDNAs encoding a range of digestive enzymes from the phytophagous beetle Phaedon cochleariae. Insect Biochem. Molec. 29: 1129-1142 Go to original source...
    27. JAUBERT S., LAFFAIRE J.-B., ABAD P. & ROSSO M.-N. 2002: A polygalacturonase of animal origin isolated from the rootknot nematode Meloidogyne incognita. FEBS Letters 522: 109-112 Go to original source...
    28. LAUREMA S. & NUORTEVA P. 1961: On the occurrence of pectic polygalacturonase in the salivary glands of Heteroptera and Homoptera Auchenorrhyncha. Ann. Entomol. Fenn. 27: 89-93
    29. LAUREMA S., VARIS A.L. & MIETTINEN H. 1985: Studies on enzymes in the salivary glands of Lygus rugulipennis (Hemiptera: Miridae). Insect Biochem. 15: 211-224 Go to original source...
    30. LI R., RIMMER R., YU M., SHARPE A.G., SEGUIN-SWARTZ G., LYDIATE D. & HEGEDUS D.D. 2003: Two Brassica napus polygalacturonase inhibitory protein genes are expressed at different levels in response to biotic and abiotic stresses. Planta 217: 299-308 Go to original source...
    31. LECKIE F., MATTEI B., CAPODICASA C., HEMMINGS A., NUSS L., ARACRI B., DE LORENZO G. & CERVONE F. 1999: The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed beta-trand / beta-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J. 18: 2352-2363 Go to original source...
    32. MA R., REESE H.C., BLACK W.C. & BRAMEL-COX P. 1990: Detection of pectinesterase and polygalacturonase from salivary secretions of living greenbugs, Schizaphis graminum (Homoptera: Aphididae). J. Insect Physiol. 36: 507-512 Go to original source...
    33. MANRIQUE V., JONES W.A., WILLIAMS III L.H. & BERNAL J. 2005: Olfactory responses of Anaphes iole (Hymenoptera: Mymaridae) to volatile signals derived from host habitat. J. Insect Behav. 18: 89-104 Go to original source...
    34. MARKOVIC O. & JANECEK S. 2001: Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution. Protein Engin. 14: 615-631 Go to original source...
    35. MARTIN W.R.JR., MORGAN P.W., STERLING W.L. & MEOLA R.W. 1988: Stimulation of ethylene production in cotton by salivary enzymes of the cotton fleahopper (Heteroptera: Miridae). Environ. Entomol. 17: 930-935 Go to original source...
    36. MILES P.W. 1972: The saliva of Hemiptera. Adv. Insect Physiol. 9: 183-255 Go to original source...
    37. MILES P.W. 1999: Aphis saliva. Biol. Rev. 74: 41-85 Go to original source...
    38. PARE P.W. & TUMLINSON J.H. 1997: Induced synthesis of plant volatiles. Nature 385: 30-31 Go to original source...
    39. RIDLEY B.L, O'NEILL M.A. & MOHNEN D. 2001: Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57: 929-67 Go to original source...
    40. RODRIGUEZ-SAONA C., CRAFTS-BRANDNER S.J., WILLIAMS III L. & PARE P.W. 2002: Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants. J. Chem. Ecol. 28: 1733-1747 Go to original source...
    41. ROMANI R., SALERNO G., FRATI F., CONTI E., ISIDORO N. & BIN F. 2005: Oviposition behaviour in Lygus rugulipennis: a morpho-functional study. Entomol. Exp. Appl. 115: 17-25 Go to original source...
    42. SHACKEL K.A., DE LA PAZ CELORIO-MANCERIO M., AHMADI H., GREVE L.C., TEUBER L.R., BACKUS E.A. & LABAVITCH J.M. 2005: Micro-injection of Lygus salivary gland proteins to simulate feeding damage in alfalfa and cotton flowers. Arch. Insect Biochem. Physiol. 58: 69-83 Go to original source...
    43. SHEN Z., REESE J.C. & REECK G. 1996: Purification and characterization of polygalacturonase from the rice weevil, Sitophilus oryzae (Coleoptera: Curculionidae). Insect Biochem. Molec. 26: 427-433. Go to original source...
    44. SHEN Z., DENTON M., MUTTI N., PAPPAN K., KANOST M.R., REESE J.C. & REECK G.R. 2003: Polygalacturonase from Sitophilus oryzae: possible horizontal transfer of a pectinase gene from fungi to weevils. J. Insect Sci. 3: 24-32 Go to original source...
    45. SOKAL R. & ROHLF F.J. 1998: Biometry. Freeman W.H., New York, 887 pp
    46. STRONG F.E. 1970: Physiology of injury caused by Lygus hesperus. J. Econ. Entomol. 63: 808-814 Go to original source...
    47. STRONG F.E. & KRUITWAGEN E.C. 1968: Polygalacturonase in the salivary apparatus of Lygus hesperus (Hemiptera). J. Insect Physiol. 14: 1113-1119 Go to original source...
    48. TAYLOR R.J. & SECOR G.A. 1988: An improved diffusion assay for quantifying the polygalacturonase content of Envinia culture filtrates. Phytopathology 78: 1101-1103 Go to original source...
    49. TJALLINGII W.F. & ESCH T.H. 1993: Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol. Entomol. 3: 317-328 Go to original source...
    50. WALLING L.L. 2000: The myriad plant responses to herbivores. J. Plant Growth Regul. 19: 195-216 Go to original source...
    51. WHEELER A.G.JR 2001: Biology of the Plant Bugs. Cornell University Press, Ithaca, New York, 506 pp
    52. ZENG F. & COHEN A.C. 2000: Comparison of D-amylase and protease activities of a zoophytophagous and two phytozoophagous Heteroptera. Comp. Biochem. Phys. (A) 126: 101-106 Go to original source...

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