Differential responses of midgut soluble aminopeptidases of Helicoverpa armigera to feeding on various host and non-host plant diets

Arthropod-Plant Interactions

Volumn 5, Issue 4, 2011, Pages 359-368

  Lomate, Purushottam R ^a   Hivrale, Vandana K ^a  

^a DR BABASAHEB AMBEDKAR MARATHWADA UNIVERSITY   (India)

Author keywords

Diet; Helicoverpa armigera; Midgut aminopeptidase; Nutrition; Serine proteinases

Indexed keywords

BIOCHEMISTRY; DIET; FEEDING; MOLECULAR ANALYSIS; MOTH; PLANT-INSECT INTERACTION; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS;

CAJANUS CAJAN; CICER ARIETINUM; HELICOVERPA ARMIGERA; HEXAPODA; MOMORDICA CHARANTIA;

EID: 81455158974     PISSN: 18728855     EISSN: 18728847     Source Type: Journal    
DOI: 10.1007/s11829-011-9140-9     Document Type: Article

References (47)

1. Angelucci C, Barrett-Wilt GA, Hunt DF, Akhurst RJ, East PD, Gordon KH, Campbell PM (2008) Diversity of aminopeptidases, derived from four lepidopteran gene duplications, and polycalins expressed in the midgut of Helicoverpa armigera: identification of proteins binding the delta-endotoxin, Cry1Ac of Bacillus thuringiensis. Insect Biochem Mol Biol 38(7): 685-696.
2. Billingsley PF (1990) Blood digestion in the mosquito, Anopheles stephensi liston (Diptera: Culicidae): partial characterization and post-feeding activity of midgut aminopeptidase. Arch Insect Biochem Physiol 15: 149-163.
3. Bolter CJ, Jongsma MA (1995) Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase inhibitors induced in potato leaves by methyl jasmonate. J Insect Physiol 41: 1071-1078.
4. Bown DP, Wilkinson HS, Gatehouse JA (1997) Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem Mol Biol 27: 625-638.
5. Bozic N, Vujcic Z (2005) Detection and quantification of leucyl aminopeptidase after native electrophoresis using leucine ρ-nitroanilide. Electrophoresis 26: 2476-2480.
6. Bozic N, Vujcic Z, Nenadovic V, Ivanovic J (2003) Partial purification and characterization of midgut leucyl aminopeptidase of Morimus funereus (Coleoptera: Cerambycidae) larvae. Com Biochem Physiol 134B: 231-241.
7. Broadway RM (1995) Are insects resistant to plant proteinase inhibitors? J Insect Physiol 41: 107-116.
8. Broadway RM (1997) Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J Insect Physiol 43(9): 855-874.
9. Chougule NP, Hivrale VK, Chhabda PJ, Giri AP, Kachole MS (2003) Differential inhibition of Helicoverpa armigera guts proteinases by proteinase inhibitors of pigeonpea (Cajanus cajan) and its wild relatives. Phytochem 64: 681-687.
10. Chougule NP, Giri AP, Sainani MN, Gupta VS (2005) Gene expression patterns of Helicoverpa armigera gut proteases. Insect Biochem Mol Biol 35: 355-367.
11. Crava CM, Bel Y, Lee SF, Manachini B, Heckel DG, Escriche B (2010) Study of the aminopeptidase N gene family in the lepidopterans Ostrinia nubilalis (Hübner) and Bombyx mori (L.): sequences, mapping and expression. Insect Biochem Mol Biol 40 (7): 506-515.
12. Damle MS, Giri AP, Sainani MN, Gupta VS (2005) Higher accumulation of proteinase inhibitors in flowers than leaves and fruits as a possible basis for differential feeding preference of Helicoverpa armigera on tomato (Lycopersicon esculentum Mill, Cv. Dhanashree). Phytochem 66: 2659-2667.
13. Davis BJ (1964) Disc electrophoresis II. Methods and application to human serum. Ann N Y Acad Sci 121: 404-427.
14. Duan X, Li X, Xue Q, Abo-El-Saad M, Xu D, Wu R (1996) Transgenic rice plants harboring an introduced potato proteinase inhibitor gene II are insect resistant. Nature Biotech 14: 494-498.
15. Dunse KM, Kaas Q, Guarino RF, Barton PA, Craik DJ, Anderson MA (2010) Molecular basis for the resistance of an insect chymotrypsin toa potato type II proteinase inhibitor. Proc Nat Acad Sci USA 107: 15016-15021.
16. Feliocioli R, Garzelli B, Vaccari L, Melfi D, Balestreri E (1970) Activity staining of protein inhibitors of proteases on gelatin containing polyacrylamide gel electrophoresis. Anal Biochem 244: 176-178.
17. Ferreira C, Terra WR (1989) Spatial organization of digestion, secretary mechanism and digestive properties in Pheropsis aequinoctialis (Coleoptera: carabidae). Insect Biochem 19: 383-387.
18. Fitt GP (1989) The ecology of Heliothis species in relation to agro ecosystems. Ann Rev Entomol 34: 17-52.
19. Gatehouse LN, Shannon AL, Burgess EPJ, Christeller JT (1997) Characterization of major midgut proteinase cDNAs from Helicoverpa armigera larvae and changes in gene expression in response to four proteinase inhibitors in the diet. Insect Biochem Mol Biol 27: 929-944.
20. Gatehouse LN, Christeller JT, Gatehouse HS, Zou XY (2002) A strong inhibitor of chymotrypsin/elastase is highly antimetabolic to Helicoverpa armigera larvae. Biotech 55: 421-428.
21. Giri AP, Harsulkar AM, Deshpande VV, Sainani MN, Gupta VS, Ranjekar PK (1998) Chickpea defensive proteinase inhibitors can be inactivated by podborer gut proteinases. Plant Physiol 116: 393-401.
22. Giri AP, Harsulkar AM, Maurice SB, Gupta VS, Deshpande VV, Ranjekar PK, Francheschia VR (2003) Identification of potent inhibitors of Helicoverpa armigera gut proteinases from winged bean seeds. Phytochem 63: 523-532.
23. Harsulkar AM, Giri AP, Patankar AG, Gupta VS, Sainani MN, Ranjekar PK, Deshpande VV (1999) Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiol 121: 497-506.
24. Hilder VA, Gatehouse AMR, Seerman SE, Barker RF, Boulter D (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 300: 160-163.
25. Hivrale VK, Lomate PR, Kalve ND, Kachole MS (2011) Periplaneta americana midgut proteases differentially expressed against dietary components from different plant seeds. Physiol Entomol (In press). doi: 10. 1111/j. 1365-3032. 2011. 00784. x.
26. Jongsma MA, Bolter C (1997) The adaptation of insects to plant protease inhibitors. J Insect Physiol 43: 885-895.
27. Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekema WJ (1995) Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of midgut proteinase activity insensitive to inhibition. Proceed Nat Acad Sci USA 92: 8041-8045.
28. Kazzazi M, Bandani AR, Hosseibkhani S (2005) Biochemical characterization of α amylase of Sunn pest Eurygaster integriceps. Entomol Sci 8: 371-377.
29. Kotkar HM, Sarate PJ, Tamhane VA, Gupta VS, Giri AP (2009) Responses of midgut amylases of Helicoverpa armigera to feeding on various host plants. J Insect Physiol 55: 663-670.
30. Kranthi KR, Jadhav DR, Kranthi S, Wanjari RR, Ali SS, Russel DA (2002) Insecticide resistance in five major insect pests of cotton in India. Crop Prot 21: 449-460.
31. Lara P, Ortego F, Gonzalez-Hidalgo E, Castanera P, Carbonero P, Diaz I (2000) Adaptation of Spodoptera exigua (Lepidoptera: Noctuidae) to barley trypsin inhibitor BTI-CMe expressed in transgenic tobacco. Transgenic Res 9: 169-178.
32. Lee MJ, Anstee JH (1995) Characterization of midgut exopeptidase activity from larval Spodoptera littoralis. Insect Biochem Mol Biol 25: 63-71.
33. Lomate PR, Hivrale VK (2010) Partial purification and characterization of Helicoverpa armigera (Lepidoptera: Noctuidae) active aminopeptidase secreted in midgut. Com Biochem Physiol 155B: 164-170.
34. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 453-464.
35. Manjunath TM, Bhatnagar VS, Pawar CS, Sithanantham S (1989) Economic importance of Heliothis spp. in India and an assessment of their natural enemies and host plants. Proceedings of the workshop on biological control of Heliothis increasing the effectiveness of natural enemies, New Delhi, India, pp 197-228.
36. Nagarkatti S, Prakash A (1974) Rearing Heliothis armigera (Hubn) on artificial diet technical bulletin, vol 17. Commonwealth Institute of Biological Control, Bangalore.
37. Patankar AG, Giri AP, Harsulkar AM, Sainani MN, Deshpande VV, Ranjekar PK, Gupta VS (2001) Complexity in specificities and expression of Helicoverpa armigera gut proteinases explains polyphagous nature of the insect pest. Insect Biochem Mol Biol 31(4-4): 453-464.
38. Rajapakse CNK, Walter GH (2007) Polyphagy and primary host plants: oviposition preference versus larval performance in the lepidopteran pest Helicoverpa armigera. Arthropod-Plant Int 1: 17-26.
39. Sivakumar S, Mohan M, Franco OL, Thayumanavan B (2006) Inhibition of insect pest α-amylases by little and finger millet inhibitors. Pest Biochem Physiol 85: 155-160.
40. Srinivasan A, Chougule NP, Giri AP, Gatehouse JA, Gupta VS (2005) Podborer (Helicoverpa armigera Hubn.) does not show specific adaptations in gut proteinases to dietary Cicer arietinum Kunitz proteinase inhibitor. J Insect Physiol 51: 1268-1276.
41. Tamhane VA, Chougule NP, Giri AP, Dixit AR, Sainani MN, Gupta VS (2005) In vivo and in vitro effect of Capsicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases. Biochim Biophys Acta 1722(2): 156-167.
42. Tamhane VA, Giri AP, Sainani MN, Gupta VS (2007) Diverse forms of Pin-II family proteinase inhibitors from Capsicum annuum adversely affect the growth and development of Helicoverpa armigera. Gene 403: 29-38.
43. Telang M, Srinivasan A, Patankar A, Harsulkar A, Joshi V, Damle A, Deshpande V, Sainani M, Ranjekar P, Gupta G, Birah A, Rani S, Kachole M, Giri AP, Gupta V (2003) Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochem 63(6): 643-652.
44. Terra WR, Ferreira C (1994) Insect digestive enzymes, compartmentalization and function. Com Biochem Physiol 109B: 1-61.
45. Vila L, Quilis J, Meynard D, Breitler JC, Marfa V, Murillo I, Vassal JM, Messeguer J, Guiderdoni E, Segundo BS (2005) Expression of the maize proteinase inhibitor (mpi) gene in rice plants enhances resistance against the striped stem borer (Chilo suppressalis): effects on larval growth and insect gut proteinases. Plant Biotechnol J 3: 187-202.
46. Volpicella M, Ceci LR, Gallerani R, Jongsma MA, Beekwilder J (2001) Functional expression on bacteriophage of the mustard trypsin inhibitor MTI-2. Biochem Biophys Res Comm 280(3): 813-817.
47. Zhang S, Cheng H, Gao Y, Wang G, Liang G, Wu K (2009) Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochem Mol Biol 39: 421-429.