Isolation and in vitro identification of proteinase inhibitors from soybean seeds inhibiting helicoverpa gut proteases

References

• Ahmad , Z , Saleemuddin , M and Siddi , M . 1980 . Purification and characterization of three alkaline proteases from the gut of the larva of army worm, Spodoptera litura . Insect Biochem. , 10 : 667 – 673 .
   Google Scholar
• Armes , NJ , Jadhav , DR and DeSouza , KR . 1996 . A survey of insecticide resistance in Helicoverpa armigera in the Indian subcontinent . Bull Entomol Res. , 86 : 499 – 514 .
   Web of Science ®Google Scholar
• Babu , SR and Subrahmanyam , B . 2010 . Bio-potency of serine proteinase inhibitors from Acacia senegal seeds on digestive proteinases, larval growth and development of Helicoverpa armigera (Hübner) . Pest Biochem Physiol. , 98 : 349 – 358 .
   Web of Science ®Google Scholar
• Barton , K , Whitely , H and Yang , NS . 1987 . Bacillus thuringiensis δ-endotoxin in transgenic Nicotiana tabacum provides resistance to lepidopteran insects . Plant Physiol. , 85 : 1103 – 1109 .
   PubMed Web of Science ®Google Scholar
• Birk , Y . 2003 . Plant protease inhibitors: significance in nutrition, plant protection, cancer prevention and genetic engineering , 170 Berlin : Springer .
   Google Scholar
• Bonade-Bottino , M , Lerin , J , Zaccomer , B and Jouanin , L . 1999 . Physiological adaptation explains the insensitivity of Baris coerulescens to transgenic oilseed rape expressing oryzacystatin I . Insect Biochem Mol Biol. , 29 : 131 – 138 .
   Web of Science ®Google Scholar
• Bradford , MM . 1976 . A rapid and sensitive method for the quantitation of microgram of quantities of protein utilizing the principal of protein-dye binding . Anal Biochem. , 72 : 248 – 254 .
   PubMed Web of Science ®Google Scholar
• Broadway , RM . 1995 . Are insects resistant to plant proteinase inhibitors? . J Insect Physiol. , 41 : 107 – 116 .
   Web of Science ®Google Scholar
• Broadway , RM . 1996 . Dietary proteinase inhibitors alter complement of midgut proteases . Arch Insect Biochem Physiol. , 32 : 39 – 53 .
   Web of Science ®Google Scholar
• Broadway , RM . 1997 . Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors . J Insect Physiol. , 43 : 855 – 874 .
   PubMed Web of Science ®Google Scholar
• Brock , RM , Forsberg , CW and Buchanan-Smith , JG . 1982 . Proteolytic activity of rumen microorganisms and effect of proteinase inhibitors . Appl Environ Microbiol. , 44 : 561 – 569 .
   PubMed Web of Science ®Google Scholar
• Brousseau R , Masson L , Hegedus D. 1999 . Insecticidal transgenic plants: are they irresistible? Review. AgBiotechNet July, ABN022 CAB International , UK , 22 .
   Google Scholar
• Brzin , J and Kidric , M . 1995 . Proteinases and their inhibitors in plants: role in normal growth and in response to various stress conditions . Biotechnol Genet Eng Rev. , 13 : 421 – 467 .
   Web of Science ®Google Scholar
• Christeller , JT , Laing , WA , Markwick , NP and Burgess , EP . 1992 . Midgut protease activities in 12 phytophagous lepidopteran larvae: dietary and protease inhibitor interactions . Insect Biochem Mol Biol. , 22 ( 7 ) : 735 – 746 .
   Web of Science ®Google Scholar
• Cloutier , C , Fournier , M , Jean , C , Yelle , S and Michaud , D . 1999 . Growth compensation and faster development of Colorado potato beetle (Coleoptera: Chrysomelidae) feeding on potato foliage expressing oryzacystatin I . Arch Insect Biochem Physiol. , 40 : 69 – 79 .
   Web of Science ®Google Scholar
• Cloutier , C , Jean , C , Fournier , M , Yelle , S and Michaud , D . 2000 . Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behaviour and overproduction of insensitive proteases . Arch Insect Biochem Physiol. , 44 : 69 – 81 .
   PubMed Web of Science ®Google Scholar
• Duan , X , Li , X , Xue , Q , Abo-el-saad , M , Xu , D and Wu , R . 1996 . Transgenic rice plants harbouring an introduced potato inhibitor II gene are insect resistant . Nat Biotechnol. , 14 : 494 – 498 .
   PubMed Web of Science ®Google Scholar
• Frutos , R , Rang , C and Royer , M . 1999 . Managing insect resistance to plants producing Bacillus thuringiensis toxins . Crit Rev Biotechnol. , 19 : 227 – 276 .
   Web of Science ®Google Scholar
• Gatehouse , AMR , Shi , Y , Powell , KS , Brough , C , Hilder , VA , Hamilton , WDO , Newell , CA , Merryweather , A , Boulter , D and Gatehouse , JA . 1993 . Approaches to insect resistance using transgenic plants . Phil Trans R Soc Lond. , B342 : 279 – 286 .
   Web of Science ®Google Scholar
• Girard , C , Le Metayer , M , Bonade-Bottino , M , Pham-Delegue , MH and Jouanin , L . 1998 . High level of resistance to proteinase inhibitors may be conferred by proteolytic cleavage in beetle larvae . Insect Biochem Mol Biol. , 28 : 229 – 237 .
   PubMed Web of Science ®Google Scholar
• Giri , AP , Harsulkar , AM , Deshpande , VV , Sainani , MN , Gupta , VS and Ranjekar , PK . 1998 . Chickpea defensive proteinase inhibitors can be inactivated by podborer gut proteinases . Plant Physiol. , 116 : 393 – 401 .
   Web of Science ®Google Scholar
• Giri , AP and Kachole , MS . 1998 . Amylase inhibitors of pigeonpea (Cajanus cajan L.) seeds . Phytochemistry. , 47 : 197 – 202 .
   PubMed Web of Science ®Google Scholar
• Haq , SK , Atif , SM and Khan , RH . 2004 . Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: natural and engineered phytoprotection . Arch Biochem Biophys. , 431 : 145 – 159 .
   PubMed Web of Science ®Google Scholar
• Harsulkar , AM , Giri , AP , Gupta , VS , Sainani , MN , Deshpande , VV , Patankar , AG and Ranjekar , PK . 1998 . Characterization of Helicoverpa armigera gut proteinases and their interaction with proteinase inhibitors using gel–X-ray film contact print technique . Electrophoresis. , 19 : 1397 – 1402 .
   PubMed Web of Science ®Google Scholar
• Harsulkar , AM , Giri , AP , Patankar , AG , Gupta , VS , Sainani , MN , Ranjekar , PK and Deshpande , VV . 1999 . Successive use of non host Plant proteinase inhibitors Required for effective inhibition of Helicovrpa armigera gut proteinases and larval growth . Plant Physiol. , 121 : 497 – 506 .
   PubMed Web of Science ®Google Scholar
• Hilder , VA and Boulter , D . 1999 . Genetic engineering of crop plants for insect resistance – a critical review . Crop Protect. , 18 : 177 – 191 .
   Web of Science ®Google Scholar
• Hilder , VA , Gatehouse , AMR and Boulter , D . 1992 . “ Transgenic plants conferring insect tolerance: protease inhibitor approach ” . In Transgenic plants , Edited by: Kung , S and Wu , R . 310 – 338 . New York (NY) : Academic Press .
   Google Scholar
• Hilder , VA , Gatehouse , AMR , Sheerman , SE , Barker , RF and Boulter , DA . 1987 . A novel mechanism of insect resistance engineered into tobacco . Nature. , 300 : 160 – 166 .
   Web of Science ®Google Scholar
• Hoffmann , MP , Zalom , FG , Wilson , LT , Smilanick , JM , Malyj , LD , Kiser , J , Hilder , VA and Barnes , WM . 1992 . Field evaluation of transgenic tobacco containing genes encoding Bacillus thuringiensis δ-endotoxin or cowpea trypsin inhibitor: efficacy against Helicoverpa zea (Lepidoptera: Noctuidae) . J Econ Entomol. , 85 : 2516 – 2522 .
   Web of Science ®Google Scholar
• Johnson , R , Narvaez , J , An , G and Ryan , C . 1989 . Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexto larvae . Proceedings of the National Academy of Sciences USA , 86 : 9871 – 9875 .
   PubMed Web of Science ®Google Scholar
• Johnston , KA , Lee , MJ , Brough , C , Hilder , VA , Gatehouse , AMR and Gatehouse , JA . 1995 . Protease activities in the larval midgut of Heliothis virescens: evidence for trypsin and chymotrypsin-like enzymes . Insect Biochem Mol Biol. , 25 ( 3 ) : 375 – 383 .
   Web of Science ®Google Scholar
• Jongsma , MA , Bakker , PL , Peters , J , Bosch , D and Stiekema , WJ . 1995 . Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition . Proc Natl Acad Sci USA. , 92 : 8041 – 8045 .
   PubMed Web of Science ®Google Scholar
• Jouanin , L , Bonade-Bottino , M , Girard , C , Morrot , G and Giband , M . 1998 . Transgenic plants for insect resistance . Plant Sci. , 131 : 1 – 11 .
   Web of Science ®Google Scholar
• Kranthi , KR , Kranthi , S , Ali , S and Banerjee , SK . 2000 . Resistance to Cry1Ac δ-endotoxin of Bacillus thuringiensis in a laboratory selected strain of Helicoverpa armigera (Hübner) . Curr Sci. , 78 : 1001 – 1004 .
   Web of Science ®Google Scholar
• Kumar PA. 2004 . Cautious use of Bt genes in transgenic crops . Curr Sci . 86 : 632 – 633 .
   Web of Science ®Google Scholar
• Laemmli , UK . 1970 . Cleavage of structural proteins during the assembly of the head of bacteriophage T4 . Nature. , 227 : 680 – 685 .
   PubMed Web of Science ®Google Scholar
• Leple , JC , Bonade-Bottino , M , Augustin , S , Pilate , G , Dumanois Le Tan , V , Delplanque , A , Cornu , D and Jouanin , L . 1995 . Toxicity to Chrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteineproteinase inhibitor . Mol Breed. , 1 : 319 – 328 .
   Web of Science ®Google Scholar
• Lewis , WJ , van Lenteren , JC , Phatak , SC and Tumlinson , III JH . 1997 . A total system approach to sustainable pest management . Proc Natl Acad Sci USA. , 94 : 12243 – 12248 .
   PubMed Web of Science ®Google Scholar
• Liota , LA and Stetler-stevenson , WG . 1990 . Cancer Biol. , 1 : 96 – 106 .
   Google Scholar
• Liu , Y , Sui , YP , Wang , JX and Zhao , XF . 2009 . Characterization of the trypsin-like protease (Ha-TLP2) constitutively expressed in the integument of the cotton bollworm, Helicoverpa armigera . Arch Insect Biochem Physiol. , 72 : 74 – 87 .
   PubMed Web of Science ®Google Scholar
• Manjunath TM , Bhatnagar VS , Pawar CS , Sithanantham S. 1989 . Economic importance of Heliothis spp. in India and assessment of their natural enemies and host plants . In King EG , Jackson RD , Proceedings of the Workshop on Biological Control of Heliothis: Increasing the Effectiveness of Natural Enemies. Far Eastern Regional Research Office , US Department of Agriculture , New Delhi , , India , 197 – 228 .
   Google Scholar
• Mayee CD. 2009 . Biotech cotton in India: current status and impact on textile industry . Proc Indian Natl Sci Acad . 79 : 195 – 211 .
   Google Scholar
• McManus , MT , White , DWR and McGregor , PG . 1994 . Accumulation of a chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests . Transgenic Res. , 3 : 50 – 58 .
   Web of Science ®Google Scholar
• Michaud , D . 1997 . Avoiding protease-mediated resistance in herbivorous pests . Trends Biotechnol. , 15 : 4 – 6 .
   Web of Science ®Google Scholar
• Mosolov , VV , Grigor'eva , LI and Valueva , TA . 2001 . Plant proteinase inhibitors as multifunctional proteins . Appl Biochem Microbiol (Moscow) , 37 : 643 – 650 .
   Google Scholar
• Mulimani , VH , Sudheendra , K and Giri , AP . 2002 . Detection of legume protease inhibitors by Gel-X-ray film contact print technique . Biochem Mol Biol Educ. , 30 : 40 – 44 .
   Web of Science ®Google Scholar
• Oliveira , AS , Pereira , RA , Lima , LM , Morais , AHA , Melo , FR , Franco , OL , Bloch , C Jr , Grossi-de-Sa , MF and Sales , MP . 2002 . Activity toward bruchid pest of a kunitz-type inhibitor seeds of the Algaroba tree (Prosopis juliflora D.C.) . Pest Biochem Physiol. , 72 : 122 – 132 .
   Web of Science ®Google Scholar
• Panda , N and Khush , GS . 1995 . Host plant resistance to insects , Oxon (London) : International Irrigation Information Center .
   Google Scholar
• Parde , VD , Sharma , HC and Kachole , MS . 2010 . In vivo inhibition of Helicoverpa armigera gut pro-proteinase activation by non-host plant protease inhibitors . J Insect Physiol. , 56 : 1315 – 1324 .
   PubMed Web of Science ®Google Scholar
• Patankar , AG , Harsulkar , AM , Giri , AP , Gupta , VS , Sainani , MN , Ranjekar , PK and Deshpande , VV . 1999 . Diversity in inhibitors of trypsin and Helicoverpa armigera gut proteinases in cheakpea (Cicer arientinum) and its wild relatives . Theor Appl Genet. , 99 : 719 – 726 .
   PubMed Web of Science ®Google Scholar
• Pichare , MM and Kachole , MS . 1994 . Detection of electrophoretically separated protease inhibitors using X-ray film . J Biochem Biophys Methods. , 28 : 215 – 224 .
   PubMedGoogle Scholar
• Schuler , TH , Poppy , GM , Kerry , BR and Denholm , I . 1998 . Insect resistant transgenic plants . Trends Biotechnol. , 16 : 168 – 175 .
   Web of Science ®Google Scholar
• Shewry , PR . 2003 . Tuber storage proteins . Ann Bot. , 91 : 755 – 769 .
   PubMed Web of Science ®Google Scholar
• Srinivasan , A , Giri , AP and Gupta , VS . 2006 . Structural and functional diversities in lepidopteran serine proteases . Cell Mol Biol Lett. , 11 : 132 – 154 .
   PubMed Web of Science ®Google Scholar
• Srinivasan , A , Giri , AP , Harsulkar , AM , Gatehouse , JA and Gupta , VS . 2005 . A Kunitz trypsin inhibitor from chickpea (Cicer arietinum L.) that exerts anti-metabolic effect on podborer (Helicoverpa armigera) larvae . Plant Mol Biol. , 57 ( 3 ) : 359 – 374 .
   PubMed Web of Science ®Google Scholar
• Tamhane , VA , Chaugule , NP , Giri , AP , Dixit , AR , Sainani , MN and Gupta , VS . 2005 . In vivo and in vitro effect of Capssicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases . Biochimica et Biophysica Acta. , 1722 : 156 – 167 .
   PubMed Web of Science ®Google Scholar
• Urwin , PE , Atkinson , HJ , Waller , DA and McPherson , MJ . 1995 . Engineered oryzacystatin I expressed in transgenic hairy roots confers resistance to Globodera pallida . Plant J. , 8 : 121 – 131 .
   PubMed Web of Science ®Google Scholar
• Vinokorov , KS , Oppert , B and Elpidina , EN . 2005 . An overlay technique for postelectrophoretic analysis of proteinase spectra in complex mixtures using p-nitroanilide substrates . Anal Biochem. , 337 : 164 – 166 .
   PubMed Web of Science ®Google Scholar