African Journal of
Plant Science

  • Abbreviation: Afr. J. Plant Sci.
  • Language: English
  • ISSN: 1996-0824
  • DOI: 10.5897/AJPS
  • Start Year: 2007
  • Published Articles: 729

Full Length Research Paper

Expression of Cocculus hirsutus trypsin inhibitor promotes endogenous defensive response against Helicoverpa armigera and enhanced levels of antioxidants

Manushree V.
  • Manushree V.
  • Department of Plant Biotechnology, University of Agricultural Sciences, GKVK, Bangalore- 560065, India.
  • Google Scholar
Devaraj V. R.
  • Devaraj V. R.
  • Department of Biochemistry, Central College Campus, Bangalore University, Bangalore-560001, India.
  • Google Scholar
Prasad D. T.
  • Prasad D. T.
  • Department of Plant Biotechnology, University of Agricultural Sciences, GKVK, Bangalore- 560065, India.
  • Google Scholar


  •  Received: 28 November 2019
  •  Accepted: 30 January 2020
  •  Published: 29 February 2020

References

Anderson P, Anton S (2014). Experience-based modulation of behavioral responses to plant volatiles and other sensory cues in insect herbivores. Plant Cell Environment 7:1820-1835.
Crossref

 

AOAC Ascorbic acid, in Official Methods of Analysis (2006). AOAC International, Gaithersburg, MD. 967.21.

 
 

AOAC, Titratable acidity of fruit products, in Official Methods of Analysis. (2000). 17 edn- AOAC International, Gaithersburg MD. 942.15.

 
 

Bacha AB, Jemel I, Moubayed NMS (2017). Purification and characterization of newly serine protease inhibitor from Rhamnus frangula with potential for use as therapeutic drug 3. Biotech 7:1-13.
Crossref

 
 

Benzie IF, Strain JJ (1996). The ferric reducing ability of plasma (FRAP) as a measure of 'antioxidant power': the FRAP assay. Annals of Biochemistry 23:70-76.
Crossref

 
 

Bhattacharjee C, Manjunath NH, Prasad DT (2010). Purification of a trypsin inhibitor from Cocculus hirsutus and identification of its biological activity. Journal of Crop Science and Biotechnology 12:253-260.
Crossref

 
 

Burge J, Mickelsen O, Nicklow C, Marsh LG (1975). Vitamin C in tomatoes: Comparison of tomatoes developed for mechanical or hand harvesting. Ecology of Food Nutrition 4:27-31.
Crossref

 
 

Chikate YR, Tamhane VA, Joshi RS, Gupta VS, Giri AP (2013). Differential protease activity augments polyphagy in Helicoverpa armigera. Insect Molecular Biology 22:258-272.
Crossref

 
 

Clemente M, Corigliano MG, Pariani SA, Sánchez-López EF, Sander VA, Ramos-Duarte VA (2019). Plant serine protease inhibitors: Biotechnology application in agriculture and molecular farming. International Journal of Molecular Sciences 20:1345-1366.
Crossref

 
 

Cloutier C, Jean C, Fournier M, Yelle S, Michaud D (2000). Adult Colorado Potato Beetles, Leptinotarsa decemlineata compensate for nutritional stress on Oryzacystatin I transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Archives of Insect Biochemistry 44:69-81.
Crossref

 
 

De Leo F, Volpicella M, Licciulli F, Liuni S, Gallerani R, Ceci LR (2002). PLANT-PIs: A database for plant protease inhibitors and their genes. Nucleic Acids Research 30:347-348.
Crossref

 
 

Doyle JJ, Doyle JL (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11-15.

 
 

Dunse KM, Stevens JA, Lay FT, Gaspar YM, Heath RL, Anderson MA (2010). Co-expression of potato type I and II proteinase inhibitors gives cotton plants protection against insect damage in the field. Proceedings of the National Academy of Sciences, USA 107:15011-15015.
Crossref

 
 

Filho JX, Moreira RDA (1978). Visualization of proteinase inhibitors in SDS-polyacrylamide gels. Annals of Biochemistry 84:296-299.
Crossref

 
 

Fluhr R, Lampl N, Roberts TH (2012). Serpin protease inhibitors in plant biology. Physiologia Plantarum 145:95-102.
Crossref

 
 

Gatehouse JA (2011). Prospects for using proteinase inhibitors to protect transgenic plants against attack by herbivorous insects. Current Protein and Peptide Science 12: 409-416.
Crossref

 
 

Ghorbani S, Hoogewijs K, Pečenková T, Fernandez A, Inzé A, Eeckhout D, Kawa D, De Jaeger G, Beeckman T, Madder A, Breusegem FV, Hilson P (2016). The SBT6.1 subtilase processes the GOLVEN1 peptide controlling cell elongation. Journal of Experimental Botany 67:4877-4887.
Crossref

 
 

Giri AP, Harsulkar AM, Deshpande VV, Sainani MN, Gupta VS, Ranjekar PK (2002). Chickpea defensive proteinase inhibitors can be inactivated by pod borer gut proteinases. Plant Physiology 116:393- 401.
Crossref

 
 

Golla SK, Rajasekhar P, Akbar SMD, Sharma HC (2018). Proteolytic activity in the midgut of Helicoverpa armigera (Noctuidae: Lepidoptera) larvae fed on wild relatives of chickpea, Cicer arietinum. Journal of Economic Entomology 111:2409-2415.
Crossref

 
 

Goulet MC, Dallaire C, Vaillancourt LP, Khalf M, Badri MA, Preradov A, Duceppe MO, Goulet C, Cloutier C, Michaud D (2008). Tailoring the specificity of a plant cystatin toward herbivorous insect digestive cysteine proteases by single mutations at positively selected amino acid sites. Plant Physiology 146:1010-1019.
Crossref

 
 

Gutiérrez-Campos R, Torres-Acosta JA, Pérez-Martínez JDJ (2001). Pleiotropic Effects in Transgenic Tobacco Plants Expressing the Oryzacystatin I Gene. Horticulture Sciences 36:118-119.
Crossref

 
 

Habib H, Fazili KM (2007). Plant protease inhibitors: A defense strategy in plants. Biotechnology and Molecular Biology 2:68-85.

 
 

Harsulkar AM, Giri AP, Patankar AG, Gupta VS, Sainani MN, Ranjekar PK, Deshpande VV (2002). Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiology 121:497-506.
Crossref

 
 

Haruta M, Major IT, Christopher ME, Patton JJ, Constabel CP (2001). A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.) : cloning, functional expression, and induction by wounding and herbivory. Plant Molecular Biology 46:347-359.
Crossref

 
 

Jamal F, Pandey PK, Singh D, Khan MY (2013). Serine protease inhibitors in plants: Nature's arsenal crafted for insect predators. Phytochemistry Review 12:1-34.
Crossref

 
 

Johnston KA, Lee ML, Gatehouse JA, Anstee JH (1991). The partial purification and characterisation of serine protease activity in midgut of larval Helicoverpa armigera. Insect Biochemistry 21:389-397.
Crossref

 
 

Jyothishwaran G, Kotresha D, Selvaraj T, Srideshikan S, Rajvanshi P, Jayabaskaran C (2007). A modified freeze thaw method for efficient transformation of Agrobacterium tumefaciens. Current Sciences 93:770-772.

 
 

Kakade ML, Simons N, Liener IE (1969). An evaluation of natural and synthetic substrates for the antitryptic activity of soybean samples. Cereal Chemistry 46:518-522.

 
 

Kansal R, Kumar M, Kuhar K, Gupta RN, Subrahmanyam B, Koundal KR, Gupta VK (2009). Purification and characterization of trypsin inhibitor from Cicerarietinum L. and its efficacy against Helicoverpa armigera. Brazilian Journal of Plant Physiology 20:313-322.
Crossref

 
 

Kim JY, Park SC, Hwang I (2009). Protease inhibitors from plants with antimicrobial activity. International Journal of Molecular Sciences 10:2860-2872.
Crossref

 
 

Kuwar SS, Pauchet Y, Vogel H, Heckel DG (2015). Adaptive regulation of digestive serine proteases in the larval midgut of Helicoverpa armigera in response to a plant protease inhibitor. Insect Biochemistry and Molecular Biology 59:18-29.
Crossref

 
 

Laluk K, Mengiste T (2011). The Arabidopsis extracellular unusual serine protease inhibitor functions in resistance to necrotrophic fungi and insect herbivory. The Plant Journal 68:480-494.
Crossref

 
 

Lichtenthaler HK (1987). Chlorophylls and carotenoids: pigments of photosynthetic bio-membranes. Methods in Enzymology 148:350-382.
Crossref

 
 

Lomate PR, Dewangan V, Mahajan NS, Yashwant K, Kulkarni A, Wang L, Saxena LS, Gupta VS, Giri AP (2018). Integrated transcriptomic and proteomic analyses suggest the participation of endogenous protease inhibitors in the regulation of protease gene expression in Helicoverpa armigera. Molecular and Cellular Proteomics 17:1324-1336.
Crossref

 
 

Manamohan M, Prakash MN, Chandra GS, Asokan R, Nagesha SN (2011). An improved protocol for rapid and efficient Agrobacterium mediated transformation of tomato (Solanumlycopersicum L.). Journal of Applied Horticulture 13:3-7.

 
 

Munger A, Coenen K, Cantin L, Goulet C, Vaillancourt LP, Goulet MC, Tweddell R, Sainsbury F, Michaud D (2012). Beneficial 'unintended effects' of a cereal cystatin in transgenic lines of potato (Solanum tuberosum). BMC Plant Biology 12:1-12.
Crossref

 
 

Ntagkas N, Woltering E, Bouras S, De Vos RCH, Dieleman JA, Nicole CCS, Labrie C, Marcelis, LFM (2019). Light-induced vitamin C accumulation in tomato fruits is independent of carbohydrate availability. Plants 8:86.
Crossref

 
 

Papolu PK, Dutta TK, Tyagi N, Urwin PE, Lilley CJ, Rao U (2016). Expression of a cystatin transgene in eggplant provides resistance to root-knot nematode, Meloidogyne incognita. Frontiers in Plant Sciences 1122:1-9.
Crossref

 
 

Parde VD, Sharma HC, Kachole MS (2010). In vivo inhibition of Helicoverpa armigera gut pro-proteinase activation by non-host plant protease inhibitors. Journal of Insect Physiology 56:1315-1324.
Crossref

 
 

Pariani S, Contreras M, Rossi FR, Sander V, Corigliano MG, Simón F, Busi MV, Gomez-Casati DF, Pieckenstain FL, Duschak VG (2016). Characterization of a novel Kazal-type serine proteinase inhibitor of Arabidopsis thaliana. Biochimie 123:85-94.
Crossref

 
 

Quilis J, Meynard D, Vila L, Aviles FX, Guiderdoni E, Segundo BS (2007). A potato carboxypeptidase inhibitor gene provides pathogen resistance in transgenic rice. Plant Biotechnology Journal 5:537-553.
Crossref

 
 

Rustgi S, Boex-Fontvieille E, Reinbothe C, Wettstein DV, Reinbothe S (2017). Serpin1 and WSCP differentially regulate the activity of the cysteine protease RD21 during plant development in Arabidopsis thaliana. Proceedings of National Academy of Sciences. USA 114:2212-2217.
Crossref

 
 

Sambrook J, Fritish EF, Maniatis T (1989). Molecular cloning. A laboratory manual. 2nd Ed. Cold Spring Harbour Laboratory Press, USA.

 
 

Santamaria ME, Diaz-Mendoza M, Diaz I, Martinez M (2014). Plant protein peptidase inhibitors: an evolutionary overview based on comparative genomics. BMC Genomics 15:812-826.
Crossref

 
 

Schluter U, Benchabane M, Munger A, Kiggundu A, Vorster J, Goulet MC, Cloutier C, Michaud D (2010). Recombinant protease inhibitors for herbivore pest control: a multitrophic perspective. Journal of Experimental Botany 61:4169-4183.
Crossref

 
 

Singleton VL, Rossi JA (1965). A colorimetry of total phenolics with phosphomolybdic -phosphotungstic acid reagents. American Journal of Enology and Viticulture 16:144-158.

 
 

Somayaji P, Prasad DT, Shivanna MB (2014). Agrobacterium-mediated transformation for development of transgenic tomato with ySAMdc gene. Indian Journal of Biotech 13:19-25.

 
 

Song SC, Yu JH, Hester PY, Kim KI (1985). Antibodies to the alpha subunit of insulin receptor from eggs of immunized hens. The Journal of Immunology 135:3354-3359.

 
 

Srinivasan A, Giri AP, Harsulkar AM, Gatehouse JA, Gupta VS (2005). A Kunitz trypsin inhibitor from chickpea (Cicerarietinum L.) that exerts anti-metabolic effect on podborer (Helicoverpa armigera) larvae. Plant Molecular Biology 57:359-374.
Crossref

 
 

Stout MJ, Fidantsef AL, Duffey SS, Bostock RM (1999). Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato (Lycopersicon esculentum). Physiology and Molecular Plant Pathology 54:115-130.
Crossref

 
 

Tamayo MC, Rufat M, Brava JM, Segundo BS (2000). Accumulation of a maize proteinase inhibitor in response to wounding and insect feeding, and characterization of its activity toward digestive proteinases of Spodoptera littoralis larvae. Planta 211:62-71.
Crossref

 
 

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. Biochimica et Biophysica Acta 1722:156-167.
Crossref

 
 

Tang QB, Jiang JW, Yan YH, Van Loon JJA, Wang CZ (2006). Genetic analysis of larval host-plant preference in two sibling species of Helicoverpa. Entomologia Experimentalis et Applicata 118:221-228.
Crossref

 
 

Tanpure RS, Barbole RS, Dawkar VV, Waichal YA, Joshi RS, Giri AP, Gupta VS (2017). Improved tolerance against Helicoverpa armigera in transgenic tomato over-expressing multi-domain proteinase inhibitor gene from Capsicum annuum. Physiology and Molecular Plant pathology 23:597-604.
Crossref

 
 

Thomas JC, Wasmann CC, Echt C, Dunn RL, Bohnert HJ, Mccoy TJ (1994). Introduction and expression of an insect proteinase inhibitor in alfalfa Medicagosativa L. Plant Cell Reports, pp. 31-36.
Crossref

 
 

Tittonell P, Degrazia J, Chiesa A (2001). Effect of nitrogen fertilization and plant population during growth on lettuce (Lactucasativa L.) postharvest quality. Proceedings of the Fourth International Conference on Postharvest Science, Acta Horticulturae 553:67-68.
Crossref

 
 

Toor RK, Savage GP (2005). Antioxidant activity in different fractions of tomatoes. Food Research International 38:487-494.
Crossref

 
 

Turra D, Bellin D, Lorito M, Gebhardt C (2009). Genotype-dependent expression of specific members of potato protease inhibitor gene families in different tissues and in response to wounding and nematode infection. Journal of Plant Physiology 166:762-774.
Crossref

 
 

Vieira P, Wantoch S, Lilley CJ, Chitwood DJ, Atkinson HJ, Kamo K (2015). Expression of a cystatin transgene can confer resistance to root lesion nematodes in Lilium longiflorum cv. 'Nellie White'. Transgenic Research 24:421- 432.
Crossref

 
 

Wang Y, Ma Y, Zhou DS, Gao SX, Zhao XC, Tang QB, Wang CZ, Van Loon JJA (2017). Higher plasticity in feeding preference of a generalist than a specialist: Experiments with two closely related Helicoverpa species. Scientific Reports 7:1-12.
Crossref

 
 

War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012). Mechanism of plant defense against insect herbivores. Plant Signaling and Behavior 7:1306- 1320.
Crossref

 
 

Wingate VPM, Franceschi VR, Ryan CA (2008). Tissue and Cellular Localization of Proteinase Inhibitors I and II in the Fruit of the Wild Tomato, Lycopersicon peruvianum (L.) Mill. Plant Physiology 97:490- 495.
Crossref

 
 

Winterer J, Bergelson J (2001). Diamondback moth compensatory consumption of protease inhibitor-transformed plants. Molecular Ecology 10:1069-1074.
Crossref

 
 

Wu J, Baldwin IT (2010). New Insights into Plant Responses to the Attack from Insect Herbivores. Annual Review of Genetics 44:1- 24.
Crossref

 
 

Wu Y, Llewellyn D, Mathews A, Elizabeth S (1997). Adaptation of Helicoverpa armigera (Lepidoptera: Noctuidae) to a proteinase inhibitor expressed in transgenic tobacco. Molecular Breeding, pp. 371-380.
Crossref

 
 

Yang F, Zhang Y, Huang Q, Yin G, Pennerman KK, Yu J, Liu Z, Li D, Guo A (2015). Analysis of key genes of jasmonic acid mediated signal pathway for defense against insect damages by comparative transcriptome sequencing. Scientific Reports 5:1-12.
Crossref

 
 

Zhu-Salzman K, Koiwa H, Salzman RA, Shade RE, Ahn JE (2003). Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Molecular Biology 12:135-145.
Crossref