Partially purified Glycine max proteinase inhibitors: potential bioactive compounds against tobacco cutworm, Spodoptera litura (Fabricius, 1775) (Lepidoptera: Noctuidae)

Partially purified Glycine max proteinase inhibitors: potential bioactive compounds against tobacco cutworm, Spodoptera litura (Fabricius, 1775) (Lepidoptera: Noctuidae)

Spodoptera litura (Fabricius, 1775), a polyphagous defoliator with broad host spectrum, causes significant damage to agriculturally important crops. Serine protease is primarily responsible for most of the proteolytic activity in the larval gut of lepidopteran insects. Second-instar larvae were reared on an artificial diet containing serine trypsin inhibitor partially purified from Glycine maxseeds. Different concentrations were amended in the diet, i.e. 25, 50, 100, 200, and 400 μg/mL. The larval development period, total developmental period, longevity, fecundity, larval weight, and mean relative growth rate were decreased at the 100 μg/mL concentration. However, with further increase in concentration, the above parameters were all found to increase. Nutritional indices revealed reduction in efficiency of conversion of digested food and approximate digestibility, whereas increase in efficiency of conversion of ingested food had significant influence on food assimilation. Trypsin activity was suppressed at 100 μg/mL with increase in exposure interval. Results reveal that soybean protease inhibitor inhibited S. litura gut proteinase and it was more effective at lower concentrations. Thus, low levels of inhibitor would be enough to affect the growth and development of the target pest for the development of transgenic plants.

___

  • Andow DA (2008). The risk of resistance evolution in insects to transgenic insecticidal crops. Collection of Biosafety Reviews 4: 142–199.
  • Armes NJ, Wightman JA, Jadhav DR, Rao GVR (1997). Status of insecticides resistance in Spodoptera litura in Andhra Pradesh, India. Pest Sci 50: 240–248.
  • Bhavani P, Bhattacherjee C, Prasad DT (2007). Bioevaluation of Subabul (Leucaena leucocephala) proteinase inhibitors on Helicoverpa armigera. Arthropod-Plant Interact 1: 255–261.
  • Boulter D (1993). Insect pest control by copying nature using genetically engineered crops. Phytochemistry 34: 1453–1466.
  • Broadway RM, Duffey SS (1986). The effect of dietary protein on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. J Insect Physiol 32: 673–680.
  • Christeller JT, Laing WA, Markwick NP, Burgess EPJ (1992). Midgut protease activities in 12 phytophagous lepidopteran larvae: dietary and protease inhibitor interactions. Insect Biochem Molec 22: 735–746.
  • Christeller JT, Laing WA, Shaw BD, Burgess EPJ (1990). Characterization and partial purification of the digestive proteases of the black field cricket, Telleogryllus commodus(Walker): elastase is a major component. Insect Biochem 20: 157–164.
  • De Leo F, Bonade-Bottino MA, Ceci LR, Gallerani R, Jouanin L (2001). Effects of mustard trypsin inhibitor expressed in different plants on three lepidopteran pests. Insect Biochem Molec 31: 593–602.
  • Dorrah MA (2004). Effect of soybean trypsin inhibitor on digestive proteases and growth of larval Spodoptera littoralis (Boisd.). Efflatounia 4: 23–30.
  • Duranti M, Barbiroli A, Scarafoni A, Tedeschi G, Morazzoni P (2003). One-step purification of Kunitz soybean tripsin inhibitor. Protein Express Purif 30: 167–170.
  • Erlandson MA, Hegedus DD, Baldwin D, Noakes A, Toprak U. (2010). Characterization of the Mamestra configurata(Lepidoptera: Noctuidae) larval midgut protease complement and adaptation to feeding on artificial diet, brassica species, and protease inhibitor. Arch Insect Biochem Physiol 75: 70–91.
  • Franco OL, dos Santos RC, Batista JA, Mendes AC, de Araujo MA, Monnerat RG, Grossi-de-Sa MF, de Freitas SM (2003). Effects of black-eyed pea trypsin/chymotrypsin inhibitor on proteolytic activity and on development of Anthonomus grandis. Phytochemistry 63: 343–349.
  • Fritig B, Heitz T, Legrand M (1998). Antimicrobial proteins in induced plant defense. Curr Opin Immunol 10: 16–22.
  • Gokulkrishnan J, Krishnappa K, Elumalai K (2012). Effect of plant oil formulations against armyworm, Spodoptera litura (Fab.), Cotton bollworm, Helicoverpa armigera (Hub.) and fruit borer, Earias vitella (Fab.) (Lepidopetra: Noctuidae). Int J Curr Life Sci 2: 1–4.
  • Gomes APG, Dias SC, Broch C Jr, Melo FR, Furtado JR Jr, Monnert RG, Grossi-de-Sa MF, Franco OL (2005). Toxicity to cotton boll weevil Anthonomus grandis of a trypsin inhibitor from chick pea seeds. Comp Biochem Physiol 140: 313–319.
  • Haq SK, Atif SM, Khan RH (2004). Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: natural and engineered phytoprotection. Arch Biochem Biophys 431: 145–159.
  • Hegedus DD, Baldwin M, O’Grady L, Braun S, Gleddie A, Sharpe D, Lydiate M (2003). Midgut proteases from Mamestra configurata (Lepidoptera: Noctuidae) larvae: characterization, cDNA cloning and expressed sequence tag analysis. Arch Insect Biochem Physiol 53: 30–47.
  • House HL (1974). Nutrition. In: Rockstein M, editor. The Physiology of Insects. New York, NY, USA: Academic press, pp. 1–62.
  • Jackson AO, Tailor CB (1996). Plant-microbe interactions: life and death at the interface. Plant Cell 8: 1651–1668.
  • Johnston KA, Gatehouse JA, Anstee JH (1993). Effect of soybean protease inhibitors on the growth and development of larval Helicoverpa armigera. J Insect Physiol 39: 657–664.
  • Johnston KA, Lee MJ, Brough C, Hilder VA, Gatehouse AMR, Gatehouse JA (1995). Protease activities in the larval midgut of Heliothis virescens: evidence for trypsin and chymotrypsin-like enzymes. Insect Biochem Molec 25: 375–383.
  • Johny S, Muralirangan MC (2000). Monitoring susceptibility to selected insecticides in Spodopteralitura (Fabricius) (Lepidoptera: Noctuidae) in Tamil Nadu (India). Pestology 24: 32–36.
  • Khan ZR, Saxena RC (1985). Behavioral and physiological responses of Sogatella furcifera (Homoptera: Delphacidae) to selected resistant and susceptible rice cultivars. J Econ Entomol 78: 1280–1286.
  • Koiwa K, Shade RE, Zhu-Salzman K, Subramanian L, Murdock LL, Nielsen SS, Bressan RA, Hasegawa PM (1998). Phage display selection can differentiate insecticidal activity of soybean cystatins. Plant J 14: 371–379.
  • Koul O, Shankar JS, Mehta N, Taneja SC, Tripathi AK, Dhar KL (1997). Bioefficacy of crude extracts of Aglaia species (Meliaceae) and some active fractions against lepidopteran larvae. J Appl Entomol 121: 245–248.
  • Koul O, Singh G, Singh R, Multani J (2005). Bioefficacy and mode-of-action of aglaroxin A from Aglaia elaeagnoidea (syn. A. roxburghiana) against Helicoverpa armigera and Spodoptera litura. Entomol Exp Appl 114: 197–204.
  • Kunitz M (1945). Crystallization of a trypsin inhibitor from soybean. Science 101: 668–669.
  • Lindroth RL (1993). Food conversion efficiencies of insect herbivores. Food Insects Newsletter 6: 9–10.
  • Macedo MLR, De Sa CM, Freire MDGM, Parra JRP (2004). A Kunitz-type inhibitor of coleopteran proteases, isolated from Adenanthera pavonina L. seeds and its effect on Callosobruchus maculatus. J Agric Food Chem 52: 2533–2540.
  • Malek K, Dietrich RA (1999). Defense on multiple fronts: How do plants cope with diverse enemies? Trends Plant Sci 4: 215–219.
  • Martinez SS, Emden HFV (2001). Growth distribution, abnormalities and mortality of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) caused by azadirachtin. Neotrop Entomol 30: 113–125.
  • McManus MT, Burgess EPJ (1995). Effects of the soybean (Kunitz) trypsin inhibitor on growth and digestive proteases of larvae of Spodoptera litura. J Insect Physiol 41: 731–738.
  • McManus MT, Burgess EPJ, Philip B, Watson LM, Laing WA, Voisey CR, White DWR (1999). Expression of the soybean (Kunitz) trypsin inhibitor in transgenic tobacco: effects on larval development of Spodoptera litura. Transgen Res 8: 383–395.
  • Michaud D (2000). Development and reproduction of ladybeetles (Coleoptera: Coccinellidae) on the citrus aphids Aphis spiraecola (Patch) and Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae). Biol Control 18: 287–297.
  • Nandeesha P, Prasad DT (2001). Characterization of serine proteinase inhibitor from subabul (Leucaena leucocephala L.) seeds. J Plant Biochem Biotechnol 10: 75–78.
  • Nathan SS, Kalaivani K (2005). Efficacy of nucleopolyhedrovirus (NPV) and azadirachtin on Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Biol Control 34: 93–98.
  • Pal GP, Betzel C, Jany KD, Saenger W (1986). Crystallization of the bifunctional proteinase/amylase inhibitor PKI-3 and of its complex with proteinase. FEBS Lett 197: 111–114.
  • Paulino da Silva L, Leite JRSA, Bloch C Jr, Maria de Freitas S (2001). Stability of a black eyed pea trypsin/chymotrypsin inhibitor (BTCI). Protein Pept Lett 8: 33–38.
  • Pompermayer P, Lopes AR, Terra WR, Parra JRP, Falco MC, Silva-Filho MC (2001). Effects of soybean proteinase inhibitor on development, survival and reproductive potential of the sugarcane borer, Diatrea sachharalis. Entomol Exp Appl 99: 79–85.
  • Ravichandran S, Sen U, Chakrabarti C, Dattagupta JK (1999). Cryocrystallography of a Kunitz-type serine protease inhibitor: the 90 K structure of winged bean chymotrypsin (WCI) at 2.13 A resolution. Acta Crystallogr55: 1814–1821.
  • Ryan CA (1990). Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28: 425–449.
  • Saadati F, Bandani AR (2011). Effects of serine protease inhibitors on growth and development and digestive serine proteinases of the Sunn pest, Eurygaster integriceps. J Insect Sci 2: 1–12.
  • Scriber JM, Slansky F (1981). The nutritional ecology of immature insects. Ann Rev Entomol 26: 183–211.
  • Shukle RH, Murdock LL (1983). Lipoxygenase, trypsin inhibitor, and lectin from soybeans effects on larval growth of Manduca sexta(Lepidoptera: Sphingidae). Environ Entomol 12: 787–791.
  • Silva CBLF, Alcazar AA, Macedo LLP, Oliveira AS, Macedo FP, Abreu LRD, Santos EA, Sales MP (2006). Digestive enzymes during development of Ceratitis capitata (Díptera: Tephritidae) and effects of SBTI on its digestive serine proteinase targets. Insect Biochem Molec 36: 561–569.
  • Tamhane VA, Chougule NP, Giri AP, Dixit AR, Sainani MN, Gupta VS (2005). In vivo and in vitro effect of Capsicum annumproteinase inhibitors on Helicoverpa armigera gut proteinases. Biochim Biophys Acta1722: 156–167.
  • Telang M, Srinivasan A, Patankar A, Harsulkar A, Joshi V, Deshpande V, Sainani M, Ranjekar P, Gupta G, Birah A et al. (2003). Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry 63: 643–652.
  • Urwin PE, Lilley CJ, McPherson MJ, Atkinson HJ (1997). Resistance to both cyst and root knot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant J 12: 455–461.
  • Vaijayanti AT, Nanasaheb PC, Ashok PG, Anirudha RD, Mohini NS, Vidya SG (2005). In vivo and in vitro effect of Capsicum annumproteinase inhibitors on Helicoverpa armigera gut proteinases. Biochim Biophys Acta 1722: 156–167.
  • Vain P, Worland B, Clarke MC, Richard G, Beavis M, Liu H, Kohli A, Leech M, Snake J, Christou P (1998). Expression of an engineered cysteine proteinase inhibitor (Oryzacystatin-I delta D86) for nematode resistance in transgenic rice plants. Theor Appl Gen 96: 266–271.
  • Vasudev A, Sohal SK (2013). Bioinsecticidal potential of partially purified proteinase inhibitors from Brassica oleracea (L.) against Spodoptera litura (Fab.) (Lepidoptera: Noctuidae). Efflatounia 13: 1–7.
  • Vasudev A, Sohal SK (2015). Evaluation of partially purified Subabul protease inhibitors as bio-insecticidal tool with potential for the control of Spodoptera litura. Int J Cur Res Rev 7: 31–37.
  • Waldbauer GP (1968). The consumption and utilization of food by insects. Adv Insect Physiol 5: 229–288.
  • Wheeler DA, Isman MB (2001). Antifeedant and toxic activity of Trichilia americana extract against the larvae of Spodoptera litura. Entomol Exp Appl98: 9–16.