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Natural Insecticidal Proteins and Their Potential in Future IPM

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Plant-Pest Interactions: From Molecular Mechanisms to Chemical Ecology
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Abstract

Increasing population and global food security is the foremost challenge for this century. Insect pests cause substantial damage to our crops by direct as well as indirect means such as vectoring plant viruses. Introduction of Bacillus thuringiensis originated toxins, namely, cry toxins, in the crop plants that showed significant resistance to insect damage during the early years (1990s). However, its societal unacceptability, nontarget effects, and the frequent development of resistance in target insects jeopardize Cry-toxin-mediated pest resistance. Alternatively, plant proteins with insecticidal activity hold great potential for future insect pest management strategies (IPM). Present chapter mainly deals with the ongoing advances in research on plant lectins. However, the entomotoxic potential of other plant proteins such as digestive inhibitors and plant peptides is also stated briefly. Further, future challenges and possibilities for developing sustainable pest management strategies are also discussed.

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References

  • Acharjee S, Sarmah BK (2013) Biotechnologically generating ‘super chickpea’ for food and nutritional security. Plant Sci 207:108–116

    Article  CAS  PubMed  Google Scholar 

  • Al Atalah B, De Vleesschauwer D, Xu J, Fouquaert E, Höfte M, Van Damme EJ (2014) Transcriptional behavior of EUL-related rice lectins toward important abiotic and biotic stresses. J Plant Physiol 171(12):986–992

    Article  PubMed  CAS  Google Scholar 

  • Alfonso-Rubí J, Ortego F, Castañera P, Carbonero P, Díaz I (2003) Transgenic expression of trypsin inhibitor CMe from barley in indica and japonica rice, confers resistance to the rice weevil Sitophilus oryzae. Transgenic Res 12(1):23–31

    Article  PubMed  Google Scholar 

  • Ali Z, Ali S, Tashkandi M, Zaidi SS-E-A, Mahfouz MM (2016) CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Sci Rep 6:26912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altpeter F, Diaz I, McAuslane H, Gaddour K, Carbonero P, Vasil IK (1999) Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Mol Breed 5(1):53–63

    Article  CAS  Google Scholar 

  • Andrews RE, Faust RM, Wabiko H, Raymond KC, Bulla LA (1987) The biotechnology of Bacillus thuringiensis. Crit Rev Biotechnol 6(2):163–232

    Article  CAS  PubMed  Google Scholar 

  • Baker S, Volova T, Prudnikova SV, Satish S, Prasad N (2017) Nanoagroparticles emerging trends and future prospect in modern agriculture system. Environ Toxicol Pharmacol 53:10–17

    Article  CAS  PubMed  Google Scholar 

  • Bala A, Roy A, Behura N, Hess D, Das S (2013a) Insight to the mode of action of Allium sativum leaf agglutinin (ASAL) expressing in T3 rice lines on brown planthopper. Am J Plant Sci 4(02):400

    Article  CAS  Google Scholar 

  • Bala A, Roy A, Das A, Chakraborti D, Das S (2013b) Development of selectable marker free, insect resistant, transgenic mustard (Brassica juncea) plants using Cre/lox mediated recombination. BMC Biotechnol 13(1):88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balzarini J, Schols D, Neyts J, Van Damme E, Peumans W, De Clercq E (1991) Alpha-(1-3)-and alpha-(1-6)-D-mannose-specific plant lectins are markedly inhibitory to human immunodeficiency virus and cytomegalovirus infections in vitro. Antimicrob Agents Chemother 35(3):410–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bandyopadhyay S, Roy A, Das S (2001) Binding of garlic (Allium sativum) leaf lectin to the gut receptors of homopteran pests is correlated to its insecticidal activity. Plant Sci 161(5):1025–1033

    Article  CAS  Google Scholar 

  • Banerjee N, Sengupta S, Roy A, Ghosh P, Das K, Das S (2011) Functional alteration of a dimeric insecticidal lectin to a monomeric antifungal protein correlated to its oligomeric status. PLoS One 6(4):e18593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbehenn RV, Constabel CP (2011) Tannins in plant–herbivore interactions. Phytochemistry 72(13):1551–1565

    Article  CAS  PubMed  Google Scholar 

  • Barbeta BL, Marshall AT, Gillon AD, Craik DJ, Anderson MA (2008) Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae. Proc Natl Acad Sci 105(4):1221–1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbieri L, Polito L, Bolognesi A, Ciani M, Pelosi E, Farini V et al (2006) Ribosome-inactivating proteins in edible plants and purification and characterization of a new ribosome-inactivating protein from Cucurbita moschata. Biochim Biophys Acta Gen Subj 1760(5):783–792

    Article  CAS  Google Scholar 

  • Barbosa AE, Albuquerque ÉV, Silva MC, Souza DS, Oliveira-Neto OB, Valencia A et al (2010) α-Amylase inhibitor-1 gene from Phaseolus vulgaris expressed in Coffea arabica plants inhibits α-amylases from the coffee berry borer pest. BMC Biotechnol 10(1):44

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barros PR, Stassen H, Freitas MS, Carlini CR, Nascimento MA, Follmer C (2009) Membrane-disruptive properties of the bioinsecticide Jaburetox-2Ec: implications to the mechanism of the action of insecticidal peptides derived from ureases. Biochim Biophys Acta Protein Proteom 1794(12):1848–1854

    Article  CAS  Google Scholar 

  • Becker-Ritt AB, Carlini CR (2012) Fungitoxic and insecticidal plant polypeptides. Pept Sci 98(4):367–384

    Article  CAS  Google Scholar 

  • Becker-Ritt AB, Portugal CS, Carlini CR (2017) Jaburetox: update on a urease-derived peptide. J Venomous Anim Toxins incl Trop Dis 23(1):32

    Article  CAS  Google Scholar 

  • Bell H, Fitches E, Marris G, Bell J, Edwards J, Gatehouse J, Gatehouse A (2001) Transgenic GNA expressing potato plants augment the beneficial biocontrol of Lacanobia oleracea (Lepidoptera: Noctuidae) by the parasitoid Eulophus pennicornis (Hymenoptera; Eulophidae). Transgenic Res 10(1):35–42

    Article  CAS  PubMed  Google Scholar 

  • Bell H, Kirkbride-Smith A, Marris G, Edwards J, Gatehouse A (2004) Oral toxicity and impact on fecundity of three insecticidal proteins on the gregarious ectoparasitoid Eulophus pennicornis (Hymenoptera: Eulophidae). Agric For Entomol 6(3):215–222

    Article  Google Scholar 

  • Birch ANE, Geoghegan IE, Majerus ME, McNicol JW, Hackett CA, Gatehouse AM, Gatehouse JA (1999) Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Mol Breed 5(1):75–83

    Article  Google Scholar 

  • Birkett MA, Pickett JA (2014) Prospects of genetic engineering for robust insect resistance. Curr Opin Plant Biol 19:59–67

    Article  CAS  PubMed  Google Scholar 

  • Bloch C, Richardson M (1991) A new family of small (5 kDa) protein inhibitors of insect α-amylases from seeds or sorghum (Sorghum bicolor (L) Moench) have sequence homologies with wheat γ-purothionins. FEBS Lett 279(1):101–104

    Article  CAS  PubMed  Google Scholar 

  • Boddupally D, Tamirisa S, Gundra SR, Vudem DR, Khareedu VR (2018) Expression of hybrid fusion protein (Cry1Ac:: ASAL) in transgenic rice plants imparts resistance against multiple insect pests. Sci Rep 8(1):8458

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonning BC, Pal N, Liu S, Wang Z, Sivakumar S, Dixon PM et al (2014) Toxin delivery by the coat protein of an aphid-vectored plant virus provides plant resistance to aphids. Nat Biotechnol 32(1):102

    Article  CAS  PubMed  Google Scholar 

  • Boulter D, Edwards GA, Gatehouse AM, Gatehouse JA, Hilder VA (1990) Additive protective effects of different plant-derived insect resistance genes in transgenic tobacco plants. Crop Prot 9(5):351–354

    Article  Google Scholar 

  • Boyd WC, Shapleigh E (1954) Antigenic relations of blood group antigens as suggested by tests with lectins. J Immunol 73(4):226–231

    Article  CAS  PubMed  Google Scholar 

  • Brown JC, Hunt RC (1978) Lectins. In: International review of cytology, vol 52. Elsevier, pp 277–349

    Google Scholar 

  • Caccia S, Van Damme EJ, De Vos WH, Smagghe G (2012) Mechanism of entomotoxicity of the plant lectin from Hippeastrum hybrid (Amaryllis) in Spodoptera littoralis larvae. J Insect Physiol 58(9):1177–1183

    Article  CAS  PubMed  Google Scholar 

  • Camaroti JRSL, de Almeida WA, do Rego Belmonte B, de Oliveira APS, de Albuquerque Lima T, Ferreira MRA et al (2018) Sitophilus zeamais adults have survival and nutrition affected by Schinus terebinthifolius leaf extract and its lectin (SteLL). Ind Crop Prod 116:81–89

    Article  CAS  Google Scholar 

  • Carlini CR, Grossi-de-Sá MF (2002) Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon 40(11):1515–1539

    Article  CAS  PubMed  Google Scholar 

  • Carlini CR, Ligabue-Braun R (2016) Ureases as multifunctional toxic proteins: a review. Toxicon 110:90–109

    Article  CAS  PubMed  Google Scholar 

  • Carlini CR, Oliveira AE, Azambuja P, Xavier-Filho J, Wells MA (1997) Biological effects of canatoxin in different insect models: evidence for a proteolytic activation of the toxin by insect cathepsin-like enzymes. J Econ Entomol 90(2):340–348

    Article  CAS  PubMed  Google Scholar 

  • Carrière Y, Crickmore N, Tabashnik BE (2015) Optimizing pyramided transgenic Bt crops for sustainable pest management. Nat Biotechnol 33(2):161

    Article  PubMed  CAS  Google Scholar 

  • Chagolla-Lopez A, Blanco-Labra A, Patthy A, Sánchez R, Pongor S (1994) A novel alpha-amylase inhibitor from amaranth (Amaranthus hypochondriacus) seeds. J Biol Chem 269(38):23675–23680

    Article  CAS  PubMed  Google Scholar 

  • Chakraborti D, Sarkar A, Mondal HA, Das S (2009) Tissue specific expression of potent insecticidal, Allium sativum leaf agglutinin (ASAL) in important pulse crop, chickpea (Cicer arietinum L.) to resist the phloem feeding Aphis craccivora. Transgenic Res 18(4):529–544

    Article  CAS  PubMed  Google Scholar 

  • Chandra NR, Ramachandraiah G, Bachhawat K, Dam TK, Surolia A, Vijayan M (1999) Crystal structure of a dimeric mannose-specific agglutinin from garlic: quaternary association and carbohydrate specificity. J Mol Biol 285(3):1157–1168

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekhar K, Vijayalakshmi M, Vani K, Kaul T, Reddy MK (2014) Phloem-specific expression of the lectin gene from Allium sativum confers resistance to the sap-sucker Nilaparvata lugens. Biotechnol Lett 36(5):1059–1067

    Article  CAS  PubMed  Google Scholar 

  • Chang T, Chen L, Chen S, Cai H, Liu X, Xiao G, Zhu Z (2003) Transformation of tobacco with genes encoding Helianthus tuberosus agglutinin (HTA) confers resistance to peach-potato aphid (Myzus persicae). Transgenic Res 12(5):607–614

    Article  CAS  PubMed  Google Scholar 

  • Chen MS (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15(2):101–114

    Article  CAS  Google Scholar 

  • Chen Y, Peumans WJ, Hause B, Bras J, Kumar M, Proost P et al (2002) Jasmonic acid methyl ester induces the synthesis of a cytoplasmic/nuclear chito-oligosaccharide binding lectin in tobacco leaves. FASEB J 16(8):905–907

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci 102(52):19237–19242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Gonzales-Vigil E, Wilkerson CG, Howe GA (2007) Stability of plant defense proteins in the gut of insect herbivores. Plant Physiol 143(4):1954–1967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi M-S, Kim Y-H, Park H-M, Seo B-Y, Jung J-K, Kim S-T et al (2009) Expression of BrD1, a plant defensin from Brassica rapa, confers resistance against brown planthopper (Nilaparvata lugens) in transgenic Rices. Mol Cells 28(2):131–137

    Article  CAS  PubMed  Google Scholar 

  • Chougule NP, Bonning BC (2012) Toxins for transgenic resistance to hemipteran pests. Toxins 4(6):405–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen E (1993) Chitin synthesis and degradation as targets for pesticide action. Arch Insect Biochem Physiol 22(1–2):245–261

    Article  CAS  PubMed  Google Scholar 

  • Collard BC, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond B: Biol Sci 363(1491):557–572

    Article  CAS  Google Scholar 

  • Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3(1):31–40

    Article  CAS  PubMed  Google Scholar 

  • Consiglio A, Grillo G, Licciulli F, Ceci LR, Liuni S, Losito N et al (2011) PlantPIs-an interactive web resource on plant protease inhibitors. Curr Protein Pept Sci 12(5):448–454

    Article  CAS  PubMed  Google Scholar 

  • Couty A, Poppy GM (2001) Does host-feeding on GNA-intoxicated aphids by Aphelinus abdominalis affect their longevity and/or fecundity? Entomol Exp Appl 100(3):331–337

    Article  Google Scholar 

  • Cristofoletti PT, Mendonça de Sousa FA, Rahbe Y, Terra WR (2006) Characterization of a membrane-bound aminopeptidase purified from Acyrthosiphon pisum midgut cells. FEBS J 273(24):5574–5588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Da Silva P, Rahioui I, Laugier C, Jouvensal L, Meudal H, Chouabe C et al (2010) Molecular requirements for the insecticidal activity of the plant peptide pea albumin 1 subunit b (PA1b). J Biol Chem 285(43):32689–32694

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dang L, Van Damme EJ (2015) Toxic proteins in plants. Phytochemistry 117:51–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das A, Ghosh P, Das S (2018) Expression of Colocasia esculenta tuber agglutinin in Indian mustard provides resistance against Lipaphis erysimi and the expressed protein is non-allergenic. Plant Cell Rep 37(6):849–863

    Article  CAS  PubMed  Google Scholar 

  • Dayler CS, Mendes PA, Prates MV, Bloch C, Franco OL, Grossi-de-Sá MF (2005) Identification of a novel bean α-amylase inhibitor with chitinolytic activity. FEBS Lett 579(25):5616–5620

    Article  CAS  PubMed  Google Scholar 

  • De Oliveira CFR, Luz LA, Paiva PMG, Coelho LCBB, Marangoni S, Macedo MLR (2011) Evaluation of seed coagulant Moringa oleifera lectin (cMoL) as a bioinsecticidal tool with potential for the control of insects. Process Biochem 46(2):498–504

    Article  CAS  Google Scholar 

  • del Carmen F-AM, Diaz D, Berbis M, Marcelo F, Cañada J, Jiménez-Barbero J (2012) Protein-carbohydrate interactions studied by NMR: from molecular recognition to drug design. Curr Protein Pept Sci 13(8):816

    Article  Google Scholar 

  • Dias SC, Franco OL, Magalhaes CP, de Oliveira-Neto OB, Laumann RA, Figueira EL et al (2005) Molecular cloning and expression of an α-amylase inhibitor from rye with potential for controlling insect pests. Protein J 24(2):113–123

    Article  CAS  PubMed  Google Scholar 

  • dos Santos IS, Carvalho ADO, de Souza-Filho GA, do Nascimento VV, Machado OL, Gomes VM (2010) Purification of a defensin isolated from Vigna unguiculata seeds, its functional expression in Escherichia coli, and assessment of its insect α-amylase inhibitory activity. Protein Expr Purif 71(1):8–15

    Article  PubMed  CAS  Google Scholar 

  • Douglas AE (2018a) Omics and the metabolic function of insect-microbial symbioses. Curr Opin Insect Sci 29:1–16

    Article  PubMed  Google Scholar 

  • Douglas AE (2018b) Strategies for enhanced crop resistance to insect pests. Annu Rev Plant Biol 69:637–660

    Article  CAS  PubMed  Google Scholar 

  • Dowd PF, Zuo W-N, Gillikin JW, Johnson ET, Boston RS (2003) Enhanced resistance to Helicoverpa zea in tobacco expressing an activated form of maize ribosome-inactivating protein. J Agric Food Chem 51(12):3568–3574

    Article  CAS  PubMed  Google Scholar 

  • Down RE, Ford L, Woodhouse SD, Raemaekers RJ, Leitch B, Gatehouse JA, Gatehouse AM (2000) Snowdrop lectin (GNA) has no acute toxic effects on a beneficial insect predator, the 2-spot ladybird (Adalia bipunctata L.). J Insect Physiol 46(4):379–391

    Article  CAS  PubMed  Google Scholar 

  • Down RE, Ford L, Woodhouse SD, Davison GM, Majerus ME, Gatehouse JA, Gatehouse AM (2003) Tritrophic interactions between transgenic potato expressing snowdrop lectin (GNA), an aphid pest (peach–potato aphid; Myzus persicae (Sulz.) and a beneficial predator (2-spot ladybird, Adalia bipunctata L.)). Transgenic Res 12(2):229–241

    Article  CAS  PubMed  Google Scholar 

  • Du J, Foissac X, Carss A, Gatehouse AM, Gatehouse JA (2000) Ferritin acts as the most abundant binding protein for snowdrop lectin in the midgut of rice brown planthoppers (Nilaparvata lugens). Insect Biochem Mol Biol 30(4):297–305

    Article  CAS  PubMed  Google Scholar 

  • Duan X, Li X, Xue Q, Abo-EI-Saad M, Xu D, Wu R (1996) Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nat Biotechnol 14(4):494

    Article  CAS  PubMed  Google Scholar 

  • Dunse K, Stevens J, Lay F, Gaspar Y, Heath R, Anderson M (2010) Coexpression of potato type I and II proteinase inhibitors gives cotton plants protection against insect damage in the field. Proc Natl Acad Sci 107(34):15011–15015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dutta I, Saha P, Majumder P, Sarkar A, Chakraborti D, Banerjee S, Das S (2005) The efficacy of a novel insecticidal protein, Allium sativum leaf lectin (ASAL), against homopteran insects monitored in transgenic tobacco. Plant Biotechnol J 3(6):601–611

    Article  CAS  PubMed  Google Scholar 

  • Ewen SW, Pusztai A (1999) Effect of diets containing genetically modified potatoes expressing Galanthus nivalis lectin on rat small intestine. Lancet 354(9187):1353–1354

    Article  CAS  PubMed  Google Scholar 

  • FAO (2009) How to feed the world 2050: high-level expert forum. Available at: fao.org/fileadmin/templates/wsfs/docs/Issues_papers/HLEF2050_Global_Agriculture.pdf. Accessed on 10 Nov 2014

  • FAO/WHO (2001) Human vitamin and mineral requirements. Report of a Joint FAO/WHO Expert Consultation, Bangkok, Thailand. Food and Nutrition Division, FAO, Rome, pp 235–247

    Google Scholar 

  • Felton GW (2005) Indigestion is a plant’s best defense. Proc Natl Acad Sci U S A 102(52):18771–18772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng GH, Richardson M, Chen MS, Kramer KJ, Morgan TD, Reeck GR (1996) α-Amylase inhibitors from wheat: amino acid sequences and patterns of inhibition of insect and human α-amylases. Insect Biochem Mol Biol 26(5):419–426

    Article  CAS  PubMed  Google Scholar 

  • Ferreira-DaSilva CT, Gombarovits MEC, Masuda H, Oliveira CM, Carlini CR (2000) Proteolytic activation of canatoxin, a plant toxic protein, by insect cathepsin-like enzymes. Arch Insect Biochem Physiol 44(4):162–171

    Article  CAS  PubMed  Google Scholar 

  • Fitches E, Gatehouse AM, Gatehouse JA (1997) Effects of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on the development of tomato moth (Lacanobia oleracea) larvae in laboratory and glasshouse trials. J Insect Physiol 43(8):727–739

    Article  CAS  PubMed  Google Scholar 

  • Fitches E, Ilett C, Gatehouse A, Gatehouse L, Greene R, Edwards J, Gatehouse J (2001a) The effects of Phaseolus vulgaris erythro-and leucoagglutinating isolectins (PHA-E and PHA-L) delivered via artificial diet and transgenic plants on the growth and development of tomato moth (Lacanobia oleracea) larvae; lectin binding to gut glycoproteins in vitro and in vivo. J Insect Physiol 47(12):1389–1398

    Article  CAS  PubMed  Google Scholar 

  • Fitches E, Woodhouse SD, Edwards JP, Gatehouse JA (2001b) In vitro and in vivo binding of snowdrop (Galanthus nivalis agglutinin; GNA) and jackbean (Canavalia ensiformis; Con A) lectins within tomato moth (Lacanobia oleracea) larvae; mechanisms of insecticidal action. J Insect Physiol 47(7):777–787

    Article  CAS  PubMed  Google Scholar 

  • Fitches E, Wiles D, Douglas AE, Hinchliffe G, Audsley N, Gatehouse JA (2008) The insecticidal activity of recombinant garlic lectins towards aphids. Insect Biochem Mol Biol 38(10):905–915

    Article  CAS  PubMed  Google Scholar 

  • Fitches EC, Pyati P, King GF, Gatehouse JA (2012) Fusion to snowdrop lectin magnifies the oral activity of insecticidal ω-hexatoxin-Hv1a peptide by enabling its delivery to the central nervous system. PLoS One 7(6):e39389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foissac X, Loc NT, Christou P, Gatehouse AM, Gatehouse JA (2000) Resistance to green leafhopper (Nephotettix virescens) and brown planthopper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivalis agglutinin; GNA). J Insect Physiol 46(4):573–583

    Article  CAS  PubMed  Google Scholar 

  • Follmer C, Real-Guerra R, Wasserman GE, Olivera-Severo D, Carlini CR (2004) Jackbean, soybean and Bacillus pasteurii ureases: biological effects unrelated to ureolytic activity. Eur J Biochem 271(7):1357–1363

    Article  CAS  PubMed  Google Scholar 

  • Franco OL, Rigden DJ, Melo FR, Grossi-de-Sá MF (2002) Plant α-amylase inhibitors and their interaction with insect α-amylases: structure, function and potential for crop protection. Eur J Biochem 269(2):397–412

    Article  CAS  PubMed  Google Scholar 

  • Fruttero LL, Moyetta NR, Uberti AF, Grahl MVC, Lopes FC, Broll V et al (2016) Humoral and cellular immune responses induced by the urease-derived peptide Jaburetox in the model organism Rhodnius prolixus. Parasit Vectors 9(1):412

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gaidamashvili M, Ohizumi Y, Iijima S, Takayama T, Ogawa T, Muramoto K (2004) Characterization of the yam tuber storage proteins from Dioscorea batatas exhibiting unique lectin activities. J Biol Chem 279(25):26028–26035

    Article  CAS  PubMed  Google Scholar 

  • Galvani GL, Fruttero LL, Coronel MF, Nowicki S, Demartini DR, Defferrari MS et al (2015) Effect of the urease-derived peptide Jaburetox on the central nervous system of Triatoma infestans (Insecta: Heteroptera). Biochim Biophys Acta (BBA)-Gen Sub 1850(2):255–262

    Article  CAS  Google Scholar 

  • García-Fraile P (2018) Roles of bacteria in the bark beetle holobiont–how do they shape this forest pest? Ann Appl Biol 172(2):111–125

    Article  Google Scholar 

  • Garcia-Pino A, Buts L, Wyns L, Imberty A, Loris R (2007) How a plant lectin recognizes high mannose oligosaccharides. Plant Physiol 144(4):1733–1741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gatehouse AM, Davison GM, Newell CA, Merryweather A, Hamilton WD, Burgess EP et al (1997) Transgenic potato plants with enhanced resistance to the tomato moth, Lacanobia oleracea: growth room trials. Mol Breed 3(1):49–63

    Article  CAS  Google Scholar 

  • Gatehouse AM, Davison GM, Stewart JN, Gatehouse LN, Kumar A, Geoghegan IE et al (1999) Concanavalin A inhibits development of tomato moth (Lacanobia oleracea) and peach-potato aphid (Myzus persicae) when expressed in transgenic potato plants. Mol Breed 5(2):153–165

    Article  CAS  Google Scholar 

  • George BS, Silambarasan S, Senthil K, Jacob JP, Dasgupta MG (2018) Characterization of an insecticidal protein from Withania somnifera against lepidopteran and hemipteran Pest. Mol Biotechnol 60(4):290–301

    Article  CAS  PubMed  Google Scholar 

  • Georges F, Ray H (2017) Genome editing of crops: a renewed opportunity for food security. GM Crops Food 8(1):1–12

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghazarian H, Idoni B, Oppenheimer SB (2011) A glycobiology review: carbohydrates, lectins and implications in cancer therapeutics. Acta Histochem 113(3):236–247

    Article  CAS  PubMed  Google Scholar 

  • Ghosh P, Roy A, Chakraborty J, Das S (2013) Biological safety assessment of mutant variant of Allium sativum leaf agglutinin (mASAL), a novel antifungal protein for future transgenic application. J Agric Food Chem 61(48):11858–11864

    Article  CAS  PubMed  Google Scholar 

  • Gowda A, Rydel TJ, Wollacott AM, Brown RS, Akbar W, Clark TL et al (2016) A transgenic approach for controlling Lygus in cotton. Nat Commun 7:12213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimaldi D, Engel MS, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    Google Scholar 

  • Grossi-de-Sá MF, Pelegrini PB, Vasconcelos IM, Carlini CR, Silva MS (2017) Entomotoxic plant proteins: potential molecules to develop genetically modified plants resistant to insect-pests. Plant Toxins:415–447

    Google Scholar 

  • Guo P, Wang Y, Zhou X, Xie Y, Wu H, Gao X (2013) Expression of soybean lectin in transgenic tobacco results in enhanced resistance to pathogens and pests. Plant Sci 211:17–22

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Das S (2012) Exploring the defensive roles and regulations of GNA domain containing monocot mannose specific lectins. Sci Cult 78:233–241

    Google Scholar 

  • Harper M, Hopkins T, Czapla T (1998) Effect of wheat germ agglutinin on formation and structure of the peritrophic membrane in European corn borer (Ostrinia nubilalis) larvae. Tissue Cell 30(2):166–176

    Article  CAS  PubMed  Google Scholar 

  • Harrison RL, Bonning BC (2010) Proteases as insecticidal agents. Toxins 2(5):935–953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54:285–302

    Article  CAS  PubMed  Google Scholar 

  • Hester G, Kaku H, Goldstein IJ, Wright CS (1995) Structure of mannose-specific snowdrop (Galanthus nivalis) lectin is representative of a new plant lectin family. Nat Struct Biol 2(6):472–479

    Article  CAS  PubMed  Google Scholar 

  • Hilder V, Powell K, Gatehouse A, Gatehouse J, Gatehouse L, Shi Y et al (1995) Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgenic Res 4(1):18–25

    Article  CAS  Google Scholar 

  • Hogervorst PA, Ferry N, Gatehouse AM, Wäckers FL, Romeis J (2006) Direct effects of snowdrop lectin (GNA) on larvae of three aphid predators and fate of GNA after ingestion. J Insect Physiol 52(6):614–624

    Article  CAS  PubMed  Google Scholar 

  • Huang Y-H, Colgrave ML, Daly NL, Keleshian A, Martinac B, Craik DJ (2009) The biological activity of the prototypic cyclotide kalata b1 is modulated by the formation of multimeric pores. J Biol Chem. jbc. M109. 003384

    Google Scholar 

  • Isaacs NW (1995) Cystine knots. Curr Opin Struct Biol 5(3):391–395

    Article  CAS  PubMed  Google Scholar 

  • Javaid S, Naz S, Amin I, Jander G, Ul-Haq Z, Mansoor S (2018) Computational and biological characterization of fusion proteins of two insecticidal proteins for control of insect pests. Sci Rep 8(1):4837

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jennings C, West J, Waine C, Craik D, Anderson M (2001) Biosynthesis and insecticidal properties of plant cyclotides: the cyclic knotted proteins from Oldenlandia affinis. Proc Natl Acad Sci 98(19):10614–10619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jennings CV, Rosengren KJ, Daly NL, Plan M, Stevens J, Scanlon MJ et al (2005) Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist: do Möbius strips exist in nature? Biochemistry 44(3):851–860

    Article  CAS  PubMed  Google Scholar 

  • Jiang B, Siregar U, Willeford KO, Luthe DS, Williams WP (1995) Association of a 33-kilodalton cysteine proteinase found in corn callus with the inhibition of fall armyworm larval growth. Plant Physiol 108(4):1631–1640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang J-H, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid–isoleucine–mediated defenses against Manduca sexta. Plant Cell 18(11):3303–3320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanrar S, Venkateswari J, Kirti P, Chopra V (2002) Transgenic Indian mustard (Brassica juncea) with resistance to the mustard aphid (Lipaphis erysimi Kalt.). Plant Cell Rep 20(10):976–981. https://doi.org/10.1007/s00299-001-0422-z

    Article  CAS  Google Scholar 

  • Kappaun K (2011) Estudos com o Jaburetox: efeito tóxico de E. coli liofilizadas carregadas com o peptídeo e análise da influencia do epitopo V5 na formação de agregados

    Google Scholar 

  • Kaur R, Kaur N, Gupta AK (2014) Structural features, substrate specificity, kinetic properties of insect α-amylase and specificity of plant α-amylase inhibitors. Pestic Biochem Physiol 116:83–93

    Article  CAS  PubMed  Google Scholar 

  • Kelemu S, Cardona C, Segura G (2004) Antimicrobial and insecticidal protein isolated from seeds of Clitoria ternatea, a tropical forage legume. Plant Physiol Biochem 42(11):867–873

    Article  CAS  PubMed  Google Scholar 

  • Khatodia S, Bhatotia K, Tuteja N (2017) Development of CRISPR/Cas9 mediated virus resistance in agriculturally important crops. Bioengineered 8(3):274–279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • King A (2017) The future of agriculture. Nature 544(7651):S21–S23

    Article  CAS  PubMed  Google Scholar 

  • Kitajima S, Kamei K, Taketani S, Yamaguchi M, Kawai F, Komatsu A, Inukai Y (2010) Two chitinase-like proteins abundantly accumulated in latex of mulberry show insecticidal activity. BMC Biochem 11(1):6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura Y, Hattori M, Kohno K (2004) Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37(3):370–378

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Verma AK, Sharma A, Kumar D, Tripathi A, Chaudhari B et al (2013) Phytohemagglutinins augment red kidney bean (Phaseolus vulgaris L.) induced allergic manifestations. J Proteome 93:50–64

    Article  CAS  Google Scholar 

  • Lacerda A, Vasconcelos ÉAR, Pelegrini PB, Grossi-de-Sa MF (2014) Antifungal defensins and their role in plant defense. Front Microbiol 5:116

    Article  PubMed  PubMed Central  Google Scholar 

  • Lagarda-Diaz I, Guzman-Partida AM, Urbano-Hernandez G, Ortega-Nieblas MM, Robles-Burgueño MR, Winzerling J, Vazquez-Moreno L (2008) Insecticidal action of PF2 lectin from Olneya tesota (Palo Fierro) against Zabrotes subfasciatus larvae and midgut glycoconjugate binding. J Agric Food Chem 57(2):689–694

    Article  CAS  Google Scholar 

  • Landsteiner K (1990) The specificity of serological reactions. Courier Corporation, New York

    Google Scholar 

  • Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in Colorado potato beetle. Biotechnol Lett 28(8):593–599

    Article  CAS  PubMed  Google Scholar 

  • Lay FT, Brugliera F, Anderson MA (2003) Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol 131(3):1283–1293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SI, Lee S-H, Koo JC, Chun HJ, Lim CO, Mun JH et al (1999) Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stål) in transgenic rice. Mol Breed 5(1):1–9

    Article  Google Scholar 

  • Lehrman A (2007) Does pea lectin expressed transgenically in oilseed rape (Brassica napus) influence honey bee (Apis mellifera) larvae? Environ Biosaf Res 6(4):271–278

    Article  CAS  Google Scholar 

  • Li Y, Chen Z, Wu X, Li S, Jiao G, Wu J et al (1998) Obtaining transgenic cotton plants with cowpea trypsin inhibitor gene. Acta Gossypii Sinica 10(5):237–243

    Google Scholar 

  • Li HM, Sun L, Mittapalli O, Muir W, Xie J, Wu J et al (2009) Transcriptional signatures in response to wheat germ agglutinin and starvation in Drosophila melanogaster larval midgut. Insect Mol Biol 18(1):21–31

    Article  CAS  PubMed  Google Scholar 

  • Liu C-L, Tsai C-C, Lin S-C, Wang L-I, Hsu C-I, Hwang M-J, Lin J-Y (2000) Primary structure and function analysis of the Abrus precatorius agglutinin a chain by site-directed mutagenesis Pro199 of amphiphilic α-HELIX H impairs protein synthesis inhibitory activity. J Biol Chem 275(3):1897–1901

    Article  CAS  PubMed  Google Scholar 

  • Liu SM, Li J, Zhu JQ, Wang XW, Wang CS, Liu SS et al (2016) Transgenic plants expressing the AaIT/GNA fusion protein show increased resistance and toxicity to both chewing and sucking pests. Insect Sci 23(2):265–276

    Article  CAS  PubMed  Google Scholar 

  • Lopez L, Camas A, Shivaji R, Ankala A, Williams P, Luthe D (2007) Mir1-CP, a novel defense cysteine protease accumulates in maize vascular tissues in response to herbivory. Planta 226(2):517–527

    Article  CAS  PubMed  Google Scholar 

  • Lord JM, Spooner RA (2011) Ricin trafficking in plant and mammalian cells. Toxins 3(7):787–801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lüthi C, Álvarez-Alfageme F, Romeis J (2018) The bean α-amylase inhibitor αAI-1 in genetically modified chickpea seeds does not harm parasitoid wasps. Pest Manag Sci 74(11):2444–2449

    Article  PubMed  CAS  Google Scholar 

  • Maag D, Dalvit C, Thevenet D, Köhler A, Wouters FC, Vassão DG et al (2014) 3-β-D-Glucopyranosyl-6-methoxy-2-benzoxazolinone (MBOA-N-Glc) is an insect detoxification product of maize 1, 4-benzoxazin-3-ones. Phytochemistry 102:97–105

    Article  CAS  PubMed  Google Scholar 

  • Macedo MLR, Oliveira CF, Oliveira CT (2015) Insecticidal activity of plant lectins and potential application in crop protection. Molecules 20(2):2014–2033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maddock S (1991) Expression in maize plants of wheatgerm agglutinin, a novel source of insect resistance. Paper presented at the 3rd International Congress of Plant Molecular Biology, Tucson, Arizona, USA, 1991

    Google Scholar 

  • Maqbool SB, Riazuddin S, Loc NT, Gatehouse AM, Gatehouse JA, Christou P (2001) Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests. Mol Breed 7(1):85–93

    Article  CAS  Google Scholar 

  • Marchetti S, Delledonne M, Fogher C, Chiaba C, Chiesa F, Savazzini F, Giordano A (2000) Soybean Kunitz, C-II and PI-IV inhibitor genes confer different levels of insect resistance to tobacco and potato transgenic plants. Theor Appl Genet 101(4):519–526

    Article  CAS  Google Scholar 

  • Martinelli AH, Kappaun K, Ligabue-Braun R, Defferrari MS, Piovesan AR, Stanisçuaski F et al (2014) Structure–function studies on jaburetox, a recombinant insecticidal peptide derived from jack bean (Canavalia ensiformis) urease. Biochim Biophys Acta (BBA)-Gen Subj 1840(3):935–944

    Article  CAS  Google Scholar 

  • Mehta D, Stürchler A, Hirsch-Hoffmann M, Gruissem W, Vanderschuren H (2018) CRISPR-Cas9 interference in cassava linked to the evolution of editing-resistant geminiviruses. BioRxiv:314542

    Google Scholar 

  • Melander M, Åhman I, Kamnert I, Strömdahl A-C (2003) Pea lectin expressed transgenically in oilseed rape reduces growth rate of pollen beetle larvae. Transgenic Res 12(5):555–567

    Article  CAS  PubMed  Google Scholar 

  • Michiels K, Van Damme EJ, Smagghe G (2010) Plant-insect interactions: what can we learn from plant lectins? Arch Insect Biochem Physiol 73(4):193–212

    Article  CAS  PubMed  Google Scholar 

  • Mochizuki A, Nishizawa Y, Onodera H, Tabei Y, Toki S, Habu Y et al (1999) Transgenic rice plants expressing a trypsin inhibitor are resistant against rice stem borers, Chilo suppressalis. Entomol Exp Appl 93(2):173–178

    Article  CAS  Google Scholar 

  • Mohan S, Ma PW, Williams WP, Luthe DS (2008) A naturally occurring plant cysteine protease possesses remarkable toxicity against insect pests and synergizes Bacillus thuringiensis toxin. PLoS One 3(3):e1786

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mondal HA, Chakraborti D, Majumder P, Roy P, Roy A, Bhattacharya SG, Das S (2011) Allergenicity assessment of Allium sativum leaf agglutinin, a potential candidate protein for developing sap sucking insect resistant food crops. PLoS One 6(11):e27716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mondal H, Roy A, Gupta S, Das S (2012) Exploring the insecticidal potentiality of Amorphophallus paeonifolius tuber agglutinin in hemipteran pest management. Am J Plant Sci 3(06):780

    Article  CAS  Google Scholar 

  • Moreira RDA, Ainouz IL, Oliveira JTAD, Cavada BS (1991) Plant lectins, chemical and biological aspects. Mem Inst Oswaldo Cruz 86:211–218

    Article  Google Scholar 

  • Morton RL, Schroeder HE, Bateman KS, Chrispeels MJ, Armstrong E, Higgins TJ (2000) Bean α-amylase inhibitor 1 in transgenic peas (Pisum sativum) provides complete protection from pea weevil (Bruchus pisorum) under field conditions. Proc Natl Acad Sci 97(8):3820–3825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulinari F (2008) Ureases de Canavalia ensiformis e peptídeo inseticida derivado

    Google Scholar 

  • Mulinari F, Staniscuaski F, Bertholdo-Vargas L, Postal M, Oliveira-Neto O, Rigden D et al (2007) Jaburetox-2Ec: an insecticidal peptide derived from an isoform of urease from the plant Canavalia ensiformis. Peptides 28(10):2042–2050

    Article  CAS  PubMed  Google Scholar 

  • Murdock LL, Shade RE (2002) Lectins and protease inhibitors as plant defenses against insects. J Agric Food Chem 50(22):6605–6611

    Article  CAS  PubMed  Google Scholar 

  • Nagadhara D, Ramesh S, Pasalu I, Rao YK, Sarma N, Reddy V, Rao K (2004) Transgenic rice plants expressing the snowdrop lectin gene (gna) exhibit high-level resistance to the whitebacked planthopper (Sogatella furcifera). Theor Appl Genet 109(7):1399–1405

    Article  CAS  PubMed  Google Scholar 

  • Nagpure A, Choudhary B, Gupta RK (2014) Chitinases: in agriculture and human healthcare. Crit Rev Biotechnol 34(3):215–232

    Article  CAS  PubMed  Google Scholar 

  • Oerke E-C (2006) Crop losses to pests. J Agric Sci 144(1):31–43

    Article  Google Scholar 

  • Ohizumi Y, Gaidamashvili M, Ohwada S, Matsuda K, Kominami J, Nakamura-Tsuruta S et al (2009) Mannose-binding lectin from yam (Dioscorea batatas) tubers with insecticidal properties against Helicoverpa armigera (Lepidoptera: Noctuidae). J Agric Food Chem 57(7):2896–2902

    Article  CAS  PubMed  Google Scholar 

  • Oliveira AS, Lossio CF, Rangel AJ, Martins MG, Nascimento FE, Andrade MLD et al (2017) Detection, purification and characterization of a lectin from freshwater green algae Spirogyra spp. An Acad Bras Cienc 89(3):2113–2117

    Article  PubMed  CAS  Google Scholar 

  • Oliveira-Neto OB, Batista JA, Rigden DJ, Franco OL, Falcão R, Fragoso RR et al (2003) Molecular cloning of α-amylases from cotton boll weevil, Anthonomus grandis and structural relations to plant inhibitors: an approach to insect resistance. J Protein Chem 22(1):77–87

    Article  CAS  PubMed  Google Scholar 

  • Olsen KM, Wendel JF (2013) A bountiful harvest: genomic insights into crop domestication phenotypes. Annu Rev Plant Biol 64:47–70

    Article  CAS  PubMed  Google Scholar 

  • Pechan T, Ye L, Chang Y-M, Mitra A, Lin L, Davis FM et al (2000) A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. Plant Cell 12(7):1031–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pechan T, Cohen A, Williams WP, Luthe DS (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proc Natl Acad Sci 99(20):13319–13323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pelegrini PB, Quirino BF, Franco OL (2007) Plant cyclotides: an unusual class of defense compounds. Peptides 28(7):1475–1481

    Article  CAS  PubMed  Google Scholar 

  • Pelegrini PB, Lay FT, Murad AM, Anderson MA, Franco OL (2008) Novel insights on the mechanism of action of α-amylase inhibitors from the plant defensin family. Protein Struct Func Bioinf 73(3):719–729

    Article  CAS  Google Scholar 

  • Peumans WJ, Van Damme E (1995) Lectins as plant defense proteins. Plant Physiol 109(2):347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peumans WJ, Hao Q, van Damme EJ (2001) Ribosome-inactivating proteins from plants: more than RNA N-glycosidases? FASEB J 15(9):1493–1506

    Article  CAS  PubMed  Google Scholar 

  • Pinto MF, Fensterseifer IC, Migliolo L, Sousa DA, de Capdville G, Arboleda-Valencia JW et al (2012) Identification and structural characterization of novel cyclotide with activity against an insect pest of sugar cane. J Biol Chem 287(1):134–147

    Article  CAS  PubMed  Google Scholar 

  • Piovesan AR, Martinelli AH, Ligabue-Braun R, Schwartz J-L, Carlini CR (2014) Canavalia ensiformis urease, Jaburetox and derived peptides form ion channels in planar lipid bilayers. Arch Biochem Biophys 547:6–17

    Article  CAS  PubMed  Google Scholar 

  • Popp J (2011) Cost-benefit analysis of crop protection measures. J Verbr Lebensm 6(1):105–112

    Article  Google Scholar 

  • Popp J, Pető K, Nagy J (2013) Pesticide productivity and food security. A review. Agron Sustain Dev 33(1):243–255

    Article  Google Scholar 

  • Postal M, Martinelli AH, Becker-Ritt AB, Ligabue-Braun R, Demartini DR, Ribeiro SF et al (2012) Antifungal properties of Canavalia ensiformis urease and derived peptides. Peptides 38(1):22–32

    Article  CAS  PubMed  Google Scholar 

  • Powell K, Gatehouse A, Hilder V, Gatehouse J (1993) Antimetabolic effects of plant lectins and plant and fungal enzymes on the nymphal stages of two important rice pests, Nilaparvata lugens and Nephotettix cinciteps. Entomol Exp Appl 66(2):119–126

    Article  CAS  Google Scholar 

  • Powell KS, Spence J, Bharathi M, Gatehouse JA, Gatehouse AM (1998) Immunohistochemical and developmental studies to elucidate the mechanism of action of the snowdrop lectin on the rice brown planthopper, Nilaparvata lugens (Stal). J Insect Physiol 44(7–8):529–539

    Article  CAS  PubMed  Google Scholar 

  • Price DR, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26(7):393–400

    Article  CAS  PubMed  Google Scholar 

  • Puchta H (2003) Marker-free transgenic plants. Plant Cell Tissue Organ Cult 74(2):123–134

    Article  CAS  Google Scholar 

  • Pusztai A, Ewen SW, Grant G, Peumans WJ, van Damme EJ, Coates ME, Bardocz S (1995) Lectins and also bacteria modify the glycosylation of gut surface receptors in the rat. Glycoconj J 12(1):22–35

    Article  CAS  PubMed  Google Scholar 

  • Pusztai A, Koninkx J, Hendriks H, Kok W, Hulscher S, Van Damme EJ et al (1996) Effect of the insecticidal Galanthus nivalis agglutinin on metabolism and the activities of brush border enzymes in the rat small intestine. J Nutr Biochem 7(12):677–682

    Article  CAS  Google Scholar 

  • Quilis J, López-García B, Meynard D, Guiderdoni E, San Segundo B (2014) Inducible expression of a fusion gene encoding two proteinase inhibitors leads to insect and pathogen resistance in transgenic rice. Plant Biotechnol J 12(3):367–377

    Article  CAS  PubMed  Google Scholar 

  • Rahbé Y, Sauvion N, Febvay G, Peumans WJ, Gatehouse AM (1995) Toxicity of lectins and processing of ingested proteins in the pea aphid Acyrthosiphon pisum. Entomol Exp Appl 76(2):143–155

    Article  Google Scholar 

  • Ramachandraiah G, Chandra NR (2000) Sequence and structural determinants of mannose recognition. Proteins Struct Func Bioinf 39(4):358–364

    Article  CAS  Google Scholar 

  • Rani A, Chand S, Thakur N, Nath AK (2018) Alpha-amylase inhibitor from local common bean selection: effect on growth and development of Corcyra cephalonica. J Stored Prod Res 75:35–37

    Article  Google Scholar 

  • Rao K, Rathore KS, Hodges TK, Fu X, Stoger E, Sudhakar D et al (1998) Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper. Plant J 15(4):469–477

    Article  CAS  PubMed  Google Scholar 

  • Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS One 8(6):e66428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romeis J, Babendreier D, Wäckers FL (2003) Consumption of snowdrop lectin (Galanthus nivalis agglutinin) causes direct effects on adult parasitic wasps. Oecologia 134(4):528–536

    Article  PubMed  Google Scholar 

  • Roy A, Das S (2015) Molecular mechanism underlying the entomotoxic effect of Colocasia esculenta tuber agglutinin against Dysdercus cingulatus. Insects 6(4):827–846

    Article  PubMed Central  Google Scholar 

  • Roy A, Gupta S, Hess D, Das KP, Das S (2014) Binding of insecticidal lectin Colocasia esculenta tuber agglutinin (CEA) to midgut receptors of Bemisia tabaci and Lipaphis erysimi provides clues to its insecticidal potential. Proteomics 14(13–14):1646–1659

    Article  CAS  PubMed  Google Scholar 

  • Sadeghi A, Broeders S, De Greve H, Hernalsteens JP, Peumans WJ, Van Damme EJ, Smagghe G (2007) Expression of garlic leaf lectin under the control of the phloem-specific promoter Asus1 from Arabidopsis thaliana protects tobacco plants against the tobacco aphid (Myzus nicotianae). Pest Manag Sci 63(12):1215–1223

    Article  CAS  PubMed  Google Scholar 

  • Sadeghi A, Smagghe G, Broeders S, Hernalsteens J-P, De Greve H, Peumans WJ, Van Damme EJ (2008) Ectopically expressed leaf and bulb lectins from garlic (Allium sativum L.) protect transgenic tobacco plants against cotton leafworm (Spodoptera littoralis). Transgenic Res 17(1):9

    Article  CAS  PubMed  Google Scholar 

  • Saha P, Majumder P, Dutta I, Ray T, Roy S, Das S (2006) Transgenic rice expressing Allium sativum leaf lectin with enhanced resistance against sap-sucking insect pests. Planta 223(6):1329

    Article  CAS  PubMed  Google Scholar 

  • Schwefel D, Maierhofer C, Beck JG, Seeberger S, Diederichs K, Möller HM et al (2010) Structural basis of multivalent binding to wheat germ agglutinin. J Am Chem Soc 132(25):8704–8719

    Article  CAS  PubMed  Google Scholar 

  • Scott JG, Michel K, Bartholomay LC, Siegfried BD, Hunter WB, Smagghe G et al (2013) Towards the elements of successful insect RNAi. J Insect Physiol 59(12):1212–1221

    Article  CAS  PubMed  Google Scholar 

  • Sengupta S, Chakraborti D, Mondal HA, Das S (2010) Selectable antibiotic resistance marker gene-free transgenic rice harbouring the garlic leaf lectin gene exhibits resistance to sap-sucking planthoppers. Plant Cell Rep 29(3):261–271

    Article  CAS  PubMed  Google Scholar 

  • Sétamou M, Bernal J, Legaspi J, Mirkov T, Legaspi B Jr (2002) Evaluation of lectin-expressing transgenic sugarcane against stalkborers (Lepidoptera: Pyralidae): effects on life history parameters. J Econ Entomol 95(2):469–477

    Article  PubMed  Google Scholar 

  • Shang C, Peumans WJ, Van Damme EJ (2014) Occurrence and taxonomical distribution of ribosome-inactivating proteins belonging to the Ricin/Shiga toxin superfamily. In: Ribosome-inactivating proteins: ricin and related proteins, pp 11–27

    Google Scholar 

  • Sharon N, Lis H (1990) Legume lectins–a large family of homologous proteins. FASEB J 4(14):3198–3208

    Article  CAS  PubMed  Google Scholar 

  • Silva CP, Terra WR, Xavier-Filho J, de Sá MFG, Isejima EM, DaMatta RA et al (2001) Digestion of legume starch granules by larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae) and the induction of α–amylases in response to different diets. Insect Biochem Mol Biol 31(1):41–50

    Article  CAS  PubMed  Google Scholar 

  • Sinha S, Gupta G, Vijayan M, Surolia A (2007) Subunit assembly of plant lectins. Curr Opin Struct Biol 17(5):498–505

    Article  CAS  PubMed  Google Scholar 

  • Solleti SK, Bakshi S, Purkayastha J, Panda SK, Sahoo L (2008) Transgenic cowpea (Vigna unguiculata) seeds expressing a bean α-amylase inhibitor 1 confer resistance to storage pests, bruchid beetles. Plant Cell Rep 27(12):1841

    Article  CAS  PubMed  Google Scholar 

  • Stahl E, Hilfiker O, Reymond P (2018) Plant–arthropod interactions: who is the winner? Plant J 93(4):703–728

    Article  CAS  PubMed  Google Scholar 

  • Stanisçuaski F, Carlini CR (2012) Plant ureases and related peptides: understanding their entomotoxic properties. Toxins 4(2):55–67

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stanisçuaski F, Ferreira-Dasilva C, Mulinari F, Pires-Alves M, Carlini C (2005) Insecticidal effects of canatoxin on the cotton stainer bug Dysdercus peruvianus (Hemiptera: Pyrrhocoridae). Toxicon 45(6):753–760

    Article  PubMed  CAS  Google Scholar 

  • Stillmark H (1992) Uber ricin, eines giftiges ferment aus den samen von Ricinus communis L. und Anderson Euphorbiacen, inaugural Disseration, University of Dorpat, Estonia. 1888.(German) IV. A fate of orally administered ricin in rats. J Pharm 15:147–156

    Google Scholar 

  • Stirpe F (2013) Ribosome-inactivating proteins: from toxins to useful proteins. Toxicon 67:12–16

    Article  CAS  PubMed  Google Scholar 

  • Sumner JB (1919) The globulins of the jack bean, canavalia ensiformis preliminary paper. J Biol Chem 37(1):137–142

    Article  CAS  Google Scholar 

  • Swamy S, Prasad N, Rao N (2009) Transgenic Bt crops: a major component of integrated pest management–an overview. Indian J Crop Sci 4(1and2):1–10

    Google Scholar 

  • Tajne S, Boddupally D, Sadumpati V, Vudem DR, Khareedu VR (2014) Synthetic fusion-protein containing domains of Bt Cry1Ac and Allium sativum lectin (ASAL) conferred enhanced insecticidal activity against major lepidopteran pests. J Biotechnol 171:71–75

    Article  CAS  PubMed  Google Scholar 

  • Taylor ME, Drickamer K (2009) Structural insights into what glycan arrays tell us about how glycan-binding proteins interact with their ligands. Glycobiology 19(11):1155–1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor SL, Hefle SL (2001) Will genetically modified foods be allergenic? J Allergy Clin Immunol 107(5):765–771

    Article  CAS  PubMed  Google Scholar 

  • Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, Kanginakudru S et al (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57(2):231–245

    Article  CAS  PubMed  Google Scholar 

  • Thevissen K, Terras FR, Broekaert WF (1999) Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl Environ Microbiol 65(12):5451–5458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Titarenko E, Chrispeels MJ (2000) cDNA cloning, biochemical characterization and inhibition by plant inhibitors of the α-amylases of the Western corn rootworm, Diabrotica virgifera virgifera. Insect Biochem Mol Biol 30(10):979–990

    Article  CAS  PubMed  Google Scholar 

  • Van Damme EJ (2014) History of plant lectin research. In: Lectins. Springer, pp 3–13

    Google Scholar 

  • Van Damme EJ, Peumans WJ, Pusztai A, Bardocz S (1998) Handbook of plant lectins: properties and biomedical applications. Wiley, Chichester

    Google Scholar 

  • Van Damme EJ, Lannoo N, Fouquaert E, Peumans WJ (2003) The identification of inducible cytoplasmic/nuclear carbohydrate-binding proteins urges to develop novel concepts about the role of plant lectins. Glycoconj J 20(7–8):449–460

    Article  Google Scholar 

  • Van Damme EJ, Lannoo N, and Peumans WJ (2008) Plant lectins. In Advances in botanical research, vol 48, pp 107–209. Elsevier

    Google Scholar 

  • Vandenborre G, Groten K, Smagghe G, Lannoo N, Baldwin IT, Van Damme EJ (2009a) Nicotiana tabacum agglutinin is active against lepidopteran pest insects. J Exp Bot 61(4):1003–1014

    Article  PubMed  CAS  Google Scholar 

  • Vandenborre G, Miersch O, Hause B, Smagghe G, Wasternack C, Van Damme EJ (2009b) Spodoptera littoralis-induced lectin expression in tobacco. Plant Cell Physiol 50(6):1142–1155

    Article  CAS  PubMed  Google Scholar 

  • Vandenborre G, Van Damme EJ, Ghesquiere B, Menschaert G, Hamshou M, Rao RN et al (2010) Glycosylation signatures in Drosophila: fishing with lectins. J Proteome Res 9(6):3235–3242

    Article  CAS  PubMed  Google Scholar 

  • Vandenborre G, Smagghe G, Van Damme EJ (2011) Plant lectins as defense proteins against phytophagous insects. Phytochemistry 72(13):1538–1550

    Article  CAS  PubMed  Google Scholar 

  • Vazquez-Padron RI, Moreno-Fierros L, Neri-Bazán L, Gustavo A, Lopez-Revilla R (1999) Intragastric and intraperitoneal administration of Cry1Ac protoxin from Bacillus thuringiensis induces systemic and mucosal antibody responses in mice. Life Sci 64(21):1897–1912

    Article  CAS  PubMed  Google Scholar 

  • Vázquez-Padrón RI, Gonzáles-Cabrera J, García-Tovar C, Neri-Bazan L, Lopéz-Revilla R, Hernández M et al (2000) Cry1Ac protoxin from Bacillus thuringiensis sp. kurstaki HD73 binds to surface proteins in the mouse small intestine. Biochem Biophys Res Commun 271(1):54–58

    Article  PubMed  CAS  Google Scholar 

  • Vijayan S, Imani J, Tanneeru K, Guruprasad L, Kogel K, Kirti P (2012) Enhanced antifungal and insect α-amylase inhibitory activities of Alpha-TvD1, a peptide variant of Tephrosia villosa defensin (TvD1) generated through in vitro mutagenesis. Peptides 33(2):220–229

    Article  CAS  PubMed  Google Scholar 

  • Vijayan S, Singh N, Shukla P, Kirti P (2013) Defensin (TvD1) from Tephrosia villosa exhibited strong anti-insect and anti-fungal activities in transgenic tobacco plants. J Pest Sci 86(2):337–344

    Article  Google Scholar 

  • Virgilio MD, Lombardi A, Caliandro R, Fabbrini MS (2010) Ribosome-inactivating proteins: from plant defense to tumor attack. Toxins 2(11):2699–2737

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waage J (1997) What does biotechnology bring to integrated pest management? Biotechnol Dev Monit 32:19–21

    Google Scholar 

  • Walski T, Van Damme EJ, Smagghe G (2014) Penetration through the peritrophic matrix is a key to lectin toxicity against Tribolium castaneum. J Insect Physiol 70:94–101

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Guo S (1999) Expression of two insect-resistant genescryIA (b&c)/GNA in transgenic tobacco plants results in added protection against both cotton bollworm and aphids. Chin Sci Bull 44(22):2051–2058

    Article  CAS  Google Scholar 

  • Wang Z, Zhang K, Sun X, Tang K, Zhang J (2005) Enhancement of resistance to aphids by introducing the snowdrop lectin genegna into maize plants. J Biosci 30(5):627–638

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Luo X, Guo H, Xiao J, Tian Y (2006) Transgenic cotton, expressing Amaranthus caudatus agglutinin, confers enhanced resistance to aphids. Plant Breed 125(4):390–394

    Article  CAS  Google Scholar 

  • Xu D, Xue Q, McElroy D, Mawal Y, Hilder VA, Wu R (1996) Constitutive expression of a cowpea trypsin inhibitor gene, CpTi, in transgenic rice plants confers resistance to two major rice insect pests. Mol Breed 2(2):167–173

    Article  CAS  Google Scholar 

  • Ye S-H, Chen S, Zhang F, Wang W, Tian Q, Liu J-Z et al (2009) Transgenic tobacco expressing Zephyranthes grandiflora agglutinin confers enhanced resistance to aphids. Appl Biochem Biotechnol 158(3):615–630

    Article  CAS  PubMed  Google Scholar 

  • Yoon J-S, Gurusamy D, Palli SR (2017) Accumulation of dsRNA in endosomes contributes to inefficient RNA interference in the fall armyworm, Spodoptera frugiperda. Insect Biochem Mol Biol 90:53–60

    Article  CAS  PubMed  Google Scholar 

  • Young NM, Oomen RP (1992) Analysis of sequence variation among legume lectins: a ring of hypervariable residues forms the perimeter of the carbohydrate-binding site. J Mol Biol 228(3):924–934

    Article  CAS  PubMed  Google Scholar 

  • Zadoks JC, Schein RD (1979) Epidemiology and plant disease management. Oxford University Press, New York/Oxford

    Google Scholar 

  • Zavala JA, Baldwin IT (2004) Fitness benefits of trypsin proteinase inhibitor expression in Nicotiana attenuata are greater than their costs when plants are attacked. BMC Ecol 4(1):11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang W, Peumans WJ, Barre A, Astoul CH, Rovira P, Rougé P et al (2000) Isolation and characterization of a jacalin-related mannose-binding lectin from salt-stressed rice (Oryza sativa) plants. Planta 210(6):970–978

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Liu F, Yao L, Luo C, Yin Y, Wang G, Huang Y (2012) Development and bioassay of transgenic Chinese cabbage expressing potato proteinase inhibitor II gene. Breed Sci 62(2):105–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R (2015) Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347(6225):991–994

    Article  CAS  PubMed  Google Scholar 

  • Zhu-Salzman K, Zeng R (2015) Insect response to plant defensive protease inhibitors. Annu Rev Entomol 60:233–252

    Article  CAS  PubMed  Google Scholar 

  • Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146(3):852–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

AR would like to acknowledge the EU project “EXTEMIT – K,” No. CZ.02.1.01/0.0/0.0/15_003/0000433 financed by OP RDE, outstanding output project and IGA from Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, for the financial support during the preparation of the book chapter. AC is supported by “EVA4.0,” No. CZ.02.1.01 /0.0 /0.0 /16_ 019/0000803 financed by OP RDE. Prof. Sampa Das lab, Bose Institute, Kolkata, India is acknowledged for their contribution in the field of plant lectins and their mode of action, which inspires writing this book chapter. 

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Roy, A., Chakraborty, A. (2021). Natural Insecticidal Proteins and Their Potential in Future IPM. In: Singh, I.K., Singh, A. (eds) Plant-Pest Interactions: From Molecular Mechanisms to Chemical Ecology. Springer, Singapore. https://doi.org/10.1007/978-981-15-2467-7_12

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