Skip to main content

Bacillus thuringiensis as Potential Biocontrol Agent for Sustainable Agriculture

  • Chapter
  • First Online:
Current Trends in Microbial Biotechnology for Sustainable Agriculture

Abstract

The global agricultural production needs to go up by 70% until 2050, to keep pace with ever-increasing human population and is a major challenge of this century. Green revolution and heavy use of chemical pesticides have helped to achieve feeding objective in the past few decades by developing high-yielding cultivars and reducing yield losses due to weeds, pests, and diseases. The use of biocontrol agents is almost a century-old concept in agriculture, but their applications were limited due to the development of highly effective chemical pesticides in the past half a dozen decades. However, chemical insecticides have prolonged leaching residual effects, leading to environmental damages and adverse effects on other organisms involved in the biogeochemical cycle. Besides, excessive use of chemical pesticides generates tolerance in pests. Therefore, safer pest management options are required to preserve environmental sustainability. The use of biocontrol agents with specificity in their targets is one of the widespread pest control approaches in plant health management. Recently, increased demand for biocontrol agents is mainly the result of the changed perception of human–society preferring a healthy environment and safety over the effectiveness with harmful side effects. Most successful of all the biocontrol agents, Bacillus thuringiensis and its potential as a biocontrol agent, is discussed in this chapter.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdullah MAF, Alzate O, Mohammad M, McNall RJ, Adang MJ, Dean DH (2003) Introduction of Culex toxicity into B. thuringiensis Cry4Ba by protein engineering. Appl Environ Microbiol 69:5343–5353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adang MJ, Crickmore N, Jurat-Fuentes JL (2014) Chapter two-diversity of Bacillus thuringiensis crystal toxins and mechanism of action. Adv Insect Physiol 47:39–87

    Article  Google Scholar 

  • Anderson K (2010) Globalization's effects on world agricultural trade, 1960–2050. Philos Trans R Soc Lond Ser B Biol Sci 365:3007–3021

    Article  Google Scholar 

  • Andrews RE, Bibilops MM, Bulla LA (1985) Protease activation of the entomocidal protoxin of Bacillus thuringiensis subsp. kurstaki. Appl Environ Microbiol 50:737–742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Angsuthanasombat C (2010) Structural basis of pore formation by mosquito-larvicidal proteins from Bacillus thuringiensis. Open Toxinol J 3:119–125

    Article  Google Scholar 

  • Aronson AI, Wu D, Zhang C (1995) Mutagenesis of specificity and toxicity regions of a Bacillus thuringiensis protoxin gene. J Bacteriol 177:4059–4065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asano SC, Yamashita C, Iizuka T, Takeuchi K, Yamanaka S, Cerf D, Yamamoto T (2003) A strain of B. thuringiensis subsp. galleriae containing a novel cry8 gene highly toxic to Anomala cuprea (Coleoptera: Scarabaeidae). Biol Control 28:191–196

    Article  CAS  Google Scholar 

  • Astuti DT, Pujiastuti Y, Suparman SHK, Damiri N, Nugraha S, Sembiring ER et al (2018) Exploration of Bacillus thuringiensis Berl. From soil and screening test its toxicity on insects of Lepidoptera order. IOP Conf Ser earth. Environ Sci 102:012063

    Google Scholar 

  • Attathom T, Chongrattanameteekul W, Chanpaisang J, Siriyan R (1995) Morphological diversity and toxicity of delta-endotoxin produced by various strains of B. thuringiensis. Bull Ent Res 85:167–173

    Article  CAS  Google Scholar 

  • Badran A, Guzov V, Huai Q, Kemp M, Vishwanath P, Kain W (2016) Continuous evolution of Bacillus thuringiensis toxins overcomes insect resistance. Nature 533:58–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ballester V, Granoro F, Tabashnik BE, Malvar T, Ferre J (1999) Integrative model for binding of Bacillus thuringiensis toxins in susceptible and resistant larvae of the diamondback moth (Plutella xylostella). Appl Environ Microbiol 65:1413–1419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baum JA, Kakefuda M, Gawron-Burke C (1996) Engineering Bacillus thuringiensis bioinsecticides with an indigenous site-specific recombination system. Appl Environ Microbiol 62:4367–4373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baxter SW, Zhao JZ, Gahan LJ, Shelton AM, Tabashnik BE, Heckel DG (2005) Novel genetic basis of field-evolved resistance to Bt toxins in Plutella xylostella. Insect Mol Biol 14:327–334

    Article  CAS  PubMed  Google Scholar 

  • Beattie SH, Halt C, Hirst D, Williams AG (1998) Discrimination among Bacillus cereus, Bacillus mycoides and Bacillus thuringiensis and some other species of the genus Bacillus by Fourier transform infrared spectroscopy. FEMS Microbiol Lett 164:201–206

    Article  CAS  PubMed  Google Scholar 

  • Beegle CC, Yamamoto T (1992) History of Bacillus thuringiensis Berliner research and development. Can Entomol 124:587–616

    Article  Google Scholar 

  • Bernhard K, Jarrett P, Meadows M, Butt J, Ellis DJ, Roberts GM, Pauli S, Rodgers P, Burges HD (1997) Natural isolates of B. thuringiensis: worldwide distribution, characterization and activity against insect pests. J Invertebr Pathol 70:59–68

    Article  Google Scholar 

  • Bideshi DK, Park HW, Hice RH, Wirth MC, Federeci BA (2017) Highly effective broad spectrum chimeric larvicide that targets vector mosquitoes using a lipophilic protein. Sci Rep 7(1):11282

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Biswas S, Kundu D, Mazumdar S, Saha A, Majumdar B, Ghorai A et al (2018) Study on the activity and diversity of bacteria in a new Gangetic alluvial soil (Eutrocrept) under rice-wheat-jute cropping system. J Environ Biol 39:379–386

    Article  CAS  Google Scholar 

  • Boonserm P, Davis P, Ellar DJ, Li J (2005) Crystal structure of the mosquito-larvicidal toxin Cry4Ba and its biological implications. J Mol Biol 348:363–382

    Article  CAS  PubMed  Google Scholar 

  • Boonserm P, Mo M, Angsuthanasombat C, Lescar J (2006) Structure of the functional form of the mosquito larvicidal Cry4Aa toxin from Bacillus thuringiensis at a 2.8-angstrom resolution. J Bacteriol 188:3391–3401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bourque SN, Valero JR, Lavoie MC, Levesque RC (1995) Comparative analysis of the 16S to 23S ribozomal intergenic spacer sequences of Bacillus thuringiensis strains and subspecies and of closely related species. Appl Environ Microbiol 61:1623–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brar SK, Verma M, Tyagi RD, Valero JRC (2006) Recent advances in downstream processing and formulations of Bacillus thuringiensis based biopesticides. Process Biochem 41:323–342

    Article  CAS  Google Scholar 

  • Bravo A, Gomez I, Conde J, MuÇoz-Garay C, Snchez J, Miranda R, Zhuang M, Gill SS, Soberon M (2004) Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochem Biophys Acta 1667:38–46

    Article  CAS  PubMed  Google Scholar 

  • Bravo A, Gill SS, Sobero NM (2005) Bacillus thuringiensis mechanisms and use. Comprehensive Molecular Insect Science 56:175–206

    Article  Google Scholar 

  • Bravo A, Gill SS, Soberon NM (2007) Mode of action of Bacillus thuringiensis toxins and their potential for insect control. Toxicon 49:423–435

    Article  CAS  PubMed  Google Scholar 

  • Bravo A, Likitvivatanavong S, Gill SS, Soberón M (2011) Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41:423–431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burton SL, Ellar DJ, Li J, Derbyshire DJ (1999) N-acetylgalactosamine on the putative insect receptor aminopeptidase N is recognized by a site on the domain III lectin like fold of a Bacillus thuringiensis insecticidal toxin. J Mol Biol 287:1011–1022

    Article  CAS  PubMed  Google Scholar 

  • Butko P (2003) Cytolytic toxin Cyt1A and its mechanism of membrane damage: data and hypotheses. Appl Environ Microbiol 69:2415–2422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabreran JG, Farinós GP, Caccia S, Mendoza MD, Castañera P, Leonardi MG, Giordana B, Ferré J (2006) Toxicity and mode of action of Bacillus thuringiensis cry proteins in the Mediterranean corn borer, Sesamia nonagrioides (Lefebvre). Appl Environ Microbiol 72:2594–2600

    Article  CAS  Google Scholar 

  • Cannon RJC (1995) Bacillus thuringiensis in pest control. In: HMT H, Lynch JM (eds) Biological control: benefits and risks. Cambridge University Press, pp 190–197

    Google Scholar 

  • Canton PE, López-Días JA, Gill SS, Bravo A, Soberon M (2014) Membrane binding and oligomer membrane insertion are necessary but insufficient for Bacillus thuringiensis Cyt1Aa toxicity. Peptides 53:286–291

    Article  CAS  PubMed  Google Scholar 

  • Carlson CR, Kolsto AB (1993) A complete physical map of a Bacillus thuringiensis chromosome. J Bacteriol 175:1053–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlson CR, Caugant DA, Kolsto AB (1994) Genotypic diversity among Bacillus cereus and Bacillus thuringiensis strains. Appl Environ Microbiol 60:1719–1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlson CR, Johansen T, Lecadet MM, Kolsto AB (1996) Genomic organization of the entomopathogenic bacterium Bacillus thuringiensis subsp. berliner 1715. Microbiol 142:1625–1634

    Article  CAS  Google Scholar 

  • Carlton BC (1996) Development and commercialization of new and improved biopesticides. Ann N Y Acad Sci 792:154–163

    Article  Google Scholar 

  • Carriere Y, Crickmore N, Tabashnik B (2015) Optimizing pyramided transgenic Bt crops for sustainable pest management. Nat Biotechnol 33:161–168

    Article  CAS  PubMed  Google Scholar 

  • Chakroun M, Banyuls N, Bel Y, Escriche B, Ferre J (2016) Bacterial vegetative insecticidal proteins (Vip) from Entomopathogenic Bacteria. Microbiol Mol Biol Rev 80(2):329–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandra A, Ghosh P, Mandoakar AD, Bera AK, Sharma RP, Das S, Kumar PA (1999) Amino acid substitution in α−helix7 Cry1Ac δ endotoxin of Bacillus thuringiensis leads to enhanced toxicity to Helicoverpa armigera Hubner. FEBS Lett 458:174–179

    Article  Google Scholar 

  • Chang C, Yu YM, Dai SM, Law SK, Gill SS (1993) High-level cryIVD and cytA gene expression does not require the 20-kilodalton protein, and the co-expressed gene products are synergistic in their toxicity to mosquitoes. Appl Environ Microbiol 59:815–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapa DF, Villalobos JR, Wong LG (2019) Toxic potential of Bacillus thuringiensis: an overview. In: Jia Y (ed) Protecting Rice Grains in the Post-Genomic Era. IntechOpen, pp 1–22

  • Chilcott CN, Wigley PJ (1994) Isolation and toxicity of B. thuringiensis from soil and insect habitats in New Zealand. J Invertebr Pathol 61:244–247

    Article  Google Scholar 

  • Chitra S, Narayanan R, Balakrishnan A, Jayaraman K (1998) A rapid and specific method for the identification of Bacillus thuringiensis strains by indirect immunofluorescence. J Invertebr Pathol 74:263–267

    Google Scholar 

  • Chougule NP, Li H, Liu S, Linz LB, Narva KE, Meade T, Bonning BC (2013) Retargeting of the Bacillus thuringiensis toxin Cyt2Aa against hemipteran insect pests. Proc Natl Acad Sci U S A 110:8465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cody V, Luft J, Jensen E, Pangborn W, English L (1992) Purification and crystalization of insecticidal delta endotoxins CryIII from Bacillus thuringiensis proteins. J Struct Funct Gen 14:324–330

    Article  CAS  Google Scholar 

  • Cohen S, Dym O, Albeck S, Ben-Dov E, Cahan R, Firer M, Zaritsky A (2008) High-resolution crystal structure of activated Cyt2Ba monomer from Bacillus thuringiensis subsp. israelensis. J Mol Biol 380:820–827

    Article  CAS  PubMed  Google Scholar 

  • Crickmore N, Zeigler DR, Feitelson J, Schnepf E, Van Rie J, Lereclus J, Baum J, Dean DH (1998) Revision of the nomenclature for the B. thuringiensis pesticidal crystal proteins. Microbiol Mol Biol Rev 62:807–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalhambar G, Steiner H (1984) Characterization of inhibitor a, a protease from Bacillus thuringiensis which degrades attacins and cecropins, two classes of antibacterial proteins in insects. Eur J Biochem 139:247–252

    Article  Google Scholar 

  • Dammak I, Dammak M, Tounsi S (2015) Histopathological and combinatorial effects of the metalloprotease InhA1 and cry proteins of Bacillus thuringiensis against Spodoptera littoralis. Int J Biol Macromol 81:759–762

    Article  CAS  PubMed  Google Scholar 

  • Davies TGE, Field LM, Williamson MS (2012) The re-emergence of the bed bug as a nuisance pest: implications of resistance to the pyrethroid insecticides. Med Vet Entomol 26:241–254

    Article  CAS  PubMed  Google Scholar 

  • De Maagd RA, Bakkar PL, Masson L, Adang MJ, Sangandala S, Stiekema W, Bosch D (1999) Domain III of the Bacillus thuringiensis delta-endotoxin Cry1Ac is involved in binding to Manduca sexta brush border membranes and to its purified amino peptidase. Mol Microbiol 31:463–471

    Article  PubMed  Google Scholar 

  • De Maagd RA, Weemen-Hendriks M, Stiekema W, Bosch D (2000) Bacillus thuringiensis delta-endotoxin Cry1C domain III can function as a specificity determinant for Spodoptera exigua in different, but not all, Cry1-Cry1C hybrids. Appl Environ Microbiol 66:1559–1563

    Article  PubMed  PubMed Central  Google Scholar 

  • De Maagd RA, Bravo A, Crickmore N (2001) How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17:193–199

    Article  PubMed  Google Scholar 

  • De Maagd RA, Bravo A, Berry C, Crickmore N, Schnepf HE (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu Rev Genet 37:409–433

    Article  PubMed  CAS  Google Scholar 

  • Deist BR, Rausch MA, Fernandez-Luna MT, Adang MJ, Bonning BC (2014) Bt toxin modification for enhanced efficacy. Toxins 6:3005–3027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denholum I, Rowland MW (1992) Tactics for management of pesticides resistant in arthropods: theory and practice. Annu Rev Ent 37:91–112

    Article  Google Scholar 

  • Derbyshire DJ, Ellar DJ, Li J (2001) Crystallization of the Bacillus thuringiensis toxin Cry1Ac and its complex with the receptor ligand N-acetyl-D-galactosamine. Acta Cryst D57:1938–1944

    CAS  Google Scholar 

  • Diehn SH, Chiy WL, De Rocher EJ, Green PJ (1998) Premature polyadenylation at multiple sites with a Bacillus thuringiensis toxin gene-coding region. Plant Physiol 117:1433–1443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding X, Luo Z, Xia L, Gao B, Sun Y, Zhang Y (2008) Improving the insecticidal activity by expression of a recombinant cry1Ac Gene with chitinase-encoding gene in acrystalliferous Bacillus thuringiensis. Curr Microbiol 56:442–447

    Article  CAS  PubMed  Google Scholar 

  • Dulmage HT, Boening OP, Rehnborg CS, Habsen GD (1971) A proposed standardized bioassay for formulations of Bacillus thuringiensis based on the international unit. J Invertebr Pathol 18:240–245

    Article  CAS  PubMed  Google Scholar 

  • Estruch JJ, Warren GW, Mullins MA, Nye GJ, Craig JA, Koziel MG (1996) Vip3A, a novel B. thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proc Natl Acad Sci U S A 93:5389–5394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feitelson JS, Payne J, Kim L (1992) B. thuringiensis: insects and beyond. Biotechnology 10:271–275

    Google Scholar 

  • Ferre J, Rie JV (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 47:501–533

    Article  CAS  PubMed  Google Scholar 

  • Flores H, Soberon X, Sanchez J, Bravo A (1997) Isolated domain II and III from the Bacillus thuringiensis Cry1Ab delta endotoxins binds to lepidopteran midgut membranes. FEBS Lett 414:313–318

    Article  CAS  PubMed  Google Scholar 

  • Forsyth G, Logan NA (2000) Isolation of Bacillus thuringiensis from northern Victoria land, Antarctica. Lett Appl Microbiol 30:263–266

    Article  CAS  PubMed  Google Scholar 

  • Galitsky N, Cody V, Wojtczak A, Ghosh D, Luft JR, Pangborn W, English L (2001) Structure of the insecticidal bacterial delta-endotoxin Cry3Bb1 of Bacillus thuringiensis. Acta Cryst D57:1101–1109

    CAS  Google Scholar 

  • Garczynski SF, Martin JA, Griset M, Willett LS, Cooper WR, Swisher KD, Unruh TR (2017) CRISPR/Cas9 editing of the codling moth (Lepidoptera: Tortricidae) cpomOR1 gene affects egg production and viability. J Econ Entomol 110:1847–1855

    Article  CAS  PubMed  Google Scholar 

  • Gatehouse AMR, Ferry N, Raemaekers RJM (2002) The case of the monarch butterfly: a verdict is returned. Trends Genet 18:249–251

    Article  CAS  PubMed  Google Scholar 

  • Gelernter WD (1997) Resistant to microbial insecticides in agriculture. In: microbial insecticides: novelty or necessity. Proc Br Crop Prot Council Symp 68:243–253

    Google Scholar 

  • Geordhiou GP, Tajeda LA (1993) The occurrence of resistant to pesticides in arthropods. FAO, Rome pp 123

    Google Scholar 

  • Gill SS, Sing GJP, Hornung JM (1987) Cell membrane activaiton of Bacillus thuringiensis subsp. israelensis cytolytic toxins. Infect Immun 55:1300–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazer AN, Nikaido H (1995) Microbial insecticides. In: Freeman WH (ed) Microbial biotechnology fundamentals of applied microbiology, New York, pp 209–229

    Google Scholar 

  • Gomez I, Snchez J, Miranda R, Bravo A, Soberon M (2002) Cadherin like receptor binding facilitates proteolytic cleavage of helix α-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis Cry1Ab toxin. FEBS Lett 513:242–246

    Article  CAS  PubMed  Google Scholar 

  • Gonzales JM, Carlton BC (1980) Patterns of plasmid DNA in crystalliferous strains of B. thuringiensis. Plasmid 3:92–98

    Article  Google Scholar 

  • Gordon RE, Haynes WC, Pang CHP (1973) The genus Bacillus. Department of Agriculture Handbook no. 427. U.S. Department of Agriculture, Washington, DC

    Google Scholar 

  • Gould F (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu Rev Entomol 43:701–726

    Article  CAS  PubMed  Google Scholar 

  • Griffitts JS, Whitacre JL, Stevens DE, Aroian RV (2001) Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme. Sci 293:860–864

    Article  CAS  Google Scholar 

  • Griffitts JS, Huffman DL, Whitacre JL, Barrows BD, Marroquin LD, Muller R, Brown JR, Hennet T, Esko JD, Aroian RV (2003) Resistance to a bacterial toxin is mediated by removal of a conserved glycosylation pathway required for toxin–host interactions. J Biol Chem 278:45594–45602

    Article  CAS  PubMed  Google Scholar 

  • Grochulski P, Masson L, Borisova S, Pusztai-Carey M, Schwartz JL, Brousseau R, Cygler M (1995) B. thuringiensis CryIA(a) insecticidal toxin: crystal structure and channel formation. J Mol Biol 254:447–464

    Article  CAS  PubMed  Google Scholar 

  • Groulx N, McGuire H, Laprade R, Schwartz JL, Blunck R (2011) Single molecule fluorescence study of the Bacillus thuringiensis toxin Cry1Aa reveals tetramerization. J Biol Chem 286:42274–42282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerchicoff A, Delécluse A, Rubinstein CP (2001) The Bacillus thuringiensis cyt genes for the hemolytic endotoxins constitute a gene family. Appl Environ Microbiol 67:1090–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gunning RV, Dang HT, Kemp FC, Nicholson IC, Moores GD (2005) New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl Environ Microbiol 71:2558–2563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo S, Ye S, Liu Y, Wei L, Xue J, Wu H, Song F, Zhang J, Wu X, Huang D, Rao Z (2009) Crystal structure of Bacillus thuringiensis Cry8Ea1: an insecticidal toxin toxic to underground pests, the larvae of Holotrichia parallela. J Struct Biol 168:259–266

    Article  CAS  PubMed  Google Scholar 

  • Hastowo S, Lay BW, Ohba M (1992) Naturally occurring B. thuringiensis in Indonesia. J Appl Bacteriol 73:108–113

    Article  Google Scholar 

  • Hautea DM, Taylo LD, Masanga APL, Sison MLJ, Narcisco JO, Quilloy RB, Hautea RA, Shotkoski FA, Shelton AM (2016) Field performance of Bt eggplants (Solanum melongena L.) in the Philippines: Cry1Ac expression and control of the eggplant fruit and shoot borer (Leucinodes orbonalis Guenée). PLoS One 11(6):e0157498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Head GP, Carroll MW, Evans SP, Rule DW, Willse AR, Clark TL, Storer NP, Flannagan RD, Samuel LW, Meinke LJ (2017) Evaluation of SmartStax and SmartStax PRO maize against western corn rootworm and northern corn rootworm: efficacy and resistance management. Pest Manag Sci 73(9):1883–1899

    Article  CAS  PubMed  Google Scholar 

  • Helgason E, Okstad OA, Caugant DA, Johansen HA, Fouet A, Mock M, Hegna I, Kolsto AB (2000) Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis one species on the basis of genetic events. Appl Environ Microbiol 66:2627–2630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hickey LT, Hafeez AN, Robinson H, Jackson SA, Leal-Bertioli SCM, Tester M, Gao C, Godwin ID, Hayes BJ, Wulff BBH (2019) Breeding crops to feed 10 billion. Nat Biotechnol 37(7):744-754

    Google Scholar 

  • Hofman C, Vanderbruggen H, Höfte H, Van-Rie J, Jansen S, Van Melleart H (1988) Specificity of Bacillus thuringiensis delta-endotoxins is correlated with the presence of high affinity binding sites in the brush border membrane of target insect midguts. Proc Natl Acad Sci U S A 85:7844–7848

    Article  Google Scholar 

  • Hofte H, Whiteley HR (1989) Insecticidal crystal proteins of B. thuringiensis. Microbiol Rev 53:242–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang F, Ghimire MN, Leonard BR, Daves C, Levy R, Baldwin J (2012) Extended monitoring of resistance to Bacillus thuringiensis Cry1Ab maize in Diatraea saccharalis (Lepidoptera: Crambidae). GM Crops 3:245–254

    Article  Google Scholar 

  • Hui F, Scheib U, Hu Y, Sommer RJ, Aroian RV, Ghosh P (2012) Structure and glycolipid binding properties of the nematicidal protein Cry5B. Biochemistry 51:9911–9921

    Article  CAS  PubMed  Google Scholar 

  • Iatsenko I, Nikolov A, Sommer RJ (2014) Identification of distinct Bacillus thuringiensis 4A4 nematicidal factors using the model nematodes Pristionchus pacificus and Caenorhabditis elegans. Toxins 6:2050–2063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • ISAAA (2017) Global status of commercialized biotech/GM crops in 2017: biotech crop adoption surges as economic benefits accumulate in 22 years. ISAAA brief no. 53. ISAAA, Ithaca, NY

    Google Scholar 

  • Jenkins JL, Lee MK, Valaitis AP, Curtiss A, Dean DH (2000) Bivalent sequential binding model of a Bacillus thuringiensis toxin to gypsy moth aminopeptidase N receptor. J Biol Chem 275:14423–14431

    Article  CAS  PubMed  Google Scholar 

  • Jouzani GS, Valijanian E, Sharafi R (2017) Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. Appl Microbiol Biotechnol 101:2691–2711

    Article  CAS  PubMed  Google Scholar 

  • Juarez-Hernández EO, Casados-Vazquez LE, del Rincon-Castro MC, Salcedo-Hernández R, Bideshi DK, Barboza-Corona JE (2015) Bacillus thuringiensis subsp. israelensis producing endochitinase ChiA74Dsp inclusions and its improved activity against Aedes aegypti. J Appl Microbiol 119:1692–1699

    Article  PubMed  CAS  Google Scholar 

  • Jurat-Fuentes JL, Adang MJ (2001) Importance of Cry1 δ-endotoxin domain II loops for binding specificity in H. virescens (L). Appl Environ Microbiol 67:323–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jurat-Fuentes JL, Adang MJ (2006) The Heliothis virescens cadherin protein expressed in Drosophila S2 cells functions as a receptor for Bacillus thuringiensis Cry1A but not Cry1Fa toxins. Biochemist 45:9688–9695

    Article  CAS  Google Scholar 

  • Karaminejadranjbar M, Eckermann KN, Ahmed HMM, CHM S, Dippel S, Marshall JM, Wimmer EA (2018) Consequences of resistance evolution in a Cas9-based sex conversion suppression gene drive for insect pest management. Proc Natl Acad Sci U S A 115:6189–6194

    Article  CAS  Google Scholar 

  • Karlova R, Weeman-Hendriks M, Naimov S, Ceron J, Dukiandjiev S, de Maagd RA (2005) Bacillus thuringiensis δ-endotoxin Cry1Ac domain–III enhances activity against Heliothis virescens in some, but not all Cry 1-Cry1Ac hybrids. J Invertebr Pathol 88:169–172

    Article  CAS  PubMed  Google Scholar 

  • Khanna HK, Raina SK (2002) Elite indica transgenic plants expressing modified cry 1Ac endotoxin of Bacillus thuringiensis show enhanced resistance to yellow stem borer (Scirpophaga incertulas). Transgenic Res 11:411–423

    Article  CAS  PubMed  Google Scholar 

  • Kido S, Doi Y, Kim F, Morishita E, Narita H, Kanaya S, Ohkubo T, Nishikawa K, Yao T, Ooi T (1995) Characterization of vitelline membrane outer layer protein I, VMO-I: amino acid sequence and structural stability. J Biochem 117:1183–1191

    Article  CAS  PubMed  Google Scholar 

  • Knowles BH (1994) Mechanism of action of Bacillus thuringiensis insecticidal δ-endotoxins. Adv Insect Physiol 24:275–308

    Article  CAS  Google Scholar 

  • Knowles BH, Knight PJ, Ellar DJ (1991) N-Acetylgalactosamine is a part of the receptor in the insect gut epithelia that recognizes an insecticidal protein from Bacillus thuringiensis. Proc R Soc Lond B 245:31–35

    Article  CAS  Google Scholar 

  • Koller CN, Bauer LS, Hollingworth RM (1992) Characterization of the pH-mediated solubility of B. thuringiensis var. sandiego native δ-endotoxin crystals. Biochem Biophys Res Commun 184:692–699

    Article  CAS  PubMed  Google Scholar 

  • Kour D, Rana KL, Yadav AN, Yadav N, Kumar M, Kumar V et al (2020) Microbial biofertilizers: bioresources and eco-friendly technologies for agricultural and environmental sustainability. Biocatal Agric Biotechnol 23:101487. https://doi.org/10.1016/j.bcab.2019.101487

    Article  Google Scholar 

  • Koziel MG, Beland GL, Bowman C, Carozzi NB, Crenshaw R, Crossland L, Dawson J, Desai N, Hill M, Kadwell S, Launis K, Maddox D, McPherson K, Meghji MR, Merlin R, Rhodes R, Warren GW, Wright M, Evola SV (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from B. thuringiensis. Bio Technol 11:194–200

    CAS  Google Scholar 

  • Krieg VA, Huger AM, Longenbruch GA, Schnetter W (1983) B. thuringiensis var. tenebrionis: a new pathotype effective against larvae of coleoptera. Z Angew Entomol 96:500

    Article  Google Scholar 

  • Kumar H, Kumar V (2004) Tomato expressing Cry1Ab insecticidal proteins from Bacillus thuringiensis protected against tomato fruit borer Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) damage in laboratory, greenhouse and field. Crop Prot 23:135–139

    Article  CAS  Google Scholar 

  • Kumar GVS, Swamy SVSG (2014) A duo-decennium of Bt cotton adoption in India: an overview. Curr Biotica 8:322–340

    Google Scholar 

  • Landen R, Bryne M, Abdel-Hameed A (1994) Distribution of B. thuringiensis strains in southern Sweden. World J Microbiol Biotechnol 10:45–50

    Article  CAS  PubMed  Google Scholar 

  • Lecadet MM, Frachon E, Dumanoir VC, Ripouteau H, Hamon S, Laurent P, Thiey I (1999) Updating the H-antigen classification of B. thuringiensis. J Appl Microbiol 86:660–672

    Article  CAS  PubMed  Google Scholar 

  • Lee MK, Milne RE, Ge AZ, Dean DH (1995) Location of a Bombyx mori receptor binding region on a Bacillus thuringiensis δ-endotoxin. J Biol Chem 267:3115–3121

    Article  Google Scholar 

  • Lee MK, Walters FS, Hart H, Palekar N, Chen JS (2003) The mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3A differs from that of Cry1Ab δ-endotoxin. Appl Environ Microbiol 69(8):4648–4657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lereclus D, Mahillon J, Menou G, Lecadet MM (1986) Identification of Tn 4430, a transposon of Bacillus thuringiensis functional in Escherichia coli. Mol Gen Genet 204:52–57

    Article  CAS  PubMed  Google Scholar 

  • Levinson BL (1990) High performance liquid charamotography analysis of two β-exotoxins produced by some Bacillus thuringiensis strains. In: Hickle LA, Fitch WL (eds) Analytical chemistry of Bacillus thuringiensis. American Chemical Society, Washington, DC, pp 114–136

    Chapter  Google Scholar 

  • Li J, Caroll J, Ellar DJ (1991) Crystal structure of insecticidal δ-endotoxin from Bacillus thuringiensis at 2.5 Å resolution. Nature 353:815–821

    Article  CAS  PubMed  Google Scholar 

  • Li J, Koni PA, Ellar DJ (1996) Structure of the mosquitocidal δ-endotoxin CytB from Bacillus thuringiensis ssp. kyushuensis and implications for membrane pore formation. J Mol Biol 257:129–152

    Article  CAS  PubMed  Google Scholar 

  • Li H, Gonzalez-Cabrera J, Opert B, Ferre J, Higgins RA, Suschman LL, Radke GA, Zhu KY, Huang F (2004) Binding analysis of Cry1Ab and Cry1Ac with membrane vesicles from Bt resistant and susceptible Ostrinia nubilalis. Biochem Biophys Res Commun 323:52–57

    Article  CAS  PubMed  Google Scholar 

  • Lin Y, Fang G, Cai F (2008) The insecticidal crystal protein Cry2Ab10 from Bacillus thuringiensis: cloning, expression, and structure simulation. Biotechnol Lett 30:513–519

    Article  CAS  PubMed  Google Scholar 

  • Lin X, Parthasarathy K, Surya W, Zhang T, Mu Y, Torres J (2014) A conserved tetrameric interaction of cry toxin helix 3 suggests a functional role for toxin oligomerization. Biochim Biophys Acta 1838:1777–1784

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Ruan L, Peng D, Li L, Sun M, Yu Z (2014) Thuringiensin: a thermostable secondary metabolite from Bacillus thuringiensis with insecticidal activity against a wide range of insects. Toxins 6:2229–2238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu Q, Hallerman E, Peng Y, Li Y (2016) Development of Bt rice and Bt maize in China and their efficacy in target pest control. Int J Mol Sci 17:E1561

    Article  PubMed  CAS  Google Scholar 

  • Liu YL, Wang YL, Shu CL, Lin KJ, Song FP, Bravo A, Sobero’n M, Zhang J (2018) Cry64Ba and Cry64Ca, two ETX/MTX2-type Bacillus thuringiensis insecticidal proteins active against hemipteran pests. Appl Environ Microbiol 84:e01996-e01917. (doi:https://doi.org/10.1128/AEM.01996-17)

  • Lopez-pazos SA, Ceron-salamanca JA (2007) Three-dimensional structure of Bacillus thuringiensis toxins: a review. Acta Biol Colomb 12(2):19–32

    Google Scholar 

  • Lovgren AM, Zang Y, Engstöm A, Dalhammar G, Landen R (1990) Molecular characterization of immune inhibitor a, a secreted virulence protease from Bacillus thuringiensis. Mol Microbiol 4:2137–2146

    Article  CAS  PubMed  Google Scholar 

  • MacIntosh SC, Kishore GM, Perlak FJ, Marrone PG, Stone TB, Sims SR, Fuchs RL (1990) Potentiation of Bacillus thuringiensis insecticidal activity by serine protease inhibitors. J Agricult Food Chem 38:1145–1152

    Article  CAS  Google Scholar 

  • Mahillon J, Rezsöhazy R, Ballet B, Delcour J (1994) IS231 and other Bacillus thuringiensis transposable elements: a review. Genetica 93:13–26

    Article  CAS  PubMed  Google Scholar 

  • Marroquin LD, Elyssnia D, Griffitts JS, Feitelson JS, Aroian RV (2000) Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Ceanorhabditis elegans. Genetics 155:1693–1699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez C, Caballero P (2002) Contents of cry genes and insecticidal toxicity of B. thuringiensis strains from terrestrial and aquatic habitats. J Appl Microbiol 92:745–752

    Article  CAS  PubMed  Google Scholar 

  • Melo AL, Soccol VT, Soccol CR (2016) Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review. Crit Rev Biotechnol 36:317–326

    Article  CAS  PubMed  Google Scholar 

  • Mendez-Lopez I, Basurto-Ríos R, Ibarra JE (2003) B. thuringiensis serovar israelensis is highly toxic to the coffee berry borer, Hypothenemus hamper Ferr. (Coleoptera: Scolytidae). FEMS Microbiol Lett 11131:1-5

    Google Scholar 

  • Moellenbeck DJ, Peters ML, Bing JW, Rouse JR, Higgins LS, Sims L, et al. (2001) Insecticidal proteins from Bacillus thuringiensis protect corn from corn root worms. Nature Biotechnol 19:668–672

    Google Scholar 

  • Morse RJ, Yamamoto T, Stroud RM (2001) Structure of Cry2Aa suggests an unexpected receptor binding epitope. Structure 9:409–417

    Article  CAS  PubMed  Google Scholar 

  • Nava PE, García GC, Camacho BJR, Vázquez MEL (2012) Bioplaguicidas: Una opción para el control biológico de plagas. Ra Ximhai 8:17–29

    Article  Google Scholar 

  • Oerke E, Dehne H (1997) Global crop production and the efficacy of crop protection-current situation and future trends. Eur J Plant Pathol 103:203–215

    Article  Google Scholar 

  • Oppert B, Kramer KJ, Beeman RW, Johnson D, McGaughey WH (1997) Proteinase mediated insect resistance to B. thuringiensis toxins. J Biochem 272:23473–23476

    CAS  Google Scholar 

  • Ounjai P, Unger VM, Sigworth FJ, Angsuthanasombat C (2007) Two conformational states of the membrane-associated Bacillus thuringiensis Cry4Ba -endotoxin complex revealed by electron crystallography: implications for toxin-pore formation. Biochem Biophys Res Commun 361:890–895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palma L, Muñoz D, Berry C, Murillo J, Caballero P (2014) Bacillus thuringiensis toxins: an overview of their Biocidal activity. Toxins 6:3296–3325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pardo-Lopez L, Gomez I, Rausell C, Snchez J, Soberon M, Bravo A (2006) Structural changes of the Cry1Ac oligomeric pre-pore from Bacillus thuringiensis induced by N-acetylgalactosamine facilitates toxin membrane insertion. Biochemistry 45:10329–10336

    Article  CAS  PubMed  Google Scholar 

  • Pardo-Lopez L, Soberon M, Bravo A (2013) Bacillus thuringiensis insecticidal three-domain cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev 37:3–22

    Article  CAS  PubMed  Google Scholar 

  • Perlak FJ, Fuchs RL, Dean DA, McPherson SL, Fischhnff DA (1991) Modification of the coding sequence enhances plant expression of insect control protein genes. Proc Natl Acad Sci U S A 88:3324–3328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perlak FJ, Stone TB, Muskopf YM, Petersen LJ, Parker GB, McPherson SA, Yman J, Love S, Reed G, Biever D (1993) Genetically improved potatoes: protection from damage by Colorado potato beetles. Plant Mol Biol 22:313–321

    Article  CAS  PubMed  Google Scholar 

  • Peyronnet O, Vachon V, Schwartz JL, Laprade R (2001) Ion channels induced in planar lipid bilayers by the Bacillus thuringiensis toxin Cry1Aa in the presence of gypsy moth (Lymantria dispar) brush border membrane. J Membr Biol 184:45–54

    Article  CAS  PubMed  Google Scholar 

  • Pimentel D, Burgess M (2014) Environmental and economic costs of the application of pesticides primarily in the United States. In: Pimentel D, Peshin R (eds) Integrated Pest management. Springer, Dordrecht, pp 47–71

    Chapter  Google Scholar 

  • Pohare MB (2010) Cloning of cry2a gene from a new isolate of Bacillus thuringiensis and its expression in E. coli (Master’s thesis). Tamil Nadu agricultural University, Coimbatore

    Google Scholar 

  • Pohare MB, Akita M (2017) A rapid and simple, recombination-based cloning method in Escherichia coli. Biosci Biotechnol Res Asia 14(1):43–52

    Article  Google Scholar 

  • Pohare MB, Bhor SA, Patil PK, Gakkula M (2017) Integrated and sustainable initiative towards better farm returns led by rural youth. Popular Kheti 5(3):113–115

    Google Scholar 

  • Pohare MB, Sharma M, Wagh SG (2019) CRISPR/Cas9 genome editing and its medical potential. In: Kumar S (ed) Advances in biotechnology and biosciences. NavNik Publications, Pusa, pp 69–90

    Google Scholar 

  • Portugal L, Gringorten JL, Caputo GF, Mario Soberón M, Muñoz-Garay C, Bravo A (2014) Toxicity and mode of action of insecticidal Cry1A proteins from Bacillus thuringiensis in an insect cell line, CF-1. Peptides 53:292–299

    Article  CAS  PubMed  Google Scholar 

  • Rajamohan N (1998) Pesticides resistance -A global scenario. Pesticide Wld 3:34–40

    Google Scholar 

  • Ramachandran S, Buntin GD, Tabashnik JN, Reymer BE, Adang PL, Pulliam MJ, Steward DA (1998) Survival, development and oviposition of resistant diamondback moth (Lepidoptera: Plutellidae) on transgenic canola toxin. J Econ Entomol 91:1239–1244

    Article  Google Scholar 

  • Ramalakshmi A, Udayasuriyan V (2010) Diversity of Bacillus thuringiensis isolated from Western Ghats of Tamil Nadu state, India. Curr Microbiol 61:13–18

    Article  CAS  PubMed  Google Scholar 

  • Ranjithkumar L, Patil BV, Ghante VN, Bheemanna M, Arunkumar H (2013) Baseline sensitivity of brinjal shoot and fruit borer, Leucinodes orbonalis (guene’e) in South India to Cry1Ac insecticidal protein of Bacillus thuringiensis. Curr Sci 105:366–370

    Google Scholar 

  • Raybould A, Vlachos D (2011) Non-target organism effects tests on Vip3A and their application to the ecological risk assessment for cultivation of MIR162 maize. Transgenic Res 20:599–611

    Article  CAS  PubMed  Google Scholar 

  • Reinoso PY, Del Rincón CMC, Ibarra EJ (2016) Characterization of a highly toxic strain of Bacillus thuringiensis serovar kurstaki very similar to the HD-73 strain. FEMS Microbiol Rev 363:1–6

    Google Scholar 

  • Reyaz AL, Balakrishnan N, Udayasuriyan V (2019) Genome sequencing of B. thuringiensis isolate T414 toxic to pink bollworm and its insecticidal genes. Microb Pathog 134:103553

    Article  CAS  PubMed  Google Scholar 

  • Sahay H, Yadav AN, Singh AK, Singh S, Kaushik R, Saxena AK (2017) Hot springs of Indian Himalayas: potential sources of microbial diversity and thermostable hydrolytic enzymes. 3. Biotech 7:1–11

    Google Scholar 

  • Sajid M, Geng C, Li M, Wang Y, Liu H, Zheng J, Peng D, Sun M (2018) Whole genomic analysis of Bacillus thuringiensis revealing partial genes as a source of novel cry toxins. Appl Microbiol Biotechnol 84:e00277–e00218

    Google Scholar 

  • Sasaki J, Asano S, Hashimoto N, Lay BW, Hastowo S, Bando H, Jizuka T (1997) Characterization of a cry2A gene cloned from an isolate of B. thuringiensis serovar sotto. Curr Microbiol 35:1–8

    Article  PubMed  Google Scholar 

  • Saxena AK, Yadav AN, Rajawat M, Kaushik R, Kumar R, Kumar M et al (2016) Microbial diversity of extreme regions: an unseen heritage and wealth. Indian J Plant Genet Resour 29:246–248

    Article  Google Scholar 

  • Saxena AK, Padaria JC, Gurjar GT, Yadav AN, Lone SA, Tripathi M et al. (2020) Insecticidal formulation of novel strain of Bacillus thuringiensis AK 47. Indian Patent 340541

    Google Scholar 

  • Schnepf HE, Whiteley HR (1981) Cloning and expression of the B. thuringiensis protein gene in E. coli. Proc Natl Acad Sci U S A 78:2989–2897

    Article  Google Scholar 

  • Schnepf HE, Crickmore N, Van Rie J, Lerecurs D, Baum J, Feitelson J, Zeigler JDR, Dean DH (1998) B. thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao E, Lin L, Chen C, Chen H, Zhuang H, Wu S, Sha L, Guan X, Huang Z (2016) Loop replacements with gut-binding peptides in Cry1Ab domain II enhanced toxicity against the brown planthopper, Nilaparvata lugens (Stal). Sci Rep 6:20106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shelake RM, Pramanik D, Kim JY (2019a) Exploration of plant-microbe interactions for sustainable agriculture in CRISPR era. Microorganisms 7(8):269

    Article  PubMed Central  Google Scholar 

  • Shelake RM, Pramanik D, Kim JY (2019b) Evolution of plant mutagenesis tools: a shifting paradigm from random to targeted genome editing. Plant Biotechnol Rep 13:423–445

    Article  Google Scholar 

  • Shelton AM, Zhao JZ, Roush RT (2002) Economic, ecological, food safety and social consequences of the deployment of Bt transgenic plants. Annu Rev Entomol 47:845–881

    Article  CAS  PubMed  Google Scholar 

  • Shelton AM, Hossain MJ, Paranjape V, Azad AK, Rahman ML, Khan ASMMR, et al. (2018) Bt eggplant project in Bangladesh: history, present status, and future direction. Front Bioeng Biotechnol 6(106):1–6

    Google Scholar 

  • Soberon M, Perez RV, Nunez-Valdez ME, Lorence A, Gomez I, Sanchez J, Bravo A (2000) Evidence for intermolecular interaction as a necessary step for pore-formation activity and toxicity of Bacillus thuringiensis Cry1Ab toxin. FEMS Microbiol Lett 191:221–225

    Article  CAS  PubMed  Google Scholar 

  • Soberon M, Pardo-Lopez L, Lopez I, Gomez I, Tabashnik B, Bravo A (2007) Engineering modified Bt toxins to counter insect resistance. Sci 318:1640–1642

    Article  CAS  Google Scholar 

  • Soufiane B, Cote JC (2009) Discrimination among Bacillus thuringiensis H serotypes, serovars and strains based on 16S rRNA, gyrB and aroE gene sequence analyses. Ant Van Leeuwen 95(1):33–45

    Article  CAS  Google Scholar 

  • Stabb EV, Jacobson LM, Handelsman J (1994) Zwittermycin A-producing strains of B. cereus from diverse soils. Appl Environ Microbiol 60:4404–4412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stahly DP, Andrews RE, Yousten AA (1991) The genus Bacillus- insect pathogens. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes, 2nd edn. Springer Science and Business Media, pp 1697–1745

    Google Scholar 

  • Tabashnik BE, Carrière Y (2017) Surge in insect resistance to transgenic crops and prospects for sustainability. Nat Biotechnol 35(10):926

    Article  CAS  PubMed  Google Scholar 

  • Tabashnik B, Finson EN, Chilcutt CF, Cushing NL, Johnson M (1994) Increasing efficiency of bioassays: evaluation of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J Econ Entomol 86:635–644

    Article  Google Scholar 

  • Tabashnik BE, Biggs RW, Higginson DM, Henderson S, Unnithan DC, Unnithan GC, Elers-Kirk C, Sisterson MS, Dennehy TJ, Carriere Y, Shai M (2005) Association between resistance to Bt cotton and cadherin genotype in pink bollworm. J Econ Entomol 98:635–644

    Article  PubMed  Google Scholar 

  • Tabashnik BE, Huang F, Ghimire MN, Leonard BR, Siegfried BD, Rangasamy M, Yang Y, Wu Y, Gahan LJ, Heckel DG, Bravo A, Soberon M (2011) Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance. Nat Biotechnol 29:1128–1131

    Article  CAS  PubMed  Google Scholar 

  • Tabashnik BE, Brevault T, Carriere Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521

    Article  CAS  PubMed  Google Scholar 

  • Tan F, Zhu J, Tang J, Tang X, Wang S, Zheng S, Li P (2009) Cloning and characterization of two novel crystal protein genes, cry54Aa1 and cry30Fa1, from Bacillus thuringiensis strain BtMC28. Curr Microbiol 58:654–659

    Article  CAS  PubMed  Google Scholar 

  • Tang H, Chen G, Chen F, Han L, Peng Y (2018) Development and relative fitness of Cry1C resistance in Chilo suppressalis. Pest Manag Sci 74:590–597

    Article  CAS  PubMed  Google Scholar 

  • Tanwar R, Dureja P, Rathore H (2012) Bio-pesticides. In: Rathore H, Nollet L (eds) Pesticides, evaluation of environmental pollution. CRC Press, Boca Raton, FL, pp 587–603

    Chapter  Google Scholar 

  • Thakore Y (2006) The bio-pesticide market for global agricultural use. Ind Biotechnol 2:194–208

    Article  Google Scholar 

  • Thomas WE, Ellar DJ (1983) Mechanism of action of Bacillus thuringiensis var israelensis insecticidal delta-endotoxins. FEBS Letter 154:362–368

    Article  CAS  Google Scholar 

  • Thomas DJ, Morgan AW, Whipps JM, Saunders JR (2001) Plasmid transfer between Bacillus thuringiensis subsp. israelensis strains in laboratory culture, river water and dipteran larvae. Appl Environ Microbiol 67:330–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson MA, Schnepf HE, Feitelson JS (1995) Structure, function and engineering of Bacillus thuringiensis toxins. In: Setlow JK (ed) Genetic engineering: principles and methods. Plenum Press, New York, pp 99–117

    Google Scholar 

  • Tigue NJ, Jacoby J, Ellar DJ (2001) The alpha-helix 4 residue, Asn135, is involved in the oligomerization of Cry1Ac1 and Cry1Ab5 Bacillus thuringiensis toxins. Appl Environ Microbiol 67:5715–5720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tikar S, Prakash S (2017) Fly ash-based Bacillus thuringiensis israelensis formulation: an ecofriendly approach. Indian J Med Res 146(6):680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres-Quintero M, Gómez I, Pacheco S, Sánchez J, Flores H, Osuna J, Mendoza G, Soberón M, Bravo A (2018) Engineering Bacillus thuringiensis Cyt1Aa toxin specificity from dipteran to lepidopteran toxicity. Sci Rep 8:4989

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Udayasuriyan V, Nakamura A, Mori A, Masaki H, Uozumi T (1994) Cloning of a new crylA(a), gene from B. thuringiensis strain FU-2-7 and analysis of chimeric cry1A(a) proteins of toxicity. Biosci Biotechnol Biochem 58:830–835

    Article  CAS  PubMed  Google Scholar 

  • Udayasuriyan V, Indra Arulselvi P, Balasubramani V, Sudha DR, Balasubramanian P, Sangeetha P (2006) Construction of new chimeric cry2AX1 gene of B. thuringiensis encoding protein with enhanced insecticidal activity. Indian Patent 244427

    Google Scholar 

  • Vadlamudi RK, Weber E, Ji I, Ji TH, Bulla LA (1995) Cloning and expression of a receptor for an insecticidal toxin of B. thuringiensis. J Biol Chem 270:5490–5494

    Article  CAS  PubMed  Google Scholar 

  • Verma P, Yadav AN, Kazy SK, Saxena AK, Suman A (2014) Evaluating the diversity and phylogeny of plant growth promoting bacteria associated with wheat (Triticum aestivum) growing in central zone of India. Int J Curr Microbiol Appl Sci 3:432–447

    Google Scholar 

  • Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK et al (2015) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Ann Microbiol 65:1885–1899

    Article  CAS  Google Scholar 

  • Verma P, Yadav AN, Khannam KS, Kumar S, Saxena AK, Suman A (2016) Molecular diversity and multifarious plant growth promoting attributes of bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India. J Basic Microbiol 56:44–58

    Article  CAS  PubMed  Google Scholar 

  • Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives, Microbial interactions and agro-ecological impacts, vol 2. Springer, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22

    Chapter  Google Scholar 

  • Verma P, Yadav AN, Khannam KS, Mishra S, Kumar S, Saxena AK et al (2019) Appraisal of diversity and functional attributes of thermotolerant wheat associated bacteria from the peninsular zone of India. Saudi J Biol Sci 26:1882–1895. https://doi.org/10.1016/j.sjbs.2016.01.042

    Article  PubMed  Google Scholar 

  • Vie V, Van-Mau N, Pomarede P, Dance C, Schwartz JL, Laprade R, Frutos R, Rang C, Masson L, Heitz CF, Grimellec L (2001) Lipid-induced pore formation of the Bacillus thuringiensis Cry1Aa insecticidal toxin. J Membr Biol 180:195–203

    Article  CAS  PubMed  Google Scholar 

  • Wagh SG, Pohare MB (2019) Current and future prospects of plant breeding with CRISPR/Cas. Current Journal of Applied Science and Technology 38(3):1–17

    Google Scholar 

  • Wang J, Boets A, Van Rie J, Ren G (2003) Characterization of cry1, cry2 and cry9 genes in B. thuringiensis isolates from China. J Invertebr Pathol 82:63–71

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Liu Y, Zhang J, Crickmore N, Song F, Gao J, Shu C (2018) Cry78Aa, a novel Bacillus thuringiensis insecticidal protein with activity against Laodelphax striatellus and Nilaparvata lugens. J Invertebr Pathol 158:1–5

    Article  CAS  PubMed  Google Scholar 

  • Watrud LS, Perlak FJ, Tran M, Kusano K, Mayer EJ, Miller-Wideman MA, Obukowicz MG, Nelson DR, Kreitinger JP, Kaufman RJ (1985) Cloning of the B. thuringiensis subsp. kurstaki delta-endotoxin gene into P. fluorescens: molecular biology and ecology of an engineered microbial pesticide. In: Halverson Pramer HO, Rogul M (eds) Engineered organisms in the environment scientific issues. American Society for Microbiology, Washington, DC, pp 40–44

    Google Scholar 

  • Wei J, Yuyuan Guo Y, Gemei Liang G, Kongming Wu K, Jie Zhang J, Bruce E, Tabashnik BE, Xianchun Li X (2015) Cross-resistance and interactions between Bt toxins Cry1Ac and Cry2Ab against the cotton bollworm. Sci Rep 5

    Google Scholar 

  • Whitehouse MEA, Wilson LJ, Davies AP, Cross D, Goldsmith P, Thompson A, Harden S, Baker G (2014) Target and non-target effects of novel “triple-stacked” Bt transgenic cotton 1: canopy arthropod communities. Environ Entomol 43:218–241

    Article  CAS  PubMed  Google Scholar 

  • Wilcks A, Jayaswal N, Lereclus D, Andrup L (1998) Characterization of plasmid pAW63, a second self-transmissible plasmid in Bacillus thuringiensis subsp. Kurstaki HD 73. Microbiol 144:1263–1270

    Article  CAS  Google Scholar 

  • Wu D, Aronson AI (1992) Localized mutagenesis defines regions of the B. thuringiensis δ-endotoxin involved in toxicity and specificity. J Biol Chem 267:2311–2317

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Huang F, Leonard BR, Moore SH (2007) Evaluation of transgenic Bacillus thuringiensis corn hybrids against Cry1Ab-susceptible and resistant sugarcane borer (Lepidoptera: Crambidae). J Econ Entomol 100:1880–1886

    Article  PubMed  Google Scholar 

  • Xiao Y, Wu K (2019) Recent progress on the interaction between insects and Bacillus thuringiensis crops. Phil Trans R Soc B 374:20180316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Yu L, Wu Y (2005) Disruption of a cadherin gene associated with resistance to Cry1Ac δ-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl Environ Microbiol 71:948–954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav AN, Saxena AK (2018) Biodiversity and biotechnological applications of halophilic microbes for sustainable agriculture. J Appl Biol Biotechnol 6:48–55

    CAS  Google Scholar 

  • Yadav AN, Sachan SG, Verma P, Saxena AK (2015a) Prospecting cold deserts of north western Himalayas for microbial diversity and plant growth promoting attributes. J Biosci Bioeng 119:683–693. https://doi.org/10.1016/j.jbiosc.2014.11.006

    Article  CAS  PubMed  Google Scholar 

  • Yadav AN, Verma P, Kumar M, Pal KK, Dey R, Gupta A et al (2015b) Diversity and phylogenetic profiling of niche-specific bacilli from extreme environments of India. Ann Microbiol 65:611–629

    Article  Google Scholar 

  • Yadav AN, Sachan SG, Verma P, Kaushik R, Saxena AK (2016a) Cold active hydrolytic enzymes production by psychrotrophic bacilli isolated from three sub-glacial lakes of NW Indian Himalayas. J Basic Microbiol 56:294–307

    Article  CAS  PubMed  Google Scholar 

  • Yadav AN, Sachan SG, Verma P, Saxena AK (2016b) Bioprospecting of plant growth promoting psychrotrophic bacilli from cold desert of north western Indian Himalayas. Indian J Exp Biol 54:142–150

    PubMed  Google Scholar 

  • Yamamoto T, Mclanghlin RE (1981) Isolation of a protein from the parasporal crystal of Bacillus thuringiensis var. kurstaki toxic to the mosquito larva, Aedes taeniorhynchus. Biochem. Biophys. Res Commun 103:414–421

    CAS  Google Scholar 

  • Yamamoto T, Powell GK (1993) Bacillus thuringiensis crystal proteins: recent advances in understanding its insecticidal activity. In: Kim L (ed) Advanced engineered pesticides. Marcel Dekker Inc, New York, pp 3–42

    Google Scholar 

  • Yu HL, Li YH, Li XJ, Romeis J, Wu KM (2013) Expression of Cry1Ac in transgenic Bt soybean lines and their efficiency in controlling lepidopteran pests. Pest Manag Sci 69:1326–1333

    Article  CAS  PubMed  Google Scholar 

  • Zhang MY, Lövgren A, Low MG, Landen R (1993) Characterization of an avirulent pleiotropic mutant of the insect pathogen Bacillus thuringiensis: reduced expression of flagellin and phospholipases. Infect Immun 61:4947–4954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Candas M, Griko NB, Taissing R Jr, Bulla LA (2006) A mechanism of cell death involving an adenylylcyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci U S A 103:9897–9902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Yin W, Zhao J, Jin L, Yang Y, Wu S, Tabashnik BE, Wu Y (2011) Early warning of cotton bollworm resistance associated with intensive planting of Bt cotton in China. PLoS One 6(8):e22874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang TT, Coates BS, Wang YQ, Wang YD, Bai SX, Wang ZY, He KL (2017) Down-regulation of aminopeptidase N and ABC transporter subfamily G transcripts in Cry1Ab and Cry1Ac resistant Asian corn borer, Ostrinia furnacalis (Lepidoptera: Crambidae). Int J Biol Sci 13:835–851

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao M, Yuan X, Wei J, Zhang W, Wang B, Khaing MM, Liang G (2017) Functional roles of cadherin, aminopeptidase-N and alkaline phosphatase from Helicoverpa armigera (HUbner) in the action mechanism of Bacillus thuringiensis Cry2Aa. Sci Rep 7:46555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng A, Zhu J, Tan F, Guan P, Yu X, Wang S, Deng Q, Li S, Liu H, Li P (2010) Characterisation and expression of a novel haplotype cry2A-type gene from Bacillus thuringiensis strain JF19-2. Ann Microbiol 60:129–134

    Article  CAS  Google Scholar 

  • Zhong C, Ellar DJ, Bishop A, Johnson C, Lin S, Hart ER (2000) Characterization of B. thuringiensis δ-endotoxin which is toxic to insects in three orders. J Invertebr Pathol 76:131–139

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Zheng A, Wang S, Liu H, Li P (2010) Characterization and expression of cry4Cb1 and cry30Ga1 from Bacillus thuringiensis strain HS18-1. J Invertebr Pathol 103:200–202

    Article  CAS  PubMed  Google Scholar 

  • Zhuang M, Oltean DI, Gomez I, Pullikuth AK, Soberion M, Bravo A, Gill SS (2002) Heliothis virescens and Manduca sexta lipid rafts are involved in Cry1A toxin binding to the midgut epithelium and subsequent pore formation. J Biol Chem 277:13863–13872

    Article  CAS  PubMed  Google Scholar 

  • Zotti M, Santos EAD, Cagliari D, Christiaens O, Taning CNT, Smagghe G (2018) RNA interference technology in crop protection against arthropod pests, pathogens and nematodes. Pest Manag Sci 74:1239–1250

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Rahul Mahadev Shelake, Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju 52828, Korea for his critical comments and English corrections. Authors are also thankful to Pallavi Kisan Patil, Research Associate, University of Sheffield, UK for her critical English corrections.

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Pohare, M.B., Wagh, S.G., Udayasuriyan, V. (2021). Bacillus thuringiensis as Potential Biocontrol Agent for Sustainable Agriculture. In: Yadav, A.N., Singh, J., Singh, C., Yadav, N. (eds) Current Trends in Microbial Biotechnology for Sustainable Agriculture . Environmental and Microbial Biotechnology. Springer, Singapore. https://doi.org/10.1007/978-981-15-6949-4_18

Download citation

Publish with us

Policies and ethics