{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T16:30:02Z","timestamp":1781627402670,"version":"3.54.5"},"reference-count":76,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,10,6]],"date-time":"2016-10-06T00:00:00Z","timestamp":1475712000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,10,6]],"date-time":"2016-10-06T00:00:00Z","timestamp":1475712000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The first generation transgenic crops used strong constitutive promoters for transgene expression. However, tissue-specific expression is desirable for more precise targeting of transgenes. Moreover, piercing\/sucking insects, which are generally resistant to insecticidal <jats:italic>Bacillus thuringiensis<\/jats:italic> (<jats:italic>Bt<\/jats:italic>) proteins, have emerged as a major pests since the introduction of transgenic crops expressing these toxins. Phloem-specific promoters isolated from <jats:italic>Banana bunchy top virus<\/jats:italic> (BBTV) were used for the expression of two insecticidal proteins, <jats:italic>Hadronyche versuta<\/jats:italic> (Blue Mountains funnel-web spider) neurotoxin (Hvt) and onion leaf lectin, in tobacco (<jats:italic>Nicotiana tabacum<\/jats:italic>). Here we demonstrate that transgenic plants expressing Hvt alone or in combination with onion leaf lectin are resistant to <jats:italic>Phenacoccus solenopsis<\/jats:italic> (cotton mealybug), <jats:italic>Myzus persicae<\/jats:italic> (green peach aphids) and <jats:italic>Bemisia tabaci<\/jats:italic> (silver leaf whitefly). The expression of both proteins under different phloem-specific promoters resulted in close to 100% mortality and provided more rapid protection than Hvt alone. Our results suggest the employment of the Hvt and onion leaf lectin transgenic constructs at the commercial level will reduce the use of chemical pesticides for control of hemipteran insect pests.<\/jats:p>","DOI":"10.1038\/srep34706","type":"journal-article","created":{"date-parts":[[2016,10,6]],"date-time":"2016-10-06T09:58:24Z","timestamp":1475747904000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":52,"title":["A transgenic approach to control hemipteran insects by expressing insecticidal genes under phloem-specific promoters"],"prefix":"10.1038","volume":"6","author":[{"given":"Shaista","family":"Javaid","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Imran","family":"Amin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georg","family":"Jander","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zahid","family":"Mukhtar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nasir A.","family":"Saeed","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shahid","family":"Mansoor","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,10,6]]},"reference":[{"key":"BFsrep34706_CR1","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1007\/s11356-014-3470-y","volume":"22","author":"N Simon-Delso","year":"2015","unstructured":"Simon-Delso, N. et al. Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environ. Sci. Pollut. R. 22, 5\u201334 (2015).","journal-title":"Environ. Sci. Pollut. R."},{"key":"BFsrep34706_CR2","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1016\/j.neuro.2011.03.004","volume":"32","author":"A Moretto","year":"2011","unstructured":"Moretto, A. & Colosio, C. Biochemical and toxicological evidence of neurological effects of pesticides: The example of Parkinson\u2019s Disease. Neurotoxicology 32, 383\u2013391 (2011).","journal-title":"Neurotoxicology"},{"key":"BFsrep34706_CR3","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1007\/s11356-014-3332-7","volume":"22","author":"J-M Bonmatin","year":"2015","unstructured":"Bonmatin, J.-M. et al. Environmental fate and exposure; neonicotinoids and fipronil. Environ. Sci. Pollut. R. 22, 35\u201367 (2015).","journal-title":"Environ. Sci. Pollut. R."},{"key":"BFsrep34706_CR4","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1098\/rspb.2006.3721","volume":"274","author":"A-M Klein","year":"2007","unstructured":"Klein, A.-M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. Lond., B, Biol. Sci. 274, 303\u2013313 (2007).","journal-title":"Proc. R. Soc. Lond., B, Biol. Sci."},{"key":"BFsrep34706_CR5","first-page":"1","volume":"128","author":"RA Morse","year":"2000","unstructured":"Morse, R. A. & Calderone, N. W. The value of honey bees as pollinators of US crops in 2000. Bee Culture 128, 1\u201315 (2000).","journal-title":"Bee Culture"},{"key":"BFsrep34706_CR6","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1006\/pest.2000.2519","volume":"69","author":"C Papaefthimiou","year":"2001","unstructured":"Papaefthimiou, C. & Theophilidis, G. The cardiotoxic action of the pyrethroid insecticide deltamethrin, the azole fungicide prochloraz and their synergy on the semi-isolated heart of the bee Apis mellifera macedonica. Pestic. Biochem. Physiol. 69, 77\u201391 (2001).","journal-title":"Pestic. Biochem. Physiol."},{"key":"BFsrep34706_CR7","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1006\/eesa.1999.1811","volume":"44","author":"N Bendahou","year":"1999","unstructured":"Bendahou, N., Bounias, M. & Fleche, C. Toxicity of cypermethrin and fenitrothion on the hemolymph carbohydrates, head acetylcholinesterase, and thoracic muscle Na+, K+-ATPase of emerging honeybees (Apis mellifera mellifera. L). Ecotoxicol. Environ. Saf. 44, 139\u2013146 (1999).","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"BFsrep34706_CR8","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1016\/S0261-2194(03)00094-2","volume":"22","author":"TV Zanuncio","year":"2003","unstructured":"Zanuncio, T. V., Serr\u00e3o, J. E., Zanuncio, J. C. & Guedes, R. N. C. Permethrin induced hormesis on the predator Supputius cincticeps (st\u00e5l, 1860) (heteroptera: Pentatomidae). Crop Prot. 22, 941\u2013947 (2003).","journal-title":"Crop Prot."},{"key":"BFsrep34706_CR9","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1002\/tox.10078","volume":"17","author":"S Van Erp","year":"2002","unstructured":"Van Erp, S., Booth, L., Gooneratne, R. & O\u2019Halloran, K. Sublethal responses of wolf spiders (Lycosidae) to organophosphorous insecticides. Environ. Toxicol. 17, 449\u2013456 (2002).","journal-title":"Environ. Toxicol."},{"key":"BFsrep34706_CR10","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1007\/s00244-004-3057-6","volume":"47","author":"R Schmuck","year":"2004","unstructured":"Schmuck, R. Effects of a chronic dietary exposure of the honeybee Apis mellifera (hymenoptera: Apidae) to imidacloprid. Arch. Environ. Contam. Toxicol. 47, 471\u2013478 (2004).","journal-title":"Arch. Environ. Contam. Toxicol."},{"key":"BFsrep34706_CR11","first-page":"55","volume":"9","author":"SK Paul","year":"1991","unstructured":"Paul, S. K., Ghosh, H. & Sahu, C. Toxic effects of insecticides in the histomorphology of tests of Diacrisia obliana walker (Arctidae lepidoptera). Ann. Entomol. 9, 55\u201360 (1991).","journal-title":"Ann. Entomol."},{"key":"BFsrep34706_CR12","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1006\/nlme.1998.3901","volume":"72","author":"SW Zhang","year":"1999","unstructured":"Zhang, S. W., Lehrer, M. & Srinivasan, M. V. Honeybee memory: Navigation by associative grouping and recall of visual stimuli. Neurobiol. Learn. Mem. 72, 180\u2013201 (1999).","journal-title":"Neurobiol. Learn. Mem."},{"key":"BFsrep34706_CR13","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1007\/s003590050337","volume":"184","author":"F W\u00e4ckers","year":"1999","unstructured":"W\u00e4ckers, F. & Lewis, W. A comparison of color, shape and pattern learning by the hymenopteran parasitoid Microplitis croceipes. J. Comp. Physiol. A 184, 387\u2013393 (1999).","journal-title":"J. Comp. Physiol. A"},{"key":"BFsrep34706_CR14","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1002\/ps.2780160417","volume":"16","author":"J Delabie","year":"1985","unstructured":"Delabie, J., Bos, C., Fonta, C. & Masson, C. Toxic and repellent effects of cypermethrin on the honeybee: Laboratory, glasshouse and field experiments. Pestic. Sci. 16, 409\u2013415 (1985).","journal-title":"Pestic. Sci."},{"key":"BFsrep34706_CR15","doi-asserted-by":"crossref","unstructured":"Jervis, M. & Kidd, N. Insect natural enemies, practical approaches to their study and evaluation. 63\u2013161 (Chapman & Hall, London, 1996).","DOI":"10.1007\/978-94-011-0013-7_2"},{"key":"BFsrep34706_CR16","doi-asserted-by":"publisher","first-page":"993","DOI":"10.1007\/BF01015194","volume":"15","author":"J Polonsky","year":"1989","unstructured":"Polonsky, J., Bhatnagar, S. C., Griffiths, D. C., Pickett, J. A. & Woodcock, C. M. Activity of quassinoids as antifeedants against aphids. J. Chem. Ecol. 15, 993\u2013998 (1989).","journal-title":"J. Chem. Ecol."},{"key":"BFsrep34706_CR17","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1007\/s11356-014-3180-5","volume":"22","author":"D Gibbons","year":"2015","unstructured":"Gibbons, D., Morrissey, C. & Mineau, P. A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ. Sci. Pollut. R. 22, 103\u2013118 (2015).","journal-title":"Environ. Sci. Pollut. R."},{"key":"BFsrep34706_CR18","unstructured":"Sanchez-Bayo, F. Insecticides mode of action in relation to their toxicity to non-target organisms. J. Environment. Analytic. Toxicol. 22\/5\/2016 (2012)."},{"key":"BFsrep34706_CR19","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1007\/s10646-005-0018-4","volume":"14","author":"P Prosser","year":"2005","unstructured":"Prosser, P. & Hart, A. Assessing potential exposure of birds to pesticide treated seeds. Ecotoxicology 14, 679\u2013691 (2005).","journal-title":"Ecotoxicology"},{"key":"BFsrep34706_CR20","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1002\/ieam.174","volume":"7","author":"P Mineau","year":"2011","unstructured":"Mineau, P. Barking up the wrong perch: Why we should stop ignoring non dietary routes of pesticide exposure in birds. Integr. Environ. Assess. Manag. 7, 297\u2013299 (2011).","journal-title":"Integr. Environ. Assess. Manag."},{"key":"BFsrep34706_CR21","doi-asserted-by":"crossref","unstructured":"Sotherton, N. & Holland, J. Indirect effects of pesticides on farmland wildlife. In: Hoffman, D. J., Rattner, B. A., Allen Burton, G. & Cairns, J. (eds) Handbook of ecotoxicology, 2nd edn. CRC Press Ltd, USA, pp 1173\u20131196 (2002).","DOI":"10.1201\/9781420032505.ch43"},{"key":"BFsrep34706_CR22","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.agee.2004.07.016","volume":"106","author":"AJ Morris","year":"2005","unstructured":"Morris, A. J., Wilson, J. D., Whittingham, M. J. & Bradbury, R. B. Indirect effects of pesticides on breeding yellowhammer (Emberiza citrinella). Agric. Ecosyst. Environ. 106, 1\u201316 (2005).","journal-title":"Agric. Ecosyst. Environ."},{"key":"BFsrep34706_CR23","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1111\/j.1474-919X.2004.00347.x","volume":"146","author":"ND Boatman","year":"2004","unstructured":"Boatman, N. D. et al. Evidence for the indirect effects of pesticides on farmland birds. IBIS 146, 131\u2013143 (2004).","journal-title":"IBIS"},{"key":"BFsrep34706_CR24","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1016\/S0167-7799(97)01018-4","volume":"15","author":"M Peferoen","year":"1997","unstructured":"Peferoen, M. Progress and prospects for field use of Bt genes in crops. Trends Biotechnol. 15, 173\u2013177 (1997).","journal-title":"Trends Biotechnol."},{"key":"BFsrep34706_CR25","first-page":"250","volume":"124","author":"S Dutta","year":"2015","unstructured":"Dutta, S. Biopesticides: An ecofriendly approach for pest control. WJPPS 124, 250\u2013265 (2015).","journal-title":"WJPPS"},{"key":"BFsrep34706_CR26","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1038\/nbt1056","volume":"23","author":"SL Bates","year":"2005","unstructured":"Bates, S. L., Zhao, J.-Z., Roush, R. T. & Shelton, A. M. Insect resistance management in GM crops: Past, present and future. Nat. Biotechnol. 23, 57\u201362 (2005).","journal-title":"Nat. Biotechnol."},{"key":"BFsrep34706_CR27","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1038\/nbt1382","volume":"26","author":"BE Tabashnik","year":"2008","unstructured":"Tabashnik, B. E., Gassmann, A. J., Crowder, D. W. & Carri\u00e8re, Y. Insect resistance to Bt crops: Evidence versus theory. Nat. Biotechnol. 26, 199\u2013202 (2008).","journal-title":"Nat. Biotechnol."},{"key":"BFsrep34706_CR28","unstructured":"Roush, R. & Tabashnik, B. E. Pesticide resistance in arthropods. (Springer Science & Business Media, 2012)."},{"key":"BFsrep34706_CR29","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/j.jip.2007.03.014","volume":"95","author":"RW Kurtz","year":"2007","unstructured":"Kurtz, R. W., McCaffery, A. & O\u2019Reilly, D. Insect resistance management for Syngenta\u2019s Vipcot\u2122 transgenic cotton. J. Invertebr. Pathol. 95, 227\u2013230 (2007).","journal-title":"J. Invertebr. Pathol."},{"key":"BFsrep34706_CR30","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1023\/A:1009644712157","volume":"7","author":"SB Maqbool","year":"2001","unstructured":"Maqbool, S. B. et al. Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests. Mol. Breed. 7, 85\u201393 (2001).","journal-title":"Mol. Breed."},{"key":"BFsrep34706_CR31","first-page":"4677","volume":"10","author":"SM DeVilliers","year":"2011","unstructured":"DeVilliers, S. M. & Hoisington, D. A. The trends and future of biotechnology crops for insect pest control. Afr. J. Biotechnol. 10, 4677\u20134681 (2011).","journal-title":"Afr. J. Biotechnol."},{"key":"BFsrep34706_CR32","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1111\/j.1467-7652.2005.00130.x","volume":"3","author":"S Bajaj","year":"2005","unstructured":"Bajaj, S. & Mohanty, A. Recent advances in rice biotechnology towards genetically superior transgenic rice. Plant Biotechnol. J. 3, 275\u2013307 (2005).","journal-title":"Plant Biotechnol. J."},{"key":"BFsrep34706_CR33","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1093\/jxb\/45.5.623","volume":"45","author":"Y Shi","year":"1994","unstructured":"Shi, Y. et al. Use of the rice sucrose synthase-1 promoter to direct phloem-specific expression of \u03b2-glucuronidase and snowdrop lectin genes in transgenic tobacco plants. J. Exp. Bot. 45, 623\u2013631 (1994).","journal-title":"J. Exp. Bot."},{"key":"BFsrep34706_CR34","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1046\/j.1365-313X.1998.00226.x","volume":"15","author":"K Rao","year":"2008","unstructured":"Rao, K. et al. Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper. Plant J. 15, 469\u2013477 (2008).","journal-title":"Plant J."},{"key":"BFsrep34706_CR35","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1023\/A:1008856703464","volume":"7","author":"D Sudhakar","year":"1998","unstructured":"Sudhakar, D. et al. Expression and immunolocalisation of the snowdrop lectin GNA in transgenic rice plants. Transgenic Res. 7, 371\u2013378 (1998).","journal-title":"Transgenic Res."},{"key":"BFsrep34706_CR36","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1016\/j.plantsci.2005.05.016","volume":"169","author":"I Dutta","year":"2005","unstructured":"Dutta, I., Majumder, P., Saha, P., Ray, K. & Das, S. Constitutive and phloem specific expression of Allium sativum leaf agglutinin (ASAL) to engineer aphid (Lipaphis erysimi) resistance in transgenic Indian mustard (Brassica juncea). Plant Sci. 169, 996\u20131007 (2005).","journal-title":"Plant Sci."},{"key":"BFsrep34706_CR37","first-page":"665","volume":"1","author":"T Schm\u00fclling","year":"1989","unstructured":"Schm\u00fclling, T., Schell, J. & Spena, A. Promoters of the rolA, B, and C genes of Agrobacterium rhizogenes are differentially regulated in transgenic plants. Plant Cell 1, 665\u2013670 (1989).","journal-title":"Plant Cell"},{"key":"BFsrep34706_CR38","first-page":"649","volume":"30","author":"S Sugaya","year":"1989","unstructured":"Sugaya, S., Hayakawa, K., Handa, T. & Uchimiya, H. Cell-specific expression of the rolC gene of the TL-DNA of Ri plasmid in transgenic tobacco plants. Plant Cell Physiol. 30, 649\u2013653 (1989).","journal-title":"Plant Cell Physiol."},{"key":"BFsrep34706_CR39","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1007\/BF00260849","volume":"220","author":"R Matsuki","year":"1989","unstructured":"Matsuki, R., Onodera, H., Yamauchi, T. & Uchimiya, H. Tissue-specific expression of the rolC promoter of the Ri plasmid in transgenic rice plants. Mol. Gen. Genet. 220, 12\u201316 (1989).","journal-title":"Mol. Gen. Genet."},{"key":"BFsrep34706_CR40","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1007\/s11262-007-0168-y","volume":"36","author":"I Amin","year":"2008","unstructured":"Amin, I., Qazi, J., Mansoor, S., Ilyas, M. & Briddon, R. W. Molecular characterisation of Banana Bunchy Top Virus (BBTV) from Pakistan. Virus Genes 36, 191\u2013198 (2008).","journal-title":"Virus Genes"},{"key":"BFsrep34706_CR41","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1099\/0022-1317-78-1-229","volume":"78","author":"PR Beetham","year":"1997","unstructured":"Beetham, P. R., Hafner, G. J., Harding, R. M. & Dale, J. L. Two mRNAs are transcribed from Banana Bunchy Top Virus DNA-1. J. Gen. Virol. 78, 229\u2013236 (1997).","journal-title":"J. Gen. Virol."},{"key":"BFsrep34706_CR42","doi-asserted-by":"publisher","first-page":"1471","DOI":"10.1099\/0022-1317-76-6-1471","volume":"76","author":"TM Burns","year":"1995","unstructured":"Burns, T. M., Harding, R. M. & Dale, J. L. The genome organization of Banana Bunchy Top Virus: Analysis of six ssDNA components. J. Gen. Virol. 76, 1471\u20131482 (1995).","journal-title":"J. Gen. Virol."},{"key":"BFsrep34706_CR43","unstructured":"Karan, M., Harding, R. M. & Dale, J. L. Association of Banana Bunchy Top Virus DNA Components 2 to 6 with Bunchy Top Disease. Mol. Plant Pathol. 12\/11\/2014 (1997)."},{"key":"BFsrep34706_CR44","unstructured":"King, A. M., Adams, M. J., Lefkowitz, E. J. & Carstens, E. B. Virus Taxonomy: IXth report of the international committee on taxonomy of viruses. 9 (2011)."},{"key":"BFsrep34706_CR45","doi-asserted-by":"publisher","first-page":"2301","DOI":"10.1099\/0022-1317-79-10-2301","volume":"79","author":"B Dugdale","year":"1998","unstructured":"Dugdale, B., Beetham, P. R., Becker, D. K., Harding, R. M. & Dale, J. L. Promoter activity associated with the intergenic regions of Banana Bunchy Top Virus DNA-1 to -6 in transgenic tobacco and banana cells. J. Gen. Virol. 79, 2301\u20132311 (1998).","journal-title":"J. Gen. Virol."},{"key":"BFsrep34706_CR46","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1007\/s002999900185","volume":"19","author":"B Dugdale","year":"2000","unstructured":"Dugdale, B., Becker, D., Beetham, P., Harding, R. & Dale, J. Promoters derived from Banana Bunchy Top Virus DNA-1 to 5 direct vascular-associated expression in transgenic banana (Musa spp.). Plant Cell Rep. 19, 810\u2013814 (2000).","journal-title":"Plant Cell Rep."},{"key":"BFsrep34706_CR47","doi-asserted-by":"crossref","first-page":"11098","DOI":"10.1016\/S0021-9258(19)78096-X","volume":"269","author":"GB Quistad","year":"1994","unstructured":"Quistad, G. B. & Skinner, W. S. Isolation and sequencing of insecticidal peptides from the primitive hunting spider, Plectreurys tristis (simon). J. Biol. Chem. 269, 11098\u201311101 (1994).","journal-title":"J. Biol. Chem."},{"key":"BFsrep34706_CR48","doi-asserted-by":"publisher","first-page":"823","DOI":"10.1146\/annurev.bi.63.070194.004135","volume":"63","author":"BM Olivera","year":"1994","unstructured":"Olivera, B. M., Miljanich, G., Ramachandran, J. & Adams, M. E. Calcium channel diversity and neurotransmitter release: The \u03c9-conotoxins and \u03c9-agatoxins. Annu. Rev. Biochem. 63, 823\u2013867 (1994).","journal-title":"Annu. Rev. Biochem."},{"key":"BFsrep34706_CR49","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1046\/j.1432-1327.1999.00622.x","volume":"264","author":"E Grishin","year":"2001","unstructured":"Grishin, E. Polypeptide neurotoxins from spider venoms. Eur. J. Biochem. 264, 276\u2013280 (2001).","journal-title":"Eur. J. Biochem."},{"key":"BFsrep34706_CR50","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1038\/nsb0797-559","volume":"4","author":"JI Fletcher","year":"1997","unstructured":"Fletcher, J. I. et al. The structure of a novel insecticidal neurotoxin, \u03c9-atracotoxin Hv1, from the venom of an Australian funnel web spider. Nat. Struct. Mol. Biol. 4, 559\u2013566 (1997).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"BFsrep34706_CR51","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1016\/0742-8413(96)00017-5","volume":"114","author":"R Atkinson","year":"1996","unstructured":"Atkinson, R., Vonarx, E. & Howden, M. Effects of whole venom and venom fractions from several Australian spiders, including Atrax (Hadronyche) species, when injected into insects. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 114, 113\u2013117 (1996).","journal-title":"Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol."},{"key":"BFsrep34706_CR52","unstructured":"Atkinson, R. K., Howden, M. E. H., Tyler, M. I. & Vonarx, E. J. Zeneca Limited. Insecticidal toxins derived from funnel web (Atrax or Hadronyche) spiders. United States Patent US 5763568 A. Jun 9 1998."},{"key":"BFsrep34706_CR53","doi-asserted-by":"publisher","first-page":"e73136","DOI":"10.1371\/journal.pone.0073136","volume":"8","author":"MC Hardy","year":"2013","unstructured":"Hardy, M. C., Daly, N. L., Mobli, M., Morales, R. A. & King, G. F. Isolation of an orally active insecticidal toxin from the venom of an Australian Tarantula. PLoS One 8, e73136 (2013).","journal-title":"PLoS One"},{"key":"BFsrep34706_CR54","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1007\/s11248-006-0007-2","volume":"15","author":"SA Khan","year":"2006","unstructured":"Khan, S. A., Zafar, Y., Briddon, R. W., Malik, K. A. & Mukhtar, Z. Spider venom toxin protects plants from insect attack. Transgenic Res. 15, 349\u2013357 (2006).","journal-title":"Transgenic Res."},{"key":"BFsrep34706_CR55","doi-asserted-by":"publisher","first-page":"1457","DOI":"10.1007\/s10529-011-0572-1","volume":"33","author":"AD Shah","year":"2011","unstructured":"Shah, A. D. et al. Spider toxin (Hvt) gene cloned under phloem specific RSs1 and rolC promoters provides resistance against american bollworm (Heliothis armigera). Biotechnol. Lett. 33, 1457\u20131463 (2011).","journal-title":"Biotechnol. Lett."},{"key":"BFsrep34706_CR56","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1111\/jen.12156","volume":"139","author":"I Ullah","year":"2015","unstructured":"Ullah, I., Hagenbucher, S., \u00c1lvarez-Alfageme, F., Ashfaq, M. & Romeis, J. Target and non-target effects of a spider venom toxin produced in transgenic cotton and tobacco plants. J. Appl. Entomol. 139, 321\u2013332 (2015).","journal-title":"J. Appl. Entomol."},{"key":"BFsrep34706_CR57","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/S0065-2296(08)00403-5","volume":"48","author":"EJ Van Damme","year":"2008","unstructured":"Van Damme, E. J., Lannoo, N. & Peumans, W. J. Plant lectins. Adv. Bot. Res. 48, 107\u2013209 (2008).","journal-title":"Adv. Bot. Res."},{"key":"BFsrep34706_CR58","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1007\/BF01976497","volume":"4","author":"V Hilder","year":"1995","unstructured":"Hilder, V. et al. Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgenic Res. 4, 18\u201325 (1995).","journal-title":"Transgenic Res."},{"key":"BFsrep34706_CR59","doi-asserted-by":"publisher","first-page":"2014","DOI":"10.3390\/molecules20022014","volume":"20","author":"MLR Macedo","year":"2015","unstructured":"Macedo, M. L. R., Oliveira, C. F. & Oliveira, C. T. Insecticidal activity of plant lectins and potential application in crop protection. Molecules 20, 2014\u20132033 (2015).","journal-title":"Molecules"},{"key":"BFsrep34706_CR60","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1002\/arch.20351","volume":"73","author":"K Michiels","year":"2010","unstructured":"Michiels, K., Van Damme, E. J. & Smagghe, G. Plant\u2010insect interactions: What can we learn from plant lectins? Arch. Insect Biochem. Physiol. 73, 193\u2013212 (2010).","journal-title":"Arch. Insect Biochem. Physiol."},{"key":"BFsrep34706_CR61","doi-asserted-by":"publisher","first-page":"1329","DOI":"10.1007\/s00425-005-0182-z","volume":"223","author":"P Saha","year":"2006","unstructured":"Saha, P. et al. Transgenic rice expressing Allium sativum leaf lectin with enhanced resistance against sap-sucking insect pests. Planta 223, 1329\u20131343 (2006).","journal-title":"Planta"},{"key":"BFsrep34706_CR62","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1016\/S0165-6147(00)01820-4","volume":"22","author":"K Matsuda","year":"2001","unstructured":"Matsuda, K. et al. Neonicotinoids: Insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol. Sci. 22, 573\u2013580 (2001).","journal-title":"Trends Pharmacol. Sci."},{"key":"BFsrep34706_CR63","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1002\/arch.20043","volume":"58","author":"R Nauen","year":"2005","unstructured":"Nauen, R. & Denholm, I. Resistance of insect pests to neonicotinoid insecticides: Current status and future prospects. Arch. Insect Biochem. Physiol. 58, 200\u2013215 (2005).","journal-title":"Arch. Insect Biochem. Physiol."},{"key":"BFsrep34706_CR64","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1038\/313810a0","volume":"313","author":"JT Odell","year":"1985","unstructured":"Odell, J. T., Nagy, F. & Chua, N.-H. Identification of DNA sequences required for activity of the Cauliflower mosaic virus 35S promoter. Nature 313, 810\u2013812 (1985).","journal-title":"Nature"},{"key":"BFsrep34706_CR65","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1242\/jeb.204.4.711","volume":"204","author":"F Grolleau","year":"2001","unstructured":"Grolleau, F. et al. Electrophysiological analysis of the neurotoxic action of a funnel web spider toxin, delta-atracotoxin-Hv1a, on insect voltage-gated Na+ channels. J. Exp. Biol. 204, 711\u2013721 (2001).","journal-title":"J. Exp. Biol."},{"key":"BFsrep34706_CR66","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1146\/annurev.en.34.010189.000453","volume":"34","author":"DM Soderlund","year":"1989","unstructured":"Soderlund, D. M. & Bloomquist, J. R. Neurotoxic actions of pyrethroid insecticides. Annu. Rev. Entomol. 34, 77\u201396 (1989).","journal-title":"Annu. Rev. Entomol."},{"key":"BFsrep34706_CR67","doi-asserted-by":"crossref","unstructured":"Guerineau, F., Mullineaux, P. & Croy, R. Plant transformation and expression vectors. Plant Mol. Biol. 121\u2013147 (1993).","DOI":"10.1016\/B978-0-08-091753-5.50010-X"},{"key":"BFsrep34706_CR68","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1023\/A:1006496308160","volume":"42","author":"RP Hellens","year":"2000","unstructured":"Hellens, R. P., Edwards, E. A., Leyland, N. R., Bean, S. & Mullineaux, P. M. pGreen: A versatile and flexible binary Ti vector for Agrobacterium mediated plant transformation. Plant Mol. Biol. 42, 819\u2013832 (2000).","journal-title":"Plant Mol. Biol."},{"key":"BFsrep34706_CR69","doi-asserted-by":"publisher","first-page":"6747","DOI":"10.1093\/nar\/17.16.6747","volume":"17","author":"D Mattanovich","year":"1989","unstructured":"Mattanovich, D. et al. Efficient transformation of Agrobacterium spp. by eletroporation. Nucleic Acids Res. 17, 6747\u20136747 (1989).","journal-title":"Nucleic Acids Res."},{"key":"BFsrep34706_CR70","doi-asserted-by":"publisher","first-page":"3901","DOI":"10.1002\/j.1460-2075.1987.tb02730.x","volume":"6","author":"RA Jefferson","year":"1987","unstructured":"Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. Gus fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901 (1987).","journal-title":"EMBO J."},{"key":"BFsrep34706_CR71","first-page":"36","volume":"11","author":"MD Abr\u00e0moff","year":"2004","unstructured":"Abr\u00e0moff, M. D., Magalh\u00e3es, P. J. & Ram, S. J. Image processing with Image J. Biophotonics 11, 36\u201342 (2004).","journal-title":"J. Biophotonics"},{"key":"BFsrep34706_CR72","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1007\/s11120-006-9098-0","volume":"90","author":"ML P\u00e9rez-Bueno","year":"2006","unstructured":"P\u00e9rez-Bueno, M. L., Ciscato, M., Garc\u00eda-Luque, I., Valcke, R. & Bar\u00f3n, M. Imaging viral infection: Studies on Nicotiana benthamiana plants infected with the Pepper mild mottle tobamovirus. Photosynth. Res. 90, 111\u2013123 (2006).","journal-title":"Photosynth. Res."},{"key":"BFsrep34706_CR73","doi-asserted-by":"publisher","first-page":"1229","DOI":"10.1126\/science.227.4691.1229","volume":"227","author":"R Horsch","year":"1985","unstructured":"Horsch, R. et al. A simple and general method for transferring genes into plants. Science 227, 1229\u20131231 (1985).","journal-title":"Science"},{"key":"BFsrep34706_CR74","first-page":"748","volume":"14","author":"CN Stewart Jr.","year":"1993","unstructured":"Stewart, C. N. Jr. & Via, L. E. A rapid C-TAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques 14, 748\u2013750 (1993).","journal-title":"Biotechniques"},{"key":"BFsrep34706_CR75","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1007\/s11262-010-0559-3","volume":"42","author":"I Amin","year":"2010","unstructured":"Amin, I. et al. Identification of a major pathogenicity determinant and suppressors of RNA silencing encoded by a south pacific isolate of Banana Bunchy Top Virus originating from Pakistan. Virus Genes 42, 272\u2013281 (2010).","journal-title":"Virus Genes"},{"key":"BFsrep34706_CR76","unstructured":"Green, S. B. & Salkind, N. J. Using SPSS for windows and macintosh: Analyzing and understanding data. (Prentice Hall Press, 2010)."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep34706.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep34706","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep34706.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T01:48:45Z","timestamp":1672883325000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep34706"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,10,6]]},"references-count":76,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,12,16]]}},"alternative-id":["BFsrep34706"],"URL":"https:\/\/doi.org\/10.1038\/srep34706","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,10,6]]},"assertion":[{"value":"16 March 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 September 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 October 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"34706"}}