Please wait a minute...
Journal of Integrative Agriculture  2024, Vol. 23 Issue (5): 1604-1617    DOI: 10.1016/j.jia.2023.11.001
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |

Functional assessment of cadherin as a shared mechanism for cross/dual resistance to Cry1Ac and Cry2Ab in Helicoverpa zea

Jizhen Wei1, 2*, Min Zhang2, 3*, Pin Li1, Zhongyuan Deng3, Xinming Yin1, Shiheng An1#, Xianchun Li2# 

1 State Key Laboratory of Wheat and Maize Crop Science/College of Plant Protection, Henan Agricultural University, Zhengzhou 450046, China

2 Department of Entomology and BIO5 Institute, University of Arizona, Tucson, AZ 85721, USA

3 School of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, China

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

美洲棉铃虫(Helicoverpa zea)是多个苏云金芽孢杆菌(Bacillus thuringiensis,Bt)杀虫蛋白(Cry1Cry2/Vip3Aa基因作物的主要害虫。实验室和田间都发现美洲棉铃虫对Cry1Ac/Cry2Ab的交互抗性双重抗性。但是,普遍存在的美洲棉铃虫Cry1Ac/Cry2Ab的交互抗性双重抗性是共同作用机制还是两个独立的抗性机制引起的还不清楚。之前报道钙黏蛋白Cry1Ac的确定受体,有研究也表明钙黏蛋白至少在三种鳞翅目中是Cry2Ab的受体。为了验证钙黏蛋白是否作为Cry1Ac/Cry2Ab交互抗性或双重抗性的共同作用机制,我们克隆了美洲棉铃虫钙黏蛋白基因并通过过表达和干扰该基因的方式分别探究了其在Cry1Ac和Cry2Ab作用机制中的功能。在美洲棉铃虫中肠细胞,脂肪体细胞及Sf9细胞中表达美洲棉铃虫钙黏蛋白基因导致三种细胞对活化的Cry1Ac敏感性增强,但对Cry2Ab的敏感性不变;对应的在美洲棉铃虫中肠细胞和脂肪体细胞中干扰钙黏蛋白基因导致细胞对Cry1Ac敏感性降低,但对Cry2Ab的敏感性不变。同样,用钙黏蛋白siRNA在活体中抑制钙黏蛋白的表达增加了幼虫对Cry1Ac的抗性。这些结果清楚地表明,HzCadheirn不是Cry2Ab的受体,因此不可能是美洲棉铃虫Cry1AcCry2Ab交互抗性双重抗性的共同机制



Abstract  

Helicoverpa zea is a major target pest of pyramided transgenic crops expressing Cry1, Cry2 and/or Vip3Aa proteins from Bacillus thuringiensis (Bt) in the United States.  Laboratory-selected Cry1Ac/Cry2Ab cross resistance and field-evolved practical dual resistance of Hzea to these two toxins have been widely reported.  Whether the widespread Cry1Ac/Cy2Ab dual resistance of Hzea has resulted from the selection of one shared or two independent resistance mechanisms by pyramided Bt crops remains unclear.  Cadherin is a well-confirmed receptor of Cry1Ac and a suggested receptor of Cry2Ab in at least three Lepidopteran species.  To test whether cadherin may serve as one shared mechanism for the cross and dual resistance of Hzea to Cry1Ac and Cry2Ab, we cloned Hzea cadherin (HzCadherin) cDNA and studied its functional roles in the mode of action of Cry1Ac and Cry2Ab by gain- and loss-of-function analyses.  Heterologous expression of HzCadherin in Hzea midgut, Hzea fat body and Sf9 cells made all three of these cell lines more susceptible to activated Cry1Ac but not activated Cry2Ab, whereas silencing HzCadherin of Hzea midgut and fat body cells significantly reduced the susceptibility to Cry1Ac but not Cry2Ab.  Likewise, suppressing HzCadherin with siRNA made Hzea larvae resistant to Cry1Ac.  These results clearly demonstrate that HzCadherin is not a receptor for Cry2Ab, and thus it is unlikely to serve as one shared mechanism for the cross and dual resistance of Hzea to Cry1Ac and Cry2Ab.

Keywords:  Bt crops        cadherin        Cry toxin        receptor        resistance mechanism   
Received: 16 May 2023   Accepted: 24 August 2023
Fund: This research was funded by the USDA National Institute of Food and Agriculture (Hatch Grant ARZT-1360890-H31-164 and multi-state grant ARZT-1370680-R31-172 (NC246)), the National Natural Science Foundation of China (NSFC)–Henan Joint Major Grant (U2004206), the State Key Laboratory of Cotton Biology Open Fund, Zhengzhou University, China (CB2020A06), the Henan Agriculture Research System, China (HARS-22-09-G3), and the earmarked fund for China Agriculture Research System (CARS-27).
About author:  Jizhen Wei, E-mail: weijizhen1986@163.com; Min Zhang, E-mail: 418078760@qq.com; #Correspondence Shiheng An, E-mail: anshiheng@aliyun.com; Xianchun Li, E-mail: lxc@email.arizona.edu * These authors contributed equally to this study.

Cite this article: 

Jizhen Wei, Min Zhang, Pin Li, Zhongyuan Deng, Xinming Yin, Shiheng An, Xianchun Li. 2024.

Functional assessment of cadherin as a shared mechanism for cross/dual resistance to Cry1Ac and Cry2Ab in Helicoverpa zea . Journal of Integrative Agriculture, 23(5): 1604-1617.

Ali M I, Luttrell R G. 2007. Susceptibility of bollworm and tobacco budworm (Lepidoptera: Noctuidae) to Cry2Ab2 insecticidal protein. Journal of Economic Entomology, 100, 921–931.

Anilkumar K J, Rodrigo-Simón A, Ferré J, Pusztai-Care M, Sivasupramaniam S, Moar W J. 2008. Production and characterization of Bacillus thuringiensis Cry1Ac-resistant cotton bollworm Helicoverpa zea (Boddie). Applied and Environmental Microbiology, 74, 462–469.

Baxter S W, Badenes-Pérez F R, Morrison A, Vogel H, Crickmore N, Kain W, Wang P, Heckel D G, Jiggins C D. 2011. Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera. Genetics, 189, 675–679.

Bretschneider A, Heckel D G, Pauchet Y. 2016. Three toxins, two receptors, one mechanism: Mode of action of Cry1A toxins from Bacillus thuringiensis in Heliothis virescens. Insect Biochemistry and Molecular Biology, 76, 109–117.

Brévault T, Heuberger S, Zhang M, Ellers-Kirk C, Ni X Z, Masson L, Li X C, Tabashnik B E, Carrière Y. 2013. Potential shortfall of pyramided transgenic cotton for insect resistance management. Proceedings of the National Academy of Sciences of the United States of America, 110, 5806–5811.

Burd A D, Gould F, Bradley J R, Van D J W, Moar W J. 2003. Estimated frequency of nonrecessive Bt resistance genes in bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in eastern North Carolina. Journal of Economic Entomology, 96, 137–142.

Caccia S, Hernández-Rodríguez C S, Mahon R J, Downes S, James W, Bautsoens N, Rie J V, Ferré J. 2010. Binding site alteration is responsible for field-isolated resistance to Bacillus thuringiensis Cry2A insecticidal proteins in two Helicoverpa species. PLoS ONE, 5, e9975.

Chang X L, Wu Q L, Wang S L, Wang R, Yang Z X, Chen D F, Jiao X G, Mao Z C, Zhang Y J. 2012. Determining the involvement of two aminopeptidase Ns in the resistance of Plutella xylostella to the Bt toxin Cry1Ac: Cloning and study of in vitro function. Journal of Biochemical and Molecular Toxicology, 2, 60–70.

Chen L, Wei J Z, Liu C, Zhang W N, Wang B J, Niu L L, Liang G M. 2018. Specific binding protein ABCC1 is associated with Cry2Ab toxicity in Helicoverpa armigera. Frontiers in Physiology, 9, 745.

Chen W B, Liu C X, Xiao Y T, Zhang D D, Zhang Y D, Li X C, Tabashnik B E, Wu K M. 2015. A toxin-binding alkaline phosphatase fragment synergizes Bt toxin Cry1Ac against susceptible and resistant Helicoverpa armigera. PLoS ONE, 4, e0126288.

Dively G P, Venugopal P D, Finkenbinder C. 2016. Field-evolved resistance in corn earworm to Cry proteins expressed by transgenic sweet corn. PLoS ONE, 11, e0169115.

Fabrick J A, Heu C C, LeRoy D M, DeGain B A, Yelich A J, Unnithan G C, Wu Y D, Li X C, Carrière Y, Tabashnik B E. 2022. Knockout of ABC transporter gene ABCA2 confers resistance to Bt toxin Cry2Ab in Helicoverpa zea. Scientific Reports, 12, 16706.

Fabrick J A, Tabashnik B E. 2012. Similar genetic basis of resistance to Bt toxin Cry1Ac in boll-selected and diet-selected strains of pink bollworm. PLoS ONE, 7, e35658.

Fabrick J A, Unnithan G C, Yelich A J, DeGain B, Masson L, Zhang J, Carrière Y, Tabashnik B E. 2015. Multi-toxin resistance enables pink bollworm survival on pyramided Bt cotton. Scientific Reports, 5, 16554.

FarmProgress 2018. Experts: Cotton farmers may face increased bollworm pressure this season. [2018-04-26]. https://www.farmprogress.com/cotton/experts-cotton-farmers-may-face-increased-bollworm-pressure-this-season

Ferré J, Van R J. 2002. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annual Review of Entomology, 47, 501–533.

Forcada C, Alcácer E, Garcerá M D, Martinez R. 1996. Differences in the midgut proteolytic activity of two Heliothis virescens strains, one susceptible and one resistant to Bacillus thuringiensis toxins. Archives of Insect Biochemistry and Physiology, 31, 257–272.

Gahan L J, Gould F, Heckel D G. 2001. Identification of a gene associated with Bt resistance in Heliothis virescens. Science, 293, 857–860.

Gahan L J, Ma Y T, Coble M L M, Gould F, Moar W J, Heckel D G. 2005. Genetic basis of resistance to Cry1Ac and Cry2Aa in Heliothis virescens (Lepidoptera: Noctuidae). Journal of Economic Entomology, 9, 1357–1368.

Gao Y, Wu K, Gould F, Shen Z. 2009. Tolerance response of Helicoverpa armigera (Lepidoptera: Noctuidae) populations from Cry1Ac cotton planting region. Journal of Economic Entomology, 102, 1217–1223.

González-Cabrera J, Escriche B, Tabashnik B E, Ferré J. 2003. Binding of Bacillus thuringiensis toxins in resistant and susceptible strains of pink bollworm (Pectinophora gossypiella). Insect Biochemistry and Molecular Biology, 33, 929–935.

Goodman C L, Wang A A, Nabli H, McIntosh A H, Wittmeyer J L, Grasela J J. 2004. Development and partial characterization of Heliothine cell lines from embryonic and differentiated tissues. In Vitro Cellular and Developmental Biology - Animal, 40, 89–94.

Gould F, Anderson A, Reynolds A, Bumgarner L, Moar W. 1995. Selection and genetic analysis of a Heliothis virescens (Lepidoptera: Noctuidae) strain with high levels of resistance to Bacillus thuringiensis toxins. Journal of Economic Entomology, 88, 1545–1559.

Gould F, Martinez-Ramirez A, Anderson A, Ferre J, Silva F J, Moar W J. 1992. Broad-spectrum resistance to Bacillus thuringiensis toxins in Heliothis virescens. Proceedings of the National Academy of Sciences of the United States of America, 89, 7986–7988.

Heckel D G. 2012. Learning the ABCs of Bt: ABC transporters and insect resistance to Bacillus thuringiensis provide clues to a crucial step in toxin mode of action. Pesticide and Biochemistry and Physiology, 104, 103–110.

Hernández C S, Ferré J. 2005. Common receptor for Bacillus thuringiensis toxins Cry1Ac, Cry1Fa, and Cry1Ja in Helicoverpa armigera, Helicoverpa zea, and Spodoptera exigua. Applied and Environmental Microbiology, 71, 5627–5629.

Hernández-Rodríguez C S, Van V A, Bautsoens N, Van R J, Ferré J. 2008. Specific binding of Bacillus thuringiensis Cry2A insecticidal proteins to a common site in the midgut of Helicoverpa species. Applied and Environmental Microbiology, 74, 7654–7659.

Huang F N, Andow D A, Buschman L L. 2011. Success of the high dose/refuge resistance management strategy after 15 years of Bt crop use in North America. Entomologia Expermentalis et Applicata, 140, 1–16.

Jackson R E, Gould F, Bradley J R J, Van D J W. 2006. Genetic variation for resistance to Bacillus thuringiensis toxins in Helicoverpa zea (Lepidoptera: Noctuidae) in eastern North Carolina. Journal of Economic Entomology, 99, 1790–1797.

Jin L, Wei Y Y, Zhang L, Yang Y H, Tabashnik B E, Wu Y D. 2013. Dominant resistance to Bt cotton and minor cross-resistance to Bt toxin Cry2Ab in cotton bollworm from China. Evolutionary Applications, 6. 1222–1235.

Jurat-Fuentes J L, Gahan L J, Gould F L, Heckel D G, Adang M J. 2004a. The HevCaLP protein mediates binding specificity of the Cry1A class of Bacillus thuringiensis toxins in Heliothis virescens. Biochemistry, 43, 14299–14305.

Jurat-Fuentes J L, Gould F L, Adang M J. 2003. Dual resistance to Bacillus thuringiensis Cry1Ac and Cry2Aa toxins in Heliothis virescens suggests multiple mechanisms of resistance. Applied and Environmental Microbiology, 69, 5898–5906.

Jurat-Fuentes J L, Gould F L, Adang M J. 2004b. Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Applied and Environmental Microbiology, 271, 3127–3135.

Jurat-Fuentes J L, Karumbaiah L, Jakka S R, Ning C M, Liu C X, Wu K M, Jackson J, Gould F, Blanco C, Portilla M, Perera O, Adang M. 2011. Reduced levels of membrane-bound alkaline phosphatase are common to Lepidopteran strains resistant to Cry toxins from Bacillus thuringiensis. PLoS ONE, 6, e17606.

Jurat-Fuentes J L, Michael J A. 2007. A proteomic approach to study Cry1Ac binding proteins and their alterations in resistant Heliothis virescens larvae. Journal of Invertebrate Pathology, 95, 187–191.

Karumbaiah L, Oppert B, Jurat-Fuentes J L, Adang M J. 2007. Analysis of midgut proteinases from Bacillus thuringiensis-susceptible and -resistant Heliothis virescens (Lepidoptera: Noctuidae). Comparative Biochemistrry and Physiology (Part B), 146, 139–146.

Kaur G. 2018. Susceptibility of field-collected pupations of the corn earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) from three Southern States of the U.S. to Cry1A.105 and Cry2Ab2 proteins. MSc thesis, Louisiana State University, USA.

Kaur G, Guo J G, Brown S, Head G P, Price P A, Paula-Moraes, S, Ni X Z, Dimase M, Huang F. 2019. Field-evolved resistance of Helicoverpa zea (Boddie) to transgenic maize expressing pyramided Cry1A.105/Cry2Ab2 proteins in northeast Louisiana, the United States. Journal of Invertebrate Pathology, 163, 11–20.

Lee M K, Rajamohan F, Gould F, Dean D H. 1995. Resistance to Bacillus thuringiensis Cry1A-endotoxins in a laboratory-selected Heliothis virescens strain is related to receptor alteration. Applied and Environmental Microbiology, 61, 3836–3842.

Liu C X, Xiao Y T, Li X C, Oppert B E, Tabashnik B E, Wu K M. 2014. Cis-mediated down-regulation of a trypsin gene associated with Bt resistance in cotton bollworm. Scientific Reports, 4, 07219.

Liu L P, Gao M J, Yang S, Liu S Y, Wu Y D, Carrière Y, Yang Y H. 2017. Resistance to Bacillus thuringiensis toxin Cry2Ab and survival on single-toxin and pyramided cotton in cotton bollworm from China. Evolutionary Applications, 10, 170–179.

Liu S S, Wang M, Li X C. 2015. Overexpression of Tyrosine hydroxylase and Dopa decarboxylase associated with pupal melanization in Spodoptera exigua. Scientific Reports, 5, 11273.

Luo S D, Wu K M, Tian Y, Liang G M, Feng X, Zhang J, Guo Y Y. 2007. Cross-resistance studies of Cry1Ac-resistant strains of Helicoverpa armigera (Lepidoptera: Noctuidae) to Cry2Ab. Economic Entomology, 100, 909–915.

Mahon R J, Olsen K M, Garsia K A, Young S R. 2007. Resistance to Bacillus thuringiensis toxin Cry2Ab in a strain of Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. Economic Entomology, 10, 894–902.

Mathew L G, Ponnuraj J, Mallappa B, Chowdary L R, Zhang J W, Tay W T, Walsh T K, Gordon K H J, Heckel D G, Downes S, Carrière Y, Li X C, Tabashnik B E, Fabrick J A. 2018. ABC transporter mis-splicing associated with resistance to Bt toxin Cry2Ab in laboratory- and field-selected pink bollworm. Scientific Reports, 8, 13531.

Morin S, Biggs R W, Sisterson M S, Shriver L, Ellers-Kirk C, Higginson D, Holley D, Gahan L J, Heckel D G, Carrière Y, Dennehy T J, Brown J K, Tabashnik B E. 2003. Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proceedings of the National Academy of Sciences of the United States of America, 100, 5004–5009.

Ocelotl J, Sánchez J, Gómez I, Tabashnik B E, Bravo A, Soberón M. 2017. ABCC2 is associated with Bacillus thuringiensis Cry1Ac toxin oligomerization and membrane insertion in diamondback moth. Scientific Reports, 7, 2386.

Pan Z Z, Xu L, Liu B, Zhang, Chen Z, Chen Q X, Zhu Y J. 2017. PxAPN5 serves as a functional receptor of Cry2Ab in Plutella xylostella (L.) and its binding domain analysis. International Journal of Biology Macromolecules, 105, 516–521.

Qi L X, Dai H Y, Jin Z, Shen H W, Guan F, Yang Y H, Tabashnik B E, Wu Y D. 2021. Evaluating cross-resistance to Cry and Vip toxins in four strains of Helicoverpa armigera with different genetic mechanisms of resistance to Bt toxin Cry1Ac. Frontiers in Microbiology, 12, 939

Qiu L, Hou L, Zhang B, Liu L, Li B, Deng P, Ma W, Wang X P, Fabrick J A, Chen L Z, Lei C L. 2015. Cadherin is involved in the action of Bacillus thuringiensis toxins Cry1Ac and Cry2Aa in the beet armyworm, Spodoptera exigua. Journal of Invertebrate Pathology, 127, 47–53.

Rajagopal R, Arora N, Sivakumar S, Rao N G V, Nimbalkar S A, Bhatnagar R K. 2009. Resistance of Helicoverpa armigera to Cry1Ac toxin from Bacillus thuringiensis is due to improper processing of the protoxin. Biochemical Journal, 419, 309–316.

Reay-Jones F P F. 2019. Pest status and management of corn earworm (Lepidoptera: Noctuidae) in field corn in the United States. Journal of Integrated Pest Management, 10, 1–9.

Reisig D D, Huseth A S, Bacheler J S, Aghaee M A, Braswell L, Burrack H J, Flanders K, Greene J K, Herbert D A, Jacobson A, Paula-Moraes S V, Roberts P, Taylor S V. 2018. Long-term empirical and observational evidence of practical Helicoverpa zea resistance to cotton with pyramided Bt toxins. Journal of Economic Entomology, 111, 1824–1833.

Santiago-González J C, Kerns D L, Head G P, Yang F. 2023. A modified F2 screen for estimating Cry1Ac and Cry2Ab resistance allele frequencies in Helicoverpa zea (Lepidoptera: Noctuidae). Journal of Economic Entomology, 116, 289–296.

Siegfried B D, Spencer T, Nearman J. 2000. Baseline susceptibility of the corn earworm (Lepidoptera: Noctuidae) to the Cry1Ab toxin from Bacillus thuringiensis. Journal of Economic Entomology, 93, 1265–1268.

Tabashnik B E, Carrière Y. 2017. Surge in insect resistance to transgenic crops and prospects for sustainability. Nature Biotechnology, 35, 926–935.

Tabashnik B E, Unnithan G C, Masson L, Crowder D W, Li X C, Carrière Y. 2009. Asymmetrical cross-resistance between Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in pink bollworm. Proceedings of the National Academy of Sciences of the United States of America, 106, 11889–11894.

Tanaka S, Endo H, Adegawa S, Iizuka A, Imamura K, Kikuta S, Sato R. 2017. Bombyx mori ABC transporter C2 structures responsible for the receptor function of Bacillus thuringiensis Cry1Aa toxin. Insect Biochemistry and Molecular Biology, 91, 44–54.

Tanaka S, Miyamoto K, Noda H, Jurat-Fuentes J L, Yoshizawa Y, Endo H, Sato R. 2013. The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for Cry toxins from Bacillus thuringiensis. The FEBS Journal, 280, 1782–1794.

Tay W T, Mahon R J, Heckel D G, Walsh T K, Downes S, James W J, Lee S F, Reineke A, Williams A K, Gordon K H J. 2015. Insect resistance to Bacillus thuringiensis toxin Cry2Ab is conferred by mutations in an ABC transporter subfamily A protein. PLoS Genetics, 11, e1005534.

Tiewsiri K, Wang P. 2011. Differential alteration of two aminopeptidases N associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper. Proceedings of the National Academy of Sciences of the United States of America, 108, 14037–14042.

US EPA (Environmental Protection Agency). 2018. White Paper on Resistance in Lepidopteran Pests of Bacillus Thuringiensis (Bt) Plant Incorporated Protectants in the United States. Environmental Protection Agency, USA.

Wang G R, Liang G M, Wu K M, Guo Y Y. 2005a. Gene cloning and sequencing of aminopeptidase N3, a putative receptor for Bacillus thuringiensis insecticidal Cry1Ac toxin in Helicoverpa armigera (Lepidoptera: Noctuidae). European Journal of Entomology, 102, 13–19.

Wang G R, Wu K M. Liang G M, Guo Y Y. 2005b. Gene cloning and expression of cadherin in midgut of Helicoverpa armigera and its Cry1A binding region. Science in China, 48, 346–356.

Wang J, Ma H H, Zhao S, Huang J L, Yang Y H, Tabashnik B E, Wu Y D. 2020a. Functional redundancy of two ABC transporter proteins in mediating toxicity of Bacillus thuringiensis to cotton bollworm. PLoS Pathogens, 16, e1008427.

Wang J, Wang H D, Liu S Y, Liu L P, Tay W T, Walsh T K, Yang Y H, Wu Y D. 2017. CRISPR/Cas9 mediated genome editing of Helicoverpa armigera with mutations of an ABC transporter gene HaABCA2 confers resistance to Bacillus thuringiensis Cry2A toxins. Insect Biochemistry and Molecular Biology, 87,147–153.

Wang J, Zhang H N, Wang H D, Zhao S, Zuo Y Y, Yang Y H, Wu Y D. 2016a. Functional validation of cadherin as a receptor of Bt toxin Cry1Ac in Helicoverpa armigera utilizing the CRISPR/Cas9 system. Insect Biochemistry and Molecular Biology, 76, 11–17.

Wang J, Zuo Y Y, Li L L, Wang H, Liu S Y, Yang Y H, Wu Y D. 2020b. Knockout of three aminopeptidase N genes does not affect susceptibility of Helicoverpa armigera larvae to Bacillus thuringiensis Cry1A and Cry2A toxins. Insect Science, 27, 440–448.

Wang L, Ma Y M, Guo X Q, Wan P, Liu K Y, Cong S B, Wang J T, Xu D, Xiao Y T, Li X C, Tabashnik B E, Wu K M. 2019. Bollworm resistance to Bt toxin Cry1Ac associated with an insertion in cadherin exon 20. Toxins, 11, 186.

Wang L, Ma Y M, Wan P, Liu K Y, Xiao Y T, Wang J T, Cong S B, Xu D, Wu K M, Fabrick J A. 2018. Resistance to Bacillus thuringiensis linked with a cadherin transmembrane mutation affecting cellular trafficking in pink bollworm from China. Insect Biochemistry and Molecular Biology, 94, 28–35.

Wang P, Zhao J Z, Rodrigo-Simón A, Kain W, Janmaat A F, Shelton A M, Ferré J, Myers J. 2007. Mechanism of resistance to Bacillus thuringiensis toxin Cry1Ac in a greenhouse population of the cabbage looper, Trichoplusia ni.
Applied and Environmental Microbiology, 73, 1199–1207.

Wang R, Tetreau G, Wang P. 2016b. Effect of crop plants on fitness costs associated with resistance to Bacillus thuringiensis toxins Cry1Ac and Cry2Ab in cabbage loopers. Scientific Reports, 6, 20959.

Wei J Z, Guo Y Y, Liang G M, Wu K M, Zhang J, Tabashnik B E, Li X C. 2015. Cross-resistance and interactions between Bt toxins Cry1Ac and Cry2Ab against the cotton bollworm. Scientific Reports, 5, 7714.

Wei J Z, Liang G M, Wu K M, Gu S H, Guo Y Y, Ni X Z, Li X C. 2018. Cytotoxicity and binding profiles of activated Cry1Ac and Cry2Ab to three insect cell lines. Insect Science, 25, 655–666.

Wei J Z, Yang S, Zhou S, Liu S K, Cao P, Liu X G, Du M F, An S H. 2021a. Suppressing calcineurin activity increases the toxicity of Cry2Ab to Helicoverpa armigera. Pest Management Science, 77, 2142–2150.

Wei J Z, Yao X, Yang S, Liu S K, Zhou S, Cen J J, Liu X G, Du M F, Tang Q B, An S H. 2021b. Suppression of calcineurin enhances the toxicity of Cry1Ac to Helicoverpa armigera. Frontiers in Microbiology, 12, 634619.

Wei J Z, Zhang M, Liang G M, Li X C. 2019. Alkaline phosphatase 2 is a functional receptor of Cry1Ac but not Cry2Ab in Helicoverpa zea. Insect Molecular Biology, 28, 372–379.

Wei J Z, Zhang M, Liang G M, Wu K M, Guo Y Y, Ni X Z, Li X C. 2016. APN1 is a functional receptor of Cry1Ac but not Cry2Ab in Helicoverpa zea. Scientific Reports, 6, 19179.

Welch K L, Unnithan G C, Degain B A, Wei J Z, Zhang J, Li X C, Tabashnik B E, Carrière Y. 2015. Cross-resistance to toxins used in pyramided Bt crops and resistance to Bt sprays in Helicoverpa zea. Journal of Invertebrate Pathology, 132, 149–156.

Xu L, Gao H J, Pan Z Z, Zhu Y J, Chen Q X, Liu B. 2014. Cloning, prokaryotic expression and homology modeling analysis of midgut aminopeptidase gene PxAPN5 in Plutella xylostella (Lepidoptera: Plutellidae). Acta Entomologica Sinica, 57, 1272–1280. (in Chinese)

Yang F, González J C S, Williams J, Cook D C, Gilreath R T, Kerns D L. 2019. Occurrence and ear damage of Helicoverpa zea on transgenic Bacillus thuringiensis maize in the field in Texas, U.S. and its susceptibility to Vip3A protein. Toxins, 11, 102.

Yang F, Kerns D, Gore J, Catchot A, Lorenz G, Stewart S. 2017. Susceptibility of field populations of the cotton bollworm in the southern U.S. to four individual Bt proteins. In: Proceedings of the Beltwide Cotton Conference. National Cotton Council of America, USA. pp. 786–797.

Yang F, Kerns D L, Little N, Brown S A, Stewart S D, Catchot A L, Tabashnik, B E. 2022. Practical resistance to Cry toxins and efficacy of Vip3Aa in Bt cotton against Helicoverpa zea. Pest Management Science, 78, 5234–5242.

Yang Y H, Yang Y J, Gao W Y, Guo J J, Wu Y H, Wu Y D. 2009. Introgression of a disrupted cadherin gene enables susceptible Helicoverpa armigera to obtain resistance to Bacillus thuringiensis toxin Cry1Ac. Bulletin Entomological Research, 99, 175–181.

Yuan J S, Reed A, Chen F, Stewart C N. 2006. Statistical analysis of real-time PCR data. BMC Bioinformatics, 7, 85.

Yuan X, Zhao M, Wei J Z, Zhang W N, Wang B J, Khaing M M, Liang G M. 2017. New insights on the role of alkaline phosphatase 2 from Spodoptera exigua (Hübner) in the action mechanism of Bt toxin Cry2Aa. Journal of Insect Physiology, 98, 101–107.

Zhang M. 2014. Mechanisms of field-evolved Cry1Ac resistance in Helicoverpa zea. Ph D thesis, University of Arizona, USA.

Zhang M, Wei J Z, Ni X Z, Zhang J, Jurat-Fuentes J L, Fabrick J A, Carrière Y, Tabashnik B E, Li X C. 2019. Decreased Cry1Ac activation by midgut proteases associated with Cry1Ac resistance in Helicoverpa zea. Pest Management Science, 75, 1099–1106.

Zhang S P, Cheng H M, Gao Y L, Wang G R, Liang G M, Wu K M. 2009. Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochemistry and Molecular Biology, 39, 421–429.

Zhang Z, Teng X L, Ma W H, Li F. 2017. Knockdown of two cadherin genes confers resistance to Cry2A and Cry1C in Chilo suppressalis. Scientific Reports, 7, 5992.

Zhao J, Jin L, Yang Y H, Wu Y D. 2010. Diverse cadherin mutations conferring resistance to Bacillus thuringiensis toxin Cry1Ac in Helicoverpa armigera. Insect Biochemistry and Molecular Biology, 40, 113–118.

Zhao M, Yuan X D, Wei J Z, Zhang W N, Wang B J, Khaing M M, Liang G M. 2017. Functional roles of cadherin, aminopeptidase-N and alkaline phosphatase from Helicoverpa armigera (Hübner) in the action mechanism of Bacillus thuringiensis Cry2Aa. Scientific Reports, 7, 46555.

No related articles found!
No Suggested Reading articles found!