Selection, effective dominance, and completeness of Cry1A.105/Cry2Ab2 dual-protein resistance in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)

doi:10.1016/j.jia.2022.09.024

Journal of Integrative Agriculture ›› 2023, Vol. 22 ›› Issue (7): 2151-2161.DOI: 10.1016/j.jia.2022.09.024

收稿日期:2022-07-22 接受日期:2022-08-31 出版日期:2023-07-20 发布日期:2022-08-31

Selection, effective dominance, and completeness of Cry1A.105/Cry2Ab2 dual-protein resistance in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)

Tiago SILVA¹, Ying NIU¹, Tyler TOWLES², Sebe BROWN³, Graham P. HEAD⁴, Wade WALKER², Fangneng HUANG^1#

¹Department of Entomology, Louisiana State University Agricultural Center, Baton Rouge, Louisiana 70817, USA
² Macon Ridge Research Station, Louisiana State University Agricultural Center, Alexandria, Louisiana 71295, USA
³ Dean Research Station, Louisiana State University Agricultural Center, Alexandria, Louisiana 71302, USA
⁴Bayer Crop Science, Chesterfield, Missouri 63017, USA

Received:2022-07-22 Accepted:2022-08-31 Online:2023-07-20 Published:2022-08-31
About author:Tiago SILVA, E-mail: TSilva@agcenter.lsu.edu; #Correspondence Fangneng HUANG, E-mail: fhuang@agcenter.lsu.edu
Supported by:
This article is published with the approval of the Director of the Louisiana Agricultural Experiment Station as manuscript No. 2022-234-37238. This project represents work supported by Bayer Crop Science (St. Louis, MO, USA), Hatch funds from the USDA National Institute of Food, and Agriculture, and USDA Regional Research Project NC-246.

摘要/Abstract

Abstract:

In the U.S., Helicoverpa zea (Boddie) is a major pest targeted by both transgenic maize and cotton expressing Bacillus thuringiensis (Bt) proteins. Resistance of insect to Bt maize and cotton containing cry1A and cry2A genes has widely occurred in the U.S. In this study, two trials were performed to investigate larval survival and development of a Cry1A.105/Cry2Ab2 dual-protein resistant (VT2P-RR), a susceptible, and an F1 heterozygous (VT2P-RS) populations of H. zea on ears of nine Bt and three non-Bt maize hybrids. The Bt maize hybrids evaluated represent five common pyramided traits expressing two or three of the Cry1A.105, Cry1Ab, Cry1F, Cry2Ab2, and Vip3Aa20 proteins. In the laboratory, neonates of the three H. zea populations were inoculated on silks of ears collected from maize at R1-R2 plant stages; and larval survivorship was checked 10 d after neonate release. All three insect populations survived normally on non-Bt maize ears. Varied numbers of VT2P-RR and VT2P-RS survived on ears of Cry1A.105/Cry2Ab2 maize, while all larvae of the three populations died or could not develop on ears of Vip3Aa20-expressing maize. The results demonstrated that the dual-protein resistant H. zea was not cross-resistant to Vip3Aa20-expressing maize, and thus traits with vip3Aa20 gene should be effective to manage Cry1A.105/Cry2Ab2-resistant H. zea. The resistance in VT2P-RR was determined to be incomplete on Cry1A.105/Cry2Ab2 maize. The effective dominance levels varied greatly, from recessive to incompletely dominant, depending on maize hybrids and trials, suggesting that proper selection of maize hybrids could be important for mitigating the Cry1A.105/Cry2Ab2 resistance. The data generated should aid in modeling multiple-protein Bt resistance in H. zea.

Key words: corn earworm , Cry1A/Cry2A , effective dominance , incomplete resistance , Bt maize resistance management

Tiago SILVA, Ying NIU, Tyler TOWLES, Sebe BROWN, Graham P. HEAD, Wade WALKER, Fangneng HUANG. [J]. Journal of Integrative Agriculture, 2023, 22(7): 2151-2161.

Tiago SILVA, Ying NIU, Tyler TOWLES, Sebe BROWN, Graham P. HEAD, Wade WALKER, Fangneng HUANG. Selection, effective dominance, and completeness of Cry1A.105/Cry2Ab2 dual-protein resistance in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)[J]. Journal of Integrative Agriculture, 2023, 22(7): 2151-2161.

参考文献

Abbott W S. 1925. A method for computing the effectiveness of an insecticide. Journal of Economic Entomology, 18, 265–267.

Anilkumar K J, Pusztai-Carey M, Moar W J. 2008. Fitness costs associated with Cry1Ac-resistant Helicoverpa zea (Lepidoptera: Noctuidae): A factor countering selection for resistance to Bt cotton? Journal of Economic Entomology, 101, 1421–1431.

Bernardi D, Bernardi O, Horikoshi R J, Salmeron E, Okuma D M, Farias J R, do Nascimento A R B, Omoto C. 2017. Selection and characterization of Spodoptera frugiperda (Lepidoptera: Noctuidae) resistance to MON89034×TC1507×NK603 maize technology. Crop Protection, 94, 64−68.

Bilbo T R, Reay-Jones F P F, Reisig D D, Greene J K. 2019. Susceptibility of corn earworm (Lepidoptera: Noctuidae) to Cry1A.105 and Cry2Ab2 in North and South Carolina. Journal of Economic Entomology, 112, 1845–1857.

Bourguet D, Genissel A, Raymond M. 2000. Insecticide resistance and dominance levels. Journal of Economic Entomology, 93, 1588−1595.

Buntin G D. 2008. Corn expressing Cry1Ab or Cry1F endotoxin for fall armyworm and corn earworm (Lepidoptera: Noctuidae) management in field corn for grain production. Florida Entomologist, 91, 523–530.

Carriére Y, Crowder D W, Tabashnik B E. 2010. Evolutionary ecology of insect adaptation to Bt crops. Evolutionary Applications, 3, 561–573.

Carriére Y, Ellers-Kirk C, Biggs R W, Nyboer M E, Unnithan G C, Dennehy T J, Tabashnik B E. 2006. Cadherin-based resistance to Bacillus thuringiensis cotton in hybrid strains of pink bollworm: fitness costs and incomplete resistance. Journal of Economic Entomology, 99, 1925–1935.

DiFonzo C. 2022. The handy Bt trait table for U.S. corn production. [2022-09-23]. https://lubbock.tamu.edu/files/2022/02/BtTraitTable-March2022.pdf

Dimase M, Oyediran I, Brown S, Walker W, Guo J, Yu W, Zhang Y, Chen J, Wen Z, Huang F. 2020. Larval movement and survival of Helicoverpa zea (Boddie) in seed blends of non-Bt and Bt maize containing Agrisure Viptera® trait: Implications for resistance management. Crop Protection, 138, 105339.

Dively G P, Kuhar T P, Taylor S, Doughty H B, Holmstrom K, Gilrein D, Nault B A, Ingerson-Mahar J, Whalen J, Reisig D, Frank D L, Fleischer S J, Owens D, Welty C, Reay-Jones F P F, Porter P, Smith J L, Saguez J, Murray S, et al.. 2021. Sweet corn sentinel monitoring for lepidopteran field-evolved resistance to Bt toxins. Journal of Economic Entomology, 114, 307–319.

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, 12, e0183637.

Ghimire M N, Huang F, Leonard R B, Head G P, Yang Y. 2011. Susceptibility of Cry1Ab-susceptible and -resistant sugarcane borer to transgenic corn plants containing single or pyramided Bacillus thuringiensis genes. Crop Protection, 30, 74–81.

Grimi D A, Parody B, Ramos M L, Machado M, Ocampo F, Willse A, Martinelli S, Head G. 2018. Field-evolved resistance to Bt maize in sugarcane borer (Diatraea saccharalis) in Argentina. Pest Management Science, 74, 905−913.

Guo J, Oyediran I, Rice M E, Brown S, Dimase M, Lin S, Walker W, Yu W, Niu Y, Huang F. 2021. Seed blends of pyramided Cry/Vip maize reduce Helicoverpa zea populations from refuge ears. Journal of Pest Science, 94, 959–968.

Head G, Jackson R E, Adamczyk J, Bradley J R, Van Duyn J, Gore J, Hardee D D, Leonard B R, Luttrell R, Ruberson J, Mullins J W, Orth R G, Sivasupramaniam S, Voth R. 2010. Spatial and temporal variability in host use by Helicoverpa zea as measured by analyses of stable carbon isotope ratios and gossypol residues. Journal of Applied Ecology, 47, 583–592.

Horner T A, Dively G P, Herbert D A. 2003. Development, survival, and fitness performance of Helicoverpa zea (Lepidoptera: Noctuidae) in MON810 Bt field corn. Journal of Economic Entomology, 96, 914–924.

Huang F. 2021a. Dominance and fitness costs of insect resistance to genetically modified Bacillus thuringiensis crops. GM Crops & Food, 12, 192–211.

Huang F. 2021b. Resistance of the fall armyworm, Spodoptera frugiperda (J. E. Smith), to transgenic Bacillus thuringiensis Cry1F corn in the Americas: lessons and implications for Bt corn IRM in China. Insect Science, 28, 574–589.

Huang F, 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 Experimentalis et Applicata, 140, 1–16.

Huang F, Niu Y, Brown S, Kerns D, Jurat-Fuentes J L, Towles T, Head G, Carroll M, Walker W, Silva T. 2022. Extended investigation of unexpected survival of corn earworm on transgenic corn hybrids expressing Vip3Aa protein in Louisiana. In: 2022 Entomological Society of American Southeastern Branch Meeting. San Juan, Puerto Rico.

ISAAA. 2019. Global Status of Commercialized Biotech/GM Crops in 2019: Biotech Crops Drive Socio-Economic Development and Sustainable Environment in the New Frontier. ISAAABrief No. 55. ISAAA, Ithaca, NY.

Jackson R E, Bradley J R, Van Duyn J, Leonard B R, Allen K C, Luttrell R, Ruberson J, Adamczyk J, Gore J, Hardee D D, Voth R, Sivasupramaniam S, Mullins J W, Head G. 2008. Regional assessment of Helicoverpa zea populations on cotton and non-cotton crop hosts. Entomologia Experimentalis et Applicata, 126, 89–106.

Kaur G, Guo J, Brown S, Head G P, Price P A, Paula-Moraes S, Ni X, 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.

Lin S, Oyediran I, Niu Y, Brown S, Cook D, Ni X, Zhang Y, Reay-Jones F P F, Chen J S, Wen Z, Dimase M, Huang F. 2022. Resistance allele frequency to Cry1Ab and Vip3Aa20 in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in Louisiana and three other southeastern U.S. states. Toxins, 4, 270.

Lingren P D, Westbrook J K, Bryant V M, Raulston J R, Esquivel J F, Jones G D. 1994. Origin of corn earworm (Lepidoptera: Noctuidae) migrants as determined by Citrus pollen markers and synoptic weather systems. Environmental Entomology, 23, 562–570.

Lynch R E, Wiseman B R, Plaisted D, Warnick D. 1999. Evaluation of transgenic sweet corn hybrids expressing CryIA(b) toxin for resistance to corn earworm and fall armyworm (Lepidoptera: Noctuidae). Journal of Economic Entomology, 92, 246–252.

Neunzig H. 1964. The eggs and early-instar larvae of Heliothis zea and Heliothis virescens (Lepidoptera: Noctuidae). Annals of Entomological Society of America, 57, 98–102.

Niu Y, Oyediran I, Yu W, Lin S, Dimase M, Brown S, Reay-Jones F P F, Cook D, Reisig D, Thrash B, Ni X, Paula-Moraes S V, Zhang Y, Chen J S, Wen Z, Huang F. 2021. Populations of Helicoverpa zea (Boddie) in the southeastern United States are commonly resistant to Cry1Ab, but still susceptible to Vip3Aa20 expressed in MIR 162 corn. Toxins, 13, 63.

Porter P, Kerns D. 2020. Corn earworm and soybean podworm. [2022-09-23]. https://extensionentomology.tamu.edu/insect_scientific_name/helicoverpa-zea/

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, Reay-Jones F P F. 2015. Inhibition of Helicoverpa zea (Lepidoptera: Noctuidae) growth by transgenic corn expressing Bt toxins and development of resistance to Cry1Ab. Environmental Entomology, 44, 1275–1285.

Rule D M, Nolting S P, Prasifka P L, Storer N P, Hopkins B W, Scherder E F, Siebert M W, Hendrix W H. 2014. Efficacy of pyramided Bt proteins Cry1F, Cry1A.105, and Cry2Ab2 expressed in SmartStax corn hybrids against lepidopteran insect pests in the northern United States. Journal of Economic Entomology, 107, 403–409.

Santiago-González J C, David L K, Graham P H, Yang F. 2022. Effective dominance and redundant killing of single- and dual-gene resistant populations of Helicoverpa zea on pyramided Bt corn and cotton. Pest Management Science, 78, 4333–4339.

SAS (Statistical Analysis System) Institute. 2016. SAS (Statistical Analysis System)/STAT User’s SAS (Statistical Analysis System)/STAT® 14.2 User’s Guide. Statistical Analysis System Institute, Cary, North Carolina, USA.

Siebert M W, Nolting S P, Hendrix W, Dhavala S, Craig C, Leonard B R, Stewart S D, All J, Musser F R, Buntin G D, Samuel L. 2012. Evaluation of corn hybrids expressing Cry1F, Cry1A.105, Cry2Ab2, Cry34Ab1/Cry35Ab1, and Cry3Bb1 against southern United States insect pests. Journal of Economic Entomology, 105, 1825–1834.

Tabashnik B E, Brévault T, Carrière Y. 2013. Insect resistance to Bt crops: Lessons from the first billion acres. Nature Biotechnology, 31, 510–521.

USEPA (United States Environmental Protection Agency). 2001. Biopesticides registration action document: Bacillus thuringiensis plant-incorporated protectants-insect resistance management. [2022-09-23]. https://www3.epa.gov/pesticides/chem_search/reg_actions/pip/bt_brad2/4-irm.pdf

USEPA (United States Environmental Protection Agency). 2010. Biopesticides registration action document: Bacillus thuringiensis Cry1A.105 and Cry2Ab2 insecticidal proteins and the genetic material necessary for their production in corn. [2022-09-23]. https://www3.epa.gov/pesticides/chem_search/reg_actions/pip/mon-89034-brad.pdf

USEPA (United States Environmental Protection Agency). 2018. White paper on resistance in lepidopteran pests of Bacillus thuringiensis (Bt) plant incorporated protectants in the united states. Published April 11, 2018. [2022-09-23]. https://www.epa.gov/sites/production/files/2018-07/documents/position_paper_07132018.pdf

USDANASS (United States Department of Agriculture-National Agricultural Statistics Service). 2020. Acreage. [2022-09-23]. https://usda.library.cornell.edu/concern/publications/j098zb09z

USDANASS (United States Department of Agriculture-National Agricultural Statistics Service). 2021. Acreage. [2022-09-23]. https://usda.library.cornell.edu/concern/publications/j098zb09z

Wu X, Leonard B R, Zhu Y C, Abel C A, Head G P, Huang F. 2009. Susceptibility of Cry1Ab-resistant and -susceptible sugarcane borer (Lepidoptera: Crambidae) to four Bacillus thuringiensis toxins. Journal of Invertebrate Pathology, 100, 29–34.

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 L, Head G P, Price P A, Levy R, Niu Y, Huang F. 2014. A challenge for the seed mixture refuge strategy in Bt maize: impact of cross-pollination on an ear-feeding pest, corn earworm. PLoS ONE, 9, e112962.

Yu W, Head G P, Price P, Brown S, Cook D, Ni X, Reay-Jones F P F, Dimase M, Huang F. 2022. Estimation of resistance allele frequencies to Cry1A.105 and Cry2Ab2 in the corn earworm (Lepidoptera: Noctuidae) with F2 isolines generated from a mass-mating method. Crop Protection, 161, 106054.

Yu W, Lin S, Dimase M, Niu Y, Brown S, Head G P, Price P A, Reay-Jones F P F, Cook D, Reisig D, Thrash B, Ni X, Paula-Moraes S V, Huang F. 2021. Extended investigation of field-evolved resistance of the corn earworm Helicoverpa zea (Lepidoptera: Noctuidae) to Bacillus thuringiensis Cry1A.105 and Cry2Ab2 proteins in the southeastern United States. Journal of Invertebrate Pathology, 183, 107560.

Selection, effective dominance, and completeness of Cry1A.105/Cry2Ab2 dual-protein resistance in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)

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