Cry1F resistance in fall armyworm Spodoptera frugiperda: Single gene versus pyramided Bt maize

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Huang, Fangneng ^a   Qureshi, Jawwad A ^b   Meagher, Robert L ^c   Reisig, Dominic D ^d   Head, Graham P ^e   Andow, David A ^f   Ni, Xinzi ^g   Kerns, David ^a   Buntin, G David ^h   Niu, Ying ^a   Yang, Fei ^a   Dangal, Vikash ^a  

^a LOUISIANA STATE UNIVERSITY AGRICULTURAL CENTER   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c CENTER FOR MEDICAL   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e MONSANTO COMPANY   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

^g AGRICULTURAL RESEARCH SERVICE   (United States)

^h UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRY1A.105 PROTEIN; CRY1F PROTEIN; CRY2AB2 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; VIP3A PROTEIN; BACTERIAL TOXIN;

ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL GENE; BIOLOGICAL PEST CONTROL; CONTROLLED STUDY; CROSS RESISTANCE; GENE FREQUENCY; INSECT RESISTANCE; MAIZE; NATURAL POPULATION; NONHUMAN; PLANT DAMAGE; PLANT DEFENSE; POPULATION MIGRATION; PROTEIN PURIFICATION; RESISTANCE MANAGEMENT; SPODOPTERA FRUGIPERDA; TRANSGENIC CROP; TRANSGENIC PLANT; UNITED STATES; ANIMAL; DISEASE RESISTANCE; GENETICS; INSECT CONTROL; MICROBIOLOGY; PARASITOLOGY; PROCEDURES; SPODOPTERA;

BACILLUS THURINGIENSIS; HEXAPODA; SPODOPTERA FRUGIPERDA; ZEA MAYS;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL TOXINS; DISEASE RESISTANCE; INSECT CONTROL; PLANTS, GENETICALLY MODIFIED; SPODOPTERA; ZEA MAYS;

EID: 84912079286     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112958     Document Type: Article

References (48)

1. Sparks AN (1979) A review of the biology of the fall armyworm. Fla Entomol 62: 82-87.
2. Pashley DP (1988) The current status of fall armyworm host strains. Fla Entomol 71: 227-234.
3. Buntin D, Flanders K (2012) Bt corn products for the southeastern United States. http://www.caes.uga.edu/commodities/fieldcrops/gagrains/documents/2012BtcornSEBtcorntraitstableNov21.pdf. Accessed 17 July 2014.
4. Frizzas MR, Neto SS, de Oliveira CM, Omoto C (2014) Genetically modified corn on fall armyworm and earwig populations under field conditions. Ciência Rural 44: 203-209.
5. NASS (National Agricultural Statistics Service) (2013). Acreage. USDA, Washington DC. USA. http://usda01.library.cornell.edu/usda/current/Acre/Acre-06-28-2013.pdf. Accessed 17 July 2014.
6. James C (2013) Global status of commercialized biotech/GM crops: 2013. ISAAA Brief No. 45. ISAAA: Ithaca, NY, USA.
7. Gould F (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Ann Rev Entomol 43: 701-726.
8. Matten SR, Frederick RJ, Reynolds AH (2012) United States Environmental Protection Agency insect resistance management programs for plant-incorporated protectants and use of simulation modeling. In: Wozniak CA, McHughen A, editors. Regulation of agricultural biotechnology: The United States and Canada. Springer. 175-267.
9. Tabashnik BE., Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 3: 510-521.
10. US-EPA (U.S. Environmental Protection Agency) (2001) Biopesticide registration action document: Bacillus thuringiensis plant-incorporated protectants. http://www.epa.gov/oppbppd1/biopesticides/pips/bt-brad2/1-overview.pdf. Accessed 17 July 2014.
11. Huang F, Andow DA, Buschman LL (2011) Success of the high dose/refuge resistance management strategy after 15 years of Bt crop use in North America. Entomol Exp App 140: 1-16.
12. Tabashnik BE, van Rensburg JBJ, Carriere Y (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol 102: 2011-2025.
13. Sumerford DV, Head GP, Shelton A, Greenplate J, Moar W (2013) Fieldevolved resistance: assessing the problem and ways to move forward. J Econ Entomol 106: 1525-1534.
14. Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, et al. (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103: 1031-1038.
15. Storer NP, Thompson GD, Head GP (2012) Application of pyramided traits against lepidoptera in insect resistance management for Bt crops. GM Crop 3: 154-162.
16. Vélez AM, Spencer TA, Alves AP, Moellenbeck D, Meagher RL, et al. (2013) Inheritance of Cry1F resistance, cross-resistance and frequency of resistant alleles in Spodoptera frugiperda (Lepidoptera: Noctuidae). Bull Entomol Res 103: 700-713.
17. Davis FM, Ng SS, Williams WP (1992) Visual rating scales for screening whorlstage corn for resistance to fall armyworm. Miss Agric Forestry Exp Stn Tech Bull 186.
18. Ritchie S W, Hanway JJ, Benson GO, Herman JC (1993) How a corn plant develops. Iowa State Uni Coop Ext Ser Sp Rep No. 48, Ames, Iowa, USA.
19. Capinera JL (1999) Fall armyworm. Uni. Fla. Publi. no. EENY-98. http://entnemdept.ufl.edu/creatures/field/fall-armyworm.htm. Accessed 17 July 2014.
20. Mitchell ER, McNeil JN, Westbrook JK, Silvant JF, Lalanne-Cassou B, et al. (1991) Seasonal periodicity of fall armyworm (Lepidoptera: Noctuidae) in the Caribbean basin and northward to Canada. J Entomol Sci 26: 39-51.
21. Nagoshi RN, Meagher RL, Jenkins DJ (2010) Puerto Rico fall armyworm has only limited interactions with those from Brazil or Texas but could have substantial exchanges with Florida populations. J Econ Entomol 103: 360-367.
22. DiFonzo C, Cullen E (2012) Handy Bt trait table. http://www3.ag.purdue.edu/agry/PCPP/Documents/Entry%20forms/Handy-Bt-Trait-Table.pdf. Accessed 17 July 2014.
23. Burkness EC, Dively G, Patton T, Morey AC, Hutchison WD (2010) Novel Vip3A Bacillus thuringiensis (Bt) maize approaches high-dose efficacy against Helicoverpa zea (Lepidoptera: Noctuidae) under field conditions. GM Crop 1: 1-7.
24. Yang F, Huang F, Qureshi JA, Leonard BR, Niu Y, et al. (2013) Susceptibility of Louisiana and Florida populations of Spodoptera frugiperda (Lepidoptera: Noctuidae) to transgenic Agrisure Viptera 3111 maize. Crop Protect 50: 37-39.
25. Niu Y, Yang F, Dangal V, Huang F (2014) Larval survival and plant injury of Cry1F-susceptible, -resistant, and -heterozygous fall armyworm (Lepidoptera: Noctuidae) on non-Bt and Bt corn containing single or pyramided genes. Crop Protect 59: 22-28.
26. Biosafety Cleaning-House. Gene and DNA sequence, Cry1A.105. https://bch.cbd.int/database/record.shtml?documentid=43771. Accessed 10 October 2014.
27. Storer NP, Kubiszak ME, King JE, Thompson GD, Santos AC (2012) Status of resistance to Bt maize in Spodoptera frugiperda: Lessons from Puerto Rico. J Invert Pathol 110: 294-300.
28. Sivasupramaniam S, Moar WJ, Ruschke LG, Osborn JA, Jiang C, et al. (2008) Toxicity and characterization of cotton expressing Bacillus thuringiensis Cry1Ac and Cry2Ab2 proteins for control of lepidopteran pests. J Econ Entomol 101: 546-554.
29. Brévault T, Prudent P, Vaissayre M, Carrière Y (2009) Susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to Cry1Ac and Cry2Ab2 insecticidal proteins in four countries of the West African cotton belt. J Econ Entomol 102: 2301-2309.
30. Wu X, Leonard BR, Zhu Y-C, Abel CA, Head GP, et al. (2009) Susceptibility of Cry1Ab-resistant and -susceptible sugarcane borer (Lepidoptera: Crambidae) to four Bacillus thuringiensis toxins. J Invert Pathol 100: 29-34.
31. Sumerford DV, Head GP (2014) Patterns of cross resistance among insecticidal Bacillus thuringiensis proteins and their implications for the durability of pyramided Bt crops. Crop Prot. In press.
32. Hernández-Rodríguez CS, Hernández-Martínez P. Van Rie J, Escriche B, Ferré J (2013) Shared midgut binding sites for Cry1A.105, Cry1Aa, Cry1Ab, Cry1Ac and Cry1Fa proteins from Bacillus thuringiensis in two important corn pests, Ostrinia nubilalis and Spodoptera frugiperda. PLoS ONE 8(7), e68164. doi:10.1371/journal.pone.0068164.
33. Sena JDA, Hernandez-Rodriguez CS, Ferré J (2009) Interaction of Bacillus thuringiensis Cry1 and Vip3A proteins with Spodoptera frugiperda midgut binding sites. App Environ Microbiol 75: 2236-2237.
34. US-EPA (U.S. Environmental Protection Agency) (2007) TC1507 maize and fall armyworm in Puerto Rico, MRID 47176001. USEPA, Washington, DC, USA.
35. Matten SR, Head GP, Quemada HD (2008) How governmental regulation can help or hinder the integration of Bt crops within IPM programs. In: Romeis J, Shelton AM, Kennedy GG editors. Integration of insect resistant genetically modified crops with IPM programs. Springer USA. 27-39.
36. Niu Y, Meagher Jr RL, Yang F, Huang F (2013) Susceptibility of field populations of the fall armyworm (Lepidopteran: Noctuidae) from Florida and Puerto Rico to purified Cry1F protein and corn leaf tissue containing single and pyramided Bt genes. Fla Entomol 96: 701-713.
37. Jakka SRK, Knight VR, Jurat-Fuentes JL (2014) Fitness costs associated with field-evolved resistance to Bt maize in Spodoptera frugiperda (Lepidoptera: Noctuidae). J Econ Entomol 107: 342-351.
38. SAS Institute Inc (2010) SAS/STAT: 9.3 User's Third Edition. Cary, NC, USA.
39. Andow DA, Alstad DN (1998) F2 screen for rare resistance alleles. J Econ Entomol 91: 572-578.
40. Yang F, Qureshi JA, Leonard BR, Head GP, Niu Y, et al. (2013) Susceptibility of Louisiana and Florida populations of Spodoptera frugiperda (Lepidoptera: Noctuidae) to pyramided Bt corn containing Genuity VT Double Pro and SmartStax traits. Fla Entomol 96: 714-723.
41. Zhang L, Huang F, Leonard BR, Chen M, Clark T, et al. (2013) Susceptibility of Cry1Ab maize.-resistant and -susceptible strains of sugarcane borer (Lepidoptera: Crambidae) to four individual Cry proteins. J Invertebr Pathol 112: 267-272.
42. Hardke JT, Leonard BR, Huang F, Jackson RE (2011) Damage and survivorship of fall armyworm (Lepidoptera: Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins. Crop Protect 30: 168-172.
43. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18: 265-267.
44. Finney DJ (1971) Probit analysis (Cambridge University Press, England).
45. Huang F, Ghimire MN, Leonard BR, Zhu Y-C, Head G (2012) Susceptibility of field populations of sugarcane borer from non-Bt and Bt maize plants to five individual Cry toxins. Ins Sci 19: 570-578.
46. Andow DA, Alstad DN (1999) Credibility interval for rare resistance allele frequencies. J Econ Entomol 92: 755-758.
47. Stodola TJ, Andow DA (2004) F2 screen variations and associated statistics. J Econ Entomol 97: 1756-1764.
48. Huang F Detection and monitoring of insect resistance to transgenic Bt crops (2006) Ins Sci 13: 73-84.