title: Field-Evolved Resistance in Corn Earworm to Cry Proteins Expressed by Transgenic Sweet Corn.
abstract: BACKGROUND
  Transgenic corn engineered with genes expressing insecticidal toxins from the bacterium Bacillus thuringiensis (Berliner) (Bt) are now a major tool in insect pest management. With its widespread use, insect resistance is a major threat to the sustainability of the Bt transgenic technology. For all Bt corn expressing Cry toxins, the high dose requirement for resistance management is not achieved for corn earworm, Helicoverpa zea (Boddie), which is more tolerant to the Bt toxins.
  We present field monitoring data using Cry1Ab (1996-2016) and Cry1A.105+Cry2Ab2 (2010-2016) expressing sweet corn hybrids as in-field screens to measure changes in field efficacy and Cry toxin susceptibility to H. zea. Larvae successfully damaged an increasing proportion of ears, consumed more kernel area, and reached later developmental stages (4th - 6th instars) in both types of Bt hybrids (Cry1Ab-event Bt11, and Cry1A.105+Cry2Ab2-event MON89034) since their commercial introduction. Yearly patterns of H. zea population abundance were unrelated to reductions in control efficacy. There was no evidence of field efficacy or tissue toxicity differences among different Cry1Ab hybrids that could contribute to the decline in control efficacy. Supportive data from laboratory bioassays demonstrate significant differences in weight gain and fitness characteristics between the Maryland H. zea strain and a susceptible strain. In bioassays with Cry1Ab expressing green leaf tissue, Maryland H. zea strain gained more weight than the susceptible strain at all concentrations tested. Fitness of the Maryland H. zea strain was significantly lower than that of the susceptible strain as indicated by lower hatch rate, longer time to adult eclosion, lower pupal weight, and reduced survival to adulthood.
  
  
  CONCLUSIONS
  After ruling out possible contributing factors, the rapid change in field efficacy in recent years and decreased susceptibility of H. zea to Bt sweet corn provide strong evidence of field-evolved resistance in H. zea populations to multiple Cry toxins. The high adoption rate of Bt field corn and cotton, along with the moderate dose expression of Cry1Ab and related Cry toxins in these crops, and decreasing refuge compliance probably contributed to the evolution of resistance. Our results have important implications for resistance monitoring, refuge requirements and other regulatory policies, cross-resistance issues, and the sustainability of the pyramided Bt technology.
authors.affiliation: Department of Entomology, University of Maryland, College Park, Maryland, United States of America.
authors.forename: Galen P
authors.initials: GP
authors.lastname: Dively
authors.affiliation: Department of Entomology, University of Maryland, College Park, Maryland, United States of America.|American Association for the Advancement of Science - Science and Technology Policy Fellowship Program, Transportation and Climate Division, Office of Transportation & Air Quality, United States Environmental Protection Agency, District of Columbia, United States of America.
authors.forename: P Dilip
authors.identifier: http://orcid.org/0000-0001-6339-5087
authors.initials: PD
authors.lastname: Venugopal
authors.affiliation: Benzon Research Inc., Carlisle, Pennsylvania, United States of America.
authors.forename: Chad
authors.initials: C
authors.lastname: Finkenbinder
mesh_terms: D000818:Animals; D001413:Bacillus thuringiensis / Q000235:genetics*; D000083722:Bacillus thuringiensis Toxins; D001426:Bacterial Proteins / Q000235:genetics* / Q000378:metabolism*; D001427:Bacterial Toxins / Q000235:genetics / Q000378:metabolism; D004731:Endotoxins / Q000235:genetics* / Q000378:metabolism*; D006460:Hemolysin Proteins / Q000235:genetics* / Q000378:metabolism*; D007306:Insecticides / Q000378:metabolism; D007814:Larva / Q000378:metabolism; D009036:Moths / Q000187:drug effects*; D010572:Pest Control, Biological / Q000379:methods*; D018515:Plant Leaves / Q000378:metabolism; D030821:Plants, Genetically Modified / Q000235:genetics*; D003313:Zea mays / Q000235:genetics* / Q000378:metabolism
chemical_list: D000083722:Bacillus thuringiensis Toxins; D001426:Bacterial Proteins; D001427:Bacterial Toxins; D004731:Endotoxins; D006460:Hemolysin Proteins; D007306:Insecticides; C030956:insecticidal crystal protein, Bacillus Thuringiensis