Field-Evolved Resistance in Corn Earworm to Cry Proteins Expressed by Transgenic Sweet Corn

• Published in: PloS one Vol. 11; no. 12; p. e0169115
• Main Authors: Dively, Galen P, Venugopal, P Dilip, Finkenbinder, Chad
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 30.12.2016; Public Library of Science (PLoS)
• Subjects: Animals; Bacillus thuringiensis; Bacillus thuringiensis - genetics; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Bacterial Toxins - genetics; Bacterial Toxins - metabolism; Binding sites; Bioassays; Biology and Life Sciences; Corn; Corn earworm; Cotton; Cross-resistance; Developmental stages; Dosage; Eclosion; Effectiveness; Endotoxins - genetics; Endotoxins - metabolism; Environmental protection; Evolution; Fitness; Gene expression; Genes; Genetically modified crops; Helicoverpa zea; Hemolysin Proteins - genetics; Hemolysin Proteins - metabolism; Hybrids; Insecticide resistance; Insecticides; Insecticides - metabolism; Insects; Instars; Laboratories; Larva - metabolism; Larvae; Lepidoptera; Medicine and Health Sciences; Monitoring; Moths - drug effects; Noctuidae; Ostrinia nubilalis; People and places; Pest control; Pest Control, Biological - methods; Plant Leaves - metabolism; Plant tissues; Plants, Genetically Modified - genetics; Proteins; Reproductive fitness; Research and Analysis Methods; Screens; Spodoptera frugiperda; Sustainability; Technology; Toxicity; Toxins; Transgenic; Weight reduction; Zea mays - genetics; Zea mays - metabolism; Brazil; Washington DC; United States > US; Maryland
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0169115

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. 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.