Performance of Genetically Modified Soybean Expressing the Cry1A.105, Cry2Ab2, and Cry1Ac Proteins Against Key Lepidopteran Pests in Brazil.

The pyramided genetically modified (GM) soybean [Glycine max L. (Merr.)] MON87751 × MON87708 × MON87701 × MON89788, expressing Cry1A.105, Cry2Ab2, and Cry1Ac from Bacillus thuringiensis Berliner, was approved for commercial use in Brazil. We conducted laboratory, greenhouse, and field studies to assess the efficacy of this Bt soybean against key soybean lepidopteran pests. Neonates of Anticarsia gemmatalis (Hübner) (Lepidoptera: Erebidae), Chrysodeixis includens (Walker), and Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) were exposed to Bt proteins in diet-overlay bioassays. MON87751 × MON87708 × MON87701 × MON89788 soybean and individual components were evaluated in laboratory (leaf disc), greenhouse (high artificial infestations), and in field conditions (natural infestations). Neonates of A. gemmatalis, C. includens, and H. armigera were highly susceptible to Cry1A.105 (LC50 from 0.79 to 48.22 ng/cm2), Cry2Ab2 (LC50 from 1.24 to 8.36 ng/cm2), and Cry1Ac (LC50 from 0.15 to 5.07 ng/cm2) in diet-overlay bioassays. In laboratory leaf disc bioassays and greenhouse trials, MON87751 × MON87708 × MON87701 × MON89788 soybean as well as the individual components were highly effective in controlling A. gemmatalis, C. includens, and H. armigera. Similarly, under field conditions, the pyramided genotypes expressing Cry1A.105, Cry2Ab2, and Cry1Ac were highly effective at protecting soybean against C. includens. We concluded that the individual Bt proteins expressed by GM soybean MON87751 × MON87708 × MON87701 × MON89788 killed all or nearly all the susceptible A. gemmatalis, C. includens, and H. armigera, fulfilling one important criterion for successfully delaying resistance to pyramided Bt crops.

High Susceptibility to Cry1Ac and Low Resistance Allele Frequency Reduce the Risk of Resistance of Helicoverpa armigers to Bt Soybean in Brazil.

The Old World bollworm, Helicoverpa armigera (Hübner), was recently introduced into Brazil, where it has caused extensive damage to cotton and soybean crops. MON 87701 × MON 89788 soybean, which expresses the Bt protein Cry1Ac, was recently deployed in Brazil, providing high levels of control against H. armigera. To assess the risk of resistance to the Cry1Ac protein expressed by MON 87701 × MON 89788 soybean in Brazil, we conducted studies to evaluate the baseline susceptibility of H. armigera to Cry1Ac, in planta efficacy including the assessment of the high-dose criterion, and the initial resistance allele frequency based on an F2 screen. The mean Cry1Ac lethal concentration (LC50) ranged from 0.11 to 1.82 µg·mL-1 of diet among all H. armigera field populations collected from crop seasons 2013/14 to 2014/15, which indicated about 16.5-fold variation. MON 87701 × MON 89788 soybean exhibited a high level of efficacy against H. armigera and most likely met the high dose criterion against this target species in leaf tissue dilution bioassays up to 50 times. A total of 212 F2 family lines of H. armigera were established from field collections sampled from seven locations across Brazil and were screened for the presence of MON 87701 × MON 89788 soybean resistance alleles. None of the 212 families survived on MON 87701 × MON 89788 soybean leaf tissue (estimated allele frequency = 0.0011). The responses of H. armigera to Cry1Ac protein, high susceptibility to MON 87701 × MON 89788 soybean, and low frequency of resistance alleles across the main soybean-producing regions support the assumptions of a high-dose/refuge strategy. However, maintenance of reasonable compliance with the refuge recommendation will be essential to delay the evolution of resistance in H. armigera to MON 87701 × MON 89788 soybean in Brazil.