Negative cross-resistance between structurally different Bacillus thuringiensis toxins may favor resistance management of soybean looper in transgenic Bt cultivars

Abstract

High adoption rates of single-gene Bacillus thuringiensis (Bt) Cry1Ac soybean impose selection pressure for resistance in the soybean looper, Chrysodeixis includens, a major defoliator in soybean and cotton crops. To anticipate and characterize resistance profiles that can evolve, soybean looper larvae collected from field crops in Brazil in 2013 were selected for resistance to Cry1Ac. Using two methods of selection viz., chronic exposure to Cry1Ac cotton leaves and the seven-day larval exposure to purified Cry1Ac on the artificial diet, 31 and 127-fold resistance was obtained in 11 and 6 generations of selection, respectively. The resistance trait had realized heritability of 0.66 and 0.72, respectively, indicating that most of the phenotypic variation in Cry1Ac susceptibility of the soybean looper larvae was due to additive genetic variation. The Cry1Ac-selected populations showed positive cross-resistance to Cry1Ab (6.7-8.7 fold), likely because these Bt toxins have a very similar molecular structure. Importantly, the Cry1Ac-selected populations became more susceptible to Cry2Aa and Cry1Fa, showing negative cross-resistance (up to 6-fold, P < 0.05). These results indicate that Cry1Ac, Cry1Fa, and Cry2A are compatible in a multi-toxin approach to minimize the risk of rapid adaptation of the soybean looper to Bt toxins.

Figure 1

Response to selection for resistance to the Cry1Ac Bacillus thuringiensis (Bt) toxin in larvae of the soybean looper as affected by two methods of selection, namely chronic exposure to Cry1Ac cotton leaves and the seven-day larval exposure to purified Cry1Ac on the artificial diet. (a) Increase in the median lethal concentration (LC₅₀) for larvae of the individuals selected in the previous generation. (b) Larval survival rates (±SE) for the selected individuals (i.e., survivors on Bt Cry1Ac cotton or diet overlaid with Cry1Ac) as compared to those reared on plain food (i.e., non-Bt isoline cotton or artificial diet).

Figure 2

Testing whether soybean looper larvae from the Cry1Ac-selected (BG1-Sel and 1Ac-Sel) and unselected populations (Bt-Unsel) survive on foliage of Cry1Ac Bt soybean. Shown are mean (±SE) 3-day survival rates for neonates (n = 200) released on foliage excised from Cry1Ac-producing and near-isoline soybean plants. Columns with same letter are not significantly different (α = 0.05, Fisher’s LSD procedure after ANOVA).