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

Nilson Rodrigues-Silva,Eliseu J G Pereira,Marcelo C Picanço,André F Teixeira,Oscar F Santos-Amaya,Afonso F Canuto,Diogo F Oliveira

doi:10.1038/s41598-018-35965-5

Nilson Rodrigues-Silva, Eliseu J G Pereira + Show 5 more

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https://doi.org/10.1038/s41598-018-35965-5

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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.

Highlights

Plant biotechnology has helped in the development of pest-resistant cultivars, which are increasingly important in the face of growing pressure to reduce broadcast pesticides typically used in crop protection[1]
The risk of Bacillus thuringiensis (Bt) resistance in the soybean looper is further increased because the larvae typically have sheltered feeding habits within the plant canopy, which is challenging for effective insecticidal sprays that may be needed for integrated pest/resistance management
Estimates of median lethal concentration (LC50) values and survival rates over the generations of selection (Fig. 1) show that soybean looper larvae increased the resistance to Cry1Ac when exposed to the Bt cotton leaf tissues throughout larval development, or to the toxin on the surface of the artificial diet for seven days of exposure

Summary

Introduction

Plant biotechnology has helped in the development of pest-resistant cultivars, which are increasingly important in the face of growing pressure to reduce broadcast pesticides typically used in crop protection[1]. Bt soybean grown predominantly over 60% of 39.1 million ha and Bt cotton occupying 70% of 1.2 million ha[2], both producing the same Cry1Ac toxin, exert tremendous selection pressure on common pests to evolve resistance. This is the case for the soybean looper, which is relatively less susceptible to Cry[1] toxins and biopesticides[10,22,23]. In order to manage pest adaptation (often referred to as insect resistance management) to Bt crops, the primary strategy has been to ensure that effective refuges of non-Bt host plants occur near Bt crops. Appropriate would be if individuals that have alleles conferring resistance to a single-toxin Bt crop are hypersusceptible to another toxin, in which case there would be negative cross-resistance between the two toxins[29]

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