Abstract
Evolution of pest resistance reduces the efficacy of insecticidal proteins from the gram-positive bacterium Bacillus thuringiensis (Bt) used widely in sprays and transgenic crops. Better understanding of the genetic basis of resistance is needed to more effectively monitor, manage, and counter pest resistance to Bt toxins. Here we used CRISPR/Cas9 gene editing to clarify the genetics of Bt resistance and the associated effects on susceptibility to other microbial insecticides in one of the world’s most damaging pests, the cotton bollworm (Helicoverpa armigera). We discovered that CRISPR-mediated knockouts of ATP-binding cassette (ABC) transporter genes HaABCC2 and HaABCC3 together caused >15,000-fold resistance to Bt toxin Cry1Ac, whereas knocking out either HaABCC2 or HaABCC3 alone had little or no effect. Inheritance of resistance was autosomal and recessive. Bioassays of progeny from interstrain crosses revealed that one wild type allele of either HaABCC2 or HaABCC3 is sufficient to sustain substantial susceptibility to Cry1Ac. In contrast with previous results, susceptibility to two insecticides derived from bacteria other than Bt (abamectin and spinetoram), was not affected by knocking out HaABCC2, HaABCC3, or both. The results here provide the first evidence that either HaABCC2 or HaABCC3 protein is sufficient to confer substantial susceptibility to Cry1Ac. The functional redundancy of these two proteins in toxicity of Cry1Ac to H. armigera is expected to reduce the likelihood of field-evolved resistance relative to disruption of a toxic process where mutations affecting a single protein can confer resistance.
Highlights
Insecticidal proteins from the gram-positive soil bacterium Bacillus thuringiensis (Bt) are used extensively in sprays and transgenic plants to control insects that devour crops and vector diseases [1,2]
We used CRISPR gene editing to clarify the genetics of resistance to Bt toxins in the cotton
Bt toxicity to cotton bollworm mediated by two ATP-binding cassette (ABC) transporters from the USDA National Institute of Food and Agriculture
Summary
Insecticidal proteins from the gram-positive soil bacterium Bacillus thuringiensis (Bt) are used extensively in sprays and transgenic plants to control insects that devour crops and vector diseases [1,2]. These Bt proteins are especially valuable because they kill some devastating pests, but are not toxic to humans and most other non-target organisms [1,3,4]. Practical resistance to Bt crops has increased from three cases in 2005 to at least 22 cases affecting nine major pest species [12,13,16]. Better understanding of the genetic basis of resistance is urgently needed to more effectively monitor, manage, and counter pest resistance to Bt toxins
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