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Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved October 5, 2018 (received for review July 15, 2018)
Significance
Crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) kill some major pests and reduce use of insecticide sprays. However, evolution of pest resistance to Bt proteins decreases these benefits. Better understanding of the genetic basis of resistance to Bt crops is urgently needed to address this problem. We discovered that a point mutation in the cotton bollworm, one of the world’s most voracious pests, confers dominantly inherited resistance to the Bt protein produced by transgenic cotton grown in China. This mutation increased 100-fold in frequency from 2006 to 2016 in China. Proactive tracking of this mutation may improve management of resistance and enhance sustainability of Bt cotton for millions of smallholder farmers in China.
Abstract
Extensive planting of crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) has suppressed some major pests, reduced insecticide sprays, enhanced pest control by natural enemies, and increased grower profits. However, rapid evolution of resistance in pests is reducing these benefits. Better understanding of the genetic basis of resistance to Bt crops is urgently needed to monitor, delay, and counter pest resistance. We discovered that a point mutation in a previously unknown tetraspanin gene in the cotton bollworm (Helicoverpa armigera), a devastating global pest, confers dominant resistance to Cry1Ac, the sole Bt protein produced by transgenic cotton planted in China. We found the mutation using a genome-wide association study, followed by fine-scale genetic mapping and DNA sequence comparisons between resistant and susceptible strains. CRISPR/Cas9 knockout of the tetraspanin gene restored susceptibility to a resistant strain, whereas inserting the mutation conferred 125-fold resistance in a susceptible strain. DNA screening of moths captured from 23 field sites in six provinces of northern China revealed a 100-fold increase in the frequency of this mutation, from 0.001 in 2006 to 0.10 in 2016. The correspondence between the observed trajectory of the mutation and the trajectory predicted from simulation modeling shows that the dominance of the mutation accelerated adaptation. Proactive identification and tracking of the tetraspanin mutation demonstrate the potential for genomic analysis, gene editing, and molecular monitoring to improve management of resistance.
Footnotes
↵1L.J. and J.W. contributed equally to this work.
- ↵2To whom correspondence should be addressed. Email: wyd{at}njau.edu.cn.
Author contributions: Y.Y. and Y.W. designed research; L.J., J.W., F.G., J.Z., S.Y., S.L., Y.X., L.L., H.A., and J.L.J.-F. performed research; S.W., X.W., and Y.Y. contributed new reagents/analytic tools; L.J., J.W., F.G., J.Z., B.E.T., and Y.W. analyzed data; B.E.T. conducted modeling; and L.J., J.W., B.E.T., and Y.W. wrote the paper.
Conflict of interest statement: B.E.T. is coauthor of a patent on modified Bacillus thuringiensis toxins, “Suppression of Resistance in Insects to Bacillus thuringiensis Cry Toxins, Using Toxins That Do Not Require the Cadherin Receptor” (patent nos. CA2690188A1, CN101730712A, EP2184293A2, EP2184293A4, EP2184293B1, WO2008150150A2, and WO2008150150A3). Amvac, Bayer CropScience, Dow AgroSciences, DuPont Pioneer, Monsanto, and Syngenta did not provide funding to support this work, but may be affected financially by publication of this paper and have funded other work by B.E.T.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1812138115/-/DCSupplemental.
Published under the PNAS license.
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Dominant point mutation in a tetraspanin gene associated with field-evolved resistance of cotton bollworm to transgenic Bt cotton
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