TY - JOUR
T1 - Epistasis confers resistance to Bt toxin Cry1Ac in the cotton bollworm
AU - Gao, Meijing
AU - Wang, Ximeng
AU - Yang, Yihua
AU - Tabashnik, Bruce E.
AU - Wu, Yidong
N1 - Funding Information:
National Natural Science Foundation of China, Grant/Award Number: 31530060; Ministry of Agriculture of China, Grant/Award Number: 2016ZX08012-004; Innovation Team Program for Jiangsu universities, Grant/Award Number: 2013-6; U.S. Department of Agriculture, Grant/Award Number: 2014-33522-22214
Funding Information:
We thank Yves Carrière for his thoughtful input, particularly the idea that the epistasis observed in this study effectively increases the dominance of resistance. This research was supported by grants from the National Natural Science Foundation of China (No. 31530060), the Ministry of Agriculture of China (No. 2016ZX08012-004), Innovation Team Program for Jiangsu universities (No. 2013-6), and by US Department of Agriculture (USDA) Biotechnology Risk Assessment Grant 2014-33522-22214.
Publisher Copyright:
© 2018 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd
PY - 2018/6
Y1 - 2018/6
N2 - Evolution of resistance by insect pests reduces the benefits of extensively cultivated transgenic crops that produce insecticidal proteins from Bacillus thuringiensis (Bt). Previous work showed that resistance to Bt toxin Cry1Ac, which is produced by transgenic cotton, can be conferred by mutations disrupting a cadherin protein that binds this Bt toxin in the larval midgut. However, the potential for epistatic interactions between the cadherin gene and other genes has received little attention. Here, we report evidence of epistasis conferring resistance to Cry1Ac in the cotton bollworm, Helicoverpa armigera, one of the world's most devastating crop pests. Resistance to Cry1Ac in strain LF256 originated from a field-captured male and was autosomal, recessive, and 220-fold relative to susceptible strain SCD. We conducted complementation tests for allelism by crossing LF256 with a strain in which resistance to Cry1Ac is conferred by a recessive allele at the cadherin locus HaCad. The resulting F1 offspring were resistant, suggesting that resistance to Cry1Ac in LF256 is also conferred by resistance alleles at this locus. However, the HaCad amino acid sequence in LF256 lacked insertions and deletions, and did not differ consistently between LF256 and a susceptible strain. In addition, most of the cadherin alleles in LF256 were not derived from the field-captured male. Moreover, Cry1Ac resistance was not genetically linked with the HaCad locus in LF256. Furthermore, LF256 and the susceptible strain were similar in levels of HaCad transcript, cadherin protein, and binding of Cry1Ac to cadherin. Overall, the results imply that epistasis between HaCad and an unknown second locus in LF256 yielded the observed resistance in the F1 progeny from the complementation test. The observed epistasis has important implications for interpreting results of the F1 screen used widely to monitor and analyze resistance, as well as the potential to accelerate evolution of resistance.
AB - Evolution of resistance by insect pests reduces the benefits of extensively cultivated transgenic crops that produce insecticidal proteins from Bacillus thuringiensis (Bt). Previous work showed that resistance to Bt toxin Cry1Ac, which is produced by transgenic cotton, can be conferred by mutations disrupting a cadherin protein that binds this Bt toxin in the larval midgut. However, the potential for epistatic interactions between the cadherin gene and other genes has received little attention. Here, we report evidence of epistasis conferring resistance to Cry1Ac in the cotton bollworm, Helicoverpa armigera, one of the world's most devastating crop pests. Resistance to Cry1Ac in strain LF256 originated from a field-captured male and was autosomal, recessive, and 220-fold relative to susceptible strain SCD. We conducted complementation tests for allelism by crossing LF256 with a strain in which resistance to Cry1Ac is conferred by a recessive allele at the cadherin locus HaCad. The resulting F1 offspring were resistant, suggesting that resistance to Cry1Ac in LF256 is also conferred by resistance alleles at this locus. However, the HaCad amino acid sequence in LF256 lacked insertions and deletions, and did not differ consistently between LF256 and a susceptible strain. In addition, most of the cadherin alleles in LF256 were not derived from the field-captured male. Moreover, Cry1Ac resistance was not genetically linked with the HaCad locus in LF256. Furthermore, LF256 and the susceptible strain were similar in levels of HaCad transcript, cadherin protein, and binding of Cry1Ac to cadherin. Overall, the results imply that epistasis between HaCad and an unknown second locus in LF256 yielded the observed resistance in the F1 progeny from the complementation test. The observed epistasis has important implications for interpreting results of the F1 screen used widely to monitor and analyze resistance, as well as the potential to accelerate evolution of resistance.
KW - Bacillus thuringiensis
KW - F screen
KW - allelism
KW - cotton bollworm
KW - genetically engineered crop
KW - resistance management
KW - second-site noncomplementation
KW - transgenic cotton
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U2 - 10.1111/eva.12598
DO - 10.1111/eva.12598
M3 - Article
AN - SCOPUS:85041741923
SN - 1752-4563
VL - 11
SP - 809
EP - 819
JO - Evolutionary Applications
JF - Evolutionary Applications
IS - 5
ER -