Mutation in the Cadherin Gene Is a Key Factor for Pink Bollworm Resistance to Bt Cotton in China

Abstract

Transgenic crops producing Bacillus thuringiensis (Bt) toxins are widely planted for insect control, but their efficacy may decrease as insects evolve resistance. Understanding the genetic basis of insect resistance is essential for developing an integrated strategy of resistance management. To understand the genetic basis of resistance in pink bollworm (Pectinophora gossypiella) to Bt cotton in the Yangtze River Valley of China, we conducted an F2 screening for alleles associated with resistance to the Bt (Cry1Ac) protein for the first time. A total of 145 valid single-paired lines were screened, among which seven lines were found to carry resistance alleles. All field parents in those seven lines carried recessive resistance alleles at the cadherin locus, including three known alleles, r1, r13 and r15, and two novel alleles, r19 and r20. The overall frequency of resistance alleles in 145 lines was 0.0241 (95% CI: 0.0106–0.0512). These results demonstrated that resistance was rare and that recessive mutation in the cadherin gene was the primary mechanism of pink bollworm resistance to Bt cotton in the Yangtze River Valley of China, which will provide a scientific basis for implementing targeted resistance management statics of pink bollworm in this region.

Molecular Genetic Basis of Lab- and Field-Selected Bt Resistance in Pink Bollworm

“…Results of modeling show that together with fitness costs associated with resistance and incomplete resistance, the increased planting of F 2 hybrids is sufficient to account for the restoration of susceptibility to Cry1Ac that was seen in bioassays conducted from 2011 to 2015 [ 44 ]. Additional monitoring discussed in more detail below ( Section 4.2.1 ) shows susceptibility to Cry1Ac was maintained at least through 2017 [ 61 , 62 ]. The voluntary planting of F 2 hybrids apparently has immediate benefits in terms of lower seed costs and higher yields, as well as serendipitous benefits for managing resistance [ 44 ].…”

“…Resistance to Cry1Ac and Cry1Ac-producing Bt cotton is associated with mutations in the pink bollworm cadherin gene PgCad1 in lab-selected strains from China and the U.S. as well as field-selected populations from India [ 51 , 62 , 84 , 96 , 98 , 99 , 100 , 101 , 104 , 108 , 109 , 119 , 120 , 121 ]. The wild-type PgCad1 protein has 1735 amino acids [ 96 ] that form four domains: a cytoplasmic domain, a transmembrane domain, and two extracellular domains ( Figure 3 ).…”

“…Cry1Ac protoxin and activated toxin bind to recombinant peptides corresponding to wild-type CR9-CR10, CR11, CR12, and MPR but not to CR7 or CR8, which are farther from the MPR [ 84 ]. Although 20 mutant PgCad1 alleles associated with resistance to Cry1Ac ( r1 – r20 ) have been reported, our analyses here do not include r18 from China [ 62 ] because its sequence has not been published yet.…”

“…None of the 11 published PgCad1 resistance alleles identified from lab-selected strains from the U.S. ( r1 – r4 and r17 ) or China ( r13 – r16 and r19 – r20 ) were found in field-selected populations from India, which are the source of eight other resistance alleles ( r5 – r12 ) ( Figure 3 , Table S1 ). Alleles r1 and r2 were first identified in a lab-selected strain from the U.S. [ 96 ] then later found in China [ 61 , 62 ]. Each of the other 17 resistance alleles have been found in only one of the three countries.…”

Chromosome-scale genome assembly of the pink bollworm,Pectinophora gossypiella, a global pest of cotton

“…To date, pink bollworm resistance to the Bt toxins Cry1Ac and Cry2Ab has been associated with the midgut cadherin PgCad1 and the ATP-binding cassette PgABCA2 genes, respectively. For Cry1Ac, a total of 20 mutations in PgCad1 have been identified in resistant pink bollworm from China, India, and the U.S. (Fabrick et al, 2014; Fabrick & Tabashnik, 2012; Morin et al, 2003; Wang et al, 2019a; Wang et al, 2018; Wang et al, 2022). Resistance to Cry1Ac in a laboratory strain of pink bollworm from Arizona was also found to involve reduced transcription of the PgCad1 gene leading to markedly lower abundance of the PgCad1 Cry1Ac receptor protein (Fabrick et al, 2020b).…”