Large genomic deletion linked to field-evolved resistance to Cry1F corn in fall armyworm (Spodoptera frugiperda) from Florida

Banerjee, Rahul; Bortoli, Caroline Placidi De; Huang, Fangneng; Lamour, Kurt; Meagher, Robert L.; Buntin, David; Ni, Xinzi; Reay‐Jones, Francis P. F.; Stewart, Scott; Jurat-Fuentes, Juan Luís

doi:10.1038/s41598-022-17603-3

Cited by 18 publications

(15 citation statements)

References 39 publications

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“…We set the frequency of the allele conferring susceptibility at one of the resistance loci to 1, which converted the two-toxin model into a model with one locus at which two alleles confer either resistance ( r ) or susceptibility ( s ) to the Bt crop. This is the simplest assumption about the genetic basis of resistance and a reasonable starting point because resistance to a single toxin produced by the Bt crop is often controlled primarily by alleles at one locus [ 48 , 49 , 50 , 51 ]. The dominance of resistance was measured with the parameter h , for which 0 indicates recessive and 1 indicates dominant inheritance [ 52 ].…”

Section: Methodsmentioning

confidence: 99%

Fitness Costs and Incomplete Resistance Associated with Delayed Evolution of Practical Resistance to Bt Crops

Carrière

Tabashnik

2023

Insects

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Insect pests are increasingly evolving practical resistance to insecticidal transgenic crops that produce Bacillus thuringiensis (Bt) proteins. Here, we analyzed data from the literature to evaluate the association between practical resistance to Bt crops and two pest traits: fitness costs and incomplete resistance. Fitness costs are negative effects of resistance alleles on fitness in the absence of Bt toxins. Incomplete resistance entails a lower fitness of resistant individuals on a Bt crop relative to a comparable non-Bt crop. In 66 studies evaluating strains of nine pest species from six countries, costs in resistant strains were lower in cases with practical resistance (14%) than without practical resistance (30%). Costs in F1 progeny from crosses between resistant and susceptible strains did not differ between cases with and without practical resistance. In 24 studies examining seven pest species from four countries, survival on the Bt crop relative to its non-Bt crop counterpart was higher in cases with practical resistance (0.76) than without practical resistance (0.43). Together with previous findings showing that the nonrecessive inheritance of resistance is associated with practical resistance, these results identify a syndrome associated with practical resistance to Bt crops. Further research on this resistance syndrome could help sustain the efficacy of Bt crops.

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Section: Methodsmentioning

confidence: 99%

Fitness Costs and Incomplete Resistance Associated with Delayed Evolution of Practical Resistance to Bt Crops

Carrière

Tabashnik

2023

Insects

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“…As far as we know, analogous comparisons of the molecular genetic basis of Bt resistance between lab-selected and practical resistance for the same pest are not yet possible for other species. Aside from pink bollworm, the only cases of practical resistance to a Bt crop where the molecular genetic basis of resistance is known to involve Spodoptera frugiperda resistance to Cry1Fa in Puerto Rico, the continental United States, and Brazil associated with mutations in an ABC transporter gene ( SfABCC2 ) [ 18 ]. We are not aware of reports of the genetic basis of lab-selected resistance of this pest to Cry1Fa.…”

Section: Discussionmentioning

confidence: 99%

“…Understanding the genetic basis of resistance can be useful for monitoring, managing, and countering pest resistance to Bt crops [ 15 , 16 , 17 , 18 ]. To facilitate development of effective resistance management strategies, scientists have determined the genetic basis of resistance to Bt toxins in many lab-selected strains, including strains derived from susceptible populations by either mass selection or selection of families generated for F 1 or F 2 screens [ 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 ].…”

Section: Introductionmentioning

confidence: 99%

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

Fabrick

Carrière

et al. 2023

Insects

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Transgenic crops producing insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) control some important insect pests. However, evolution of resistance by pests reduces the efficacy of Bt crops. Here we review resistance to Bt cotton in the pink bollworm, Pectinophora gossypiella, one of the world’s most damaging pests of cotton. Field outcomes with Bt cotton and pink bollworm during the past quarter century differ markedly among the world’s top three cotton-producing countries: practical resistance in India, sustained susceptibility in China, and eradication of this invasive lepidopteran pest from the United States achieved with Bt cotton and other tactics. We compared the molecular genetic basis of pink bollworm resistance between lab-selected strains from the U.S. and China and field-selected populations from India for two Bt proteins (Cry1Ac and Cry2Ab) produced in widely adopted Bt cotton. Both lab- and field-selected resistance are associated with mutations affecting the cadherin protein PgCad1 for Cry1Ac and the ATP-binding cassette transporter protein PgABCA2 for Cry2Ab. The results imply lab selection is useful for identifying genes important in field-evolved resistance to Bt crops, but not necessarily the specific mutations in those genes. The results also suggest that differences in management practices, rather than genetic constraints, caused the strikingly different outcomes among countries.

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“…As an alternative, DNA-based resistance monitoring could provide higher sensitivity while reducing labor and costs, although this depends on identification of resistance genes to screen for resistance alleles. Fortunately, all characterized cases of practical resistance to the Cry1F PIP in S. frugiperda have been linked to a single genetic locus: an ABC transporter superfamily C2 gene ( SfABCC2 ) (Banerjee et al 2017, 2022, Flagel et al 2018, Boaventura et al 2020). This locus encodes the SfABCC2 protein, a functional receptor for Cry1F, Cry1Ab, and Cry1A.105 PIPs (Banerjee et al 2017, Flagel et al 2018, Liu et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…Consequently, diverse levels of cross-resistance to Cry1.105 and Cry1Ab PIPs are observed in S. frugiperda strains where resistance to Cry1F is linked to disruptive SfABCC2 mutations (Vélez et al 2013; Bernardi et al 2015, Huang et al 2014, Jakka et al 2014a, 2014b, 2016, Flagel et al 2018). Recessive resistance alleles in SfABCC2 have been identified, including a 2-bp frameshift insertion ( SfABCC2mut allele) in Puerto Rico (Banerjee et al 2017), recessive missense mutations in extracellular loops of SfABCC2 vital to Cry1F susceptibility (Liu et al 2021, Franz et al 2022) in Brazil (Boaventura et al 2020), and a large genomic deletion affecting the SfABCC2 locus in Florida (Banerjee et al 2022). At a minimum, this information allows for targeted DNA-based screening for SfABCC2 resistance alleles in S. frugiperda populations.…”

Section: Introductionmentioning

confidence: 99%

Screening for resistance alleles to Cry1 proteins through targeted sequencing in the native and invasive range of Spodoptera frugiperda (Lepidoptera: Noctuidae)

Tandy

Lamour

Bortoli

et al. 2023

Journal of Economic Entomology

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The fall armyworm, Spodoptera frugiperda (J. E. Smith), is a highly polyphagous pest native to the tropical Americas that has recently spread to become a global super-pest threatening food and fiber production. Transgenic crops producing insecticidal Cry and Vip3Aa proteins from Bacillus thuringiensis (Bt) are used for control of this pest in its native range. The evolution of practical resistance represents the greatest threat to sustainability of this technology and its potential efficacy in the S. frugiperda invasive range. Monitoring for resistance is vital to management approaches delaying S. frugiperda resistance to Bt crops. DNA-based resistance screening provides higher sensitivity and cost-effectiveness than currently used bioassay-based monitoring. So far, practical S. frugiperda resistance to Bt corn-producing Cry1F has been genetically linked to mutations in the SfABCC2 gene, providing a model to develop and test monitoring tools. In this study, we performed targeted SfABCC2 sequencing followed by Sanger sequencing to confirm the detection of known and candidate resistance alleles to Cry1F corn in field-collected S. frugiperda from continental USA, Puerto Rico, Africa (Ghana, Togo, and South Africa), and Southeast Asia (Myanmar). Results confirm that the distribution of a previously characterized resistance allele (SfABCC2mut) is limited to Puerto Rico and identify 2 new candidate SfABCC2 alleles for resistance to Cry1F, one of them potentially spreading along the S. frugiperda migratory route in North America. No candidate resistance alleles were found in samples from the invasive S. frugiperda range. These results provide support for the potential use of targeted sequencing in Bt resistance monitoring programs.

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Large genomic deletion linked to field-evolved resistance to Cry1F corn in fall armyworm (Spodoptera frugiperda) from Florida

Cited by 18 publications

References 39 publications

Fitness Costs and Incomplete Resistance Associated with Delayed Evolution of Practical Resistance to Bt Crops

Fitness Costs and Incomplete Resistance Associated with Delayed Evolution of Practical Resistance to Bt Crops

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

Screening for resistance alleles to Cry1 proteins through targeted sequencing in the native and invasive range of Spodoptera frugiperda (Lepidoptera: Noctuidae)

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