An Extended Investigation of Unexpected Helicoverpa zea (Boddie) Survival and Ear Injury on a Transgenic Maize Hybrid Expressing Cry1A/Cry2A/Vip3A Toxins

Huang, Fangneng; Niu, Ying; Silva, Tiago Nunes; Brown, Sebe; Towles, Tyler; Kerns, Dawson; Jurat-Fuentes, Juan Luís; Head, Graham P.; Carroll, Matthew; Walker, Wade; Lin, Shucong

doi:10.3390/toxins15070474

Cited by 5 publications

(2 citation statements)

References 28 publications

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“…More studies may be needed to understand the genetic changes in FAW susceptibility to Vip3Aa/Cry insecticidal proteins and help inform decision making for resistance management [32,43,45]. FAW population pressure on host crops is likely influenced by the genetic background of field populations and their environmental factors, including climatic variables, native or transgenic plant resistance traits, and pest and crop management practices [3,20,46,47].…”

Section: Discussionmentioning

confidence: 99%

Susceptibility of Fall Armyworm Field Populations to Vip3Aa/Cry Bt Maize in a Tropical Agricultural Region

Silva,

Malaquias

et al. 2024

Agronomy

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Fall armyworm (FAW, Spodoptera frugiperda) is a polyphagous and migratory lepidopteran pest insect in field crops and is notoriously invasive worldwide. In large portions of the Americas, its populations are managed using transgenic maize or cotton varieties producing insecticidal proteins from Bacillus thuringiensis (Bt), primarily Vip3Aa pyramided with Cry Bt proteins. We determined the susceptibility of FAW field populations from locations pressured with such maize hybrids for over five years. We used time–mortality bioassays with F1 third-instar larvae of six geographically distinct populations collected in maize fields of a tropical agricultural region encompassing four Brazilian states. We maintained the neonate progeny from the field populations on an artificial diet until the third instar, and then determined their survival curves on the foliage of three Vip3Aa/Cry-producing Bt maize hybrids. Death of the mid-size, third-instar FAWs occurred relatively rapidly, with larval mortality rates reaching 98–100% in less than five days regardless of Bt maize hybrid. However, median survival time (ST50) for the larvae differed among the populations, with the lowest and highest ST50 values occurring for PI-Cr (42 h, 1.75 d) and PI-Ur populations (66–90 h, 2.75–3.75 h), respectively. Therefore, the F1 third-instar larvae of FAW populations were largely susceptible to Vip3Aa/Cry-producing maize foliage, and the most contrasting susceptibility occurred in the insects from Piauí state, Brazil. These results indicate that progeny of FAWs from areas highly pressured with Vip3Aa/Cry Bt maize hybrids are killed on maize foliage producing Vip3Aa and Cry Bt proteins despite field reports of increased leaf damage by the larvae in some locations. This research informs decision making for Bt-crop resistance management by producers, technicians, and researchers in local, regional, and world agriculture.

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Section: Discussionmentioning

confidence: 99%

Susceptibility of Fall Armyworm Field Populations to Vip3Aa/Cry Bt Maize in a Tropical Agricultural Region

Silva,

Malaquias

et al. 2024

Agronomy

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“…By 2016, resistance to Cry1 toxins had become common throughout the US and Cry2 resistance was emerging (Dively et al 2016; Reisig et al 2018). Recent studies concluded that resistance to Cry2Ab2 has become common, and that selection was ongoing as of 2019 (Yu et al 2021; Huang et al 2023). The genetic basis of Bt resistance is known to be complex and likely arose from standing variation, with unique genetic architectures underlying resistance to different Cry toxins (Taylor et al 2021; Benowitz et al 2022).…”

Section: Introductionmentioning

confidence: 99%

Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

North,

Fu,

Metz

et al. 2023

Preprint

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Insect crop pests threaten global food security. This threat is amplified through the spread of non-native species and the evolution of pesticide resistance, which can be introduced to a population thoughde novomutation or gene flow. We investigate these processes in an economically important noctuid crop pest,Helicoverpa zea, which has rapidly evolved resistance to several pesticides. Its sister speciesHelicoverpa armigera, first detected as an invasive species in Brazil in 2013, introduced the pyrethroid resistance geneCYP337B3to South AmericanH. zeavia introgression. To understand whether this contributes to pesticide resistance in North America, we sequenced 237H. zeagenomes across 10 sample sites in the US. First, we reportH. armigeraintrogression into the North AmericanH. zeapopulation. Two individuals sampled in Texas in 2019 carryH. armigerahaplotypes in a 4Mbp region containingCYP337B3. Second, we show that the remarkable dispersal ability ofH. zearesults in a panmictic North American population. Third, we detect signatures of selection in non-admixedH. zea, identifying a selective sweep at a second pesticide resistance locus with a similar name:CYP333B3. We estimate that its derived allele conferred a ∼4.9% fitness advantage and show that this estimate explains independently observed rare nonsynonymousCYP333B3mutations approaching fixation over a ∼20-year period. We also detect putative signatures of selection at a kinesin gene associated with Bt resistance. Our results show that pesticide resistance inH. zeaevolved rapidly and recently via two independent mechanisms: interspecific introgression and rapid intraspecific adaptation.

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Cross-pollination in seed-blended refuge and selection for Vip3A resistance in a lepidopteran pest as detected by genomic monitoring

Pezzini,

Taylor,

Reisig

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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The evolution of pest resistance to management tools reduces productivity and results in economic losses in agricultural systems. To slow its emergence and spread, monitoring and prevention practices are implemented in resistance management programs. Recent work suggests that genomic approaches can identify signs of emerging resistance to aid in resistance management. Here, we empirically examined the sensitivity of genomic monitoring for resistance management in transgenic Bt crops, a globally important agricultural innovation. Whole genome resequencing of wild North American Helicoverpa zea collected from non-expressing refuge and plants expressing Cry1Ab confirmed that resistance-associated signatures of selection were detectable after a single generation of exposure. Upon demonstrating its sensitivity, we applied genomic monitoring to wild H. zea that survived Vip3A exposure resulting from cross-pollination of refuge plants in seed-blended plots. Refuge seed interplanted with transgenic seed exposed H. zea to sublethal doses of Vip3A protein in corn ears and was associated with allele frequency divergence across the genome. Some of the greatest allele frequency divergence occurred in genomic regions adjacent to a previously described candidate gene for Vip3A resistance. Our work highlights the power of genomic monitoring to sensitively detect heritable changes associated with field exposure to Bt toxins and suggests that seed-blended refuge will likely hasten the evolution of resistance to Vip3A in lepidopteran pests.

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An Extended Investigation of Unexpected Helicoverpa zea (Boddie) Survival and Ear Injury on a Transgenic Maize Hybrid Expressing Cry1A/Cry2A/Vip3A Toxins

Cited by 5 publications

References 28 publications

Susceptibility of Fall Armyworm Field Populations to Vip3Aa/Cry Bt Maize in a Tropical Agricultural Region

Susceptibility of Fall Armyworm Field Populations to Vip3Aa/Cry Bt Maize in a Tropical Agricultural Region

Rapid evolution of pesticide resistance via adaptation and interspecific introgression in a major North American crop pest

Cross-pollination in seed-blended refuge and selection for Vip3A resistance in a lepidopteran pest as detected by genomic monitoring

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