Occurrence and Ear Damage of Helicoverpa zea on Transgenic Bacillus thuringiensis Maize in the Field in Texas, U.S. and Its Susceptibility to Vip3A Protein

Yang, Fei; González, José C. Santiago; Williams, Jayme; Cook, Donald R; Gilreath, Ryan T; Kerns, David L.

doi:10.3390/toxins11020102

Cited by 82 publications

(154 citation statements)

References 37 publications

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“…Therefore, we used 3.0 μg/cm 2 Vip3Aa39 as the diagnostic concentration for the F 2 screens. Susceptibility to Vip3Aa39 of the F 2 families of H. zea was evaluated using a diet-overlay bioassay as described in Yang et al 15 . Briefly, 0.8 ml of liquid diet (Southland Product, Inc. Lake Village, AR) was dispensed using repeater pipets into each well of 128-well bioassay trays (C-D International, Pitman, NJ).…”

Section: Methodsmentioning

confidence: 99%

“…Currently, field-evolved resistance of H. zea to Cry1 and Cry2 proteins has been widely reported in the U.S., especially in the Southern states 15,[18][19][20][21] . For example, Yang et al 15 and Kaur et al 21 documented field-evolved practical resistance of H. zea populations in Texas and Louisiana to Cry1A.105/Cry2Ab2 corn, respectively. In 2018, Reisig et al 19 reported field-evolved practical resistance of H. zea to Bt cotton containing Cry1Ac/Cry1F and Cry1Ac/ Cry2Ab proteins in North Carolina.…”

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confidence: 99%

“…Studies have shown that Vip3Aa is highly effective for control of H. zea in the field 24,25 and Vip3Aa is currently used in combination with Cry1/Cry2 proteins in almost all Bt corn and Bt cotton products in the U.S 17 . However, widespread field resistance to Cry1 and Cry2 proteins in H. zea populations in the U.S 15,[18][19][20][21] . makes Vip3Aa the only remaining effective protein against this pest in commercialized Bt crops.…”

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First documentation of major Vip3Aa resistance alleles in field populations of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in Texas, USA

Yang

González

Little

et al. 2020

Sci Rep

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the corn earworm, Helicoverpa zea, is a major target pest of the insecticidal Vip3Aa protein used in pyramided transgenic Bt corn and cotton with Cry1 and Cry2 proteins in the U.S. The widespread resistance to Cry1 and Cry2 proteins in H. zea will challenge the long-term efficacy of Vip3Aa technology. Determining the frequency of resistant alleles to Vip3Aa in field populations of H. zea is critically important for resistance management. Here, we provided the first F 2 screen study to estimate the resistance allele frequency for Vip3Aa in H. zea populations in Texas, U.S. In 2019, 128 H. zea neonates per isofamily for a total of 114 F 2 families were screened with a diagnostic concentration of 3.0 μg/cm 2 of Vip3Aa39 protein in diet-overlay bioassays. The F 2 screen detected two families carrying a major Vip3Aa resistance allele. The estimated frequency of major resistance alleles against Vip3Aa39 in H. zea in texas from this study was 0.0065 with a 95% CI of 0.0014-0.0157. A Vip3Aa-resistant strain (RR) derived from the f 2 screen showed a high level of resistance to Vip3Aa39 protein, with a resistance ratio of >588.0fold relative to a susceptible population (SS) based on diet-overlay bioassays. We provide the first documentation of a major resistance allele conferring high levels of Vip3Aa resistance in a field-derived strain of H. zea in the U.S. Data generated from this study contribute to development of management strategies for the sustainable use of the Vip3Aa technology to control H. zea in the U.S. Genetically engineered crops producing insecticidal Cry and Vip proteins from the bacterium Bacillus thuringiensis (Bt) have been planted for control of insect pests for more than two decades 1. Field efficacy of these Bt crops has been outstanding in controlling most target species, resulting in substantial economic, environmental and social gains 2-7. However, with large scale adoption comes intense selection pressure for development of resistance and challenges for long-term sustainability 8,9. To date, field-evolved practical resistance to Bt crops has been globally reported in at least 21 cases 10-15. To delay insect resistance development, an insecticide resistance management (IRM) plan based on a "high-dose refuge" strategy has been implemented in the U.S 16. Monitoring for evolution of resistance in field populations of the target insect species is an essential component of this IRM plan to maintain sustainability of Bt crop technologies. The corn earworm/cotton bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), is a major target pest of both Bt cotton and Bt corn in North America. Control of lepidopteran pests is achieved by the adoption of corn hybrids producing combinations of Cry1Ab, Cry1F, Cry1A.105, Cry2Ab2 and Vip3Aa20 insecticidal Bt proteins, and Bt cotton varieties producing combinations of Cry1Ac, Cry1F, Cry1Ab, Cry2Ab, Cry2Ae, and Vip3Aa19 17 .

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Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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confidence: 99%

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First documentation of major Vip3Aa resistance alleles in field populations of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in Texas, USA

Yang

González

Little

et al. 2020

Sci Rep

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“…It is interesting that the 15bp insertion, which produces a DNTAT amino acid sequence in GA-R, is present in the reference genome. The strain of H. zea used for genome sequencing was described as highly susceptible to Cry1A toxins by Pearce et al (2017), which is true relative to levels of resistance recently described in H. zea (Brévault et al, 2013; Dively et al, 2016; Reisig et al, 2018; Yang et al, 2019). Yet in the early 1990s, before Bt crops were commercialized, this long-term laboratory-reared strain was less susceptible to Cry1Ac than most strains derived recently from the field, including a >400-fold difference in one case (Luttrell et al, 1999).…”

Section: Discussionmentioning

confidence: 99%

“…Helicoverpa zea is one lepidopteran species targeted by Bt crops with low susceptibility to Cry proteins (Stone and Sims, 1993; Ali et al, 2006; Sivasupramaniam et al, 2008). A major pest of both corn and cotton in the U.S., H. zea has evolved resistance to several Cry proteins (Welch et al, 2015; Dively et al, 2016; Reisig et al, 2018; Kaur et al, 2019; Yang et al, 2019). While some efforts have been made to understand the molecular mechanisms underlying Cry resistance in H. zea (Caccia et al, 2012; Zhang et al, 2019), we still know little about how selection by Cry proteins has shaped genotype frequencies in this important pest.…”

Section: Introductionmentioning

confidence: 99%

Mutations in a novel cadherin gene associated with Bt resistance inHelicoverpa zea

Fritz

Nunziata

Guo

et al. 2019

Preprint

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20Transgenic corn and cotton produce crystalline (Cry) proteins derived from the soil 21 bacterium Bacillus thuringiensis (Bt) that are toxic to lepidopteran larvae. Helicoverpa zea, a 22 key pest of corn and cotton in the U.S., has evolved widespread resistance to these proteins 23 produced in Bt corn and cotton. While the genomic targets of Cry selection and the mutations 24 that produce resistant phenotypes are known in other lepidopteran species, little is known about 25 how Cry proteins shape the genome of H. zea. We scanned the genomes of Cry1Ac-selected and 26 unselected H. zea lines, and identified eleven genes on six scaffolds that showed evidence of 27 selection by Cry1Ac, including cadherin-86C (cad-86C), a gene from a family that is involved in 28 Cry1A resistance in other lepidopterans. Although this gene was expressed in the H. zea larval 29 midgut, the protein it encodes has only 17 to 22% identity with cadherin proteins from other 30 species previously reported to be involved in Bt resistance. An analysis of midgut-expressed 31 cDNAs showed significant between-line differences in the frequencies of putative 32 nonsynonymous substitutions (both SNPs and indels). Our results indicate that cad-86C is a 33 target of Cry1Ac selection in H. zea. Future work should investigate phenotypic effects of these 34 nonsynonymous substitutions and their impact on phenotypic resistance in field populations.

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JAZ Genes in Cotton: Prospects for Improvements to Vegetative and Fibre Growth by Addressing Lepidopteran Herbivory Resistance Mechanisms

Rock,

Adhikari,

Parajulee

2024

Annual Plant Reviews Online

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Evolution of insect resistance is the primary threat to the long‐term efficacy of Bacillus thuringiensis (Bt) transgene technologies. Plants have a deeply conserved defence response to pests: Jasmonic acid (JA) hormone signalling mediated by transcriptional repressors called JASMONATE‐ZIM‐DOMAIN/JAZ. JAZs normally limit expression of plant defence pathways, promoting assimilate partitioning towards growth and reproduction, by their carboxyl terminal Jas motif that antagonises MYeloCytomatosis (MYC) master transcription factor activities. Deletion, alternative splicing/intron retention, or disruption of the Jas motif results in JA insensitivity and increased resistance to pathogens including arthropod herbivores, for example by production of secondary metabolites and new leaves with higher trichome density. JA‐mediated trichome initiation and elongation also impact cotton fibre production. Since its release in 2017, the third‐generation stacked commercial Bt insecticidal Vip3A protein traits are increasingly under severe pressure for evolution of Helicoverpa zea (bollworm) resistance. Regional differences in efficacy of Bollgard ® 3 and WideStrike ® 3 against lepidopteran pests and increasing pesticide use are emerging issues. Future transgenic field control failures from bollworm infestations and incursions of Helicoverpa armigera from Central America are likely in the U.S. Cotton Belt. In this systematic primer on the problem, we take a conceptual approach to consider JAZ genes as means to leverage ‘internal’ host‐derived herbivore resistance in cotton. We consider the genetic redundancy and pleiotropic nature of JAZ master regulators on tissue‐specific growth, development, crosstalk with hormonal and small RNA pathways as nodes in networks, and limitations of JAZ efficacy due to fitness costs/growth trade‐offs versus prospects for enhancing resistance networks to orchestrate transgressive segregation (generation of extreme phenotypes in breeding progeny not seen in parental lines).

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Occurrence and Ear Damage of Helicoverpa zea on Transgenic Bacillus thuringiensis Maize in the Field in Texas, U.S. and Its Susceptibility to Vip3A Protein

Cited by 82 publications

References 37 publications

First documentation of major Vip3Aa resistance alleles in field populations of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in Texas, USA

First documentation of major Vip3Aa resistance alleles in field populations of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in Texas, USA

Mutations in a novel cadherin gene associated with Bt resistance inHelicoverpa zea

JAZ Genes in Cotton: Prospects for Improvements to Vegetative and Fibre Growth by Addressing Lepidopteran Herbivory Resistance Mechanisms

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