Decreased Cry1Ac activation by midgut proteases associated with Cry1Ac resistance in <scp><i>Helicoverpa zea</i></scp>

Zhang, Min; Wei, Jizhen; Ni, Xinzhi; Zhang, Jie; Jurat-Fuentes, Juan Luís; Fabrick, Jeffrey A.; Carrière, Yves; Tabashnik, Bruce E.; Li, Xianchun

doi:10.1002/ps.5224

Cited by 31 publications

(16 citation statements)

References 51 publications

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“…They proposed this as the mechanism of resistance to Cry1Ac because of reduced toxin binding and increased degradation by proteolysis. Zhang et al [15] found no differences in ALP activity between their H. zea resistant and susceptible strains but instead came to the conclusion that a decrease in Cry1Ac activation by midgut proteases partially contributed to Cry1Ac resistance in their GA (a field-selected population) and GA-R (derived from GA and further selected in the laboratory for increased resistance) strains. Lawrie et al [16] also suggested that an enhanced immune system may be involved, shown by the increased differential expression of three immune pathways in RNAseq comparisons of Bt-resistant versus susceptible strains of H. zea.…”

Section: Introductionmentioning

confidence: 99%

Bacterial Microbiota of Field-Collected Helicoverpa zea (Lepidoptera: Noctuidae) from Transgenic Bt and Non-Bt Cotton

et al. 2021

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The bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), is an important agricultural pest in U.S. cotton and is managed using transgenic hybrids that produce insecticidal proteins from the bacterium, Bacillus thuringiensis (Bt). The reduced efficacy against H. zea caterpillars of Bt plants expressing Cry toxins is increasing in the field. In a first step towards understanding Bt cotton–bollworm–microbiota interactions, we investigated the internal bacterial microbiota of second–third stadium H. zea collected in the field from non-Bt versus Bt (WideStrike) cotton in close proximity (in North Carolina, USA). The bacterial populations were analyzed using culture-dependent and -independent molecular approaches. We found that WideStrike samples had a higher bacterial density and diversity per larva than insects collected from non-Bt cotton over two field seasons: 8.42 ± 0.23 and 5.36 ± 0.75 (log10 colony forming units per insect) for WideStrike compared to 6.82 ± 0.20 and 4.30 ± 0.56 for non-Bt cotton for seasons 1 and 2, respectively. Fifteen phyla, 103 families, and 229 genera were identified after performing Illumina sequencing of the 16S rRNA. At the family level, Enterobacteriaceae and Enterococcaceae were the most abundant taxa. The Enterococcaceae family was comprised mostly of Enterococcus species (E. casseliflavus and another Enterococcus sp.). Members of the Enterococcus genus can acidify their environment and can potentially reduce the alkaline activation of some Bt toxins. These findings argue for more research to better understand the role of cotton–bollworm–bacteria interactions and the impact on Bt toxin caterpillar susceptibility.

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Section: Introductionmentioning

confidence: 99%

Bacterial Microbiota of Field-Collected Helicoverpa zea (Lepidoptera: Noctuidae) from Transgenic Bt and Non-Bt Cotton

et al. 2021

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“…In P. gossypiella, this resistance was associated with alternative splicing generating aberrant transcripts of cadherin, a receptor for Cry1Ac in that insect (Fabrick et al, 2014). This lack of functional receptor cadherin is associated with reduced Cry1Ac binding and resistance (Ojha et al, 2014) Although the mechanistic description of resistance in H. zea remains elusive, mutations in a novel cadherin gene (Fritz et al, 2020) and reduced Cry1Ac processing (Zhang et al, 2019) have been proposed as putative.…”

Section: Introductionmentioning

confidence: 99%

Genetic Knockouts Indicate That the ABCC2 Gene in the Bollworm Helicoverpa Zea Is Not a Major Receptor for the Cry1Ac Insecticidal Protein.

Perera¹,

Little²,

Abdelgaffar³

et al. 2021

Preprint

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Members of the insect ATP binding cassette transporter subfamily C2 (ABCC2) in several moth species are known as receptors for the Cry1Ac insecticidal protein from Bacillus thuringiensis (Bt). Mutations that abolish the functional domains of ABCC2 are known to cause resistance to Cry1Ac, although the reported levels of resistance vary widely depending on insect species. In this study, the function of the ABCC2 gene as putative Cry1Ac receptor in Helicoverpa zea, a major pest of over 300 crops, was evaluated using CRISPR/Cas9 to progressively eliminate different functional ABCC2 domains. Results from bioassays with edited insect lines support that muta-tions in ABCC2 was associated with Cry1Ac resistance ratios (RR) ranging from 7.3- to 39.8-fold. No significant differences in susceptibility to Cry1Ac were detected between H. zea with partial or complete ABCC2 knockout, although highest levels of tolerance were observed when knocking out half of ABCC2. Based on >500-1,000-fold RRs reported in similar studies for closely related moth species, the low RRs observed in H. zea knockouts support that ABCC2 is not a major Cry1Ac receptor in this insect.

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“…Functional changes in the ATP-binding cassette (ABC) transport proteins was reported [26,27], and a dominant point mutation in tetraspanin proteins (TSPAN) in field resistant Helicoverpa armigera was found in China [28]. Decreases is Cry1Ac midgut protease cleavage was described in resistant H. zea [29]. A shotgun, global transcriptomics approach was used in this study in order to assess differences in gene expression between field-obtained, Bt-resistant versus laboratory Bt-susceptible (unfed) neonates of H. zea both reared under the same laboratory conditions.…”

Section: Introductionmentioning

confidence: 99%

Multiple Known Mechanisms and a Possible Role of an Enhanced Immune System in Bt-Resistance in a Field Population of the Bollworm, Helicoverpa zea: Differences in Gene Expression with RNAseq

Lawrie

Mitchell

Deguenon

et al. 2020

IJMS

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Several different agricultural insect pests have developed field resistance to Bt (Bacillus thuringiensis) proteins (ex. Cry1Ac, Cry1F, etc.) expressed in crops, including corn and cotton. In the bollworm, Helicoverpa zea, resistance levels are increasing; recent reports in 2019 show up to 1000-fold levels of resistance to Cry1Ac, a major insecticidal protein in Bt-crops. A common method to analyze global differences in gene expression is RNA-seq. This technique was used to measure differences in global gene expression between a Bt-susceptible and Bt-resistant strain of the bollworm, where the differences in susceptibility to Cry1Ac insecticidal proteins were 100-fold. We found expected gene expression differences based on our current understanding of the Bt mode of action, including increased expression of proteases (trypsins and serine proteases) and reduced expression of Bt-interacting receptors (aminopeptidases and cadherins) in resistant bollworms. We also found additional expression differences for transcripts that were not previously investigated, i.e., transcripts from three immune pathways-Jak/STAT, Toll, and IMD. Immune pathway receptors (ex. PGRPs) and the IMD pathway demonstrated the highest differences in expression. Our analysis suggested that multiple mechanisms are involved in the development of Bt-resistance, including potentially unrecognized pathways.

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Decreased Cry1Ac activation by midgut proteases associated with Cry1Ac resistance in Helicoverpa zea

Cited by 31 publications

References 51 publications

Bacterial Microbiota of Field-Collected Helicoverpa zea (Lepidoptera: Noctuidae) from Transgenic Bt and Non-Bt Cotton

Bacterial Microbiota of Field-Collected Helicoverpa zea (Lepidoptera: Noctuidae) from Transgenic Bt and Non-Bt Cotton

Genetic Knockouts Indicate That the ABCC2 Gene in the Bollworm Helicoverpa Zea Is Not a Major Receptor for the Cry1Ac Insecticidal Protein.

Multiple Known Mechanisms and a Possible Role of an Enhanced Immune System in Bt-Resistance in a Field Population of the Bollworm, Helicoverpa zea: Differences in Gene Expression with RNAseq

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