Resistance of Pests to Insecticidal Proteins from Bacillus thuringiensis (Bt)

A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Pest and Vector Management".

Deadline for manuscript submissions: closed (30 September 2023) | Viewed by 23078

Special Issue Editors

Department of Entomology, The University of Arizona, Tucson, AZ, USA
Interests: plant–insect interactions; insecticide and Bt resistance; P450; transposable elements; toxicology; insect molecular biology
USDA, US Arid Land Agricultural Research Center, Maricopa, AZ, USA
Interests: Bacillus thuringiensis (Bt); insect pests; biochemical and physiological

Special Issue Information

Dear Colleagues,

Bacillus thuringiensis (Bt) are Gram-positive bacteria that produce different insecticidal proteins, named Cry, Vip, and Cyt, during the sporulation phase of growth. They are applied to manage and control agricultural pests. Bt toxins are believed the most successful alternatives to synthetic pesticides. However, today, the most severe threat to the sustainability of Bt insecticidal proteins (toxins) is the evolution of resistance in target pests. Thus, the importance of studying pest resistance to insecticidal proteins from Bacillus thuringiensis (Bt) to support improvement of Bt technology and its sustainability in pest control cannot be overestimated.

We would like to invite all works, including original research and/or review articles, covering studies on the selection and monitoring of pest resistance to Bt toxins (Cry, Vip and Cyt), dominance and fitness of Bt resistance, cross-resistance and interactions between Bt toxins and other toxins (plant toxins and insecticides), genetic/molecular mechanisms of Bt resistance, cross-resistance and synergistic/antagonistic interactions, and strategies/tactics to delay, mitigate, and manage Bt resistance. 

Prof. Dr. Xianchun Li
Dr. Jeffrey A. Fabrick
Guest Editors

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Keywords

  • Bacillus thuringiensis toxins
  • resistance selection
  • resistance monitoring
  • fitness cost
  • resistance/cross resistance mechanism
  • interaction mechanism
  • allelochemicals
  • insecticides
  • resistance management

Published Papers (15 papers)

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Research

Jump to: Review

13 pages, 889 KiB  
Article
Exposure to Cry1 Toxins Increases Long Flight Tendency in Susceptible but Not in Cry1F-Resistant Female Spodoptera frugiperda (Lepidoptera: Noctuidae)
by Caroline P. De Bortoli, Rafael F. Santos, Giordano J. Assirati, Xiaocun Sun, Lucas Hietala and Juan Luis Jurat-Fuentes
Insects 2024, 15(1), 7; https://doi.org/10.3390/insects15010007 - 22 Dec 2023
Viewed by 1108
Abstract
The fall armyworm (JE Smith) (Spodoptera frugiperda) is a polyphagous pest targeted by selected Cry and Vip3A insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) that are produced in transgenic Bt corn and cotton. Available evidence suggests that sublethal larval exposure [...] Read more.
The fall armyworm (JE Smith) (Spodoptera frugiperda) is a polyphagous pest targeted by selected Cry and Vip3A insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) that are produced in transgenic Bt corn and cotton. Available evidence suggests that sublethal larval exposure to Cry1Ac increases flight activity in adult Spodoptera spp. However, it is not known whether this effect is also observed in survivors from generally lethal exposure to Cry1Ac. Moreover, while multiple cases of field-evolved resistance to Bt proteins have been described in the native range of S. frugiperda, the effect of resistance on flight behavior has not been examined. Long-distance migratory flight capacity of S. frugiperda is of concern given its ongoing global spread and the possibility that migrants may be carrying resistance alleles against pesticides and Bt crops. In this study, we used rotational flight mills to test the effects of generally lethal exposure to Cry1Ac in susceptible and sublethal exposure in Cry1F-resistant S. frugiperda strains. The results detected altered pupal weight after larval feeding on diet containing Cry proteins, which only translated in significantly increased tendency for longer flights in female moths from the susceptible strain. This information has relevant implications when considering current models and assumptions for resistance management of Bt crops. Full article
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11 pages, 3699 KiB  
Article
Engineered Expression of Vip3A in Green Tissues as a Feasible Approach for the Control of Insect Pests in Maize
by Guangsheng Yuan, Cheng Zeng, Haoya Shi, Yong Yang, Juan Du, Chaoying Zou, Langlang Ma, Guangtang Pan and Yaou Shen
Insects 2023, 14(10), 803; https://doi.org/10.3390/insects14100803 - 06 Oct 2023
Viewed by 904
Abstract
Genetic engineering technology offers opportunities to improve many important agronomic traits in crops, including insect-resistance. However, genetically modified (GM) exogenous proteins in edible tissues of transgenic crops has become an issue of intense public concern. To advance the application of GM techniques in [...] Read more.
Genetic engineering technology offers opportunities to improve many important agronomic traits in crops, including insect-resistance. However, genetically modified (GM) exogenous proteins in edible tissues of transgenic crops has become an issue of intense public concern. To advance the application of GM techniques in maize, a Cre/loxP-based strategy was developed for manipulating the transgenes in green tissues while locking them in non-green tissues. In the strategy, the site-specific excision can be used to switch on or off the expression of transgenes at specific tissues. In this work, two basic transgenic maize, named KEY, carrying the Cre gene, and LOCK, containing the Vip3A gene with a blocked element, were obtained based on their separate fusion gene cassettes. The expression level and concentration of Vip3A were observed with a high specific accumulation in the green tissues (leaf and stem), and only a small amount was observed in the root and kernel tissues in the KEY × LOCK hybrids. The insect resistance of transgenic maize against two common lepidopteran pests, Ostrinia furnacalis and Spodoptera frugiperda, was assessed in the laboratory and field. The results indicate that the hybrids possessed high resistance levels against the two pests, with mortality rates above 73.6% and damage scales below 2.4 compared with the control group. Our results suggest that the Cre/loxP-mediated genetic engineering approach has a competitive advantage in GM maize. Overall, the findings from this study are significant for providing a feasible strategy for transgenes avoiding expression in edible parts and exploring novel techniques toward the biosafety of GM plants. Full article
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14 pages, 1705 KiB  
Article
Sequential and Simultaneous Interactions of Plant Allelochemical Flavone, Bt Toxin Vip3A, and Insecticide Emamectin Benzoate in Spodoptera frugiperda
by Kaiyuan Huang, Haibo He, Shan Wang, Min Zhang, Xuewei Chen, Zhongyuan Deng, Xinzhi Ni and Xianchun Li
Insects 2023, 14(9), 736; https://doi.org/10.3390/insects14090736 - 31 Aug 2023
Viewed by 894
Abstract
Target pests of genetically engineered crops producing both defensive allelochemicals and Bacillus thuringiensis (Bt) toxins often sequentially or simultaneously uptake allelochemicals, Bt toxins, and/or insecticides. How the three types of toxins interact to kill pests remains underexplored. Here we investigated the interactions of [...] Read more.
Target pests of genetically engineered crops producing both defensive allelochemicals and Bacillus thuringiensis (Bt) toxins often sequentially or simultaneously uptake allelochemicals, Bt toxins, and/or insecticides. How the three types of toxins interact to kill pests remains underexplored. Here we investigated the interactions of Bt toxin Vip3A, plant allelochemical flavone, and insecticide emamectin benzoate in Spodoptera frugiperda. Simultaneous administration of flavone LC25 + Vip3A LC25, emamectin benzoate LC25 + Vip3A LC25, and flavone LC15 + emamectin benzoate LC15 + Vip3A LC15 but not flavone LC25 + emamectin LC25 yielded a mortality significantly higher than their expected additive mortality (EAM). One-day pre-exposure to one toxin at LC5 followed by six-day exposure to the same toxin at LC5 plus another toxin at LC50 showed that the mortality of flavone LC5 + Vip3A LC50, emamectin benzoate LC5 + Vip3A LC50, and Vip3A LC5 + emamectin benzoate LC50 were significantly higher than their EAM, while that of flavone LC5 + emamectin benzoate LC50 was significantly lower than their EAM. No significant difference existed among the mortalities of Vip3A LC5 + flavone LC50, emamectin benzoate LC5 + flavone LC50, and their EAMs. The results suggest that the interactions of the three toxins are largely synergistic (inductive) or additive, depending on their combinations and doses. Full article
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16 pages, 706 KiB  
Article
Extended Sentinel Monitoring of Helicoverpa zea Resistance to Cry and Vip3Aa Toxins in Bt Sweet Corn: Assessing Changes in Phenotypic and Allele Frequencies of Resistance
by Galen P. Dively, Tom P. Kuhar, Sally V. Taylor, Helene Doughty, Kristian Holmstrom, Daniel O. Gilrein, Brian A. Nault, Joseph Ingerson-Mahar, Anders Huseth, Dominic Reisig, Shelby Fleischer, David Owens, Kelley Tilmon, Francis Reay-Jones, Pat Porter, Jocelyn Smith, Julien Saguez, Jason Wells, Caitlin Congdon, Holly Byker, Bryan Jensen, Chris DiFonzo, William D. Hutchison, Eric Burkness, Robert Wright, Michael Crossley, Heather Darby, Tom Bilbo, Nicholas Seiter, Christian Krupke, Craig Abel, Brad S. Coates, Bradley McManus, Billy Fuller, Jeffrey Bradshaw, Julie A. Peterson, David Buntin, Silvana Paula-Moraes, Katelyn Kesheimer, Whitney Crow, Jeffrey Gore, Fangneng Huang, Dalton C. Ludwick, Amy Raudenbush, Sebastian Jimenez, Yves Carrière, Timothy Elkner and Kelly Hambyadd Show full author list remove Hide full author list
Insects 2023, 14(7), 577; https://doi.org/10.3390/insects14070577 - 25 Jun 2023
Cited by 4 | Viewed by 1338
Abstract
Transgenic corn and cotton that produce Cry and Vip3Aa toxins derived from Bacillus thuringiensis (Bt) are widely planted in the United States to control lepidopteran pests. The sustainability of these Bt crops is threatened because the corn earworm/bollworm, Helicoverpa zea (Boddie), is evolving [...] Read more.
Transgenic corn and cotton that produce Cry and Vip3Aa toxins derived from Bacillus thuringiensis (Bt) are widely planted in the United States to control lepidopteran pests. The sustainability of these Bt crops is threatened because the corn earworm/bollworm, Helicoverpa zea (Boddie), is evolving a resistance to these toxins. Using Bt sweet corn as a sentinel plant to monitor the evolution of resistance, collaborators established 146 trials in twenty-five states and five Canadian provinces during 2020–2022. The study evaluated overall changes in the phenotypic frequency of resistance (the ratio of larval densities in Bt ears relative to densities in non-Bt ears) in H. zea populations and the range of resistance allele frequencies for Cry1Ab and Vip3Aa. The results revealed a widespread resistance to Cry1Ab, Cry2Ab2, and Cry1A.105 Cry toxins, with higher numbers of larvae surviving in Bt ears than in non-Bt ears at many trial locations. Depending on assumptions about the inheritance of resistance, allele frequencies for Cry1Ab ranged from 0.465 (dominant resistance) to 0.995 (recessive resistance). Although Vip3Aa provided high control efficacy against H. zea, the results show a notable increase in ear damage and a number of surviving older larvae, particularly at southern locations. Assuming recessive resistance, the estimated resistance allele frequencies for Vip3Aa ranged from 0.115 in the Gulf states to 0.032 at more northern locations. These findings indicate that better resistance management practices are urgently needed to sustain efficacy the of corn and cotton that produce Vip3Aa. Full article
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15 pages, 1198 KiB  
Article
Movement of Striacosta albicosta (Smith) (Lepidoptera: Noctuidae) Larvae on Transgenic Bt and Non-Bt Maize
by Débora G. Montezano, Thomas E. Hunt, Priscila M. Colombo da Luz, Kelsey Karnik, Stephen D. Kachman, Ana M. Vélez and Julie A. Peterson
Insects 2023, 14(6), 524; https://doi.org/10.3390/insects14060524 - 05 Jun 2023
Viewed by 978
Abstract
Exposure of lepidopteran pests to Bacillus thuringiensis (Bt) proteins has been shown to affect the behavior of larvae, including increased movement and avoidance of Bt-expressing plants or diet. Therefore, we hypothesized that the behavior of western bean cutworm, Striacosta albicosta [...] Read more.
Exposure of lepidopteran pests to Bacillus thuringiensis (Bt) proteins has been shown to affect the behavior of larvae, including increased movement and avoidance of Bt-expressing plants or diet. Therefore, we hypothesized that the behavior of western bean cutworm, Striacosta albicosta (Smith) (Lepidoptera: Noctuidae), an important pest of maize, could be affected when exposed to Bt plants. To test this hypothesis, we conducted a series of artificial arena and on-plant experiments to determine S. albicosta neonate behavior when exposed to Bt and non-Bt plant tissue. Video tracking experiments presented neonate larvae with the choice of Bt or non-Bt pollen in a Petri dish for 15 min while being video recorded for analysis with EthoVision software. This study showed an increase in mean velocity and total time spent moving for larvae in the presence of Cry1F vs. non-Bt when compared with Vip3A vs. non-Bt or Cry1F vs. Vip3A. However, there was no difference in total distance moved or time spent in the food zone for all scenarios. Maize tissue choice experiments allowed neonatal larvae the choice of feeding on Bt or non-Bt tassel or leaves for 9 h in Petri dish arenas. This experiment showed that larvae preferred tassel tissue over leaves but did not indicate that larvae could distinguish between Bt and non-Bt tissue. In contrast, on-plant experiments (including a whole plant neonate dispersal study under controlled conditions and an in-field silking behavior experiment) indicated that the presence of Cry1F and Vip3A Bt toxins increased plant abandonment, suggesting that larvae are able to detect and avoid Bt toxins. The discrepancy of these results is likely due to the on-plant studies providing more field-realistic environmental conditions and a longer duration of exposure to Bt toxins for the behavioral experiments. Our results represent the first steps in understanding the complex behavior of S. albicosta when exposed to Bt plants. A better understanding of the response of larvae when exposed to Bt traits can aid in the management of this pest, particularly for the design of resistance management strategies and refuge design. Full article
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16 pages, 4371 KiB  
Article
Using Sentinel Plots to Monitor for Changes in Thrips Susceptibility to MON 88702 Cotton Containing the Cry51Aa2.834_16 Bt Protein
by Ashley D. Yates-Stewart, Benjamin T. Yorke, Alan Willse, Jennifer Fridley and Graham P. Head
Insects 2023, 14(6), 497; https://doi.org/10.3390/insects14060497 - 27 May 2023
Cited by 1 | Viewed by 983
Abstract
Transgenic Bt crops are important tools for growers to manage insect pests, but their durability is threatened by the evolution of insect resistance. Implementing a resistance monitoring program is essential to detect and mitigate resistance. For non-high-dose Bt crops, resistance monitoring is challenging, [...] Read more.
Transgenic Bt crops are important tools for growers to manage insect pests, but their durability is threatened by the evolution of insect resistance. Implementing a resistance monitoring program is essential to detect and mitigate resistance. For non-high-dose Bt crops, resistance monitoring is challenging, because insect control is not complete, so targeted insects and insect damage will be present even without resistance. Given these challenges, sentinel plots have been used to monitor for insect resistance to non-high-dose crops by assessing changes in the efficacy of a Bt crop over time relative to a non-Bt control. We optimized a sentinel plot resistance monitoring approach for MON 88702 ThryvOn™ cotton, a new non-high-dose Bt product targeting two sucking pest taxa—Lygus (L. lineolaris and L. hesperus) and thrips (Frankliniella fusca and F. occidentalis)—and report here on the thrips monitoring methods and results. Quantifying thrips immatures was the best metric to characterize the impact of the trait, with at least a 40–60% average reduction of thrips immatures on ThryvOn relative to the control cotton at all sites with higher thrips densities. These data can be used within a ThryvOn resistance monitoring program and represent a case study for establishing a resistance monitoring approach for a non-high-dose trait product. Full article
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15 pages, 6361 KiB  
Article
Factors Affecting Population Dynamics of Helicoverpa zea (Lepidoptera: Noctuidae) in a Mixed Landscape with Bt Cotton and Peanut
by Izailda Barbosa dos Santos, Silvana V. Paula-Moraes, Julien M. Beuzelin, Daniel A. Hahn, Omaththage P. Perera and Clyde Fraisse
Insects 2023, 14(4), 395; https://doi.org/10.3390/insects14040395 - 19 Apr 2023
Cited by 1 | Viewed by 1350
Abstract
In North America, weather and host-plant abundance drive the population dynamics of the migratory pest Helicoverpa zea. The objectives of this study were to (i) estimate monthly abundance of H. zea moths in Bt cotton and peanut fields, (ii) document the effects of [...] Read more.
In North America, weather and host-plant abundance drive the population dynamics of the migratory pest Helicoverpa zea. The objectives of this study were to (i) estimate monthly abundance of H. zea moths in Bt cotton and peanut fields, (ii) document the effects of weather on H. zea trap catches, and (iii) determine larval hosts supporting H. zea populations from 2017 to 2019. Year-round trapping of H. zea moths was conducted in 16 commercial fields in two regions of the Florida Panhandle using delta traps. H. zea moth catches were associated with temperature, rainfall, and relative humidity. Larval hosts were determined by isotopic carbon analysis. Our results showed year-round H. zea flights in both regions across two years, with the highest and lowest moth catches occurring from July to September and November to March, respectively. There was no difference in catches between traps set on Bt cotton and peanut. In the Santa Rosa/Escambia counties, weather explained 59% of the variance in H. zea catches, with significant effects of temperature, relative humidity, and rainfall. In Jackson County, weather explained 38% of H. zea catches, with significant effects of temperature and relative humidity. Carbon isotopic data showed that feeding on C3 plants, including Bt cotton, occurred over most of the year, although feeding on C4 hosts, including Bt corn, occurred during the summer months. Hence overwintering and resident populations of H. zea in the Florida Panhandle may be continually exposed to Bt crops, increasing the risk for the evolution of resistance. Full article
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9 pages, 261 KiB  
Article
Magnitude and Extent of Helicoverpa zea Resistance Levels to Cry1Ac and Cry2Ab2 across the Southeastern USA
by Dominic Reisig, G. David Buntin, Jeremy K. Greene, Silvana V. Paula-Moraes, Francis Reay-Jones, Phillip Roberts, Ron Smith and Sally V. Taylor
Insects 2023, 14(3), 262; https://doi.org/10.3390/insects14030262 - 07 Mar 2023
Cited by 4 | Viewed by 1206
Abstract
After resistance is first detected, continued resistance monitoring can inform decisions on how to effectively manage resistant populations. We monitored for resistance to Cry1Ac (2018 and 2019) and Cry2Ab2 (2019) from southeastern USA populations of Helicoverpa zea. We collected larvae from various [...] Read more.
After resistance is first detected, continued resistance monitoring can inform decisions on how to effectively manage resistant populations. We monitored for resistance to Cry1Ac (2018 and 2019) and Cry2Ab2 (2019) from southeastern USA populations of Helicoverpa zea. We collected larvae from various plant hosts, sib-mated the adults, and tested neonates using diet-overlay bioassays and compared them to susceptible populations for resistance estimates. We also compared LC50 values with larval survival, weight and larval inhibition at the highest dose tested using regression, and found that LC50 values were negatively correlated with survival for both proteins. Finally, we compared resistance rations between Cry1Ac and Cry2Ab2 during 2019. Some populations were resistant to Cry1Ac, and most were resistant to CryAb2; Cry1Ac resistance ratios were lower than Cry2Ab2 during 2019. Survival was positively correlated with larval weight inhibition for Cry2Ab. This contrasts with other studies in both the mid-southern and southeastern USA, where resistance to Cry1Ac, Cry1A.105, and Cry2Ab2 increased over time and was found in a majority of populations. This indicates that cotton expressing Cry proteins in the southeastern USA was at variable risk for damage in this region. Full article
12 pages, 320 KiB  
Article
Resistance Allele Frequency of Helicoverpa zea to Vip3Aa Bacillus thuringiensis Protein in the Southeastern U.S.
by José C. Santiago-González, David L. Kerns and Fei Yang
Insects 2023, 14(2), 161; https://doi.org/10.3390/insects14020161 - 07 Feb 2023
Cited by 8 | Viewed by 1325
Abstract
Helicoverpa zea is a major target pest of Bt crops expressing Cry and/or Vip3Aa proteins in the U.S.A. Widespread practical resistance of H. zea to the Cry1 and Cry2 proteins makes Vip3Aa the only effective Bt protein against this pest. Understanding the frequency [...] Read more.
Helicoverpa zea is a major target pest of Bt crops expressing Cry and/or Vip3Aa proteins in the U.S.A. Widespread practical resistance of H. zea to the Cry1 and Cry2 proteins makes Vip3Aa the only effective Bt protein against this pest. Understanding the frequency of resistance alleles against Vip3Aa in field populations of H. zea is crucial for resistance management and the sustainability of Vip3Aa technology. Using a modified F2 screen method by crossing susceptible laboratory female moth with feral male moth of H. zea, we successfully screened a total of 24,576 neonates from 192 F2 families of H. zea collected from Arkansas, Louisiana, Mississippi, and Tennessee during 2019–2020. We found five F2 families containing ≥3rd instar survivors on the diagnostic concentration of 3.0 µg/cm2 Vip3Aa39. Dose-response bioassays confirmed the high levels of Vip3Aa resistance in these F2 families, with an estimated resistance ratio of >909.1-fold relative to the susceptible strain. The estimated resistance allele frequency against Vip3Aa in H. zea for these four southern states is 0.0155 with a 95% CI of 0.0057–0.0297. These data should provide critical information for understanding the risks of Vip3Aa resistance in H. zea and help design appropriate resistance management strategies for the sustainability of the Vip3Aa technology. Full article
8 pages, 1063 KiB  
Article
Rotation of Multiple Single-Gene Transgenic Crops Did Not Slow the Evolution of Resistance to Cry1F or Cry1Ie in Ostrinia furnacalis
by Yueqin Wang, Yudong Quan, Zhenying Wang and Kanglai He
Insects 2023, 14(1), 74; https://doi.org/10.3390/insects14010074 - 12 Jan 2023
Viewed by 1457
Abstract
A common strategy for delaying the evolution of resistance to transgenic crops that produce insecticidal proteins from Bacillus thuringiensis is to ensure that insect pests are exposed to multiple toxins with different mechanisms of action (MoAs). This can take the form of planting [...] Read more.
A common strategy for delaying the evolution of resistance to transgenic crops that produce insecticidal proteins from Bacillus thuringiensis is to ensure that insect pests are exposed to multiple toxins with different mechanisms of action (MoAs). This can take the form of planting crops in a rotation pattern when different crops expressing single toxins are available on the market. The efficacy of a rotation strategy is reliant on mathematical models based on biological assumptions. Here, we designed laboratory evolution experiments to test whether Bt-based insecticidal proteins with different MoAs used in rotation could delay resistance from developing in Asian corn borer (ACB), Ostrinia furnacalis. We investigated the proteins Cry1Ab, Cry1F, and Cry1Ie, which are widely utilized for commercial insect control. We found that rotation of multiple toxins did not slow the evolution of resistance to Cry1F or Cry1Ie. Furthermore, the evolution of ACB to the Cry1Ab toxin develops faster when Cry1F or Cry1Ie is present, as compared to Cry1Ab exposure only. Our results suggest that toxins used in a rotation fashion do not work as an effective strategy in delaying ACB resistance evolution to Cry toxins over one-toxin exposure. Our result highlights the need to better understand the biological factors leading to insecticidal protein resistance and to develop IRM strategies against target insects. Full article
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11 pages, 553 KiB  
Article
Inheritance of Resistance to Cry1A.105 in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)
by Wenbo Yu, Graham P. Head and Fangneng Huang
Insects 2022, 13(10), 875; https://doi.org/10.3390/insects13100875 - 27 Sep 2022
Cited by 2 | Viewed by 1217
Abstract
Cry1A.105 is a bioengineered Bacillus thuringiensis (Bt) insecticidal protein consisting of three domains derived from Cry1Ac, Cry1Ab, and Cry1F. It is one of the two pyramided Bt toxins expressed in the MON 89034 event, a commonly planted Bt maize trait in the Americas. [...] Read more.
Cry1A.105 is a bioengineered Bacillus thuringiensis (Bt) insecticidal protein consisting of three domains derived from Cry1Ac, Cry1Ab, and Cry1F. It is one of the two pyramided Bt toxins expressed in the MON 89034 event, a commonly planted Bt maize trait in the Americas. Recent studies have documented that field resistance of the corn earworm, Helicoverpa zea (Boddie), to the Cry1A.105 toxin in maize plants has become widespread in the United States. To investigate the inheritance of resistance to Cry1A.105 in H. zea, two independent tests, each with various genetic crosses among susceptible and Cry1A.105-resistant populations, were performed. The responses of these susceptible, resistant, F1, F2, and backcrossed insect populations to Cry1A.105 were assayed using a diet overlay method. The bioassays showed that the resistance to Cry1A.105 in H. zea was inherited as a single, autosomal, nonrecessive gene. The nonrecessive nature of the resistance could be an important factor contributing to the widespread resistance of maize hybrids containing Cry1A.105 in the United States. The results indicate that resistance management strategies for Bt crops need to be refined to ensure that they are effective in delaying resistance evolution for nonrecessive resistance (nonhigh dose). Full article
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Review

Jump to: Research

17 pages, 705 KiB  
Review
Fitness Costs and Incomplete Resistance Associated with Delayed Evolution of Practical Resistance to Bt Crops
by Yves Carrière and Bruce E. Tabashnik
Insects 2023, 14(3), 214; https://doi.org/10.3390/insects14030214 - 21 Feb 2023
Cited by 4 | Viewed by 1536
Abstract
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. [...] Read more.
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. Full article
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22 pages, 2015 KiB  
Review
Molecular Genetic Basis of Lab- and Field-Selected Bt Resistance in Pink Bollworm
by Jeffrey A. Fabrick, Xianchun Li, Yves Carrière and Bruce E. Tabashnik
Insects 2023, 14(2), 201; https://doi.org/10.3390/insects14020201 - 17 Feb 2023
Cited by 12 | Viewed by 2757
Abstract
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 [...] Read more.
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. Full article
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13 pages, 1259 KiB  
Review
Managing Practical Resistance of Lepidopteran Pests to Bt Cotton in China
by Yudong Quan and Kongming Wu
Insects 2023, 14(2), 179; https://doi.org/10.3390/insects14020179 - 10 Feb 2023
Cited by 4 | Viewed by 2238
Abstract
China is one of the major cotton producers globally with small farmers. Lepidopteran pests have always been the main factor affecting cotton production. To reduce the occurrence of and damage caused by lepidopteran pests, China has employed a pest control method focused on [...] Read more.
China is one of the major cotton producers globally with small farmers. Lepidopteran pests have always been the main factor affecting cotton production. To reduce the occurrence of and damage caused by lepidopteran pests, China has employed a pest control method focused on planting Bt (Cry1Ac) cotton since 1997. Chinese resistance management tactics for the main target pests, the cotton bollworm and pink bollworm, were also implemented. For polyphagous (multiple hosts) and migratory pests such as the cotton bollworm (Helicoverpa armigera), the “natural refuge” strategy, consisting of non-Bt crops such as corn, soybean, vegetables, peanuts, and other host crops, was adopted in the Yellow River Region (YRR) and Northwest Region (NR). For a single host and weak migration ability pest, such as the pink bollworm (Pectinophora gossypiella), the seed mix refuge strategy yields a random mixture within fields of 25% non-Bt cotton by sowing second-generation (F2) seeds. According to field monitoring results for more than 20 years in China, practical resistance (Bt cotton failure) of target pests was avoided, and there were no cases of Bt (Cry1Ac) failure of pest control in cotton production. This indicated that this Chinese resistance management strategy was very successful. The Chinese government has decided to commercialize Bt corn, which will inevitably reduce the role of natural refuges; therefore, this paper also discusses adjustments and future directions of cotton pest resistance management strategies. Full article
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15 pages, 2777 KiB  
Review
Involvement of an Enhanced Immunity Mechanism in the Resistance to Bacillus thuringiensis in Lepidopteran Pests
by Zeyu Xiao, Xue Yao, Sufen Bai, Jizhen Wei and Shiheng An
Insects 2023, 14(2), 151; https://doi.org/10.3390/insects14020151 - 01 Feb 2023
Cited by 7 | Viewed by 2110
Abstract
Bacillus thuringiensis (Bt) is the safest, economically successful entomopathogen to date. It is extensively produced in transgenic crops or used in spray formulations to control Lepidopteran pests. The most serious threat to the sustainable usage of Bt is insect resistance. The [...] Read more.
Bacillus thuringiensis (Bt) is the safest, economically successful entomopathogen to date. It is extensively produced in transgenic crops or used in spray formulations to control Lepidopteran pests. The most serious threat to the sustainable usage of Bt is insect resistance. The resistance mechanisms to Bt toxins depend not only on alterations in insect receptors, but also on the enhancement of insect immune responses. In this work, we review the current knowledge of the immune response and resistance of insects to Bt formulations and Bt proteins, mainly in Lepidopteran pests. We discuss the pattern recognition proteins for recognizing Bt, antimicrobial peptides (AMPs) and their synthetic signaling pathways, the prophenoloxidase system, reactive oxygen species (ROS) generation, nodulation, encapsulation, phagocytosis, and cell-free aggregates, which are involved in immune response reactions or resistance to Bt. This review also analyzes immune priming, which contributes to the evolution of insect resistance to Bt, and puts forward strategies to improve the insecticidal activity of Bt formulations and manage insect resistance, targeting the insect immune responses and resistance. Full article
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