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Toxins
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Insect Resistance to Bacillus thuringiensis Toxins
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Insect Resistance to Bacillus thuringiensis Toxins

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Bacterial Toxins".

Deadline for manuscript submissions: closed (30 November 2021) | Viewed by 16779

Special Issue Editor

Prof. Dr. Yidong Wu

E-Mail Website
Guest Editor
Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
Interests: Bacillus thuringiensis; Bacillus thuringiensis toxins; Bt resistance; CRISPR/Cas9,and P450s and xenobiotic metabolism in lepidopteran pests

Special Issue Information

Dear Colleagues, 

The insecticidal toxins (Cry and VIP proteins) produced by the bacterium Bacillus thuringiensis (Bt) have been successfully used to control some major insect pests via both Bt formulation sprays and transgenic crops. The global planting area of Bt crops increased from 1 million hectares in 1996 to 108 million hectares in 2019. However, practical resistance to Bt crops has been reported in at least nine major pest insects. The evolution of resistance to Bt toxins by target pests has been a major threat to the long-term effectiveness of Bt crops. Understanding the evolution and mechanism of Bt resistance is essential for developing sensitive resistance detection methods and adaptive resistance management strategies.

The aim of this Special Issue is to create a collection of recent advances in all aspects of insect resistance to Bt toxins, including detection and monitoring of Bt resistance, genetics and mechanisms of Bt resistance, mode of action of Bt toxins, and resistance management strategies. Both original research and review articles are welcomed.

Prof. Dr. Yidong Wu
Guest Editor

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Bt crops
  • Resistance detection
  • Resistance mechanism
  • Resistance management
  • Cry proteins
  • VIP proteins
  • Mode of action
  • Bt receptors

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Published Papers (5 papers)

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12 pages, 1788 KiB  
Article
An Integrative Analysis of Transcriptomics and Proteomics Reveals Novel Insights into the Response in the Midgut of Spodoptera frugiperda Larvae to Vip3Aa
by Minghui Jin, Yinxue Shan, Yan Peng, Ping Wang, Qi Li, Songmiao Yu, Lei Zhang and Yutao Xiao
Toxins 2022, 14(1), 55; https://doi.org/10.3390/toxins14010055 - 13 Jan 2022
Cited by 11 | Viewed by 2965
Abstract
The insecticidal Vip3 proteins, secreted by Bacillus thuringiensis (Bt) during its vegetative growth phase, are currently used in Bt crops to control insect pests, and are genetically distinct from known insecticidal Cry proteins. Compared with Cry toxins, the mechanisms of Vip3 [...] Read more.
The insecticidal Vip3 proteins, secreted by Bacillus thuringiensis (Bt) during its vegetative growth phase, are currently used in Bt crops to control insect pests, and are genetically distinct from known insecticidal Cry proteins. Compared with Cry toxins, the mechanisms of Vip3 toxins are still poorly understood. Here, the responses of Spodoptera frugiperda larvae after Vip3Aa challenge are characterized. Using an integrative analysis of transcriptomics and proteomics, we found that Vip3Aa has enormous implications for various pathways. The downregulated genes and proteins were mainly enriched in metabolic pathways, including the insect hormone synthesis pathway, whereas the upregulated genes and proteins were mainly involved in the caspase-mediated apoptosis pathway, along with the MAPK signaling and endocytosis pathways. Moreover, we also identified some important candidate genes involved in apoptosis and MAPKs. The present study shows that exposure of S. frugiperda larvae to Vip3Aa activates apoptosis pathways, leading to cell death. The results will promote our understanding of the host response process to the Vip3Aa, and help us to better understand the mode of action of Vip3A toxins. Full article
(This article belongs to the Special Issue Insect Resistance to Bacillus thuringiensis Toxins)
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10 pages, 1351 KiB  
Article
Alteration of a Cry1A Shared Binding Site in a Cry1Ab-Selected Colony of Ostrinia furnacalis
by Daniel Pinos, Yueqin Wang, Patricia Hernández-Martínez, Kanglai He and Juan Ferré
Toxins 2022, 14(1), 32; https://doi.org/10.3390/toxins14010032 - 2 Jan 2022
Cited by 4 | Viewed by 1930
Abstract
The Asian corn borer, Ostrinia furnacalis (Guenée, 1854), is a highly damaging pest in Asia and the Pacific islands, and larvae feed mainly from corn crops. To determine the suitability of Bt-corn technology for the future control of this pest, understanding the potential [...] Read more.
The Asian corn borer, Ostrinia furnacalis (Guenée, 1854), is a highly damaging pest in Asia and the Pacific islands, and larvae feed mainly from corn crops. To determine the suitability of Bt-corn technology for the future control of this pest, understanding the potential to develop resistance to Cry1Ab and the basis of cross-resistance to other Cry1 proteins is of great interest. Here, we have explored the binding of Cry1A proteins to brush border membrane vesicles from two O. furnacalis colonies, one susceptible (ACB-BtS) and one laboratory-selected with Cry1Ab (ACB-AbR). The insects developed resistance to Cry1Ab and showed cross-resistance to Cry1Aa, Cry1Ac, and Cry1F. Binding assays with radiolabeled Cry1Ab and brush border membrane vesicles from susceptible insects showed that Cry1A proteins shared binding sites, though the results were not conclusive for Cry1F. The results were confirmed using radiolabeled Cry1Aa. The resistant insects showed a reduction of the specific binding of both Cry1Ab and Cry1Aa, suggesting that part of the binding sites were lost or altered. Competition binding assays showed full competition between Cry1Ab and Cry1Aa proteins in the susceptible colony but only partial competition in resistant insects, confirming the alteration of some, but not all, binding sites for these two proteins. The binding site model for Cry1A proteins in O. furnacalis is in agreement with the occurrence of multiple membrane receptors for these proteins. Full article
(This article belongs to the Special Issue Insect Resistance to Bacillus thuringiensis Toxins)
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14 pages, 1866 KiB  
Article
Cadherin Protein Is Involved in the Action of Bacillus thuringiensis Cry1Ac Toxin in Ostrinia furnacalis
by Wenzhong Jin, Yuqian Zhai, Yihua Yang, Yidong Wu and Xingliang Wang
Toxins 2021, 13(9), 658; https://doi.org/10.3390/toxins13090658 - 15 Sep 2021
Cited by 12 | Viewed by 2803
Abstract
Transgenic crops expressing Bacillus thuringiensis (Bt) insecticidal proteins have been extensively planted for insect pest control, but the evolution of Bt resistance in target pests threatens the sustainability of this approach. Mutations of cadherin in the midgut brush border membrane was associated with [...] Read more.
Transgenic crops expressing Bacillus thuringiensis (Bt) insecticidal proteins have been extensively planted for insect pest control, but the evolution of Bt resistance in target pests threatens the sustainability of this approach. Mutations of cadherin in the midgut brush border membrane was associated with Cry1Ac resistance in several lepidoptera species, including the Asian corn borer, Ostrinia furnacalis, a major pest of maize in Asian–Western Pacific countries. However, the causality of O. furnacalis cadherin (OfCad) with Cry1Ac resistance remains to be clarified. In this study, in vitro and in vivo approaches were employed to examine the involvement of OfCad in mediating Cry1Ac toxicity. Sf9 cells transfected with OfCad showed significant immunofluorescent binding with Cry1Ac toxin and exhibited a concentration-dependent mortality effect when exposed to Cry1Ac. The OfCad knockout strain OfCad-KO, bearing homozygous 15.4 kb deletion of the OfCad gene generated by CRISPR/Cas9 mutagenesis, exhibited moderate-level resistance to Cry1Ac (14-fold) and low-level resistance to Cry1Aa (4.6-fold), but no significant changes in susceptibility to Cry1Ab and Cry1Fa, compared with the original NJ-S strain. The Cry1Ac resistance phenotype was inherited as autosomal, recessive mode, and significantly linked with the OfCad knockout in the OfCad-KO strain. These results demonstrate that the OfCad protein is a functional receptor for Cry1Ac, and disruption of OfCad confers a moderate Cry1Ac resistance in O. furnacalis. This study provides new insights into the mode of action of the Cry1Ac toxin and useful information for designing resistance monitoring and management strategies for O. furnacalis. Full article
(This article belongs to the Special Issue Insect Resistance to Bacillus thuringiensis Toxins)
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16 pages, 705 KiB  
Article
Early Warning of Resistance to Bt Toxin Vip3Aa in Helicoverpa zea
by Fei Yang, David L. Kerns, Nathan S. Little, José C. Santiago González and Bruce E. Tabashnik
Toxins 2021, 13(9), 618; https://doi.org/10.3390/toxins13090618 - 2 Sep 2021
Cited by 37 | Viewed by 4372
Abstract
Evolution of resistance by pests can reduce the benefits of crops genetically engineered to produce insecticidal proteins from Bacillus thuringiensis (Bt). Because of the widespread resistance of Helicoverpa zea to crystalline (Cry) Bt toxins in the United States, the vegetative insecticidal protein Vip3Aa [...] Read more.
Evolution of resistance by pests can reduce the benefits of crops genetically engineered to produce insecticidal proteins from Bacillus thuringiensis (Bt). Because of the widespread resistance of Helicoverpa zea to crystalline (Cry) Bt toxins in the United States, the vegetative insecticidal protein Vip3Aa is the only Bt toxin produced by Bt corn and cotton that remains effective against some populations of this polyphagous lepidopteran pest. Here we evaluated H. zea resistance to Vip3Aa using diet bioassays to test 42,218 larvae from three lab strains and 71 strains derived from the field during 2016 to 2020 in Arkansas, Louisiana, Mississippi, Tennessee, and Texas. Relative to the least susceptible of the three lab strains tested (BZ), susceptibility to Vip3Aa of the field-derived strains decreased significantly from 2016 to 2020. Relative to another lab strain (TM), 7 of 16 strains derived from the field in 2019 were significantly resistant to Vip3Aa, with up to 13-fold resistance. Susceptibility to Vip3Aa was significantly lower for strains derived from Vip3Aa plants than non-Vip3Aa plants, providing direct evidence of resistance evolving in response to selection by Vip3Aa plants in the field. Together with previously reported data, the results here convey an early warning of field-evolved resistance to Vip3Aa in H. zea that supports calls for urgent action to preserve the efficacy of this toxin. Full article
(This article belongs to the Special Issue Insect Resistance to Bacillus thuringiensis Toxins)
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11 pages, 1087 KiB  
Brief Report
Recombinant Expression of ABCC2 Variants Confirms the Importance of Mutations in Extracellular Loop 4 for Cry1F Resistance in Fall Armyworm
by Laura Franz, Klaus Raming and Ralf Nauen
Toxins 2022, 14(2), 157; https://doi.org/10.3390/toxins14020157 - 21 Feb 2022
Cited by 15 | Viewed by 3742
Abstract
Fall armyworm (FAW), Spodoptera frugiperda, is a highly destructive and invasive global noctuid pest. Its control is based on insecticide applications and Bacillus thuringiensis (Bt) insecticidal Cry toxins expressed in transgenic crops, such as Cry1F in Bt corn. Continuous selection pressure has [...] Read more.
Fall armyworm (FAW), Spodoptera frugiperda, is a highly destructive and invasive global noctuid pest. Its control is based on insecticide applications and Bacillus thuringiensis (Bt) insecticidal Cry toxins expressed in transgenic crops, such as Cry1F in Bt corn. Continuous selection pressure has resulted in populations that are resistant to Bt corn, particularly in Brazil. FAW resistance to Cry1F was recently shown to be conferred by mutations of ATP-binding cassette transporter C2 (ABCC2), but several mutations, particularly indels in extracellular loop 4 (ECL4), are not yet functionally validated. We addressed this knowledge gap by baculovirus-free insect cell expression of ABCC2 variants (and ABCC3) by electroporation technology and tested their response to Cry1F, Cry1A.105 and Cry1Ab. We employed a SYTOXTM orange cell viability test measuring ABCC2-mediated Bt toxin pore formation. In total, we tested seven different FAW ABCC2 variants mutated in ECL4, two mutants modified in nucleotide binding domain (NBD) 2, including a deletion mutant lacking NBD2, and S. frugiperda ABCC3. All tested ECL4 mutations conferred high resistance to Cry1F, but much less to Cry1A.105 and Cry1Ab, whereas mutations in NBD2 hardly affected Bt toxin activity. Our study confirms the importance of indels in ECL4 for Cry1F resistance in S. frugiperda ABCC2. Full article
(This article belongs to the Special Issue Insect Resistance to Bacillus thuringiensis Toxins)
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