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Resistance to Insect-Killing Proteins from the Bacillus thuringiensis (Bt) Toxins
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Resistance to Insect-Killing Proteins from the Bacillus thuringiensis (Bt) Toxins

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

Deadline for manuscript submissions: closed (31 January 2024) | Viewed by 10937

Special Issue Editor

Dr. Jiangjiang Gu

E-Mail Website
Guest Editor
College of Chemistry, Huazhong Agricultural University, Wuhan 430070, China
Interests: functional nanomaterials; quantum dots; environmental analytical chemistry; plant nanotechnology; agriculture; resistance control of Bt toxins
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

I would like to invite you to contribute to this Special Issue focused on “Resistance to Insect-Killing Proteins from the Bacillus thuringiensis (Bt) Toxins”.

As alternatives to toxic synthetic pesticides, bacterium bacillus thuringiensis (Bt) proteins show specific insecticidal properties for some target pests without influencing non-target organisms. These insect-killing biotoxins can be directly expressed by transgenic plants with incorporated Bt genes, which have been successfully applied for pest control in wide crops such as corn, rice, cotton, and soybean. However, one of them has been recently reported to potentially threaten the development of field resistance and will decrease the efficacy of Bt toxins to insects over time. It is vital to use various biochemical and molecular techniques to study resistance mechanisms, contributing factors, and physiological processes, including identifying the resistance genes and related receptor proteins, deciphering the protein-binding sites, and investigating the insect microbial communities. Furthermore, effective monitoring methods and resistance management strategies should be developed for delaying the resistance evolution to Bt proteins, which can help the sustainable utilization of Bt crop biotechnology.

The types of Original Research, Communication, Review, and Mini Review articles are welcome.

Dr. Jiangjiang Gu
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a double-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Toxins is an international peer-reviewed open access monthly journal published by MDPI.

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

  • Bacillus thuringiensis (Bt) proteins
  • transgenic plants
  • resistance mechanism
  • physiological process
  • monitoring method
  • resistance-management strategy

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Published Papers (5 papers)

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Research

13 pages, 2648 KiB  
Article
Insecticidal Effects of Transgenic Maize Bt-Cry1Ab, Bt-Vip3Aa, and Bt-Cry1Ab+Vip3Aa against the Oriental Armyworm, Mythimna separata (Walker) in Southwest China
by Zhenghao Zhang, Xianming Yang, Wenhui Wang and Kongming Wu
Toxins 2024, 16(3), 134; https://doi.org/10.3390/toxins16030134 - 4 Mar 2024
Cited by 5 | Viewed by 2089
Abstract
The oriental armyworm, Mythimna separata (Walker), an important migratory pest of maize and wheat, is posing a severe threat to maize production in Asian countries. As source areas of spring–summer emigratory populations, the control of M. separata in southwestern China is of great [...] Read more.
The oriental armyworm, Mythimna separata (Walker), an important migratory pest of maize and wheat, is posing a severe threat to maize production in Asian countries. As source areas of spring–summer emigratory populations, the control of M. separata in southwestern China is of great significance for East Asian maize production. To assess the toxicity of Bt maize against the pest, bioassays of Bt-(Cry1Ab+Vip3Aa) maize (event DBN3601T), Bt-Cry1Ab maize (event DBN9936), and Bt-Vip3Aa maize (event DBN9501) were conducted in Yunnan province of southwest China. There were significant differences in insecticidal activity between the three Bt maize events, and DBN3601T presented the highest insecticidal role. The results also indicated that the insecticidal effect of various Bt maize tissues took an order in leaf > kernel > silk, which is highly consistent with the expression amounts of Bt insecticidal protein in leaf (69.69 ± 1.18 μg/g), kernel (11.69 ± 0.75 μg/g), and silk (7.32 ± 0.31 μg/g). In field trials, all larval population densities, plant damage rates, and leaf damage levels of DBN3601T maize were significantly lower than the conventional maize. This research indicated that the DBN3601T event had a high control efficiency against M. separata and could be deployed in southwest China for the management of M. separata. Full article
(This article belongs to the Special Issue Resistance to Insect-Killing Proteins from the Bacillus thuringiensis (Bt) Toxins)
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13 pages, 591 KiB  
Article
Toxic Effects of Bt-(Cry1Ab+Vip3Aa) Maize on Storage Pest Paralipsa gularis (Zeller)
by Shuang Chen, Wenhui Wang, Guodong Kang, Xianming Yang and Kongming Wu
Toxins 2024, 16(2), 92; https://doi.org/10.3390/toxins16020092 - 7 Feb 2024
Cited by 2 | Viewed by 1630
Abstract
Paralipsa gularis (Zeller) is a storage pest; however, in recent years it has evolved into a considerable maize pest during the late growth stage in the border region between China and other Southeast Asian countries. Bt transgenic insect-resistant maize is an effective measure [...] Read more.
Paralipsa gularis (Zeller) is a storage pest; however, in recent years it has evolved into a considerable maize pest during the late growth stage in the border region between China and other Southeast Asian countries. Bt transgenic insect-resistant maize is an effective measure in controlling a wide range of lepidopteran pests, but there is a lack of research on the toxic effects of storage pests. We tested the toxicity of Bt-Cry1Ab, Vip3Aa, and their complex proteins against P. gularis via bioassay and investigated the efficiency of Bt-(Cry1Ab+Vip3Aa) maize in controlling P. gularis during the late growth stage of maize in the period 2022–2023. The bioassay results show that the susceptibilities of P. gularis to the two Bt proteins and their complex proteins were significantly different. The LC50 values of DBNCry1Ab (“DBN9936” event), DBNVip3Aa (“DBN9501” event), DBN Cry1Ab+Vip3Aa (“DBN3601T” event), and Syngenta Cry1Ab+Vip3Aa (“Bt11” event × “MIR162” event) were 0.038 μg/g, 0.114 μg/g, 0.110 μg/g, and 0.147 μg/g, and the GIC50 values were 0.014 μg/g, 0.073 μg/g, 0.027 μg/g, and 0.026 μg/g, respectively. Determination of the expression content of the insecticidal protein in different tissues of Bt-(Cry1Ab+Vip3Aa) maize shows that the total Bt protein content in different tissues was in the following order: stalk > bract > cob > kernel. However, the bioassay results show that the mortalities of P. gularis feeding on Bt-(Cry1Ab+Vip3Aa) maize in different tissues at different growth stages were all above 93.00%. The field trial indicates that the occurrence density of larvae and plant damage rate for conventional maize were 422.10 individuals/100 plants and 94.40%, respectively, whereas no larvae were found on Bt-(Cry1Ab+Vip3Aa) maize. In summary, this study implies that Bt-(Cry1Ab+Vip3Aa) maize has a high potential for control of P. gularis, providing a new technical measure for the management of the pest. Full article
(This article belongs to the Special Issue Resistance to Insect-Killing Proteins from the Bacillus thuringiensis (Bt) Toxins)
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16 pages, 2505 KiB  
Article
An Extended Investigation of Unexpected Helicoverpa zea (Boddie) Survival and Ear Injury on a Transgenic Maize Hybrid Expressing Cry1A/Cry2A/Vip3A Toxins
by Fangneng Huang, Ying Niu, Tiago Silva, Sebe Brown, Tyler Towles, Dawson Kerns, Juan Luis Jurat-Fuentes, Graham P. Head, Matthew Carroll, Wade Walker and Shucong Lin
Toxins 2023, 15(7), 474; https://doi.org/10.3390/toxins15070474 - 22 Jul 2023
Cited by 4 | Viewed by 1613
Abstract
The wide occurrence of resistance to Cry1A and Cry2A insecticidal toxins from Bacillus thuringiensis (Bt) in the corn earworm/bollworm Helicoverpa zea (Boddie) leaves the Vip3A toxin produced during the vegetative stage of Bt as the only fully active toxin expressed in [...] Read more.
The wide occurrence of resistance to Cry1A and Cry2A insecticidal toxins from Bacillus thuringiensis (Bt) in the corn earworm/bollworm Helicoverpa zea (Boddie) leaves the Vip3A toxin produced during the vegetative stage of Bt as the only fully active toxin expressed in transgenic crops to control H. zea in the U.S.A. During 2021, the first unexpected survival of H. zea and injury (UXI) on a maize hybrid expressing Cry1A.105, Cry2Ab2, and Vip3Aa in Louisiana, U.S.A. were observed in two sentinel plots used for resistance monitoring. A follow-up intensive investigation was conducted with two H. zea populations established from larvae collected from the two UXI plots. The main goal of this study was to reveal if the unexpected damage was due to resistance development in the insect to the Bt toxins expressed in the maize hybrid. Diet-overlay bioassays showed that the two populations were highly resistant to Cry1A.105, moderately resistant to Cry2Ab2, but still highly susceptible to Vip3Aa when compared to a reference susceptible strain. In 10 d assays with detached ears, the larvae of the two UXI populations exhibited survival on ears expressing only Cry toxins but presented near 100% mortality on maize hybrids containing both cry and vip3A transgenes. Multiple field trials over three years demonstrated that natural H. zea populations in Louisiana were highly resistant to maize expressing only Cry toxins but remained susceptible to all tested hybrids containing cry and vip3A genes. Altogether, the results of this study suggest that the observed UXIs in Louisiana were associated with a resistance to Cry toxins but were not due to a resistance to Vip3A. The possible causes of the UXIs are discussed. The results generated and procedures adopted in this study help in determining thresholds for defining UXIs, assessing resistance risks, and documenting field resistance. Full article
(This article belongs to the Special Issue Resistance to Insect-Killing Proteins from the Bacillus thuringiensis (Bt) Toxins)
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9 pages, 933 KiB  
Communication
Transgenic Drosophila to Functionally Validate Fall Armyworm ABCC2 Mutations Conferring Bt Resistance
by Rafaela Panteleri, Amalia Anthousi, Shane Denecke, Debora Boaventura, Ralf Nauen and John Vontas
Toxins 2023, 15(6), 386; https://doi.org/10.3390/toxins15060386 - 7 Jun 2023
Cited by 2 | Viewed by 2545
Abstract
The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith; Lepidoptera: Noctuidae) is an invasive agricultural pest with a global distribution, causing major crop losses annually. Its control strategies largely rely on chemical insecticides and transgenic crops expressing Bacillus thuringiensis insecticidal proteins (Cry and Vip [...] Read more.
The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith; Lepidoptera: Noctuidae) is an invasive agricultural pest with a global distribution, causing major crop losses annually. Its control strategies largely rely on chemical insecticides and transgenic crops expressing Bacillus thuringiensis insecticidal proteins (Cry and Vip toxins); however, the development of high resistance poses a significant issue. The ATP-binding cassette transporter C2 (ABCC2) has been linked to Cry toxin pore formation, acting as a receptor of some Cry toxins. Recently detected mutations in the SfABCC2 gene in extracellular loop 4 (ECL4) have been associated with Bt toxin resistance in FAW. In the present study, we expressed the SfABCC2 gene in Drosophila melanogaster, a species normally unaffected by the Bt toxins. We demonstrate that susceptibility can be introduced by the ectopic and tissue-specific expression of wildtype SfABCC2. Next, we introduced mutations into ECL4—both individually and in combination—that have been recently described in Brazilian FAW and functionally validated by toxicity bioassays against the foliar Bt product Xentari. Our results provide an efficient demonstration of the suitability of transgenic Drosophila for validating FAW ABCC2 resistance mutations in ECL4 against Bt toxins, and potential cross-resistance issues between closely related proteins that use ABCC2. Full article
(This article belongs to the Special Issue Resistance to Insect-Killing Proteins from the Bacillus thuringiensis (Bt) Toxins)
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Graphical abstract

11 pages, 1483 KiB  
Article
Seven Years of Monitoring Susceptibility to Cry1Ab and Cry1F in Asian Corn Borer
by Yueqin Wang, Wenlu Zhao, Shuang Han, Lianxia Wang, Xue Chang, Kaiqiang Liu, Yudong Quan, Zhenying Wang and Kanglai He
Toxins 2023, 15(2), 137; https://doi.org/10.3390/toxins15020137 - 7 Feb 2023
Cited by 8 | Viewed by 1803
Abstract
Resistance monitoring in the Asian corn borer, Ostrinia furnacalis, is necessary to accommodate the commercial introduction and stewardship of Bt maize in China. The susceptibility of 56 O. furnacalis field populations, collected between 2015 and 2021 from the corn belt regions of [...] Read more.
Resistance monitoring in the Asian corn borer, Ostrinia furnacalis, is necessary to accommodate the commercial introduction and stewardship of Bt maize in China. The susceptibility of 56 O. furnacalis field populations, collected between 2015 and 2021 from the corn belt regions of China, to Cry1Ab and Cry1F toxins was determined. Neonate larvae (within 12 h after hatching) were placed on the surface of semi-artificial agar-free diet incorporating a series of concentrations of purified toxins, and mortality was evaluated after 7d. The median lethal concentration (LC50) values of Cry1Ab and Cry1F were 0.05 to 0.37 µg/g (protein/diet) and 0.10 to 1.22 µg/g, respectively. Although interpopulation variation in susceptibility to the toxins was observed, the magnitude of the differences was 5.8-fold and 8.3-fold for Cry1Ab and Cry1F, respectively. These results suggested that the observed susceptibility differences reflect natural geographical variation in response and not variation caused by prior exposure to selection pressures. Therefore, the O. furnacalis populations were apparently still susceptible to Cry1Ab and Cry1F across their range within China. The monitoring data established here will serve as a comparative reference for early warning signs of field-evolved resistance after the cultivation of Bt maize in China. Full article
(This article belongs to the Special Issue Resistance to Insect-Killing Proteins from the Bacillus thuringiensis (Bt) Toxins)
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