A single amino acid polymorphism in ABCC2 loop 1 is responsible for differential toxicity of Bacillus thuringiensis Cry1Ac toxin in different Spodoptera (Noctuidae) species

Liu, Leilei; Chen, Zuwen; Yang, Yuanxiao; Xiao, Yutao; Liu, Chenxi; Ma, Ye; Soberón, Mário; Bravo, Alejandra; Yang, Yong; Liu, Kaiyu

doi:10.1016/j.ibmb.2018.06.004

Cited by 37 publications

(24 citation statements)

References 33 publications

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“…Silva et al (2016) in studies of effects on the biology of insect pests did not observe adverse effects on the development and reproduction of S. cosmioides. Similar studies within the same genus; Liu et al (2018) mentioned that S. litura and S. frugiperda; belonging to the same genus; however, S. litura is tolerant to Cry1Ac, while S. frugiperda is susceptible. Murua et al 2018reported that S. eridania and S. cosmioides were not susceptible to Cry1 Ac protein in soybean MON 87701-2 × MON 89788-1 in greenhouse evaluations.…”

Section: Introductionsupporting

confidence: 61%

Toxicity of the Bt Protein Cry1Ac Expressed in Leaves of the Event of Transgenic Soybean Released in Paraguay Against Spodoptera cosmioides

Sosa¹,

Gómez²,

Ramírez³

et al. 2020

JAS

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Spodoptera cosmioides Walk (Lepidoptera: Noctuidae) is a polyphagous species, considered a secondary pest in soybean crop. The Intacta soybean (Bt soybean) event was released in Paraguay with Bt proteins which are supposed to be toxic for caterpillars. However, the effects of these proteins in the Spodoptera cosmioides biology still uncertainty. This study evaluated the biological activity of Bt soybean in S. cosmioides that were fed on Bt and non-Bt soybean leaves under laboratory conditions. The experiment was carried out at the Laboratory of Entomology; temperature 26±2 ºC; relative humidity: 60±10%; photoperiod: 14:00 h where 150 neonate larvae were used per treatment. The period and viability of each stage, the mortality of larval, number of eggs and neonate per couple, and the period of larvae to adult were the assessed variables. Higher mortality was observed in larvae fed with intact soybeans, but without statistical differences with non-Bt soybeans. For larval survival, period, number and total period, no statistical differences were verified. Higher percentage of fertility was observed in soybeans non-Bt but no statistical differences.

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Section: Introductionsupporting

confidence: 61%

Toxicity of the Bt Protein Cry1Ac Expressed in Leaves of the Event of Transgenic Soybean Released in Paraguay Against Spodoptera cosmioides

Sosa¹,

Gómez²,

Ramírez³

et al. 2020

JAS

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“…mori , the extracellular loop 1 (ECL1) in BmABCC2/3 transporters determines receptor specificity for Cry1A toxins [ 33 ]. The loop 1 Q125 residue of SfABCC2 is also the key factor for the high toxicity of Cry1Ac to Hi5 cells expressing this protein [ 34 ]. Structure-based evidence therefore is necessary to further verify the roles of ECL1 in determining the specificity of PxABCC2 and PxABCC3 for Cry1Ac toxicity, and to better address their potential synergism in terms of functional complementation or redundancy.…”

Section: Discussionmentioning

confidence: 99%

Resistance to Bacillus thuringiensis Cry1Ac toxin requires mutations in two Plutella xylostella ATP-binding cassette transporter paralogs

Xiang

et al. 2020

PLoS Pathog

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The diamondback moth, Plutella xylostella, is a cosmopolitan pest and the first species to develop field resistance to toxins from the gram-positive bacterium Bacillus thuringiensis (Bt). Although previous work has suggested that mutations of ATP-binding cassette transporter subfamily C2 (ABCC2) or C3 (ABCC3) genes can confer Cry1Ac resistance, here we reveal that P. xylostella requires combined mutations in both PxABCC2 and PxABCC3 to achieve high-level Cry1Ac resistance, rather than simply a mutation of either gene. We identified natural mutations of PxABCC2 and PxABCC3 that concurrently occurred in a Cry1Acresistant strain (Cry1S1000) of P. xylostella, with a mutation (R A2) causing the mis-splicing of PxABCC2 and another mutation (R A3) leading to the premature termination of PxABCC3. Genetic linkage analysis showed that R A2 and R A3 were tightly linked to Cry1Ac resistance. Introgression of R A2 and R A3 enabled a susceptible strain (G88) of P. xylostella to obtain high resistance to Cry1Ac, confirming that these genes confer resistance. To further support the role of PxABCC2 and PxABCC3 in Cry1Ac resistance, frameshift mutations were introduced into PxABCC2 and PxABCC3 singly and in combination in the G88 strain with CRISPR/Cas9 mediated mutagenesis. Bioassays of CRISPR-based mutant strains, plus genetic complementation tests, demonstrated that the deletion of PxABCC2 or PxABCC3 alone provided < 4-fold tolerance to Cry1Ac, while disruption of both genes together conferred >8,000-fold resistance to Cry1Ac, suggesting the redundant/complementary roles of PxABCC2 and PxABCC3. This work advances our understanding of Bt resistance in P. xylostella by demonstrating mutations within both PxABCC2 and PxABCC3 genes are required for high-level Cry1Ac resistance.

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“…Furthermore, while ABCC2 proteins have been identified as Cry1 toxin receptors in Lepidoptera, extracellular loops 1 and 4 (ECL1 and ECL4) have been shown to be important for selective binding 37 . The importance of ECL1 to binding was demonstrated by a single amino acid polymorphism (Q 125 vs. E 125 ) identified to be responsible for differential toxicity of Cry1Ac against Spodoptera litura (highly sensitive) compared to Spodopter a frugiperda (less sensitive) where the sequence alignment of amino acids between two ABCC2 proteins have 97% identity 59 . Greater sequence homology is observed in ECL1 and ECL4 between CtABCB1 and DvABCB1 than between the loops of either of them when compared to those of DvABCB2 (Supplementary Fig.…”

Section: Discussionmentioning

confidence: 99%

Functional validation of DvABCB1 as a receptor of Cry3 toxins in western corn rootworm, Diabrotica virgifera virgifera

Niu

Kassa

Hasler

et al. 2020

Sci Rep

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Western corn rootworm (WCR), Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae), is a serious insect pest in the major corn growing areas of North America and in parts of Europe. WCR populations with resistance to Bacillus thuringiensis (Bt) toxins utilized in commercial transgenic traits have been reported, raising concerns over their continued efficacy in WCR management. Understanding the modes of action of Bt toxins is important for WCR control and resistance management. Although different classes of proteins have been identified as Bt receptors for lepidopteran insects, identification of receptors in WCR has been limited with no reports of functional validation. Our results demonstrate that heterologous expression of DvABCB1 in Sf9 and HEK293 cells conferred sensitivity to the cytotoxic effects of Cry3A toxins. The result was further validated using knockdown of DvABCB1 by RNAi which rendered WCR larvae insensitive to a Cry3A toxin. However, silencing of DvABCB2 which is highly homologous to DvABCB1 at the amino acid level, did not reduce the sensitivity of WCR larvae to a Cry3A toxin. Furthermore, our functional studies corroborate different mode-of-actions for other insecticidal proteins including Cry34Ab1/35Ab1, Cry6Aa1, and IPD072Aa against WCR. Finally, reduced expression and alternatively spliced transcripts of DvABCB1 were identified in a mCry3A-resistant strain of WCR. Our results provide the first clear demonstration of a functional receptor in the molecular mechanism of Cry3A toxicity in WCR and confirmed its role in the mechanism of resistance in a mCry3A resistant strain of WCR.

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A single amino acid polymorphism in ABCC2 loop 1 is responsible for differential toxicity of Bacillus thuringiensis Cry1Ac toxin in different Spodoptera (Noctuidae) species

Cited by 37 publications

References 33 publications

Toxicity of the Bt Protein Cry1Ac Expressed in Leaves of the Event of Transgenic Soybean Released in Paraguay Against Spodoptera cosmioides

Toxicity of the Bt Protein Cry1Ac Expressed in Leaves of the Event of Transgenic Soybean Released in Paraguay Against Spodoptera cosmioides

Resistance to Bacillus thuringiensis Cry1Ac toxin requires mutations in two Plutella xylostella ATP-binding cassette transporter paralogs

Functional validation of DvABCB1 as a receptor of Cry3 toxins in western corn rootworm, Diabrotica virgifera virgifera

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