Investigation of Cry3Bb1 resistance and intoxication in western corn rootworm by RNA sequencing

Rault, Leslie C.; Siegfried, Blair D.; Gassmann, Aaron J.; Wang, Haichuan; Brewer, Gary J.; Miller, Nicholas J.

doi:10.1111/jen.12502

Cited by 12 publications

(18 citation statements)

References 104 publications

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“…Contreras et al (2013) found a type of cadherinlike Cry3Aa receptor in Tribolium Castanea (Coleoptera: Tenebrionidae) and confirmed through gene silencing that the cadherin-like protein was a representative Cry receptor. In this study, one CAD gene was downregulated in A vs. CK, which was similar to the response of western corn root worm to Cry3Bb1 (Rault et al, 2018), which may be related to the pore formation model. Both APN and ALP are glycosylphosphatidylinositol (GPI)-anchored proteins, which play a role in the process of membrane insertion and pore formation.…”

Section: Transcriptional Response Of a Glabripennis Larvae To Bt Toxinsupporting

confidence: 68%

Exogenous Gene Expression and Insect Resistance in Dual Bt Toxin Populus × euramericana ‘Neva’ Transgenic Plants

et al. 2021

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Bacillus thuringiensis (Bt) insecticidal protein genes are important tools in efforts to develop insect resistance in poplar. In this study, the Cry1Ac and Cry3A Bt toxin genes were simultaneously transformed into the poplar variety Populus × euramericana ‘Neva’ by Agrobacterium-mediated transformation to explore the exogenous gene expression and insect resistance, and to examine the effects of Bt toxin on the growth and development of Anoplophora glabripennis larvae after feeding on the transgenic plant. Integration and expression of the transgenes were determined by molecular analyses and the insect resistance of transgenic lines was evaluated in feeding experiments. Sixteen transgenic dual Bt toxin genes Populus × euramericana ‘Neva’ lines were obtained. The dual Bt toxin genes were expressed at both the transcriptional and translational levels; however, Cry3A protein levels were much higher than those of Cry1Ac. Some of the transgenic lines exhibited high resistance to the first instar larvae of Hyphantria cunea and Micromelalopha troglodyta, and the first and second instar larvae and adults of Plagiodera versicolora. Six transgenic lines inhibited the growth and development of A. glabripennis larvae. The differences in the transcriptomes of A. glabripennis larvae fed transgenic lines or non-transgenic control by RNA-seq analyses were determined to reveal the mechanism by which Bt toxin regulates the growth and development of longicorn beetle larvae. The expression of genes related to Bt prototoxin activation, digestive enzymes, binding receptors, and detoxification and protective enzymes showed significant changes in A. glabripennis larvae fed Bt toxin, indicating that the larvae responded by regulating the expression of genes related to their growth and development. This study lay a theoretical foundation for developing resistance to A. glabripennis in poplar, and provide a foundation for exploring the mechanism of Bt toxin action on Cerambycidae insects.

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Section: Transcriptional Response Of a Glabripennis Larvae To Bt Toxinsupporting

confidence: 68%

Exogenous Gene Expression and Insect Resistance in Dual Bt Toxin Populus × euramericana ‘Neva’ Transgenic Plants

et al. 2021

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“…Several protein families including the ATP-binding cassette (ABC) transporters, cadherin, aminopeptidase N (APN), and alkaline phosphatase (ALP) have been identified as receptors of Cry toxins in Lepidoptera where more extensive studies were performed 36,37 . Interestingly, some of these protein classes are differentially expressed in Cry3-resistant WCR or WCR treated with Bt toxins (Cry34/35Ab1, Cry3Bb1, or eCry3.1Ab) 35,38,39 but have yet to be validated as functional receptors.…”

Section: Western Corn Rootworm (Wcr) Diabrotica Virgifera Virgifera mentioning

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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“… Ingber and Gassmann (2015 ) found differences between Hopkinton and Cresco in the life-history traits displaying fitness costs, the inheritance of resistance, and the magnitude of resistance, and it also appears that these strains differ in the extent to which ecological conditions may affect the manifestation of fitness costs. Furthermore, a recent study examining gene expression showed that Cry3Bb1 does not elicit a stress response in Hopkinton, further demonstrating that resistance in this strain is robust ( Rault et al 2018 ). This may also partially explain why Cresco was affected by differing larval densities, while Hopkinton was not.…”

Section: Discussionmentioning

confidence: 97%

Applying a Selection Experiment to Test for Fitness Costs of Bt Resistance in Western Corn Rootworm (Coleoptera: Chrysomelidae) and the Effect of Density on Fitness Costs

Clair

Clifton

Dunbar

et al. 2020

Journal of Economic Entomology

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Western corn rootworm, Diabrotica virgifera virgifera LeConte, is a serious pest of corn and is often managed with transgenic corn producing insecticidal toxins from the bacterium Bacillus thuringiensis (Bt). This pest has developed field-evolved resistance to all commercially available Bt traits, beginning with Cry3Bb1 in 2009. Fitness costs may accompany Bt resistance, where individuals with alleles for Bt resistance have reduced fitness on non-Bt corn compared to Bt-susceptible individuals. In conjunction with non-Bt refuges, fitness costs can delay the evolution of Bt resistance. Importantly, ecological factors may affect the presence and magnitude of fitness costs. For western corn rootworm, available data suggest that fitness costs of Bt resistance may be present in some cases. Using two Cry3Bb1-resistant western corn rootworm strains (Hopkinton and Cresco), a fitness-cost experiment was performed by rearing rootworm in the absence of Bt for six generations to test for fitness costs of Cry3Bb1 resistance and the effect of larval rearing density on fitness costs. Fitness costs were detected for both strains; however, strains were still resistant to Cry3Bb1 corn at the end of the experiment. Cresco experienced a greater loss of resistance at low versus high density, but no effect of density was detected in Hopkinton. Our study shows that fitness costs can accompany Bt resistance in western corn rootworm and may be more pronounced under low larval density. Even though fitness costs were present, it appears that rootworm populations may remain resistant to Cry3Bb1 corn for years after resistance has evolved.

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Investigation of Cry3Bb1 resistance and intoxication in western corn rootworm by RNA sequencing

Cited by 12 publications

References 104 publications

Exogenous Gene Expression and Insect Resistance in Dual Bt Toxin Populus × euramericana ‘Neva’ Transgenic Plants

Exogenous Gene Expression and Insect Resistance in Dual Bt Toxin Populus × euramericana ‘Neva’ Transgenic Plants

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

Applying a Selection Experiment to Test for Fitness Costs of Bt Resistance in Western Corn Rootworm (Coleoptera: Chrysomelidae) and the Effect of Density on Fitness Costs

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