Mutational disruption of the ABCC2 gene in fall armyworm, Spodoptera frugiperda, confers resistance to the Cry1Fa and Cry1A.105 insecticidal proteins

Flagel, Lex; Lee, Young Wha; Wanjugi, Humphrey; Swarup, Shilpa; Brown, Ashley N.; Wang, Jinling; Kraft, Edward; Greenplate, John T.; Simmons, Jeni; Adams, Nancy E.; Wang, Yanfei; Martinelli, Samuel; Haas, Jeffrey A.; Gowda, A. S. Prakasha; Head, Graham P.

doi:10.1038/s41598-018-25491-9

Cited by 85 publications

(113 citation statements)

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“…The characterization of the inheritance of Bt resistance will provide important information for evaluating the risks of evolution of resistance and will make it possible to formulate effective resistance management strategies. Based on previous reports, resistance to Cry1-type toxins mediated by ABCC2 mutations was recessive or incompletely recessive [22][23][24]27,28,30,32,33]. Consistent with these results, both the high-level resistance to Cry1Fa (>300-fold) and low-level resistance to Cry1Ac (~8-fold) were inherited as a recessive mode in the knockout OfC2-KO strain of O. furnacalis.…”

Section: Discussionsupporting

confidence: 86%

“…One of the major mechanisms of resistance to Cry toxin is reduced toxin binding to their specific larval midgut receptors through the disruption of the receptor genes [21]. Since the disruption of the ABC transporter subfamily C2 (ABCC2) gene was first identified to confer Cry1Ac resistance in Heliothis virescens [22], mutations of the homologous ABCC2 genes associated with Cry1A and/or Cry1F resistance have been found in several lepidopteran insects, including Plutella xylostella, Trichoplusia ni [23], Bombyx mori [24], Helicoverpa armigera [25], Spodoptera exigua [26], and Spodoptera frugiperda [27][28][29]. Recently, the CRISPR/Cas9 system has been applied to investigate the in vivo role of insect ABCC2 in the mode of action and resistance mechanisms of Bt toxins.…”

Section: Introductionmentioning

confidence: 99%

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CRISPR-Mediated Knockout of the ABCC2 Gene in Ostrinia furnacalis Confers High-Level Resistance to the Bacillus thuringiensis Cry1Fa Toxin

Wang

Huang

et al. 2020

Toxins

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The adoption of transgenic crops expressing Bacillus thuringiensis (Bt) insecticidal crystalline (Cry) proteins has reduced insecticide application, increased yields, and contributed to food safety worldwide. However, the efficacy of transgenic Bt crops is put at risk by the adaptive resistance evolution of target pests. Previous studies indicate that resistance to Bacillus thuringiensis Cry1A and Cry1F toxins was genetically linked with mutations of ATP-binding cassette (ABC) transporter subfamily C gene ABCC2 in at least seven lepidopteran insects. Several strains selected in the laboratory of the Asian corn borer, Ostrinia furnacalis, a destructive pest of corn in Asian Western Pacific countries, developed high levels of resistance to Cry1A and Cry1F toxins. The causality between the O. furnacalis ABCC2 (OfABCC2) gene and resistance to Cry1A and Cry1F toxins remains unknown. Here, we successfully generated a homozygous strain (OfC2-KO) of O. furnacalis with an 8-bp deletion mutation of ABCC2 by the CRISPR/Cas9 approach. The 8-bp deletion mutation results in a frame shift in the open reading frame of transcripts, which produced a predicted protein truncated in the TM4-TM5 loop region. The knockout strain OfC2-KO showed much more than a 300-fold resistance to Cry1Fa, and low levels of resistance to Cry1Ab and Cry1Ac (<10-fold), but no significant effects on the toxicities of Cry1Aa and two chemical insecticides (abamectin and chlorantraniliprole), compared to the background NJ-S strain. Furthermore, we found that the Cry1Fa resistance was autosomal, recessive, and significantly linked with the 8-bp deletion mutation of OfABCC2 in the OfC2-KO strain. In conclusion, in vivo functional investigation demonstrates the causality of the OfABCC2 truncating mutation with high-level resistance to the Cry1Fa toxin in O. furnacalis. Our results suggest that the OfABCC2 protein might be a functional receptor for Cry1Fa and reinforces the association of this gene to the mode of action of the Cry1Fa toxin.

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Section: Discussionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

CRISPR-Mediated Knockout of the ABCC2 Gene in Ostrinia furnacalis Confers High-Level Resistance to the Bacillus thuringiensis Cry1Fa Toxin

Wang

Huang

et al. 2020

Toxins

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“…Further, the use of highly hazardous pesticides is not considered a sustainable long term control measure for any pest (FAO 2018). In addition, S. frugiperda is known to readily develop resistance to most chemical insecticides (e.g., pyrethroids, organophosphates and carbamates) and to transgenic maize that are used to control it (Yu 1991; Jakka et al 2016; Banerjee et al 2017; Flagel et al 2018; Botha et al 2019). In light of this, there is a great need for alternative, cost-effective control strategies for S. frugiperda (FAO 2018).…”

Section: Introductionmentioning

confidence: 99%

Diversity of fall armyworm, Spodoptera frugiperda and their gut bacterial community in Kenya

Gichuhi

Subramanian

Khamis

et al. 2019

Preprint

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9The invasive fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith) is a polyphagous pest that causes 10 widespread damage particularly to maize and sorghum in Africa. The microbiome associated with S. 11frugiperda could play a role in their success and adaptability. However, these bacterial communities remain 12 poorly studied, especially for S. frugiperda in Africa. We investigated the composition, abundance and 13 diversity of microbiomes associated with larval and adult specimens of S. frugiperda collected from four 14 maize growing regions in Kenya through high throughput sequencing of bacterial 16S rRNA gene. We 15 identified Proteobacteria and Firmicutes as the most dominant phyla and lesser proportions of 16 Bacteroidetes and Actinobacteria. We also observed differences in bacterial microbiome diversity between 17 larvae and adults that are a likely indication that some prominent larval bacterial groups are lost during 18 metamorphosis. Several bacterial groups were found in both adults and larvae suggesting that they are 19 transmitted across developmental stages. Reads corresponding to several known entomopathogenic 20 bacterial clades as well as the non-bacterial entomopathogen, Metarhizium rileyi (Farl.) Kepler, Rehner & 21 Humber (2014), were observed. Mitochondrial DNA haplotyping of the S. frugiperda population in Kenya 22 indicated the presence of both 'Rice' and 'Corn' strains, with a higher prevalence of the 'Rice' strain. Insights 23 into the microbiota may ultimately provide alternative avenues for controlling of this pest.24

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“…In addition, S. frugiperda have been reported to evolve resistance to most chemical insecticides (e.g. pyrethroids, organophosphates and carbamates) (Yu 1991) and to transgenic maize that are used in its control (Jakka et al 2016;Banerjee et al 2017;Flagel et al 2018;Botha et al 2019). As a consequence, there is a great need for alternative, cost-effective control strategies for S. frugiperda (FAO, 2018).…”

Section: Manuscript To Be Reviewedmentioning

confidence: 99%

Peer Review #1 of "Diversity of fall armyworm, Spodoptera frugiperda and their gut bacterial community in Kenya (v0.1)"

2020

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Background The invasive fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith) is a polyphagous pest that causes widespread damage particularly to maize and sorghum in Africa. The microbiome associated withS. frugiperda could play a role in the insects' success and adaptability. However, bacterial communities in S. frugiperda remain poorly studied. Methods We investigated the composition, abundance and diversity of microbiomes associated with larval and adult specimens of S. frugiperda collected from four maize growing regions in Kenya through high throughput sequencing of the bacterial 16S rRNA gene. The population structure of S. frugiperda in Kenya was assessed through amplification of the mitochondrial cytochrome oxidase subunit I gene. Results We identified Proteobacteria and Firmicutes as the most dominant bacterial phyla and lesser proportions of Bacteroidetes and Actinobacteria. We also observed differences in bacterial microbiome diversity between larvae and adults that are a likely indication that some prominent larval bacterial groups are lost during metamorphosis. However, several bacterial groups were found in both adults and larvae suggesting that they are transmitted across developmental stages. Reads corresponding to several known entomopathogenic bacterial clades as well as the fungal entomopathogen, Metarhizium rileyi, were observed. Mitochondrial DNA haplotyping of the S. frugiperda population in Kenya indicated the presence of both 'Rice' and 'Corn' strains, with a higher prevalence of the 'Rice' strain.

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Mutational disruption of the ABCC2 gene in fall armyworm, Spodoptera frugiperda, confers resistance to the Cry1Fa and Cry1A.105 insecticidal proteins

Cited by 85 publications

References 40 publications

CRISPR-Mediated Knockout of the ABCC2 Gene in Ostrinia furnacalis Confers High-Level Resistance to the Bacillus thuringiensis Cry1Fa Toxin

CRISPR-Mediated Knockout of the ABCC2 Gene in Ostrinia furnacalis Confers High-Level Resistance to the Bacillus thuringiensis Cry1Fa Toxin

Diversity of fall armyworm, Spodoptera frugiperda and their gut bacterial community in Kenya

Peer Review #1 of "Diversity of fall armyworm, Spodoptera frugiperda and their gut bacterial community in Kenya (v0.1)"

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