Bill James

Commonwealth Scientific and Industrial Research Organisation

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Tom Walsh

Commonwealth Scientific and Industrial Research Organisation

Sharon Downes

Commonwealth Scientific and Industrial Research Organisation

Juan Ferré

Universitat de València

Maissa Chakroun

National Center for Genetic Engineering and Biotechnology

Nonthakorn Apirajkamol

Macquarie University

Wee Tek Tay

Macquarie University

Karl Gordon

Commonwealth Scientific and Industrial Research Organisation

Michelle Williams

Commonwealth Scientific and Industrial Research Organisation

Angela McGaughran

University of Waikato

Lisa J. Bird

TriHealth

Cooperative Institutions

Commonwealth Scientific and Industrial Research Organisation

ACT Government

Health Sciences and Nutrition

Australian National University

CSIRO Land and Water

Ecosystem Sciences

Macquarie University

University of Melbourne

Universitat de València

CSIRO Health and Biosecurity

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Analysis of cross-resistance to Vip3 proteins in eight insect colonies, from four insect species, selected for resistance to Bacillus thuringiensis insecticidal proteins

Journal of Invertebrate Pathology (2018)

Joaquín Gomis-Cebolla Yuequin Wang Yudong Quan Kanglai He Tom Walsh

Bacillus thuringiensis

Ostrinia furnacalis

Cross-resistance

10.1016/j.jip.2018.05.004

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Citations (22)

Vip3A Resistance Alleles Exist at High Levels in Australian Targets before Release of Cotton Expressing This Toxin

PLoS ONE (2012)

Rod Mahon Sharon Downes Bill James

Crops engineered to produce insecticidal crystal (Cry) proteins from the soil bacterium Bacillus thuringiensis (Bt) have revolutionised pest control in agriculture. However field-level resistance to Bt has developed in some targets. Utilising novel vegetative insecticidal proteins (Vips), also derived from Bt but genetically distinct from Cry toxins, is a possible solution that biotechnical companies intend to employ. Using data collected over two seasons we determined that, before deployment of Vip-expressing plants in Australia, resistance alleles exist in key targets as polymorphisms at frequencies of 0.027 (n = 273 lines, 95% CI = 0.019–0.038) in H. armigera and 0.008 (n = 248 lines, 0.004–0.015) in H. punctigera. These frequencies are above mutation rates normally encountered. Homozygous resistant neonates survived doses of Vip3A higher than those estimated in field-grown plants. Fortunately the resistance is largely, if not completely, recessive and does not confer resistance to the Bt toxins Cry1Ac or Cry2Ab already deployed in cotton crops. These later characteristics are favourable for resistance management; however the robustness of Vip3A inclusive varieties will depend on resistance frequencies to the Cry toxins when it is released (anticipated 2016) and the efficacy of Vip3A throughout the season. It is appropriate to pre-emptively screen key targets of Bt crops elsewhere, especially those such as H. zea in the USA, which is not only closely related to H. armigera but also will be exposed to Vip in several varieties of cotton and corn.

Bacillus thuringiensis

Cry1Ac

Bt Cotton

10.1371/journal.pone.0039192

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Citations (107)

Use of a Cry1Ac-Resistant Line of Helicoverpa armigera (Lepidoptera: Noctuidae) to Detect Novel Insecticidal Toxin Genes in Bacillus thuringiensis

Current Microbiology (2008)

Cheryl E. Beard Leon Court Roslyn G. Mourant Bill James Jeroen Van Rie

Bacillus thuringiensis

Cry1Ac

10.1007/s00284-008-9098-8

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Oxidative stress delays development and alters gene function in the agricultural pest moth,Helicoverpa armigera

bioRxiv (Cold Spring Harbor Laboratory) (2020)

Nonthakorn Apirajkamol Bill James Tom Walsh Angela McGaughran

Abstract Stress is a widespread phenomenon that all organisms must endure. Common in nature is oxidative stress, which can interrupt cell homeostasis to cause cell damage and may be derived from respiration or from environmental exposure thought diet. As a result of the routine exposure from respiration, many organisms can mitigate the effects of oxidative stress, but less is known about responses to oxidative stress from other sources. Helicoverpa armigera is a major agricultural pest moth that causes significant damage to crops worldwide. Here, we examined the effects of oxidative stress on H. armigera by chronically exposing individuals to paraquat - a free radical producer - and measuring changes in development (weight, developmental rate, lifespan), and gene expression. We found that oxidative stress strongly affected development in H. armigera , with stressed samples spending more time as caterpillars than control samples (>24 vs. ∼15 days, respectively) and living longer overall. We found 1,618 up- and 761 down-regulated genes, respectively, in stressed vs. control samples. In the up-regulated gene set were genes associated with cell senescence and apoptosis and an over-representation of biological processes related to cuticle and chitin development, glycine metabolism, and oxidation-reduction. Oxidative stress clearly impacts physiology and biochemistry in H. armigera and the interesting finding of an extended lifespan in stressed individuals could demonstrate hormesis, the process whereby toxic compounds can actually be beneficial at low doses. Collectively, our findings provide new insights into genomic responses to oxidative stress in invertebrates.

Hormesis

10.1101/2020.01.14.906958

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Cry1 resistance in a CRISPR/Cas9‐mediated HaCad1 gene knockout strain of the Australian cotton bollworm Helicoverpa armigera conferta (Lepidoptera: Noctuidae)

Pest Management Science (2024)

Cao Fang Bill James Michelle Williams Andy Bachler Wee Tek Tay

Abstract BACKGROUND Helicoverpa armigera is a highly polyphagous species that causes huge losses to agricultural and horticultural crops worldwide. In the cotton industry, H. armigera, including the Australian subspecies Helicoverpa armigera conferta , is largely managed using genetically modified crops that express insecticidal toxins, such as Cry1Ac. Resistance to Cry1 proteins occurs and, in some cases, is mediated by changes to HaCad1 , a gene that encodes the midgut protein cadherin. Around the world, numerous resistance‐associated polymorphisms have been identified in the HaCad1 gene of H. armigera , but Cry1Ac resistance is rare in the Australian subspecies. We used CRISPR/Cas9 to disrupt the cadherin gene in H. armigera conferta and characterised the resulting phenotype with bioassays and transcriptomics. RESULTS Compared to the parental strain, the newly generated HaCad1 knockout strain is 44‐fold and 16‐fold more resistant to Cry1Ac and Cry1A.105, respectively, while wild‐type and knockout insects were equally insensitive to Cry1F. CONCLUSION The disruption of the HaCad1 gene causes Cry1Ac resistance in Australian H. armigera conferta . However, Cry1Ac resistance remains rare in Australian field populations suggesting that Australia's approach to pest management in cotton has prevented widespread Cry1Ac resistance. © 2024 CSIRO. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Cry1Ac

10.1002/ps.8500

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Resistance to Ingard Cotton by the Cotton Bollworm, Helicoverpa armigera

Bill James R.J. Akhurst Lisa J. Bird

Bollworm

Bt Cotton

Source

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Citations (14)

Efficacy and Resistance Management Potential of a Modified Vip3C Protein for Control of Spodoptera frugiperda in Maize

Scientific Reports (2018)

Theodore W. Kahn Maissa Chakroun Jayme Williams Tom Walsh Bill James

Abstract A modified Vip3C protein has been developed that has a spectrum of activity that has the potential to be commercially useful for pest control, and shows good efficacy against Spodoptera frugiperda in insect bioassays and field trials. For the first time Vip3A and Vip3C proteins have been compared to Cry1 and Cry2 proteins in a complete set of experiments from insect bioassays to competition binding assays to field trials, and the results of these complementary experiments are in agreement with each other. Binding assays with radiolabelled toxins and brush border membrane vesicles from S . frugiperda and Helicoverpa armigera show that the modified Vip3C protein shares binding sites with Vip3A, and does not share sites with Cry1F or Cry2A. In agreement with the resulting binding site model, Vip3A-resistant insects were also cross-resistant to the modified Vip3C protein. Furthermore, maize plants expressing the modified Vip3C protein, but not those expressing Cry1F protein, were protected against Cry1F-resistant S . frugiperda in field trials.

10.1038/s41598-018-34214-z

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Citations (14)

Mining novel Bacillus thuringiensis toxins and secondary metabolites for invasive fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) control

Austral Entomology (2025)

Nonthakorn Apirajkamol Bill James Timothy Michael Hogarty Bishwo P. Mainali Phillip W. Taylor

Abstract Bacillus thuringiensis ( Bt ) endotoxins are often considered environmentally friendly pest control tools. However, the development of resistance to Bt toxins and emergence of exotic pests necessitate the characterisation of new Bt isolates. This study aims to identify and characterise novel Bt toxins and bioactive compounds that may be utilised to mitigate the impact of Spodoptera frugiperda (fall armyworm, FAW), a polyphagous agricultural pest species that has recently established populations in over 80 countries including Australia. Eight Bt isolates were used in bioassays to ascertain toxicity to FAW neonates. Six Bt isolates (Bt_01‐02 and Bt_05‐08) exhibited potential insecticidal activities. Three isolates including Bt_01 and Bt_07‐08 caused 100% mortality, while Bt_02, Bt_05, and Bt_06 induced 71.27 ± 21.17, 98.44 ± 2.21 and 92.19 ± 11.05% mortality, respectively. Genome analysis was conducted to characterise the toxins and secondary metabolite gene clusters of each isolate. Four isolates (Bt_01, Bt_06, Bt_07, Bt_08) contained the Cry1Na‐partial and Cry1I toxins, while Bt_05 contained Cry2A, Cry1H and Cry1‐like amino acid sequences. In addition, the gene cluster for zwittermicin A, a crystal toxin enhancer, was present in all isolates. However, no known toxins or insecticidal compounds were identified in Bt_02 despite inducing high mortality. The pathogenicity of Bt_02 was also tested against two Australian native pest species: Helicoverpa armigera conferta and H. punctigera . This includes both the susceptible and Cry1Ac‐resistant (Hp9‐3784) lines of H. punctigera . Bt_02 caused 74.88 ± 19.82% mortality in H. armigera , 95.65 ± 6.15% mortality in H. punctigera and 90.91 ± 12.86% mortality in Hp9‐3784. This suggests that Bt_02 may possess unknown toxins or bioactive compounds responsible for its effectiveness against three species of lepidopteran pests including those that exhibited Cry1Ac resistance.

Bacillus thuringiensis

Cry1Ac

Biopesticide

Bt Cotton

Fall armyworm

10.1111/aen.70000

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Identification of a novel resistance gene which provides insight into Vip3Aa mode of action inHelicoverpa armigera

bioRxiv (Cold Spring Harbor Laboratory) (2024)

Andreas Bachler Amanda Padovan Craig Anderson Yiyun Wei Yidong Wu

Abstract The global reliance on Bacillus thuringiensis (Bt) proteins for controlling lepidopteran pests in cotton, corn, and soybean crops underscores the critical need to understand resistance mechanisms. Vip3Aa, one of the most widely deployed and currently effective Bt proteins in genetically modified crops, plays a pivotal role in pest management. This study identifies the molecular basis of Vip3Aa resistance in Australian Helicoverpa armigera through genetic crosses, and integrated genomic and transcriptomic analyses. We identified a previously uncharacterized gene, LOC110373801 (designated HaVipR1 ), as a crucial determinant of Vip3Aa resistance in two field-derived resistant lines. Functional validation using CRISPR-Cas9 knockout in susceptible lines confirmed the gene’s role in conferring resistance. Despite extensive laboratory selection of Vip3Aa-resistant colonies in Lepidoptera, the biochemical mechanisms underlying resistance have remained elusive. Our research demonstrates that HaVipR1 -mediated resistance operates independently of known resistance genes, including midgut-specific chitin synthase and the transcription factor SfMyb. The identification of HaVipR1 offers further insights into the Vip3Aa mechanism of action. This discovery is vital for devising strategies to counteract resistance and sustain the efficacy of Bt crops. Future research should focus on elucidating the biochemical pathways involving HaVipR1 and investigating its interactions with other resistance mechanisms. Our findings underscore the utility of analysing field-derived resistant lines in providing biologically relevant insights and stress the necessity for comprehensive management strategies to maintain agricultural productivity. Significance Statement This is the first identification of a specific gene in Helicoverpa armigera which mediates resistance to the Bacillus thuringiensis (Bt) protein Vip3Aa. We identify that this gene is disrupted in two different ways in separate field-derived resistant lines, one being a large transposable element insertion in the first intron of the HaVipR1 gene, confirmed using long-read sequencing. Disruption of this gene using CRISPR-Cas9 knockout in a susceptible H. armigera line confers Vip3A resistance. The identification of a specific gene is important for molecular monitoring and management of H. armigera as well as other global pests of concern like Spodoptera frugiperda . These findings also offer insights for researchers aiming to understand how Vip3Aa functions, as the action pathway remains unclear.

Bacillus thuringiensis

Bt Cotton

10.1101/2024.08.11.607516

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Citations (2)

Isolating, characterising and identifying a Cry1Ac resistance mutation in field populations of Helicoverpa punctigera

Scientific Reports (2018)

Tom Walsh Bill James Maissa Chakroun Juan Ferré Sharon Downes

Abstract Transgenic cotton expressing insecticidal proteins from Bacillus thuringiensis (Bt) has been grown in Australia for over 20 years and resistance remains the biggest threat. The native moth, Helicoverpa punctigera is a significant pest of cotton. A genotype causing resistance to Cry1Ac in H. punctigera was isolated from the field and a homozygous line established. The phenotype is recessive and homozygous individuals possess 113 fold resistance to Cry1Ac. Individuals that carry Cry1Ac resistance genes are rare in Australia with a frequency of 0.033 being detected in field populations. RNAseq, RT-PCR and DNA sequencing reveals a single nucleotide polymorphism at a splice site in the cadherin gene as the causal mutation, resulting in the partial transcription of the intron and a premature stop codon. Analysis of Cry1Ac binding to H. punctigera brush border membrane vesicles showed that it is unaffected by the disrupted cadherin gene. This suggests that the major Cry1Ac target is not cadherin but that this molecule plays a key role in resistance and therefore the mode of action. This work adds to our knowledge of resistance mechanisms in H. punctigera and the growing literature around the role of cadherin in the mode of action of Cry1 type Bt proteins.

Cry1Ac

Bacillus thuringiensis

10.1038/s41598-018-21012-w

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Citations (18)