Recent Advances in the Understanding of Molecular Mechanisms of Resistance in Noctuid Pests

A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Molecular Biology and Genomics".

Deadline for manuscript submissions: closed (31 March 2021) | Viewed by 42168

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Guest Editor
Université Côte d’Azur, INRAE, CNRS, ISA, F-06903 Sophia Antipolis, France
Interests: insecticide resistance; insect functional genomic; cytochrome P450; plant-insect interaction
Special Issues, Collections and Topics in MDPI journals
Bayer AG, Crop Science Division, R & D, Pest Control, 40789 Monheim, Germany
Interests: insecticide resistance; insect toxicogenomics; insecticide mode of action; functional genomics; cytochrome P450
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

This Special Issue is an opportunity to focus on the mechanisms of insecticide resistance developed by lepidopterans belonging to the family of Noctuidae (moth species), which are among the most devastating crop pests on the planet. Some of these noctuids are able to feed on more than 40 different plant families and have a high invasive potential. An example is the fall armyworm, Spodoptera frugiperda. This insect, initially present on the American continent, has recently invaded Africa in 2016 and is currently spreading in Asia and Australia. Its invasion of the European continent is highly likely. In addition to attacking a wide range of crops, such as maize and rice, it has developed resistance to many classes of insecticides and Bacillus thuringiensis (B.t.) pore-forming Cry toxins. Other close species of the genus Spodoptera, such as S. litura, S. littoralis, and S. exigua have the same adaptive capacities. Another important Noctuid subfamily are the heliothine moths, e.g., cotton bollworm, Helicoverpa armigera, a highly polyphagous species, resistant to many insecticides, that have extended its range from Europe, Asia, Africa, and Australia to South America. Understanding how these insects become resistant to chemical insecticides and B.t. toxins is essential for sustainable control and appropriate resistance management tactics. With the advent of the genomes of these noctuids in recent years, the development of techniques such as CRISPR/Cas9 and GWAS have considerably improved the identification and validation of molecular mechanisms underlying insecticide resistance.

We invite colleagues working on noctuid moths that have developed resistance to chemical insecticides and B.t. toxins to submit original papers, short communications, or reviews. Studies may focus on resistance mechanisms based on target-site mutations and/or metabolic detoxification. Genome comparison analyses between these species are also welcome.

Dr. Gaelle Le Goff
Dr. Ralf Nauen
Guest Editors

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Keywords

  • Noctuidae
  • insecticide resistance
  • B.t. toxin resistance
  • mechanisms of resistance

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Published Papers (11 papers)

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Editorial

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2 pages, 176 KiB  
Editorial
Recent Advances in the Understanding of Molecular Mechanisms of Resistance in Noctuid Pests
by Gaëlle Le Goff and Ralf Nauen
Insects 2021, 12(8), 674; https://doi.org/10.3390/insects12080674 - 27 Jul 2021
Cited by 4 | Viewed by 1612
Abstract
Noctuid moths are among the most devastating crop pests on the planet [...] Full article

Research

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15 pages, 1989 KiB  
Article
Genetic Screening to Identify Candidate Resistance Alleles to Cry1F Corn in Fall Armyworm Using Targeted Sequencing
by Katrina Schlum, Kurt Lamour, Peter Tandy, Scott J. Emrich, Caroline Placidi de Bortoli, Tejas Rao, Diego M. Viteri Dillon, Angela M. Linares-Ramirez and Juan Luis Jurat-Fuentes
Insects 2021, 12(7), 618; https://doi.org/10.3390/insects12070618 - 08 Jul 2021
Cited by 12 | Viewed by 3233
Abstract
Evolution of practical resistance is the main threat to the sustainability of transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt crops). Monitoring of resistance to Cry and Vip3A proteins produced by Bt crops is critical to mitigate the development of resistance. Currently, [...] Read more.
Evolution of practical resistance is the main threat to the sustainability of transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt crops). Monitoring of resistance to Cry and Vip3A proteins produced by Bt crops is critical to mitigate the development of resistance. Currently, Cry/Vip3A resistance allele monitoring is based on bioassays with larvae from inbreeding field-collected moths. As an alternative, DNA-based monitoring tools should increase sensitivity and reduce overall costs compared to bioassay-based screening methods. Here, we evaluated targeted sequencing as a method allowing detection of known and novel candidate resistance alleles to Cry proteins. As a model, we sequenced a Cry1F receptor gene (SfABCC2) in fall armyworm (Spodoptera frugiperda) moths from Puerto Rico, a location reporting continued practical field resistance to Cry1F-producing corn. Targeted sequencing detected a previously reported Cry1F resistance allele (SfABCC2mut), in addition to a resistance allele originally described in S. frugiperda populations from Brazil. Moreover, targeted sequencing detected mutations in SfABCC2 as novel candidate resistance alleles. These results support further development of targeted sequencing for monitoring resistance to Bt crops and provide unexpected evidence for common resistance alleles in S. frugiperda from Brazil and Puerto Rico. Full article
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8 pages, 1044 KiB  
Communication
Evaluation of Reference Genes and Expression Level of Genes Potentially Involved in the Mode of Action of Cry1Ac and Cry1F in a Susceptible Reference Strain of Chrysodeixis includens
by Macarena Martin, Debora Boaventura and Ralf Nauen
Insects 2021, 12(7), 598; https://doi.org/10.3390/insects12070598 - 30 Jun 2021
Cited by 2 | Viewed by 2436
Abstract
Soybean looper (SBL), Chrysodeixis includens (Walker), is one of the major lepidopteran pests of soybean in the American continent. SBL control relies mostly on the use of insecticides and genetically modified crops expressing Bacillus thuringiensis (Bt) insecticidal Cry proteins. Due to the high [...] Read more.
Soybean looper (SBL), Chrysodeixis includens (Walker), is one of the major lepidopteran pests of soybean in the American continent. SBL control relies mostly on the use of insecticides and genetically modified crops expressing Bacillus thuringiensis (Bt) insecticidal Cry proteins. Due to the high selection pressure exerted by these control measures, resistance has developed to different insecticides and Bt proteins. Nevertheless, studies on the mechanistic background are still scarce. Here, the susceptibility of the laboratory SBL-Benzon strain to the Bt proteins Cry1Ac and Cry1F was determined in diet overlay assays and revealed a greater activity of Cry1Ac than Cry1F, thus confirming results obtained for other sensitive SBL strains. A reference gene study across larval stages with four candidate genes revealed that RPL10 and EF1 were the most stable genes for normalization of gene expression data obtained by RT-qPCR. Finally, the basal expression levels of eight potential Bt protein receptor genes in six larval instars were analyzed, including ATP-binding cassette (ABC) transporters, alkaline phosphatase, aminopeptidases, and cadherin. The results presented here provide fundamental knowledge to support future SBL resistance studies. Full article
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12 pages, 1172 KiB  
Article
Geographic Monitoring of Insecticide Resistance Mutations in Native and Invasive Populations of the Fall Armyworm
by Sudeeptha Yainna, Nicolas Nègre, Pierre J. Silvie, Thierry Brévault, Wee Tek Tay, Karl Gordon, Emmanuelle dAlençon, Thomas Walsh and Kiwoong Nam
Insects 2021, 12(5), 468; https://doi.org/10.3390/insects12050468 - 18 May 2021
Cited by 32 | Viewed by 4769
Abstract
Field evolved resistance to insecticides is one of the main challenges in pest control. The fall armyworm (FAW) is a lepidopteran pest species causing severe crop losses, especially corn. While native to the Americas, the presence of FAW was confirmed in West Africa [...] Read more.
Field evolved resistance to insecticides is one of the main challenges in pest control. The fall armyworm (FAW) is a lepidopteran pest species causing severe crop losses, especially corn. While native to the Americas, the presence of FAW was confirmed in West Africa in 2016. Since then, the FAW has been detected in over 70 countries covering sub-Saharan Africa, the Middle East, North Africa, South Asia, Southeast Asia, and Oceania. In this study, we tested whether this invasion was accompanied by the spread of resistance mutations from native to invasive areas. We observed that mutations causing Bt resistance at ABCC2 genes were observed only in native populations where the mutations were initially reported. Invasive populations were found to have higher gene numbers of cytochrome P450 genes than native populations and a higher proportion of multiple resistance mutations at acetylcholinesterase genes, supporting strong selective pressure for resistance against synthetic insecticides. This result explains the susceptibility to Bt insecticides and resistance to various synthetic insecticides in Chinese populations. These results highlight the necessity of regular and standardized monitoring of insecticide resistance in invasive populations using both genomic approaches and bioassay experiments. Full article
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9 pages, 12941 KiB  
Article
A Dynamic Energy Budget Approach for the Prediction of Development Times and Variability in Spodoptera frugiperda Rearing
by Andre Gergs and Christian U. Baden
Insects 2021, 12(4), 300; https://doi.org/10.3390/insects12040300 - 29 Mar 2021
Cited by 7 | Viewed by 2434
Abstract
A major challenge in insect rearing is the need to provide certain life cycle stages at a given time for the initiation of experimental trials. The timing of delivery, organism quality, and variability directly affect the outcome of such trials. Development times and [...] Read more.
A major challenge in insect rearing is the need to provide certain life cycle stages at a given time for the initiation of experimental trials. The timing of delivery, organism quality, and variability directly affect the outcome of such trials. Development times and intraspecific variability are directly linked to the availability of food and to the ambient temperature. Varying temperature regimes is an approach to adapt development times to fulfill experimental needs without impairment of larval quality. However, current practices of temperature setting may lead to increased variability in terms of development times and the frequency of particular life stages at a given point in time. In this study, we analyzed how resource availability and ambient temperature may affect the larval development of the economically important noctuid species Spodoptera frugiperda by means of dynamic energy budget modeling. More specifically, we analyzed how rearing practices such as raising of temperatures may affect the variability in larval development. Overall, the presented modeling approach provides a support system for decisions that must be made for the timely delivery of larvae and reduction of variability. Full article
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12 pages, 1764 KiB  
Article
Screening of Helicoverpa armigera Mobilome Revealed Transposable Element Insertions in Insecticide Resistance Genes
by Khouloud KLAI, Benoît CHÉNAIS, Marwa ZIDI, Salma DJEBBI, Aurore CARUSO, Françoise DENIS, Johann CONFAIS, Myriam BADAWI, Nathalie CASSE and Maha MEZGHANI KHEMAKHEM
Insects 2020, 11(12), 879; https://doi.org/10.3390/insects11120879 - 11 Dec 2020
Cited by 19 | Viewed by 4178
Abstract
The cotton bollworm Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) is an important pest of many crops that has developed resistance to almost all groups of insecticides used for its management. Insecticide resistance was often related to Transposable Element (TE) insertions near specific [...] Read more.
The cotton bollworm Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) is an important pest of many crops that has developed resistance to almost all groups of insecticides used for its management. Insecticide resistance was often related to Transposable Element (TE) insertions near specific genes. In the present study, we deeply retrieve and annotate TEs in the H. armigera genome using the Pipeline to Retrieve and Annotate Transposable Elements, PiRATE. The results have shown that the TE library consists of 8521 sequences representing 236,132 TE copies, including 3133 Full-Length Copies (FLC), covering 12.86% of the H. armigera genome. These TEs were classified as 46.71% Class I and 53.29% Class II elements. Among Class I elements, Short and Long Interspersed Nuclear Elements (SINEs and LINEs) are the main families, representing 21.13% and 19.49% of the total TEs, respectively. Long Terminal Repeat (LTR) and Dictyostelium transposable element (DIRS) are less represented, with 5.55% and 0.53%, respectively. Class II elements are mainly Miniature Inverted Transposable Elements (MITEs) (49.11%), then Terminal Inverted Repeats (TIRs) (4.09%). Superfamilies of Class II elements, i.e., Transib, P elements, CACTA, Mutator, PIF-harbinger, Helitron, Maverick, Crypton and Merlin, were less represented, accounting for only 1.96% of total TEs. In addition, we highlighted TE insertions in insecticide resistance genes and we successfully identified nine TE insertions belonging to RTE, R2, CACTA, Mariner and hAT superfamilies. These insertions are hosted in genes encoding cytochrome P450 (CyP450), glutathione S-transferase (GST), and ATP-binding cassette (ABC) transporter belonging to the G and C1 family members. These insertions could therefore be involved in insecticide resistance observed in this pest. Full article
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11 pages, 4035 KiB  
Article
Development of a Species Diagnostic Molecular Tool for an Invasive Pest, Mythimna loreyi, Using LAMP
by Hwa Yeun Nam, Min Kwon, Hyun Ju Kim and Juil Kim
Insects 2020, 11(11), 817; https://doi.org/10.3390/insects11110817 - 19 Nov 2020
Cited by 12 | Viewed by 2692
Abstract
The Mythimna loreyi (Duponchel) is one of the well-known invasive noctuid pests in Africa, Australia, and many Asian countries. However, it is difficult to identify the invasive and morphologically similar species, Mythimna separate, which occur at the cornfield in the larvae stage. [...] Read more.
The Mythimna loreyi (Duponchel) is one of the well-known invasive noctuid pests in Africa, Australia, and many Asian countries. However, it is difficult to identify the invasive and morphologically similar species, Mythimna separate, which occur at the cornfield in the larvae stage. Currently, the molecular biology method for diagnosing M. loreyi species is only using the mtCO1 universal primer (LCO1490, HCO2198), which requires a lot of time and effort, such as DNA extraction, PCR, electrophoresis, and sequencing. In this study, the LAMP assay was developed for rapid, simple, effective species identification. By analyzing the mitochondrial genome, the species-specific sequence was found at the coding region of the NADH dehydrogenase subunit 5 gene. Based on this unique sequence, four LAMP primers and two loop primers were designed. The F3 and B3 primers were able to diagnose species-specific, in general, and multiplex PCR and specifically reacted within the inner primers in LAMP assay. The optimal incubation condition of the LAMP assay was 61 °C for 60 min with four LAMP primers, though additional loop primers, BF and LF, did not significantly shorten the amplification time. The broad range of DNA concentration was workable in LAMP assay, in which the minimum detectable DNA concentration was 100 pg. DNA releasing method was applied, which took five minutes of incubation at 95 °C without the DNA extraction process. Only some pieces of tissue of larvae and adult samples were needed to extract DNA. The incidence of invasive pests is gradually diversifying. Therefore, this simple and accurate LAMP assay is possibly applied in the intensive field monitoring for invasive pests and integrated management of Mythimna loreyi. Full article
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15 pages, 1953 KiB  
Article
A Novel Insecticidal Molecule Extracted from Alpinia galanga with Potential to Control the Pest Insect Spodoptera frugiperda
by Torranis Ruttanaphan, Georges de Sousa, Anchulee Pengsook, Wanchai Pluempanupat, Hannah-Isadora Huditz, Vasakorn Bullangpoti and Gaëlle Le Goff
Insects 2020, 11(10), 686; https://doi.org/10.3390/insects11100686 - 11 Oct 2020
Cited by 9 | Viewed by 3116
Abstract
Spodoptera frugiperda, a highly polyphagous insect pest from America, has recently invaded and widely spread throughout Africa and Asia. Effective and environmentally safe tools are needed for successful pest management of this invasive species. Natural molecules extracted from plants offer this possibility. [...] Read more.
Spodoptera frugiperda, a highly polyphagous insect pest from America, has recently invaded and widely spread throughout Africa and Asia. Effective and environmentally safe tools are needed for successful pest management of this invasive species. Natural molecules extracted from plants offer this possibility. Our study aimed to determine the insecticidal efficacy of a new molecule extracted from Alpinia galanga rhizome, the 1′S-1′-acetoxychavicol acetate (ACA). The toxicity of ACA was assessed by topical application on early third-instar larvae of S. frugiperda. Results showed that ACA caused significant larval growth inhibition and larval developmental abnormalities. In order to further explore the effects of this molecule, experiments have been performed at the cellular level using Sf9 model cells. ACA exhibited higher toxicity on Sf9 cells as compared to azadirachtin and was 38-fold less toxic on HepG2 cells. Inhibition of cell proliferation was observed at sublethal concentrations of ACA and was associated with cellular morphological changes and nuclear condensation. In addition, ACA induced caspase-3 activity. RT-qPCR experiments reveal that ACA induces the expression of several caspase genes. This first study on the effects of ACA on S. frugiperda larvae and cells provides evidence that ACA may have potential as a botanical insecticide for the control of S. frugiperda. Full article
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15 pages, 1672 KiB  
Article
Monitoring of Target-Site Mutations Conferring Insecticide Resistance in Spodoptera frugiperda
by Debora Boaventura, Macarena Martin, Alberto Pozzebon, David Mota-Sanchez and Ralf Nauen
Insects 2020, 11(8), 545; https://doi.org/10.3390/insects11080545 - 18 Aug 2020
Cited by 49 | Viewed by 6465
Abstract
Fall armyworm (FAW), Spodoptera frugiperda, a major pest of corn and native to the Americas, recently invaded (sub)tropical regions worldwide. The intensive use of insecticides and the high adoption of crops expressing Bacillus thuringiensis (Bt) proteins has led to many cases of [...] Read more.
Fall armyworm (FAW), Spodoptera frugiperda, a major pest of corn and native to the Americas, recently invaded (sub)tropical regions worldwide. The intensive use of insecticides and the high adoption of crops expressing Bacillus thuringiensis (Bt) proteins has led to many cases of resistance. Target-site mutations are among the main mechanisms of resistance and monitoring their frequency is of great value for insecticide resistance management. Pyrosequencing and PCR-based allelic discrimination assays were developed and used to genotype target-site resistance alleles in 34 FAW populations from different continents. The diagnostic methods revealed a high frequency of mutations in acetylcholinesterase, conferring resistance to organophosphates and carbamates. In voltage-gated sodium channels targeted by pyrethroids, only one population from Indonesia showed a mutation. No mutations were detected in the ryanodine receptor, suggesting susceptibility to diamides. Indels in the ATP-binding cassette transporter C2 associated with Bt-resistance were observed in samples collected in Puerto Rico and Brazil. Additionally, we analyzed all samples for the presence of markers associated with two sympatric FAW host plant strains. The molecular methods established show robust results in FAW samples collected across a broad geographical range and can be used to support decisions for sustainable FAW control and applied resistance management. Full article
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Review

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27 pages, 3912 KiB  
Review
Resistance in the Genus Spodoptera: Key Insect Detoxification Genes
by Frédérique Hilliou, Thomas Chertemps, Martine Maïbèche and Gaëlle Le Goff
Insects 2021, 12(6), 544; https://doi.org/10.3390/insects12060544 - 11 Jun 2021
Cited by 54 | Viewed by 5765
Abstract
The genus Spodoptera (Lepidoptera: Noctuidae) includes species that are among the most important crop pests in the world. These polyphagous species are able to feed on many plants, including corn, rice and cotton. In addition to their ability to adapt to toxic compounds [...] Read more.
The genus Spodoptera (Lepidoptera: Noctuidae) includes species that are among the most important crop pests in the world. These polyphagous species are able to feed on many plants, including corn, rice and cotton. In addition to their ability to adapt to toxic compounds produced by plants, they have developed resistance to the chemical insecticides used for their control. One of the main mechanisms developed by insects to become resistant involves detoxification enzymes. In this review, we illustrate some examples of the role of major families of detoxification enzymes such as cytochromes P450, carboxyl/cholinesterases, glutathione S-transferases (GST) and transporters such as ATP-binding cassette (ABC) transporters in insecticide resistance. We compare available data for four species, Spodoptera exigua, S. frugiperda, S. littoralis and S. litura. Molecular mechanisms underlying the involvement of these genes in resistance will be described, including the duplication of the CYP9A cluster, over-expression of GST epsilon or point mutations in acetylcholinesterase and ABCC2. This review is not intended to be exhaustive but to highlight the key roles of certain genes. Full article
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16 pages, 1505 KiB  
Review
The Essential and Enigmatic Role of ABC Transporters in Bt Resistance of Noctuids and Other Insect Pests of Agriculture
by David G. Heckel
Insects 2021, 12(5), 389; https://doi.org/10.3390/insects12050389 - 28 Apr 2021
Cited by 33 | Viewed by 4113
Abstract
In the last ten years, ABC transporters have emerged as unexpected yet significant contributors to pest resistance to insecticidal pore-forming proteins from Bacillus thuringiensis (Bt). Evidence includes the presence of mutations in resistant insects, heterologous expression to probe interactions with the three-domain Cry [...] Read more.
In the last ten years, ABC transporters have emerged as unexpected yet significant contributors to pest resistance to insecticidal pore-forming proteins from Bacillus thuringiensis (Bt). Evidence includes the presence of mutations in resistant insects, heterologous expression to probe interactions with the three-domain Cry toxins, and CRISPR/Cas9 knockouts. Yet the mechanisms by which ABC transporters facilitate pore formation remain obscure. The three major classes of Cry toxins used in agriculture have been found to target the three major classes of ABC transporters, which requires a mechanistic explanation. Many other families of bacterial pore-forming toxins exhibit conformational changes in their mode of action, which are not yet described for the Cry toxins. Three-dimensional structures of the relevant ABC transporters, the multimeric pore in the membrane, and other proteins that assist in the process are required to test the hypothesis that the ATP-switch mechanism provides a motive force that drives Cry toxins into the membrane. Knowledge of the mechanism of pore insertion will be required to combat the resistance that is now evolving in field populations of insects, including noctuids. Full article
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