Whole‐genome sequencing to detect mutations associated with resistance to insecticides and Bt proteins in Spodoptera frugiperda

Abstract

The fall armyworm (FAW), Spodoptera frugiperda, is a major pest native to the Americas that has recently invaded the Old World. Point mutations in the target-site proteins acetylcholinesterase-1 (ace-1), voltage-gated sodium channel (VGSC) and ryanodine receptor (RyR) have been identified in S. frugiperda as major resistance mechanisms to organophosphate, pyrethroid and diamide insecticides respectively. Mutations in the adenosine triphosphate-binding cassette transporter C2 gene (ABCC2) have also been identified to confer resistance to Cry1F protein. In this study, we applied a whole-genome sequencing (WGS) approach to identify point mutations in the target-site genes in 150 FAW individuals collected from China, Malawi, Uganda and Brazil. This approach revealed three amino acid substitutions (A201S, G227A and F290V) of S. frugiperda ace-1, which are known to be associated with organophosphate resistance. The Brazilian population had all three ace-1 point mutations and the 227A allele (mean frequency = 0.54) was the most common. Populations from China, Malawi and Uganda harbored two of the three ace-1 point mutations (A201S and F290V) with the 290V allele (0.47-0.58) as the dominant allele. Point mutations in VGSC (T929I, L932F and L1014F) and RyR (I4790M and G4946E) were not detected in any of the 150 individuals. A novel 12-bp insertion mutation in exon 15 of the ABCC2 gene was identified in some of the Brazilian individuals but absent in the invasive populations. Our results not only demonstrate robustness of the WGS-based genomic approach for detection of resistance mutations, but also provide insights for improvement of resistance management tactics in S. frugiperda.

Monitoring of Target-Site Mutations Conferring Insecticide Resistance in Spodoptera frugiperda

“…However, to avoid any identification bias, we used a second marker, Tpi, and the obtained data revealed that all samples, including those from Kenya and Indonesia, resemble corn strain and none rice strain. This discrepancy between COI and Tpi markers has already been noticed by other authors, especially with samples from Africa and Asia, where strain characterization is dependent on the molecular marker used [16,18,65]. However, the exclusive identification of the corn strain in our samples by using the Tpi marker is in accordance with the preferred host, suggesting that it is a more accurate strain marker than COI.…”

“…While we identified the described GC insertion and GY deletion in many samples from Puerto Rico and Brazil, respectively, none of the above-mentioned mutations were found in populations from Kenya or Indonesia, supporting the absence/very low frequency of these mutations in the field and a lack of selection pressure by transgenic corn expressing Cry1F in those countries. Recent whole-genome sequencing of FAW samples collected in China, Malawi, Uganda and Brazil revealed a novel ABCC2 resistance allele in FAW collected in Brazil, leading to a truncated and likely non-functional protein [65].…”

Parasitoid Distribution and Parasitism of the Fall Armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Different Maize Producing Regions of Uganda

“…Prolonged use of synthetic insecticides could lead to the development of resistance in target pest species. Insecticide resistance in FAW was detected in the New World (e.g., [ 15 , 16 , 17 ]) as well as in introduced populations (e.g., [ 18 , 19 , 20 ]) and this generates economic and biosecurity concerns. The management of FAW should, therefore, explore alternative options including the use of beneficial insects where possible.…”

Global FAW population genomic signature supports complex introduction events across the Old World

“…Indeed a meteorological data-based simulation study (i.e., wind currents, monsoon wind patterns) concluded the Yunnan FAW populations originated from Myanmar, consistent with FAW being officially reported earlier in Myanmar (December 2018 48,49 ) than in China (January 2019 35 ). Other work has examined the impact and implications for global plant health and agricultural biosecurity (e.g., 28,50 ), integrated pest management (IPM) and bioeconomics 51–53 , and insecticide resistance 37,45,54 .…”