Screening of Helicoverpa armigera Mobilome Revealed Transposable Element Insertions in Insecticide Resistance Genes

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 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.

Resistance in the Genus Spodoptera: Key Insect Detoxification Genes

“…The mechanisms resulting in blooming in the CYP9A family in the Spodoptera complex still remain to be deciphered. Several origins are possible, one of which corresponds to transposable elements as they have been shown to be prevalent in the surrounding of CYP genes in Lepidoptera [25,30,31], Drosophila [32] or mosquito [33]. Other mechanisms include duplications (tandem, chromosome or genome duplications) and retropositions [26].…”

Genome size evolution in the beetle genusDiabrotica

“…Cases of resistance to Bacillus thuringiensis (Bt) toxins have also been reported in Heliothis virescens which is caused by disruption of a cadherin-superfamily gene by TE insertion (Gahan, 2001). TE insertions in xenobiotic metabolism related genes such as those encoding cytochrome P450 monooxygenases and glutathione S-transferases in Helicoverpa armigera are the cause of resistance to insecticides (Klai et al, 2020) . Another example demonstrating that TEs can produce adaptive mutations has been reported in D. melanogaster (Rostant et al, 2012;Gilbert et al, 2021).…”

A Genomic Survey of Mayetiola destructor Mobilome Provides New Insights into the Evolutionary History of Transposable Elements in the Cecidomyiid Midges

“…These tools include de novo methods such as REPET, RepeatModeler and PiRATE pipelines [ 19 – 21 ], knowledge-based TE detection methods like Repeatmasker and TEseeker [ 22 , 23 ] as well as comparative population genomics methods using PoPoolationTE2 [ 24 ]. These various tools have hastened insights concerning the molecular genetic basis of many insect phenotypes and recent findings indicate that TEs are involved in insect adaptations and are powerful facilitators of their genome evolution [ 25 – 28 ].…”