Characterization of irritans mariner-like elements in the olive fruit fly Bactrocera oleae (Diptera: Tephritidae): evolutionary implications

Abstract

Genomic variation among species is commonly driven by transposable element (TE) invasion; thus, the pattern of TEs in a genome allows drawing an evolutionary history of the studied species. This paper reports in vitro and in silico detection and characterization of irritans mariner-like elements (MLEs) in the genome and transcriptome of Bactrocera oleae (Rossi) (Diptera: Tephritidae). Eleven irritans MLE sequences have been isolated in vitro using terminal inverted repeats (TIRs) as primers, and 215 have been extracted in silico from the sequenced genome of B. oleae. Additionally, the sequenced genomes of Bactrocera tryoni (Froggatt) and Bactrocera cucurbitae (Diptera: Tephritidae) have been explored to identify irritans MLEs. A total of 129 sequences from B. tryoni have been extracted, while the genome of B. cucurbitae appears probably devoid of irritans MLEs. All detected irritans MLEs are defective due to several mutations and are clustered together in a monophyletic group suggesting a common ancestor. The evolutionary history and dynamics of these TEs are discussed in relation with the phylogenetic distribution of their hosts. The knowledge on the structure, distribution, dynamic, and evolution of irritans MLEs in Bactrocera species contributes to the understanding of both their evolutionary history and the invasion history of their hosts. This could also be the basis for genetic control strategies using transposable elements.

An overview of irritans-mariner transposons in two Mayetiola species (Diptera: Cecidomyiidae)

“…Moreover, these gaps are fl anked by microhomologies. The association of microhomology with deletion breakpoints is reported in Mos1 (Brunet et al, 2002), mauritiana (Kharrat et al, 2015) and irritans elements (Ben Lazhar-Ajroud et al, 2016). These deletions do not occur randomly and could result from a host genome control, as well as from additional mechanisms, such as abortive gap repair (Rubin & Levy, 1997) and/or ectopic recombination between homologous short sequences leading to different deletion forms (Negoua et al, 2013;Kharrat et al, 2015).…”

“…Class I elements, also known as retrotransposons, transpose via an RNA intermediate according to the "copy and paste" model. Class II elements, also named transposons move via a DNA intermediate according to the The identifi ed MLEs are mostly inactive owing to mutations affecting different parts of the elements and it has also been shown that many defective copies contain internal deletions that occur non randomly as ascertained by small direct repeats (SDRs) called microhomologies bordering deletion break points (BPs) (Brunet et al, 2002;Kharrat et al, 2015;Ben Lazhar-Ajroud et al, 2016).…”

Insights on mauritiana-like elements diversity in Mayetiola destructor and M. hordei (Diptera: Cecidomyiidae)

“…Similar studies carried on ants highlighted a vertical transmission with differential evolutionary success and spread into different genomes during species-separation processes (Sanllorente et al, 2020). Other studies have revealed the establishment of irritans D r a f t subfamily elements in closely related Bactrocera species originating from the expansion from a common ancestor (Ben Lazhar-Ajroud et al, 2016) .…”

“…More interestingly, some deletions were found to cover the same positions in both Mayetiola species. This could be a mechanism contributing to defective MLEs or element decay as described in the irritans subfamily (Ben Amara et al, 2017, Ben Lazhar-Ajroud et al, 2016. Furthermore, Desmar1, MauCons1 and MauCons2-like elements exhibited high sequence identity between M. destructor and M. hordei which may indicate an eventual vertical inheritance of these MLEs from an intermediate common ancestor.…”

“…Genomic DNA (500 ng) were individually extracted from M. destructor and M. hordei and digested with 5U of restriction endonuclease EcoRI or DraI or HindIII (Promega®) at 37°C for 1h then circularized in 150 μl volume reaction containing 100 U of T4 DNA Ligase (New England BioLabs) and 30 μl of reaction buffer. After incubation for 5 hours at 37°C, a volume of 10 μl of circularized products is used to perform iPCR and nPCR using primers reported in Table 1 and conditions described by (Ben Lazhar-Ajroud et al, 2016). The products of iPCR and nPCR were subsequently purified, cloned and sequenced on both strands following the experimental protocol of Kharrat et al (2015).…”