RNA helicase domains of viral origin in proteins of insect retrotransposons: possible source for evolutionary advantages

Abstract

Recently, a novel phenomenon of horizontal gene transfer of helicase-encoding sequence from positive-stranded RNA viruses to LINE transposons in insect genomes was described. TRAS family transposons encoding an ORF2 protein, which comprised all typical functional domains and an additional helicase domain, were found to be preserved in many families during the evolution of the order Lepidoptera. In the present paper, in species of orders Hemiptera and Orthoptera, we found helicase domain-encoding sequences integrated into ORF1 of retrotransposons of the Jockey family. RNA helicases encoded by transposons of TRAS and Jockey families represented separate brunches in a phylogenetic tree of helicase domains and thus could be considered as independently originated in the evolution of insect transposons. Transcriptome database analyses revealed that both TRAS and Jockey transposons encoding the helicase domain represented transcribed genome sequences. Moreover, the transposon-encoded helicases were found to contain the full set of conserved motifs essential for their enzymatic activities. Taking into account the previously reported ability of RNA helicase encoded by TRAS ORF2 to suppress post-transcriptional RNA silencing, we propose possible scenarios of evolutionary fixation of actively expressed functional helicases of viral origin in insect retrotransposons as genetic elements advantageous for both transposons and their insect hosts.

A novel insect-infecting virga/nege-like virus group and its pervasive endogenization into insect genomes

“…Likewise, a similar manner of acquisition of virus-related sequences, such as those from nodaviruses and two (-)ssRNA viruses (phleboviruses and rhabdoviruses), might have occurred in LTR-retrotransposons of insects (Drosophila) and nematodes (Caenorhabditis elegans and Bursaphelenchus xylophilus) (Ballinger et al, 2012;Cotton et al, 2016;Malik et al, 2000). The acquisition of viral HEL domains by retrotransposons may be associated with the RNA silencing suppression activity of the HEL-like domains as demonstrated by Lazareva et al (2015), and is probably linked to the counteraction of the RNA silencing-based defense against retrotransposons in insect cells (Morozov et al, 2017).…”

Potential Role of Accessory Domains in Polyproteins Encoded by Retrotransposons in Anti-viral Defense of Host Cells

“…These data were further confirmed and extended for the chromosome-integrated HEL sequences of plus-RNA viruses in orders Diptera, Lepidoptera, Hymenoptera, and Thysanoptera (Kondo et al, 2017; Geisler, 2018). Transposon-encoded helicases were found to contain the full set of conserved motifs essential for their enzymatic activities (Morozov et al, 2017) and exhibit a weak, but detectable, ability to suppress RNA silencing in plant experimental system, as it was previously demonstrated for RNA helicase domains of some replicative tobamovirus proteins (Csorba et al, 2007; Wang et al, 2012; Lazareva et al, 2015). Importantly, it is well-known that silencing suppressors of insect viruses are also active in plants (Maliogka et al, 2012).…”

“…Previously we presented evidence for integration of the viral superfamily 1 RNA helicase (SF1 HEL or SF1H) coding sequences into insect genomes through acquisition by the retrotransposons containing no long terminal repeats (LTRs) (non-LTR-retrotransposons), namely, Long interspersed nuclear element-like (LINE-like) TRAS (Telomeric Repeat-Associated Element) of R1 clade in order Lepidoptera and LINEs of Jockey family in orders Hemiptera and Orthoptera. Moreover, in orders Diptera and Hymenoptera, the SF1 HEL domains were found to be translationally fused to proteins encoded by LTR retrotransposons (Lazareva et al, 2015; Morozov et al, 2017). These data were further confirmed and extended for the chromosome-integrated HEL sequences of plus-RNA viruses in orders Diptera, Lepidoptera, Hymenoptera, and Thysanoptera (Kondo et al, 2017; Geisler, 2018).…”

“…Importantly, it is well-known that silencing suppressors of insect viruses are also active in plants (Maliogka et al, 2012). Moreover, although helicase-coding sequences represent actively transcribed insect genome regions, RNA helicase domains seem to perform no essential functions in retrotransposition and the transposon transcription/translation, and their functions can be considered as only accessory (Morozov et al, 2017).…”

“…We proposed hypothetic evolutionary scenarios explaining the natural selection-supported preservation of the retrotransposon SF1H domains in insect genomes and considered two basic alternatives to explain the long-term evolutionary fixation of SF1 HEL in retrotransposons, namely, significance of this genetic element as advantageous for (i) transposons themselves or (ii) their insect hosts (Morozov et al, 2017). In one scenario, we supposed that both siRNA- and piRNA-mediated pathways blocking expression and transposition of retroelements (Ito, 2012; Lazareva et al, 2015; Guida et al, 2016; Mondal et al, 2018) can be suppressed by the encoded SF1H silencing suppressor activity.…”