Search bioRxiv⌕ Search

Biology subjects

Chary, S.

Publications and source records attributed to Chary, S..

3 recordsLinked to original sources

Conserved but mechanistically diverse piRNA defence against gypsy LTR retrotransposons in insect ovaries

Organisms have evolved highly adaptable defence systems to silence mobile genetic elements such as transposons. While individual transposons may emerge and vanish over time, the long-term evolutionary stability of the pathways that suppress them remains poorly understood. In the ovarian somatic cells of Drosophila, envelope-carrying gypsy long terminal repeat (LTR) retrotransposons are silenced by the Piwi-interacting RNA (piRNA) pathway, which depends exclusively on Piwi - an evolutionary derivative of an Aubergine/Piwi gene duplication unique to flies. Recent studies, however, have revealed that envelope-carrying gypsy elements are widespread across metazoans and particularly abundant in insect genomes, raising questions about the origin of ovarian somatic piRNA defence. Here we demonstrate that Aedes and Anopheles mosquitoes, as well as stingless bees and crickets, all produce piRNAs targeting gypsy elements in ovarian somatic cells, indicating a continuous arms race in this cellular niche for more than 400 million years of insect evolution. Notably, in Aedes aegypti, ovarian somatic cells express the same piRNA clusters as other somatic tissues, where they are known to target RNA viruses - suggesting a shared origin of anti-viral and anti-retrotransposon defences. Furthermore, we reveal striking lineage-specific differences in ovarian somatic piRNA biogenesis: slicing-independent phasing dominates in dipterans, ping-pong amplification in bees, and slicing-dependent phasing in crickets. Together, these findings indicate that distinct piRNA pathways have independently evolved at different timepoints to silence the same class of retrotransposons in insect evolution.

evolutionary biology↗

Ancient origins of endogenous retroviruses in Metazoans

Retrotransposons or endogenous retroviruses (ERVs) essentially carry open reading frames of gag and pol, which are utilized to selfishly replicate themselves in the host germline genome. One rare example of ERVs that additionally carry envelope genes is Ty3/gypsy errantiviruses in Drosophila. Though they are structurally analogous to retroviruses, it remained unclear whether envelope-containing Ty3/gypsy elements represent recent, lineage-specific acquisitions of viral fusogens or an ancient association between retrotransposons and envelope-like genes. We systematically searched for intact envelope-containing ERVs that are homologous to Ty3/gypsy in invertebrate metazoan genomes and found that they are widespread across taxa including ancient animals such as cnidarians, ctenophores and tunicates. Many elements occur as multiple highly similar copies in their respective genomes, consistent with recent genomic expansion in some host lineages. Envelope genes are classified into those that resemble glycoprotein F from paramyxoviruses and glycoprotein B from herpesviruses, and both types are equally abundant and widespread. Phylogenetic and structural analyses revealed that envelope genes have largely diverged with pol genes as well as with the host organisms throughout their evolutionary history and recombined infrequently, suggesting that the envelope acquisition to ERVs is ancient and likely dates to before the split of bilaterian and non-bilaterian animals in Pre-Cambrian era.

evolutionary biology↗

Mechanistic divergence of piRNA biogenesis in Drosophila

Organisms require mechanisms to distinguish self and non-self RNA. This distinction is crucial to initiate the biogenesis of piRNAs. In Drosophila ovaries, PIWI-guided slicing and the recognition of piRNA precursor transcripts by the DEAD-box RNA helicase Yb are the two known mechanisms to licence an RNA for piRNA biogenesis in the germline and the soma, respectively. Both, the PIWI proteins and Yb are highly conserved across most Drosophila species and are thought to be essential to the piRNA pathway and for silencing transposons. However, we find that species closely related to D. melanogaster have lost the yb gene, as well as the PIWI gene Ago3. We show that the precursor RNA is still selected in the absence of Yb to abundantly generate transposon antisense piRNAs in the soma. We further demonstrate that D. eugracilis, which lacks Ago3, is completely devoid of ping-pong piRNAs and exclusively produces phased piRNAs in the absence of slicing. Thus, there are more possible routes through which the piRNA pathway can achieve specificity than previously suggested.

molecular biology↗