Transposable element and host silencing activity in gigantic genomes

Abstract

Transposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the question of whether TE silencing also deviates from typical conditions. To address this question, we characterize TE silencing via two pathways—the piRNA pathway and KRAB-ZFP transcriptional repression—in the male and female gonads of Ranodon sibiricus, a salamander species with a ∼21 Gb genome. We quantify 1) genomic TE diversity, 2) TE expression, and 3) small RNA expression and find a significant relationship between the expression of piRNAs and TEs they target for silencing in both ovaries and testes. We also quantified TE silencing pathway gene expression in R. sibiricus and 14 other vertebrates with genome sizes ranging from 1 to 130 Gb and find no association between pathway expression and genome size. Taken together, our results reveal that the gigantic R. sibiricus genome includes at least 19 putatively active TE superfamilies, all of which are targeted by the piRNA pathway in proportion to their expression levels, suggesting comprehensive piRNA-mediated silencing. Testes have higher TE expression than ovaries, suggesting that they may contribute more to the species’ high genomic TE load. We posit that apparently conflicting interpretations of TE silencing and genomic gigantism in the literature, as well as the absence of a correlation between TE silencing pathway gene expression and genome size, can be reconciled by considering whether the TE community or the host is currently “on the attack” in the arms race dynamic.

Limited stress and tissue-specific transcriptional and translational activity of transposable elements in mosquitoes

“…The high number of expressed TE families contrasts with the classical notion that most TEs are silenced and only a very limited number successfully achieve transcriptional expression (92). However, these findings are consistent with recent observations in other animal species, exemplified by the widespread TE expression observed in the salamander Ranodon sibiricus (93), and rats Rattus norvegicus , where 54% of TEs are expressed in at least one different organ (94). Furthermore, even in unrelated organisms such as the pathogenic fungus Zymoseptoria tritici , the majority of TE families are expressed in some strains under natural conditions (95).…”

“…The repression of TEs in ovaries relative to somatic tissues and testes is nearly a rule among animals. TE expression in mosquitos is in line with high repression in the ovaries (between 8% and 46% of the TEs of a species) and that had been previously observed in other organisms (15, 93, 115–117). Only in a few species, such as the Japanese flounder Paralichthys olivaceus and two species of crow, TEs are more expressed in the ovaries than in the testes (118, 119).…”

“…This TE expression pattern in mosquito gonads adds another layer of evidence indicating a sex-biased TE expression in germline tissues of most animals, with overexpression of TEs in the testes. This pattern of expression is found in many species, such as the case of D. melanogaster (115), a species that belongs to the Diptera order (just like mosquitoes), and the case of very distantly related organisms, as vertebrates, where TEs show a higher expression in testes than in ovaries (15, 93). In certain species, such as Rattus norvegicus , TE expression levels in the testis surpass those in most somatic tissues (94).…”

“…The same pathway seems to be active in vertebrates, such as the zebrafish, in which piRNAs are expressed only in germline tissues and, among those piRNAs that map against TEs, in higher abundance in the ovaries than in the testes (123). However, this is not always the case, in salamander R. sibiricus , there are more piRNAs in the testis than in the ovaries (93). Although there are currently no RNA-Seq experiments targeting small RNAs to confirm the hypothesis of a higher amount of piRNAs acting in the mosquito ovaries, we can use expression data of proteins that participate in some steps of the silencing cascade.…”

Metamorphosis Imposes Variable Constraints on Genome Expansion through Effects on Development

“…TE activity can be nearly neutral, largely missing functional genomic regions, and therefore resulting in negligible fitness consequences ( Arkhipova 2018 ). Salamanders are particularly prone to stochastic increases in genome size through TE accumulation ( Sun et al 2012 ; Keinath et al 2015 ; Nowoshilow et al 2018 ) because they possess low TE deletion rates and incomplete TE silencing ( Sun and Mueller 2014 ; Frahry et al 2015 ; Madison-Villar et al 2016 ; Wang et al 2023 ).…”