Hijacking Oogenesis Enables Massive Propagation of LINE and Retroviral Transposons

Abstract

Although animals have evolved multiple mechanisms to suppress transposons, "leaky" mobilizations that cause mutations and diseases still occur. This suggests that transposons employ specific tactics to accomplish robust propagation. By directly tracking mobilization, we show that, during a short and specific time window of oogenesis, retrotransposons achieve massive amplification via a cell-type-specific targeting strategy. Retrotransposons rarely mobilize in undifferentiated germline stem cells. However, as oogenesis proceeds, they utilize supporting nurse cells-which are highly polyploid and eventually undergo apoptosis-as factories to massively manufacture invading products. Moreover, retrotransposons rarely integrate into nurse cells themselves but, instead, via microtubule-mediated transport, they preferentially target the DNA of the interconnected oocytes. Blocking microtubule-dependent intercellular transport from nurse cells significantly alleviates damage to the oocyte genome. Our data reveal that parasitic genomic elements can efficiently hijack a host developmental process to propagate robustly, thereby driving evolutionary change and causing disease.

Natural depletion of H1 in sex cells causes DNA demethylation, heterochromatin decondensation and transposon activation

“…TE activation in the VC – a cell that engulfs the male plant gametes – has been proposed as a defense strategy, which generates small RNAs that enhance TE silencing in sperm (Calarco et al, 2012; Ibarra et al, 2012; Martinez et al, 2016; Slotkin et al, 2009). However, TEs can also use companion cells as staging grounds for invasion of the gametes (Wang, Dou, Moon, Tan, & Zhang, 2018). Our demonstration that programmed DME demethylation, which is facilitated by developmental heterochromatin decondensation, is the predominant cause of VC TE activation is consistent with a defensive, host-beneficial model.…”

Genomic Accumulation of Retrotransposons Was Facilitated by Repressive RNA‐Binding Proteins: A Hypothesis

“…Hence, there is an equilibrium with the host repressing retrotransposon transcription globally versus selective escape by the retrotransposons targeting the germline. This dynamic is best embodied in Drosophila, where the I‐element retrotransposon propagates via the oocyte nursing cells, which effectively excludes any fitness cost to the individuum itself; as well as the mammalian testis, in which activation of IAV elements in the male mouse occurs in spermatogonia …”

piRNA clusters need a minimum size to control transposable element invasions

“…This TE reactivation may lead to diverse defects. The I-element causes developmental defects that prevent hatching of larvae (Bucheton et al, 1976(Bucheton et al, , 1992Wang et al, 2018). Hobo and P-element activity lead to dysgenic and mostly sterile ovaries (Kidwell, 1983;Kidwell et al, 1977;Blackman et al, 1987;Hill et al, 2016).…”