Transposable elements: Self‐seekers of the germline, team‐players of the soma

Abstract

The germ track is the cellular path by which genes are transmitted to future generations whereas somatic cells die with their body and do not leave direct descendants. Transposable elements (TEs) evolve to be silent in somatic cells but active in the germ track. Thus, the performance of most bodily functions by a sequestered soma reduces organismal costs of TEs. Flexible forms of gene regulation are permissible in the soma because of the self-imposed silence of TEs, but strict licensing of transcription and translation is maintained in the germ track to control proliferation of TEs. Delayed zygotic genome activation (ZGA) and maternally inherited germ granules are adaptations that enhance germ-track security. Mammalian embryos exhibit very early ZGA associated with extensive mobilization of retroelements. This window of vulnerability to retrotransposition in early embryos is an indirect consequence of evolutionary conflicts within the mammalian genome over postzygotic maternal provisioning.

Retrotransposons Mimic Germ Plasm Determinants to Promote Transgenerational Inheritance

“…In this way, certain mobile elements appear to invade rudimentary components of germ cells that eventually form ‘grandchildren’ through the maternal lineage. Hence, germ plasm targeting could represent a fitness strategy that promotes transmission in subsequent generations and, at the same time, may evade un-necessary costs associated with transposition in somatic cells [35]. We found compelling support for this in our case study of the Drosophila Tahre retroelement.…”

Transposable Element Domestication As an Adaptation to Evolutionary Conflicts

“…This conflict is predicted to result in an evolutionary arms race driving rapid placental evolution and potentially Syncytin evolution. The model is supported by several genetic observations, including certain patterns of gene expression (imprinting; that reveals that the conflict might even start as a mother-father conflict [75, 76]) and evolution (positive selection) that are prevalent for placental-specific genes, and at an anatomical level by the remarkable diversification of this organ during mammalian evolution [69, 74, 77, 78]. …”

“…A placenta feature that might facilitate the recurrent Syncytin cooption for placenta function could be the low level of DNA methylation relative to other tissues, which tends to promote the expression of TEs and endogenous retroviruses in particular in this organ [76, 79, 80]. In addition to the Syncytins , i.e., endogenous retrovirus gene domestication, numerous ERV and other TE sequences have been coopted as cis-regulatory elements to coordinate placental or uterine gene expression during pregnancy [81, 82].…”

Two modes of targeting transposable elements by piRNA pathway in human testis

“…At the postnatal phase, pachytene cluster-driven piRNA production targets almost all TE subfamilies in late spermatogenesis. Despite this intricate mechanism designed for the purpose of tackling TE expansion, repeats have been consistently overcoming barriers to their transposition and spreading throughout genomes and populations (Haig 2016). This host-parasite coevolution is reminiscent of an arms race (Jacobs et al 2014); it is also conceivable, however, that repeat expansion is successful partly due to the co-option of TEs within host regulatory networks (Chuong et al 2016(Chuong et al , 2017Shapiro 2016).…”