Transposable elements: genome innovation, chromosome diversity, and centromere conflict

Abstract

Although it was nearly 70 years ago when transposable elements (TEs) were first discovered “jumping” from one genomic location to another, TEs are now recognized as contributors to genomic innovations as well as genome instability across a wide variety of species. In this review, we illustrate the ways in which active TEs, specifically retroelements, can create novel chromosome rearrangements and impact gene expression, leading to disease in some cases and species-specific diversity in others. We explore the ways in which eukaryotic genomes have evolved defense mechanisms to temper TE activity and the ways in which TEs continue to influence genome structure despite being rendered transpositionally inactive. Finally, we focus on the role of TEs in the establishment, maintenance, and stabilization of critical, yet rapidly evolving, chromosome features: eukaryotic centromeres. Across centromeres, specific types of TEs participate in genomic conflict, a balancing act wherein they are actively inserting into centromeric domains yet are harnessed for the recruitment of centromeric histones and potentially new centromere formation.

Islands of retroelements are the major components ofDrosophilacentromeres

“…The finding that CENP-A can bind to several different sequences that are not uniquely associated with centromere regions is consistent with the epigenetic model of centromere specification, which proposes that specific sequences alone do not govern centromere activity [3]. Yet it is possible that the diverse sequence arrangements observed at each centromere somehow contribute to centromere activity or specification [18,39]. Possible mechanisms include the promotion of unusual types of transcription, as reported for fission yeast [64], or the formation of non-B DNA structures (e.g.…”

“…We also find G2/Jockey-3 enriched at the centromeres of D. simulans, which has centromeric satellite arrays highly divergent from those of D. melanogaster [16]. Collectively, these data are consistent with the model that retroelements may have a conserved role in centromere specification and function, as proposed for other species (for review see [18]).…”

“…Why retroelements are such ubiquitous components of centromeres and if they play an active role in centromere function remain open questions. In maize, centromeric retroelements invade neocentromeres following their inception [47], suggesting a preference for DNA sequences associated with CENP-A chromatin for retroelement insertion [18]. On the other hand, a LINE-element was found to be an integral component of a human neocentromere [48,49], raising the possibility that it is CENP-A that may bind preferentially to retroelementassociated genomic regions [18].…”

“…In maize, centromeric retroelements invade neocentromeres following their inception [47], suggesting a preference for DNA sequences associated with CENP-A chromatin for retroelement insertion [18]. On the other hand, a LINE-element was found to be an integral component of a human neocentromere [48,49], raising the possibility that it is CENP-A that may bind preferentially to retroelementassociated genomic regions [18]. Other models have proposed that retroelements could produce non-coding RNAs that affect centromere specification [18,48], and that retroelement activity could help maintain centromere size through retrotransposition or by giving rise to tandem repeats via recombination-mediated mechanisms (e.g.…”

The Mobilome of Reptiles: Evolution, Structure, and Function

“…TEs can increase genome size through copy number increase via transposition, TE-induced ectopic recombination resulting in changes in genome size, and by TE-mediated satellite expansions [Canapa et al, 2015;Klein and O'Neill, 2018]. While genomes may increase in size with TE activity, recombination-driven deletions counteract this effect, in some cases maintaining genome size even in the face of TE activity .…”