Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes

Abstract

Autonomous transposable elements, generally considered as junk and selfish, encode transposition proteins that can bind, copy, break, join or degrade nucleic acids as well as process or interact with other proteins. Such a repertoire of activities might be of interest for the host cell. There is indeed substantial evidence that mobile DNA can serve as a dynamic reservoir for new cellular functions. Transposable element genes encoding transposase, integrase, reverse transcriptase as well as structural and envelope proteins have been repeatedly recruited by their host during evolution in most eukaryotic lineages. Such domesticated sequences protect us against infections, are necessary for our reproduction, allow the replication of our chromosomes and control cell proliferation and death; others are essential for plant development. Many new candidates for domesticated sequences have been revealed by sequencing projects. Their functional analysis will uncover new aspects of evolutionary alchemy, the turning of junk into gold within genomes.

Transposable elements as drivers of genomic and biological diversity in vertebrates

“…Finally, extinction of transposable element families might be linked to molecular domestication events. In many cases, the original transposable element source of the exapted sequence has been eliminated (Volff 2006). This might prevent uncontrolled mobilization in trans and multiplication of the new gene and avoid its integration in unfavourable transcriptional contexts.…”

“…New lineage-specific protein-coding genes have been derived from transposable elements during vertebrate evolution (Volff 2006). Hundreds of such genes have been identified in the human genome, some of them with important functions in various major biological processes (Zdobnov et al 2005).…”

“…Interestingly, Syncytin-like genes have been introduced into primate, murine and ovine lineages through independent retroviral infections. Other envelope genes with unknown functions, as well as genes derived from integrases and retroviral-like proteases, are present in mammalian and other vertebrate genomes, where they await further characterization (Krylov & Koonin 2001, Blaise et al 2003, Volff 2006.…”

“…At first glance, transposable elements behave as Fjunk_ DNA or genomic parasites exploiting host resources for selfish purposes (Doolittle & Sapienza 1980, Orgel & Crick 1980. However, this view has been seriously challenged by a wave of observations supporting a major role of mobile DNA in the structural and functional evolution of genes and genomes in a variety of organisms (Kazazian 2004, Biémont & Vieira 2006 Thornburg et al 2006, Volff 2006, Piriyapongsa et al 2007, Volff & Brosius 2007. Many of these sequences fulfil biological functions important to the host.…”

Transposable elements and genomics

“…TEs are considered indispensable genomic treasures during eukaryotic species evolution and supply raw materials for evolution by creating novel variation and allelic diversity (Volff 2006;Oliver et al 2013). TEs are found ubiquitously with high copies in nearly all eukaryotic species.…”