DNA Transfer from Organelles to the Nucleus: The Idiosyncratic Genetics of Endosymbiosis

Abstract

In eukaryotes, DNA is exchanged between endosymbiosis-derived compartments (mitochondria and chloroplasts) and the nucleus. Organelle-to-nucleus DNA transfer involves repair of double-stranded breaks by nonhomologous end-joining, and resulted during early organelle evolution in massive relocation of organelle genes to the nucleus. A large fraction of the products of the nuclear genes so acquired are retargeted to their ancestral compartment; many others now function in new subcellular locations. Almost all present-day nuclear transfers of mitochondrial or plastid DNA give rise to noncoding sequences, dubbed nuclear mitochondrial DNAs (NUMTs) and nuclear plastid DNAs (NUPTs). Some of these sequences were recruited as exons, thus introducing new coding sequences into preexisting nuclear genes by a novel mechanism. In organisms derived from secondary or tertiary endosymbiosis, serial gene transfers involving nucleus-to-nucleus migration of DNA have also occurred. Intercompartmental DNA transfer therefore represents a significant driving force for gene and genome evolution, relocating and refashioning genes and contributing to genetic diversity.

Diversification of DnaA dependency for DNA replication in cyanobacterial evolution

“…Subsequently, the reorganization of genetic material and regulatory mechanisms, including those pertaining to DNA replication, occurred between the nucleus and the symbiont (Kleine et al, 2009;. Twinkle, an organelle DNA helicase and primase, is shared by plastids and mitochondria in green plants, whereas cyanobacterial dnaB helicase and dnaG primase are conserved in red algae.…”

Genetic aspects of mitochondrial genome evolution

“…Early in evolution this has led to the transfer of a large fraction of the mitogenomic information to the nuclear genome. The products of many of these genes are now re-imported while other genes of mitochondrial origin have acquired novel functions elsewhere (Kleine et al, 2009). Recent nuclear inserts of mitochondrial sequences, which occur at surprisingly high rate probably limited by the rates of double strand breaks (Hazkani-Covo et al, 2010), however, give rise to non coding and typically non-functional sequences.…”

Analysis of plastid and mitochondrial DNA insertions in the nucleus (NUPTs and NUMTs) of six plant species: size, relative age and chromosomal localization

“…There are still debates about the mechanism of DNA transfer from organelles to nucleus and the mode of integration (Leister, 2005;Kleine et al, 2009). It was suggested that the insertion mechanism involves double-strand break repair via NHEJ (Hazkani-Covo and Covo, 2008).…”