Gorgeous mosaic of mitochondrial genes created by horizontal transfer and gene conversion

Abstract

The best known outcome of horizontal gene transfer (HGT) is the introduction of novel genes, but other outcomes have been described. When a transferred gene has a homolog in the recipient genome, the native gene may be functionally replaced (and subsequently lost) or partially overwritten by gene conversion with transiently present foreign DNA. Here we report the discovery, in two lineages of plant mitochondrial genes, of novel gene combinations that arose by conversion between coresident native and foreign homologs. These lineages have undergone intricate conversion between native and foreign copies, with conversion occurring repeatedly and differentially over the course of speciation, leading to radiations of mosaic genes involved in respiration and intron splicing. Based on these findings, we develop a model-the duplicative HGT and differential gene conversion model-that integrates HGT and ongoing gene conversion in the context of speciation. Finally, we show that one of these HGT-driven geneconversional radiations followed two additional types of conversional chimerism, namely, intramitochondrial retroprocessing and interorganellar gene conversion across the 2 billion year divide between mitochondria and chloroplasts. These findings expand our appreciation of HGT and gene conversion as creative evolutionary forces, establish plant mitochondria as a premiere system for studying the evolutionary dynamics of HGT and its genetic reverberations, and recommend careful examination of bacterial and other genomes for similar, likely overlooked phenomena.gene duplication | recombination

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

“…For instance, ∼13% (∼130 kb) of the zucchini mtDNA is represented by plastid-and nuclear-derived sequences, almost all of which are noncoding (82). Other angiosperms, like Plantago and ginger species, contain mitochondrial gene mosaics, formed by gene conversion between native and foreign homologs (83). Even more impressive is the mtDNA of the shrub Amborella trichopoda, which harbors the equivalent of six horizontally acquired mitochondrial genomes (84).…”

The evolution of land plants: a perspective from horizontal gene transfer

“…However, because acquired mitochondrial genes can be transferred to the nucleus or recombine with endogenous organellar DNA fragments, they may increase genetic variation of the recipient plant taxon [14,55,56]. Indeed, it has been demonstrated that gene acquisition and subsequent recombination/gene conversion led to some mosaic mitochondrial genes in plants [53,55,56].…”

Kde začínáme a kde končíme

“…Například jedna z nejstarších krytosemenných rostlin světa novokaledonská Amborella trichuta získala horizontálním transferem dvě třetiny svých mitochondriálních genů, přičemž pro třetinu výpůjček sáhla dokonce až k mechům (Bergthorsson et al 2004). Ještě "fantasmagoričtější" geny lze pozorovat v dědičné informaci portorického stromu Ternstroemia stahlii (Hao et al 2010). Jeden z jeho genů je složen jako puzzle z pěti dílků původního genu stromu a pěti podstatně větších dílů analogického genu brusnice (Viccinia).…”