Dynamic evolution of Geranium mitochondrial genomes through multiple horizontal and intracellular gene transfers

Abstract

Summary The exchange of genetic material between cellular organelles through intracellular gene transfer (IGT) or between species by horizontal gene transfer (HGT) has played an important role in plant mitochondrial genome evolution. The mitochondrial genomes of Geraniaceae display a number of unusual phenomena including highly accelerated rates of synonymous substitutions, extensive gene loss and reduction in RNA editing. Mitochondrial DNA sequences assembled for 17 species of Geranium revealed substantial reduction in gene and intron content relative to the ancestor of the Geranium lineage. Comparative analyses of nuclear transcriptome data suggest that a number of these sequences have been functionally relocated to the nucleus via IGT. Evidence for rampant HGT was detected in several Geranium species containing foreign organellar DNA from diverse eudicots, including many transfers from parasitic plants. One lineage has experienced multiple, independent HGT episodes, many of which occurred within the past 5.5 Myr. Both duplicative and recapture HGT were documented in Geranium lineages. The mitochondrial genome of Geranium brycei contains at least four independent HGT tracts that are absent in its nearest relative. Furthermore, G. brycei mitochondria carry two copies of the cox1 gene that differ in intron content, providing insight into contrasting hypotheses on cox1 intron evolution.

Foreign Plastid Sequences in Plant Mitochondria are Frequently Acquired Via Mitochondrion-to-Mitochondrion Horizontal Transfer

“…To determine the origin of the 1,385 MTPTs mentioned above (Table S1), all MTPTs with highest similarity to the ptDNA of an unrelated lineage were considered putatively foreign and were analyzed phylogenetically to confirm its origin and to determine the donor lineage. In addition to the 31 previously described cases815161727, 15 new foreign MTPTs were identified in this work (Table 1). MTPTs were considered foreign when phylogenetic analyses showed unexpected relationships with bootstrap support (BS) higher than 70% (Figure S2).…”

“…For example, MTPTs can create new gene forms or promoters, or may introduce novel functional tRNA genes10111213. Interestingly, some MTPTs were acquired by HGT from distant angiosperm species814151617. Whether these sequences were acquired directly from the donor plastid or indirectly from the donor mitochondria is still unclear and it is the focus of the present study.…”

Loss of aTrans-Splicingnad1Intron from Geraniaceae and Transfer of the Maturase GenematRto the Nucleus inPelargonium

“…Source of plant materials and procedures for nucleic acid extraction and Illumina sequencing were described previously (Weng et al 2014; Park et al 2015). Draft mitochondrial genomes were assembled with Velvet 1.1.06 (Zerbino and Birney 2008) using a combination of kmer (51–91) and expected coverage (20–500) values as previously described (Grewe et al 2014; Zhu et al 2014).…”

“…In Viscum album , matR was established as a freestanding gene due to loss of the host gene nad1 (Petersen et al 2015). The matR gene is also freestanding in several species of Geranium , presumably by translocation prior to the loss of the host intron (Park et al 2015). In the gnetophyte Welwitschia mirabilis , matR is no longer adjacent to any nad1 exons, but it is flanked by segments of the nad1i728 intron and may still be associated with the intron through a double trans -splicing event (Guo et al 2016).…”

“…In some other species of Viscum (Petersen et al 2015; Skippington et al 2015) and two species within Malpighiales (Wurdack and Davis 2009), the matR gene appears to be missing completely from the mitochondrial genome. Using the extensive genomic and transcriptomic data available for many species within Geraniaceae (Weng et al 2014; Park et al 2015; Zhang et al 2015; Blazier et al 2016), we assessed the status of matR and nad1 in this family and present an evolutionary scenario to explain the unusual structural and functional diversity among species.…”