Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes

Abstract

BackgroundHorizontal gene transfer (HGT) is relatively common in plant mitochondrial genomes but the mechanisms, extent and consequences of transfer remain largely unknown. Previous results indicate that parasitic plants are often involved as either transfer donors or recipients, suggesting that direct contact between parasite and host facilitates genetic transfer among plants.ResultsIn order to uncover the mechanistic details of plant-to-plant HGT, the extent and evolutionary fate of transfer was investigated between two groups: the parasitic genus Cuscuta and a small clade of Plantago species. A broad polymerase chain reaction (PCR) survey of mitochondrial genes revealed that at least three genes (atp1, atp6 and matR) were recently transferred from Cuscuta to Plantago. Quantitative PCR assays show that these three genes have a mitochondrial location in the one species line of Plantago examined. Patterns of sequence evolution suggest that these foreign genes degraded into pseudogenes shortly after transfer and reverse transcription (RT)-PCR analyses demonstrate that none are detectably transcribed. Three cases of gene conversion were detected between native and foreign copies of the atp1 gene. The identical phylogenetic distribution of the three foreign genes within Plantago and the retention of cytidines at ancestral positions of RNA editing indicate that these genes were probably acquired via a single, DNA-mediated transfer event. However, samplings of multiple individuals from two of the three species in the recipient Plantago clade revealed complex and perplexing phylogenetic discrepancies and patterns of sequence divergence for all three of the foreign genes.ConclusionsThis study reports the best evidence to date that multiple mitochondrial genes can be transferred via a single HGT event and that transfer occurred via a strictly DNA-level intermediate. The discovery of gene conversion between co-resident foreign and native mitochondrial copies suggests that transferred genes may be evolutionarily important in generating mitochondrial genetic diversity. Finally, the complex relationships within each lineage of transferred genes imply a surprisingly complicated history of these genes in Plantago subsequent to their acquisition via HGT and this history probably involves some combination of additional transfers (including intracellular transfer), gene duplication, differential loss and mutation-rate variation. Unravelling this history will probably require sequencing multiple mitochondrial and nuclear genomes from Plantago.See Commentary: http://www.biomedcentral.com/1741-7007/8/147.

Horizontal gene transfer from a flowering plant to the insular pine Pinus canariensis (Chr. Sm. Ex DC in Buch)

“…The angiosperm-derived exons 1 and 2 contained premature stop codons and thus were nonfunctional (see above), indicating pseudogenization of the foreign nad5-1 in the host' genome after acquisition by HGT. Gene conversion between native and foreign gene copies has been reported in previous studies of HGT Mower et al, 2010), but this was not detected between the two nad5-1 copies in P. canariensis. Future sequencing of the whole mt genome of P. canariensis is needed in order to clarify the accurate location of the two segments in the mt genome of P. canariensis, and the extent of mt HGT in this species.…”

“…To determine the genomic location of the angiosperm-type nad5-1 in P. canariensis, we applied a quantitative PCR (qPCR) strategy similar to that used by Mower et al (2010). This approach is based on the fact that the copy numbers of the plastid (highest), mt (intermediate) and nuclear (lowest) genomes differ widely in a plant cell (Petit and Vendramin, 2007), and genes with a similar number of copies should be amplified at similar rates.…”

“…In cases where HGT has occurred between species without parasitic or epiphytic relationships, transfer of foreign DNA via vectors such as bacteria or fungi has been suggested as an alternative route (Bergthorsson et al, 2003;Won and Renner, 2003;Bock, 2010). After gene transfer via HGT, foreign genes often undergo modifications such as gene conversion, differential gene loss and a change in mutation rate (Won and Renner, 2003;Hao et al, 2010;Mower et al, 2010). These processes are creative forces in the generation of mt genetic diversity and have an important role in plant mt genome evolution (Archibald and Richards, 2010;Hao et al, 2010;Mower et al, 2010).…”

“…Generally, HGT is less common in multicellular than in unicellular eukaryotes (Keeling and Palmer, 2008). In vascular plants, HGT appears to be rare in plastid and nuclear genomes but is frequent in the mitochondrial (mt) genome (Richardson and Palmer, 2007;Bock, 2010), and is facilitated by intimate physical associations between donor and recipient species through parasitism or epiphytism (Davis et al, 2005;Mower et al, 2010;Rice et al, 2013;Xi et al, 2013). The most extensive mt HGT events have been detected in the basal angiosperm Amborella, which acquired more than one megabase of foreign mtDNA, including four entire mt genomes from its epiphytes (Rice et al, 2013).…”

“…After gene transfer via HGT, foreign genes often undergo modifications such as gene conversion, differential gene loss and a change in mutation rate (Won and Renner, 2003;Hao et al, 2010;Mower et al, 2010). These processes are creative forces in the generation of mt genetic diversity and have an important role in plant mt genome evolution (Archibald and Richards, 2010;Hao et al, 2010;Mower et al, 2010).…”