Horizontal gene transfers dominate the functional mitochondrial gene space of a holoparasitic plant

Abstract

Summary Although horizontal gene transfer (HGT) is common in angiosperm mitochondrial DNAs (mtDNAs), few cases of functional foreign genes have been identified. The one outstanding candidate for large‐scale functional HGT is the holoparasite Lophophytum mirabile, whose mtDNA has lost most native genes but contains intact foreign homologs acquired from legume host plants. To investigate the extent to which this situation results from functional replacement of native by foreign genes, functional mitochondrial gene transfer to the nucleus, and/or loss of mitochondrial biochemical function in the context of extreme parasitism, we examined the Lophophytum mitochondrial and nuclear transcriptomes by deep paired‐end RNA sequencing. Most foreign mitochondrial genes in Lophophytum are highly transcribed, accurately spliced, and efficiently RNA edited. By contrast, we found no evidence for functional gene transfer to the nucleus or loss of mitochondrial functions in Lophophytum. Many functional replacements occurred via the physical replacement of native genes by foreign genes. Some of these events probably occurred as the final act of HGT itself. Lophophytum mtDNA has experienced an unprecedented level of functional replacement of native genes by foreign copies. This raises important questions concerning population‐genetic and molecular regimes that underlie such a high level of foreign gene takeover.

Transcriptional Landscape and Splicing Efficiency in Arabidopsis Mitochondria

“…We analyzed each of the three data sets individually and combined, totaling 617,847,968 pairedend reads. This volume of data is comparable with previous, large-scale RNAseq studies on angiosperm mitochondria [23,33,45]. The pooled RNAseq reads were aligned strand specifically to the corrected sequence of the A. thaliana ecotype Columbia mtDNA, NCBI accession number BK010421 [46].…”

“…Occasionally, non-coding regions show high RNA read depth suggesting a possible role as long non-coding RNAs. These regions are generally not conserved and have not been further characterized [33][34][35].…”

“…The splicing process of intron-containing genes in plant mitochondria has been analyzed for the most part in mutants in order to identify the nuclear factors involved [25,[37][38][39]. However, the efficiency of the splicing activity has only rarely been studied in wild type plants [26,33] with no comparative analyses among introns, either group I or II, or cis-and trans-spliced introns that co-exist in plant mitochondrial genomes.…”

Complete Plastid and Mitochondrial Genomes of Aeginetia indica Reveal Intracellular Gene Transfer (IGT), Horizontal Gene Transfer (HGT), and Cytoplasmic Male Sterility (CMS)

“…This gene clustered closely with monocot species ( Figure 3 D), and monocots like Miscanthus sinensis are known A. indica hosts, which suggest that the atpI chloroplast gene was transferred from a host to A. indica . Most HGT events typically occur between mitochondrial or between chloroplast genomes of different species [ 8 , 42 , 43 ]. However, the atpI gene in the A. indica mitochondrial genome was acquired from the chloroplast genome of another species.…”

Mitochondrial genomes of two parasiticCuscutaspecies lack clear evidence of horizontal gene transfer and retain unusually fragmentedccmFCgenes

“…An extreme example of incorporated foreign DNA in a mitogenome is Lophophytum mirabile (Balanophoraceae), which is inferred to have acquired approximately 80% of its genes and 60% of its sequence from its host [22, 23]. Another example includes members of Rafflesiaceae, for which up to 40% of their mitochondrial genes are inferred to have been transferred, with many of the putatively transferred genes shown to be actively transcribed [24], though whether the inferred transfers are indeed foreign and/or functional has recently been questioned [25].…”