Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella

Abstract

Several plants are known to have acquired a single mitochondrial gene by horizontal gene transfer (HGT), but whether these or any other plants have acquired many foreign genes is entirely unclear. To address this question, we focused on Amborella trichopoda, because it was already known to possess one horizontally acquired gene and because it was found in preliminary analyses to contain several more. We comprehensively sequenced the mitochondrial protein gene set of Amborella, sequenced a variable number of mitochondrial genes from 28 other diverse land plants, and conducted phylogenetic analyses of these sequences plus those already available, including the five sequenced mitochondrial genomes of angiosperms. Results indicate that Amborella has acquired one or more copies of 20 of its 31 known mitochondrial protein genes from other land plants, for a total of 26 foreign genes, whereas no evidence for HGT was found in the five sequenced genomes. Most of the Amborella transfers are from other angiosperms (especially eudicots), whereas others are from nonangiosperms, including six striking cases of transfer from (at least three different) moss donors. Most of the transferred genes are intact, consistent with functionality and͞or recency of transfer. Amborella mtDNA has sustained proportionately more HGT than any other eukaryotic, or perhaps even prokaryotic, genome yet examined. Genome sequencing has revealed that horizontal gene transfer (HGT), the transfer of genes between nonmating species, is remarkably common and important in bacterial evolution (1). The current picture of HGT in eukaryotes is decidedly mixed. Other than the special case of mobile genetic elements (and plant mitochondrial genomes, see below), HGT is largely unknown in multicellular eukaryotes but is more or less common in diverse groups of unicellular protists, which contain several to many genes derived by HGT from both prokaryotes and other protists (2).Recent studies indicate that plant mtDNAs are unusually active in HGT relative to all other organellar genomes and nuclear genomes of multicellular eukaryotes. Four papers (3-6) have reported a total of nine cases of mitochondrial HGT within seed plants. Three transfers involve parasitic angiosperms as putative donors or recipients and implicate direct, plant-to-plant transfer of DNA as one mechanism of HGT (5, 6). Each of the nine transfers involves a different set of recipient plants. For this reason, and because only a few mitochondrial genes have been scrutinized for potential HGT in these or any other plants, it is unclear whether these cases are singular exceptions in each genome or whether they are harbingers of perhaps massive mitochondrial HGT in certain plants.To address this uncertainty, we have assessed the origin and history of the mitochondrial protein gene set of Amborella trichopoda and the five angiosperms whose mtDNAs have been sequenced. Amborella was chosen because it was already known to contain one foreign gene (3) and because preliminary studies suggested it might be u...

Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants

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Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns

“…To date, most documented examples of plant-to-plant HGT involve mitochondrial DNA and/or parasite-host transfers (29)(30)(31)(32)(33)(34)(35)(36); only a handful of cases include functional nuclear genes (34, 37, 38), and even fewer have possible adaptive implications (39). Consequently, plant-to-plant HGT generally has been overlooked as a potentially significant factor in plant evolution.…”

Cyto-Nuclear Epistasis: Two-Locus Random Genetic Drift in Hermaphroditic and Dioecious Species

“…Adams and Palmer (2003) and Bergthorsson et al (2003Bergthorsson et al ( , 2004) discovered molecular evidence of intergenomic gene transfer from the mitochondrion to the host nuclear genome. In some species, there is evidence of massive transfer with evidence for 30-40 different events, while in other species the number of transfer events is only one or two Bergthorsson et al 2003Bergthorsson et al , 2004. Bergthorsson et al (2004) proposed that the mechanism for the process of gene transfer begins with the duplication of a gene(s) in the mitochondrial genome.…”

“…When inherited together, it is possible to select directly on an epistatic interaction between cytoplasmic and nuclear genes. In addition, to the extent that such gene combinations tend to be inherited together, genomic conflict is mitigated and intergenomic gene transfer (Bergthorsson 2003(Bergthorsson , 2004) is facilitated, because the evolutionary fate of genes in both genomes is conjoined.…”