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 and/or recency of transfer. Amborella mtDNA has sustained proportionately more HGT than any other eukaryotic, or perhaps even prokaryotic, genome yet examined.

Fig. 1.

Phylogenetic evidence for horizontal acquisition of genes from mosses and angiosperms in Amborella. Shown are ML trees. Bootstrap values (100 ML replicates) >50% are shown. H and V indicate Amborella genes of putatively horizontal and vertical transmission, respectively. Amborella genes are in red, core eudicot genes are in blue (basal eudicots commonly included are Platanus, Eschscholzia, and Mahonia), and moss genes are in green. Note that for nad7, cox2, and nad4, seed and nonseed plants were analyzed separately. Scale bars correspond to 0.01 substitutions per site.

Fig. 2.

Amborella acquired three genes from different moss donors. The solid parts of the cladogram and nonparenthetical bootstrap values are from the nad5 intron phylogeny of Fig. 6. The dashed lines and other bootstrap values indicate the relationship to the indicated mosses of the moss-derived cox2 and nad7 genes of Amborella, as per the cox2 gene tree of Fig. 1 and the nad7 intron tree of Fig. 6.

Fig. 3.

Phylogenetic evidence for horizontal acquisition of 13 genes from angiosperms (mostly eudicots) in Amborella. Shown are ML trees. Bootstrap values (100 ML replicates) >50% are shown. H and V indicate Amborella genes of putatively horizontal and vertical transmission, respectively. Amborella genes are in red, and core eudicot genes are in blue (see Fig. 1 for basal eudicots). Scale bars correspond to 0.01 substitutions per site.

Fig. 4.

A. trichopoda leaf from a cloud forest at Massif de l'Aoupinié (Province Nord in New Caledonia) at 801 m altitude. Note the greenish bryophyte (liverwort) growth covering the leaf tip, and the small spots of lichens and other epiphytes elsewhere on the leaf. Photograph courtesy of Sean Graham, Centre for Plant Research, University of British Columbia, Vancouver.