Abstract
BackgroundMitochondrial gene loss and functional transfer to the nucleus is an ongoing process in many lineages of plants, resulting in substantial variation across species in mitochondrial gene content. The Caryophyllaceae represents one lineage that has experienced a particularly high rate of mitochondrial gene loss relative to other angiosperms.ResultsIn this study, we report the first complete mitochondrial genome sequence from a member of this family, Silene latifolia. The genome can be mapped as a 253,413 bp circle, but its structure is complicated by a large repeated region that is present in 6 copies. Active recombination among these copies produces a suite of alternative genome configurations that appear to be at or near "recombinational equilibrium". The genome contains the fewest genes of any angiosperm mitochondrial genome sequenced to date, with intact copies of only 25 of the 41 protein genes inferred to be present in the common ancestor of angiosperms. As observed more broadly in angiosperms, ribosomal proteins have been especially prone to gene loss in the S. latifolia lineage. The genome has also experienced a major reduction in tRNA gene content, including loss of functional tRNAs of both native and chloroplast origin. Even assuming expanded wobble-pairing rules, the mitochondrial genome can support translation of only 17 of the 61 sense codons, which code for only 9 of the 20 amino acids. In addition, genes encoding 18S and, especially, 5S rRNA exhibit exceptional sequence divergence relative to other plants. Divergence in one region of 18S rRNA appears to be the result of a gene conversion event, in which recombination with a homologous gene of chloroplast origin led to the complete replacement of a helix in this ribosomal RNA.ConclusionsThese findings suggest a markedly expanded role for nuclear gene products in the translation of mitochondrial genes in S. latifolia and raise the possibility of altered selective constraints operating on the mitochondrial translational apparatus in this lineage.
Highlights
Mitochondrial gene loss and functional transfer to the nucleus is an ongoing process in many lineages of plants, resulting in substantial variation across species in mitochondrial gene content
Plant mitochondrial genomes contain genes for their own rRNA subunits as well as for some of the ribosomal proteins and tRNAs required for translation (Figure 1), but many necessary ribosomal protein and tRNA genes are located in the nuclear genome, so their gene products must be imported into the mitochondrion [15]
Adams et al [19] used Southern blots to show that 2 genera from this family (Dianthus and Stellaria) lack most mitochondrial protein genes outside the core set of 24 genes that are nearly universally conserved throughout angiosperms, and we recently reported that 2 species from a third genus (Silene) are reduced in gene content [22]
Summary
Mitochondrial gene loss and functional transfer to the nucleus is an ongoing process in many lineages of plants, resulting in substantial variation across species in mitochondrial gene content. The mitochondrial genomes of flowering plants exhibit a number of characteristics that distinguish them from the mitochondrial genomes of other eukaryotes [1] They are large and variable in size with ample non-coding content [2], including substantial amounts of “promiscuous” DNA of nuclear and chloroplast origin [3,4] as well as sequences of horizontal origin acquired from the mitochondrial genomes of other land plants [5,6]. The tRNA population within plant mitochondria represents a complex assemblage derived from at least 3 anciently divergent classes of genes [15,16,17]: 1) “native” tRNAs encoded in the mitochondrial genome and inherited from the a-proteobacterial progenitor of mitochondria, 2) chloroplast-like tRNAs, which are encoded in the mitochondrial genome but which were acquired by functional gene transfer from the chloroplast genome during land plant evolution, and 3) nuclear-encoded tRNAs imported from the cytosol
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