We summarize our recent studies showing that angiosperm mitochondrial (mt) genomes have experienced remarkably high rates of gene loss and concomitant transfer to the nucleus and of intron acquisition by horizontal transfer. Moreover, we find substantial lineage-specific variation in rates of these structural mutations and also point mutations. These findings mostly arise from a Southern blot survey of gene and intron distribution in 281 diverse angiosperms. These blots reveal numerous losses of mt ribosomal protein genes but, with one exception, only rare loss of respiratory genes. Some lineages of angiosperms have kept all of their mt ribosomal protein genes whereas others have lost most of them. These many losses appear to reflect remarkably high (and variable) rates of functional transfer of mt ribosomal protein genes to the nucleus in angiosperms. The recent transfer of cox2 to the nucleus in legumes provides both an example of interorganellar gene transfer in action and a starting point for discussion of the roles of mechanistic and selective forces in determining the distribution of genetic labor between organellar and nuclear genomes. Plant mt genomes also acquire sequences by horizontal transfer. A striking example of this is a homing group I intron in the mt cox1 gene. This extraordinarily invasive mobile element has probably been acquired over 1,000 times separately during angiosperm evolution via a recent wave of cross-species horizontal transfers. Finally, whereas all previously examined angiosperm mtDNAs have low rates of synonymous substitutions, mtDNAs of two distantly related angiosperms have highly accelerated substitution rates.
Plant mitochondrial (mt) genomes have long been known to evolve slowly in sequence. Here we show remarkable departure from this pattern of conservative evolution in a genus of flowering plants. Substitution rates at synonymous sites vary substantially among lineages within Plantago. At the extreme, rates in Plantago exceed those in exceptionally slow plant lineages by Ϸ4,000-fold. The fastest Plantago lineages set a new benchmark for rapid evolution in a DNA genome, exceeding even the fastest animal mt genome by an order of magnitude. All six mt genes examined show similarly elevated divergence in Plantago, implying that substitution rates are highly accelerated throughout the genome. In contrast, substitution rates show little or no elevation in Plantago for each of four chloroplast and three nuclear genes examined. These results, combined with relatively modest elevations in rates of nonsynonymous substitutions in Plantago mt genes, indicate that major, reversible changes in the mt mutation rate probably underlie the extensive variation in synonymous substitution rates. These rate changes could be caused by major changes in any number of factors that control the mt mutation rate, from the production and detoxification of oxygen free radicals in the mitochondrion to the efficacy of mt DNA replication and͞or repair. genome evolution ͉ plant mitochondria ͉ Plantago ͉ rate variation ͉ synonymous substitution rates I n a pioneering study 25 years ago, Brown et al.(1) discovered that primate mitochondrial (mt) DNA evolves rapidly at the sequence level compared with nuclear DNA. With rare exception (2), most animal mt DNAs have been found to evolve rapidly in sequence (3-6). Rapid mt evolution may be the rule in other groups of eukaryotes, although this conclusion must be tempered by the scanty data and distant comparisons available for most groups (7,8). Plants are the most glaring exception to the general rule that mt DNA evolves rapidly in sequence. In 1987, Wolfe et al. (9) showed that rates of synonymous substitution in angiosperm mt genes are anomalously low, a few-fold lower than in chloroplast genes, Ϸ10-to 20-fold lower than in nuclear genes of both angiosperms and mammals, and Ϸ50-to 100-fold lower than in mammalian mt genes. A year later, Palmer and Herbon (10) extended the inference of low rates of sequence change to the entire plant mt genome (most of which is noncoding) and showed that rates of sequence and structural evolution are dramatically uncoupled in plant mt DNA.All subsequent studies have confirmed that nucleotide substitution rates are in general quite low in land plant mt genomes (11,12). At the same time, moderate variation in synonymous substitution rates (R S ) (up to 7-fold) has been found in comparing several groups of plants (13)(14)(15)(16). In most cases, correlated rate changes are seen for chloroplast and͞or nuclear genes. Forces operating across the two organelle genomes or all three genomes, such as paternal transmission of organelles or generation-time effects, respectively, hav...
Group I introns are mobile, self-splicing genetic elements found principally in organellar genomes and nuclear rRNA genes. The only group I intron known from mitochondrial genomes of vascular plants is located in the cox1 gene of Peperomia, where it is thought to have been recently acquired by lateral transfer from a fungal donor. Southern-blot surveys of 335 diverse genera of land plants now show that this intron is in fact widespread among angiosperm cox1 genes, but with an exceptionally patchy phylogenetic distribution. Four lines of evidence-the intron's highly disjunct distribution, many incongruencies between intron and organismal phylogenies, and two sources of evidence from exonic coconversion tracts-lead us to conclude that the 48 angiosperm genera found to contain this cox1 intron acquired it by 32 separate horizontal transfer events. Extrapolating to the over 13,500 genera of angiosperms, we estimate that this intron has invaded cox1 genes by cross-species horizontal transfer over 1,000 times during angiosperm evolution. This massive wave of lateral transfers is of entirely recent occurrence, perhaps triggered by some key shift in the intron's invasiveness within angiosperms.Many group I introns encode site-specific endonucleases that catalyze their efficient spread from intron-containing to intronless alleles of the same gene in genetic crosses (1-3). This process, termed intron ''homing,'' has been observed for introns located in a variety of mitochondrial (mt) and chloroplast genes (4-7), in nuclear rRNA genes of the slime mold Physarum (8), and in protein genes of T-even phage (9). Homing is initiated by the intron-encoded endonuclease, which makes a staggered double-strand break at its target site within a recipient intronless allele, and is thought to then proceed by the double-strand-break repair pathway (10).The evolutionary importance of intron homing to the spread of group I introns across species barriers has been unclear, as relatively few cases of the horizontal transfer of group I introns between identical genomic sites of nonmating organisms are documented (11-17). Most of these cases involve the same genome and species belonging to the same phylum, usually fungi (11-13). Two notable exceptions are the transfer of two group I introns between identical sites of rRNA genes located in the chloroplast of a Chlamydomonas-type green alga and the mitochondrion of an Acanthamoeba-like ameboid (15).The only group I intron known from vascular plant mt genomes (which contain many group II introns) is also thought to have been acquired by homing-mediated horizontal transfer from a distantly related organism. This intron is present in the cox1 (cytochrome oxidase subunit 1) gene of the angiosperm Peperomia (16, 17) at the same location as related introns in the nonvascular plant Marchantia, the green alga Prototheca, the slime mold Dictyostelium, and several diverse fungi (see ref. 18 and references therein). This cox1 intron is thought to have been recently acquired by Peperomia, most likel...
The first evidence for the emergence of land plants (embryophytes) consists of mid-Ordovician spore tetrads (approximately 476 Myr old). The identity of the early plants that produced these spores is unclear; they are sometimes claimed to be liverworts, but there are no associated megafossils, and similar spores can be produced by a diversity of plants. Indeed, the earliest unequivocal megafossils of land plants consist of early vascular plants and various plants of uncertain affinity. Different phylogenetic analyses have identified liverworts, hornworts and bryophytes as each being the first lineage of land plants; the consensus of these conflicting topologies yields an unresolved polychotomy at the base of land plants. Here we survey 352 diverse land plants and find that three mitochondrial group II introns are present, with occasional losses, in mosses, hornworts and all major lineages of vascular plants, but are entirely absent from liverworts, green algae and all other eukaryotes. These results indicate that liverworts are the earliest land plants, with the three introns having been acquired in a common ancestor of all other land plants, and have important implications concerning the early stages of plant evolution.
Horizontal gene transfer is surprisingly common among plant mitochondrial genomes. The first well-established case involves a homing group I intron in the mitochondrial cox1 gene shown to have been frequently acquired via horizontal transfer in angiosperms. Here, we report extensive additional sampling of angiosperms, including 85 newly sequenced introns from 30 families. Analysis of all available data leads us to conclude that, among the 640 angiosperms (from 212 families) whose cox1 intron status has been characterized thus far, the intron has been acquired via roughly 70 separate horizontal transfer events. We propose that the intron was originally seeded into angiosperms by a single transfer from fungi, with all subsequent inferred transfers occurring from one angiosperm to another. The pattern of angiosperm-to-angiosperm transfer is biased toward exchanges between plants belonging to the same family. Illegitimate pollination is proposed as one potential factor responsible for this pattern, given that aberrant, cross-species pollination is more likely between close relatives. Other potential factors include shared vectoring agents or common geographic locations. We report the first apparent cases of loss of the cox1 intron; losses are accompanied by retention of the exonic coconversion tract, which is located immediately downstream of the intron and which is a product of the intron's self-insertion mechanism. We discuss the many reasons why the cox1 intron is so frequently and detectably transferred, and rarely lost, and conclude that it should be regarded as the "canary in the coal mine" with respect to horizontal transfer in angiosperm mitochondria.
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