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

ABSTRACT: 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 approximately 4,000-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 and/or repair.

SUBMITTER: Cho Y

PROVIDER: S-EPMC539783 | biostudies-literature | 2004 Dec

REPOSITORIES: biostudies-literature

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

Cho Yangrae Y Mower Jeffrey P JP Qiu Yin-Long YL Palmer Jeffrey D JD

Proceedings of the National Academy of Sciences of the United States of America 20041214 51

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 approximately 4,000-fold. The fastest Plantago lineages set a new benchmark for rapid evolution in a DNA genome, exceeding even t ...[more]

PMID: 15598738

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Project description:It has long been known that rates of synonymous substitutions are unusually low in mitochondrial genes of flowering and other land plants. Although two dramatic exceptions to this pattern have recently been reported, it is unclear how often major increases in substitution rates occur during plant mitochondrial evolution and what the overall magnitude of substitution rate variation is across plants.A broad survey was undertaken to evaluate synonymous substitution rates in mitochondrial genes of angiosperms and gymnosperms. Although most taxa conform to the generality that plant mitochondrial sequences evolve slowly, additional cases of highly accelerated rates were found. We explore in detail one of these new cases, within the genus Silene. A roughly 100-fold increase in synonymous substitution rate is estimated to have taken place within the last 5 million years and involves only one of ten species of Silene sampled in this study. Examples of unusually slow sequence evolution were also identified. Comparison of the fastest and slowest lineages shows that synonymous substitution rates vary by four orders of magnitude across seed plants. In other words, some plant mitochondrial lineages accumulate more synonymous change in 10,000 years than do others in 100 million years. Several perplexing cases of gene-to-gene variation in sequence divergence within a plant were uncovered. Some of these probably reflect interesting biological phenomena, such as horizontal gene transfer, mitochondrial-to-nucleus transfer, and intragenomic variation in mitochondrial substitution rates, whereas others are likely the result of various kinds of errors.The extremes of synonymous substitution rates measured here constitute by far the largest known range of rate variation for any group of organisms. These results highlight the utility of examining absolute substitution rates in a phylogenetic context rather than by traditional pairwise methods. Why substitution rates are generally so low in plant mitochondrial genomes yet occasionally increase dramatically remains mysterious.

Dataset Information

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

Publications

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

Similar Datasets

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