Broad-Scale Analysis Contradicts the Theory That Generation Time Affects Molecular Evolutionary Rates in Plants

Whittle, Carrie-Ann; Johnston, Mark O.

doi:10.1007/s00239-002-2395-0

Cited by 63 publications

(70 citation statements)

References 67 publications

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“…As a result, generation time can provide a useful proxy of the overall rate of genome replication in animals, but is unlikely to do so in plants. This may explain why the evidence for the generation time hypothesis is very strong for animals [16][17][18] , but mixed for plants 1,[19][20][21] . Despite this, generation time will remain tightly associated with long-term rates of meiosis in plants, because an extant plant genome would have experienced one meiosis in each generation through which it has passed.…”

Section: Discussionmentioning

confidence: 99%

“…In all three of these cases, the faster-evolving plants (annuals, herbs and non-arborescent ferns) are likely to have higher rates of mitosis than their more slowly evolving relatives (perennials, woody species and tree ferns), although we also note that the faster-evolving plants are also likely to have shorter generation times in all of these cases. The ROM hypothesis might also explain why generation times correlate with rates of molecular evolution in animals, but not in plants 20,21,36 , because generation times are a reliable predictor of rates of mitosis in animals, but not in plants. Finally, the ROM hypothesis might explain previously observed correlations between rates of molecular evolution and environmental energy 3 , latitude 2 and water availability 5 in plants.…”

Section: Article Nature Communications | Doi: 101038/ncomms2836mentioning

confidence: 99%

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Taller plants have lower rates of molecular evolution

et al. 2013

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Rates of molecular evolution have a central role in our understanding of many aspects of species' biology. However, the causes of variation in rates of molecular evolution remain poorly understood, particularly in plants. Here we show that height accounts for about onefifth of the among-lineage rate variation in the chloroplast and nuclear genomes of plants. This relationship holds across 138 families of flowering plants, and when accounting for variation in species richness, temperature, ultraviolet radiation, latitude and growth form. Our observations can be explained by a link between height and rates of genome copying in plants, and we propose a mechanistic hypothesis to account for this-the 'rate of mitosis' hypothesis. This hypothesis has the potential to explain many disparate observations about rates of molecular evolution across the tree of life. Our results have implications for understanding the evolutionary history and future of plant lineages in a changing world.

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Section: Discussionmentioning

confidence: 99%

Section: Article Nature Communications | Doi: 101038/ncomms2836mentioning

confidence: 99%

Taller plants have lower rates of molecular evolution

et al. 2013

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“…1, Table 1, and Table 6), we conclude that rate variation in Plantago mt genes is probably a direct consequence of underlying changes in the mt mutation rate. In contrast, most previously reported cases of (much more modest) synonymous site variation in plant mt DNA have been postulated to reflect generation time effects (13)(14)(15), although this interpretation has been questioned (41).…”

Section: Underlying Basis Of Extreme Molecular Divergence In Plantagomentioning

confidence: 93%

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

Cho

Mower

Qiu

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

251

240

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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...

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“…(Thomas et al, 2010). Although under-examined, the predicted correlation between generation time and rates of molecular evolution has been observed in some groups of invertebrates, flowering plants, host-parasite systems and mammalian nuclear sequences (Nikolaev et al, 2007;Smith and Donoghue, 2008;Welch et al, 2008;Thomas et al, 2010), but not for other plants or mammal mtDNA (Whittle and Johnston, 2003;Nabholz et al, 2008). Ohta (1992) suggested that variation in generation time and population size was the cause of the discrepancy between observed rates of protein and nucleotide evolution.…”

Section: The Process Behind the Patternmentioning

confidence: 99%

Molecular evolution and the latitudinal biodiversity gradient

2013

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Species density is higher in the tropics (low latitude) than in temperate regions (high latitude) resulting in a latitudinal biodiversity gradient (LBG). The LBG must be generated by differential rates of speciation and/or extinction and/or immigration among regions, but the role of each of these processes is still unclear. Recent studies examining differences in rates of molecular evolution have inferred a direct link between rate of molecular evolution and rate of speciation, and postulated these as important drivers of the LBG. Here we review the molecular genetic evidence and examine the factors that might be responsible for differences in rates of molecular evolution. Critical to this is the directionality of the relationship between speciation rates and rates of molecular evolution.

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Broad-Scale Analysis Contradicts the Theory That Generation Time Affects Molecular Evolutionary Rates in Plants

Cited by 63 publications

References 67 publications

Taller plants have lower rates of molecular evolution

Taller plants have lower rates of molecular evolution

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

Molecular evolution and the latitudinal biodiversity gradient

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