Selection on Amino Acid Substitutions in Arabidopsis

Foxe, John Paul; Dar, Vaqaar-un-Nisa; Zheng, Honggang; Nordborg, Magnus; Gaut, Brandon S.; Wright, Stephen I.

doi:10.1093/molbev/msn079

Cited by 74 publications

(77 citation statements)

References 46 publications

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“…Excess rare polymorphisms and higher r pd for nonsynonymous compared to synonymous variation appear to be general patterns in viral (Edwards et al 2006;Pybus et al 2006;Hughes 2009) and bacterial genomes (Hughes 2005;Charlesworth and Eyre-Walker 2006;Rocha et al 2006;Hughes et al 2008) as well as in animal mtDNA (Ballard and Kreitman 1994;Nachman et al 1996;Rand and Kann 1996;Hasegawa et al 1998;Wise et al 1998;Weinreich and Rand 2000;Gerber et al 2001;Subramanian et al 2009). Similar patterns have been noted in nuclear genes from yeast (Doniger et al 2008;Liti et al 2009), Drosophila (Akashi 1996;Fay et al 2002;Loewe et al 2006;Andolfatto et al 2011), humans (Cargill et al 1999;Sunyaev et al 2000;Hughes et al 2003;Williamson et al 2005;Boyko et al 2008;Keightley and Halligan 2011;Subramanian 2012), mice (Halligan et al 2010), and plants (Bustamante et al 2002;Nordborg et al 2005;Foxe et al 2008;Fujimoto et al 2008;Gossmann et al 2010;Branca et al 2011;. Excess rare polymorphism could reflect very strongly deleterious mutations if the number of sampled chromosomes is very high, but sample sizes in most of these studies do not approach such levels.…”

Section: Within-lineage Contrasts Of Polymorphism and Divergencementioning

confidence: 55%

Weak Selection and Protein Evolution

2012

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The "nearly neutral" theory of molecular evolution proposes that many features of genomes arise from the interaction of three weak evolutionary forces: mutation, genetic drift, and natural selection acting at its limit of efficacy. Such forces generally have little impact on allele frequencies within populations from generation to generation but can have substantial effects on long-term evolution. The evolutionary dynamics of weakly selected mutations are highly sensitive to population size, and near neutrality was initially proposed as an adjustment to the neutral theory to account for general patterns in available protein and DNA variation data. Here, we review the motivation for the nearly neutral theory, discuss the structure of the model and its predictions, and evaluate current empirical support for interactions among weak evolutionary forces in protein evolution. Near neutrality may be a prevalent mode of evolution across a range of functional categories of mutations and taxa. However, multiple evolutionary mechanisms (including adaptive evolution, linked selection, changes in fitness-effect distributions, and weak selection) can often explain the same patterns of genome variation. Strong parameter sensitivity remains a limitation of the nearly neutral model, and we discuss concave fitness functions as a plausible underlying basis for weak selection.U NDER the neutral model, newly arising mutations fall into two major fitness classes: strongly deleterious and selectively neutral (Kimura 1968;King and Jukes 1969). The first class is well supported by mutation accumulation experiments (reviewed in Simmons and Crow 1977;Halligan and Keightley 2009) and early DNA sequence comparisons (Grunstein et al. 1976;Kafatos et al. 1977) and is shared among competing evolutionary models. The novel and controversial aspect of the neutral theory was the proposition that, among mutations that go to fixation, the vast majority are selectively neutral. Advantageous substitutions, although important in phenotypic evolution, are sufficiently rare at the molecular level that they need not be considered to adequately model the process. Under the neutral theory, within-and between-species variation sample two aspects of a process of origination by mutation and changes in gene frequency dominated by drift and, for some mutations, negative selection (Kimura and Ohta 1971a). In contrast, polymorphism and divergence may be "uncoupled" under selection models (Gillespie 1987). Protein polymorphism and the neutral model: invariance of heterozygosityClear predictions for levels of polymorphism within populations and divergence among species are appealing aspects of the neutral model. However, within a few years of its proposal, the notion of drift-dominated evolution was challenged by overall patterns of allozyme polymorphism and contrasts between DNA and protein divergence.Although evolutionary geneticists were generally surprised by the extent of naturally occurring variation revealed by allozyme gel electrophoresis in the 197...

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Section: Within-lineage Contrasts Of Polymorphism and Divergencementioning

confidence: 55%

Weak Selection and Protein Evolution

2012

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“…Our estimates of N e s (À30 for the additive model in A. arenosa; -10 in A. lyrata) in fact suggest stronger purifying selection in A. arenosa than in A. lyrata, potentially reflecting a larger long-term effective population size, as suggested by comparisons of levels of nucleotide diversity in this study with previous estimates in A. lyrata. Interestingly, patterns of polymorphism at nonsynonymous compared to synonymous sites in the orthologous genes from these two species also follow this trend; from the analysis of these same orthologous loci in A. lyrata by Foxe and colleagues ( Foxe et al 2008), the ratio of numbers of nonsynonymous (164) to synonymous (212) polymorphic sites is significantly elevated compared with the ratio in A. arenosa (176 vs. 323; Fisher's exact test, P , 0.05). Taken together, this suggests that the increased effective size in the autotetraploid species dominates over any relaxation of selection associated with masking of deleterious recessive mutations.…”

Section: Discussionmentioning

confidence: 84%

Contrasting Patterns of Transposable-Element Insertion Polymorphism and Nucleotide Diversity in Autotetraploid and Allotetraploid Arabidopsis Species

et al. 2008

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It has been hypothesized that polyploidy permits the proliferation of transposable elements, due to both the masking of deleterious recessive mutations and the breakdown of host silencing mechanisms. We investigated the patterns of insertion polymorphism of an Ac-like transposable element and nucleotide diversity at 18 gene fragments in the allotetraploid Arabidopsis suecica and the autotetraploid A. arenosa. All identified insertions were fixed in A. suecica, and many were clearly inherited from the parental species A. thaliana or A. arenosa. These results are inconsistent with a rapid increase in transposition associated with hybrid breakdown but support the evidence from nucleotide polymorphism patterns of a recent single origin of this species leading to genomewide fixations of transposable elements. In contrast, most insertions were segregating at very low frequencies in A. arenosa samples, showing a significant departure from neutrality in favor of purifying selection, even when we account for population subdivision inferred from sequence variation. Patterns of nucleotide variation at reference genes are consistent with the TE results, showing evidence for higher effective population sizes in A. arenosa than in related diploid taxa but a near complete population bottleneck associated with the origins of A. suecica.

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“…We did MK tests to assess the significance of any differences in fixation of either slightly deleterious or advantageous mutations, by comparing the ratios of replacement to synonymous changes between sites diverged between A. lyrata and A. thaliana, and polymorphic within A. lyrata [supplemental Table 1 shows the results for the pericentromere region loci and loci from chromosomes AL6 and AL7; the AL1 and AL2 arm locus data are published in Foxe et al (2008) and are not shown here]. No significant differences were observed between the low-and high-diversity centromeres, and there were no significant MK test results for any individual pericentromere region loci, or in pooled data for each centromere.…”

Section: Resultsmentioning

confidence: 99%

High DNA Sequence Diversity in Pericentromeric Genes of the Plant Arabidopsis lyrata

et al. 2008

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Differences in neutral diversity at different loci are predicted to arise due to differences in mutation rates and from the ''hitchhiking'' effects of natural selection. Consistent with hitchhiking models, Drosophila melanogaster chromosome regions with very low recombination have unusually low nucleotide diversity. We compared levels of diversity from five pericentromeric regions with regions of normal recombination in Arabidopsis lyrata, an outcrossing close relative of the highly selfing A. thaliana. In contrast with the accepted theoretical prediction, and the pattern in Drosophila, we found generally high diversity in pericentromeric genes, which is consistent with the observation in A. thaliana. Our data rule out balancing selection in the pericentromeric regions, suggesting that hitchhiking is more strongly reducing diversity in the chromosome arms than the pericentromere regions.

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Selection on Amino Acid Substitutions in Arabidopsis

Cited by 74 publications

References 46 publications

Weak Selection and Protein Evolution

Weak Selection and Protein Evolution

Contrasting Patterns of Transposable-Element Insertion Polymorphism and Nucleotide Diversity in Autotetraploid and Allotetraploid Arabidopsis Species

High DNA Sequence Diversity in Pericentromeric Genes of the Plant Arabidopsis lyrata

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