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      Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution

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          Abstract

          Background

          Centromeres are essential for chromosome segregation, yet their DNA sequences evolve rapidly. In most animals and plants that have been studied, centromeres contain megabase-scale arrays of tandem repeats. Despite their importance, very little is known about the degree to which centromere tandem repeats share common properties between different species across different phyla. We used bioinformatic methods to identify high-copy tandem repeats from 282 species using publicly available genomic sequence and our own data.

          Results

          Our methods are compatible with all current sequencing technologies. Long Pacific Biosciences sequence reads allowed us to find tandem repeat monomers up to 1,419 bp. We assumed that the most abundant tandem repeat is the centromere DNA, which was true for most species whose centromeres have been previously characterized, suggesting this is a general property of genomes. High-copy centromere tandem repeats were found in almost all animal and plant genomes, but repeat monomers were highly variable in sequence composition and length. Furthermore, phylogenetic analysis of sequence homology showed little evidence of sequence conservation beyond approximately 50 million years of divergence. We find that despite an overall lack of sequence conservation, centromere tandem repeats from diverse species showed similar modes of evolution.

          Conclusions

          While centromere position in most eukaryotes is epigenetically determined, our results indicate that tandem repeats are highly prevalent at centromeres of both animal and plant genomes. This suggests a functional role for such repeats, perhaps in promoting concerted evolution of centromere DNA across chromosomes.

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          Most cited references79

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          Testing for phylogenetic signal in comparative data: behavioral traits are more labile.

          The primary rationale for the use of phylogenetically based statistical methods is that phylogenetic signal, the tendency for related species to resemble each other, is ubiquitous. Whether this assertion is true for a given trait in a given lineage is an empirical question, but general tools for detecting and quantifying phylogenetic signal are inadequately developed. We present new methods for continuous-valued characters that can be implemented with either phylogenetically independent contrasts or generalized least-squares models. First, a simple randomization procedure allows one to test the null hypothesis of no pattern of similarity among relatives. The test demonstrates correct Type I error rate at a nominal alpha = 0.05 and good power (0.8) for simulated datasets with 20 or more species. Second, we derive a descriptive statistic, K, which allows valid comparisons of the amount of phylogenetic signal across traits and trees. Third, we provide two biologically motivated branch-length transformations, one based on the Ornstein-Uhlenbeck (OU) model of stabilizing selection, the other based on a new model in which character evolution can accelerate or decelerate (ACDC) in rate (e.g., as may occur during or after an adaptive radiation). Maximum likelihood estimation of the OU (d) and ACDC (g) parameters can serve as tests for phylogenetic signal because an estimate of d or g near zero implies that a phylogeny with little hierarchical structure (a star) offers a good fit to the data. Transformations that improve the fit of a tree to comparative data will increase power to detect phylogenetic signal and may also be preferable for further comparative analyses, such as of correlated character evolution. Application of the methods to data from the literature revealed that, for trees with 20 or more species, 92% of traits exhibited significant phylogenetic signal (randomization test), including behavioral and ecological ones that are thought to be relatively evolutionarily malleable (e.g., highly adaptive) and/or subject to relatively strong environmental (nongenetic) effects or high levels of measurement error. Irrespective of sample size, most traits (but not body size, on average) showed less signal than expected given the topology, branch lengths, and a Brownian motion model of evolution (i.e., K was less than one), which may be attributed to adaptation and/or measurement error in the broad sense (including errors in estimates of phenotypes, branch lengths, and topology). Analysis of variance of log K for all 121 traits (from 35 trees) indicated that behavioral traits exhibit lower signal than body size, morphological, life-history, or physiological traits. In addition, physiological traits (corrected for body size) showed less signal than did body size itself. For trees with 20 or more species, the estimated OU (25% of traits) and/or ACDC (40%) transformation parameter differed significantly from both zero and unity, indicating that a hierarchical tree with less (or occasionally more) structure than the original better fit the data and so could be preferred for comparative analyses.
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            TimeTree: a public knowledge-base of divergence times among organisms.

            Biologists and other scientists routinely need to know times of divergence between species and to construct phylogenies calibrated to time (timetrees). Published studies reporting time estimates from molecular data have been increasing rapidly, but the data have been largely inaccessible to the greater community of scientists because of their complexity. TimeTree brings these data together in a consistent format and uses a hierarchical structure, corresponding to the tree of life, to maximize their utility. Results are presented and summarized, allowing users to quickly determine the range and robustness of time estimates and the degree of consensus from the published literature. TimeTree is available at http://www.timetree.net
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              Genome sequence, comparative analysis, and population genetics of the domestic horse.

              We report a high-quality draft sequence of the genome of the horse (Equus caballus). The genome is relatively repetitive but has little segmental duplication. Chromosomes appear to have undergone few historical rearrangements: 53% of equine chromosomes show conserved synteny to a single human chromosome. Equine chromosome 11 is shown to have an evolutionary new centromere devoid of centromeric satellite DNA, suggesting that centromeric function may arise before satellite repeat accumulation. Linkage disequilibrium, showing the influences of early domestication of large herds of female horses, is intermediate in length between dog and human, and there is long-range haplotype sharing among breeds.
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                Author and article information

                Contributors
                Journal
                Genome Biol
                Genome Biol
                Genome Biology
                BioMed Central
                1465-6906
                1465-6914
                2013
                30 January 2013
                : 14
                : 1
                : R10
                Affiliations
                [1 ]Department of Molecular and Cell Biology and Genome Center, University of California, Davis, 1 Shields Ave, Davis, CA 95616, USA
                [2 ]Department of Plant Biology, University of California, Davis, 1 Shields Ave, Davis, CA 95616, USA
                [3 ]USDA-ARS, Western Regional Research Center, 800 Buchanan St, Albany, CA 94710, USA
                [4 ]Department of Evolution and Ecology, University of California, Davis, 1 Shields Ave, Davis, CA 95616, USA
                [5 ]Department of Biochemistry and Biophysics, University of California, San Francisco, 1700 4th St, San Francisco, CA 94158, USA
                [6 ]Pacific Biosciences, 1380 Willow Rd, Menlo Park, CA 94025, USA
                [7 ]Department of Animal Production and Health, Universidade Estadual Paulista, IAEA Collaborating Centre in Animal Genomics and Bioinformatics, Rua Clóvis Pestana, 793-16050-680, Aracatuba, SP, Brazil
                [8 ]Howard Hughes Medical Institute, 4000 Jones Bridge Rd, Chevy Chase, MD 20815, USA
                [9 ]USDA-ARS, US Meat Animal Research Center, State Spur 18D, Clay Center, NE 68933, USA
                [10 ]Department of Plant Sciences, Center for Population Biology, and Genome Center, University of California, Davis, 1 Shields Ave, Davis, CA 95616, USA
                Article
                gb-2013-14-1-r10
                10.1186/gb-2013-14-1-r10
                4053949
                23363705
                4c256f75-0a8b-4537-915e-a618ff8c2629
                Copyright © 2013 Melters et al.; licensee BioMed Central Ltd.

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 29 September 2012
                : 20 December 2012
                : 30 January 2013
                Categories
                Research

                Genetics
                Genetics

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