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      Exceptional Diversity, Non-Random Distribution, and Rapid Evolution of Retroelements in the B73 Maize Genome

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Recent comprehensive sequence analysis of the maize genome now permits detailed discovery and description of all transposable elements (TEs) in this complex nuclear environment. Reiteratively optimized structural and homology criteria were used in the computer-assisted search for retroelements, TEs that transpose by reverse transcription of an RNA intermediate, with the final results verified by manual inspection. Retroelements were found to occupy the majority (>75%) of the nuclear genome in maize inbred B73. Unprecedented genetic diversity was discovered in the long terminal repeat (LTR) retrotransposon class of retroelements, with >400 families (>350 newly discovered) contributing >31,000 intact elements. The two other classes of retroelements, SINEs (four families) and LINEs (at least 30 families), were observed to contribute 1,991 and ∼35,000 copies, respectively, or a combined ∼1% of the B73 nuclear genome. With regard to fully intact elements, median copy numbers for all retroelement families in maize was 2 because >250 LTR retrotransposon families contained only one or two intact members that could be detected in the B73 draft sequence. The majority, perhaps all, of the investigated retroelement families exhibited non-random dispersal across the maize genome, with LINEs, SINEs, and many low-copy-number LTR retrotransposons exhibiting a bias for accumulation in gene-rich regions. In contrast, most (but not all) medium- and high-copy-number LTR retrotransposons were found to preferentially accumulate in gene-poor regions like pericentromeric heterochromatin, while a few high-copy-number families exhibited the opposite bias. Regions of the genome with the highest LTR retrotransposon density contained the lowest LTR retrotransposon diversity. These results indicate that the maize genome provides a great number of different niches for the survival and procreation of a great variety of retroelements that have evolved to differentially occupy and exploit this genomic diversity.

          Author Summary

          Although TEs are a major component of all studied plant genomes, and are the most significant contributors to genome structure and evolution in almost all eukaryotes that have been investigated, their properties and reasons for existence are not well understood in any eukaryotic genome. In order to begin a comprehensive study of TE contributions to the structure, function, and evolution of both genes and genomes, we first identified all of the TEs in maize and then investigated whether there were non-random patterns in their dispersal. We used homology and TE structure criteria in an effort to discover all of the retroelements in the recently sequenced genome from maize inbred B73. We found that the retroelements are incredibly diverse in maize, with many hundreds of families that show different insertion and/or retention specificities across the maize chromosomes. Most of these element families are present in low copy numbers and had been missed by previous searches that relied on a high-copy-number criterion. Different element families exhibited very different biases for accumulation across the chromosomes, indicating that they can detect and utilize many different chromatin environments.

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          Most cited references 36

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          The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla.

          The analysis of the first plant genomes provided unexpected evidence for genome duplication events in species that had previously been considered as true diploids on the basis of their genetics. These polyploidization events may have had important consequences in plant evolution, in particular for species radiation and adaptation and for the modulation of functional capacities. Here we report a high-quality draft of the genome sequence of grapevine (Vitis vinifera) obtained from a highly homozygous genotype. The draft sequence of the grapevine genome is the fourth one produced so far for flowering plants, the second for a woody species and the first for a fruit crop (cultivated for both fruit and beverage). Grapevine was selected because of its important place in the cultural heritage of humanity beginning during the Neolithic period. Several large expansions of gene families with roles in aromatic features are observed. The grapevine genome has not undergone recent genome duplication, thus enabling the discovery of ancestral traits and features of the genetic organization of flowering plants. This analysis reveals the contribution of three ancestral genomes to the grapevine haploid content. This ancestral arrangement is common to many dicotyledonous plants but is absent from the genome of rice, which is a monocotyledon. Furthermore, we explain the chronology of previously described whole-genome duplication events in the evolution of flowering plants.
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            SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny.

            SEAVIEW and PHYLO_WIN are two graphic tools for X Windows-Unix computers dedicated to sequence alignment and molecular phylogenetics. SEAVIEW is a sequence alignment editor allowing manual or automatic alignment through an interface with CLUSTALW program. Alignment of large sequences with extensive length differences is made easier by a dot-plot-based routine. The PHYLO_WIN program allows phylogenetic tree building according to most usual methods (neighbor joining with numerous distance estimates, maximum parsimony, maximum likelihood), and a bootstrap analysis with any of them. Reconstructed trees can be drawn, edited, printed, stored, evaluated according to numerous criteria. Taxonomic species groups and sets of conserved regions can be defined by mouse and stored into sequence files, thus avoiding multiple data files. Both tools are entirely mouse driven. On-line help makes them easy to use. They are freely available by anonymous ftp at biom3.univ-lyon1.fr/pub/ mol_phylogeny or http:@acnuc.univ-lyon1.fr/, or by e-mail to galtier@biomserv.univ-lyon1.fr.
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              Rapid recent growth and divergence of rice nuclear genomes.

              By employing the nuclear DNA of the African rice Oryza glaberrima as a reference genome, the timing, natures, mechanisms, and specificities of recent sequence evolution in the indica and japonica subspecies of Oryza sativa were identified. The data indicate that the genome sizes of both indica and japonica have increased substantially, >2% and >6%, respectively, since their divergence from a common ancestor, mainly because of the amplification of LTR-retrotransposons. However, losses of all classes of DNA sequence through unequal homologous recombination and illegitimate recombination have attenuated the growth of the rice genome. Small deletions have been particularly frequent throughout the genome. In >1 Mb of orthologous regions that we analyzed, no cases of complete gene acquisition or loss from either indica or japonica were found, nor was any example of precise transposon excision detected. The sequences between genes were observed to have a very high rate of divergence, indicating a molecular clock for transposable elements that is at least 2-fold more rapid than synonymous base substitutions within genes. We found that regions prone to frequent insertions and deletions also exhibit higher levels of point mutation. These results indicate a highly dynamic rice genome with competing processes for the generation and removal of genetic variation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                November 2009
                November 2009
                20 November 2009
                : 5
                : 11
                Affiliations
                [1 ]Department of Genetics, University of Georgia, Athens, Georgia, United States of America
                [2 ]Department of Plant Biology, University of Georgia, Athens, Georgia, United States of America
                [3 ]Université de Perpignan, Via Domitia, CNRS UMR5096 LGDP, Perpignan, France
                [4 ]Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana, United States of America
                Fred Hutchinson Cancer Research Center, United States of America
                Author notes

                Conceived and designed the experiments: RSB JCE CC JMD RPW PJS JLB. Performed the experiments: RSB JCE CC NU AJ JMD RPW PJS JLB. Analyzed the data: RSB JCE CC NU AJ JMD RPW PJS JLB. Contributed reagents/materials/analysis tools: RSB JCE CC JMD RPW PJS JLB. Wrote the paper: RSB JCE CC JMD RPW PJS JLB.

                Article
                09-PLGE-RA-MZ-1510R2
                10.1371/journal.pgen.1000732
                2774510
                19936065
                Baucom et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 13
                Categories
                Research Article
                Genetics and Genomics
                Genetics and Genomics/Genome Projects
                Genetics and Genomics/Genomics
                Genetics and Genomics/Plant Genomes and Evolution

                Genetics

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