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      Rapid and Recent Evolution of LTR Retrotransposons Drives Rice Genome Evolution During the Speciation of AA-Genome Oryza Species

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          Abstract

          The dynamics of long terminal repeat (LTR) retrotransposons and their contribution to genome evolution during plant speciation have remained largely unanswered. Here, we perform a genome-wide comparison of all eight Oryza AA-genome species, and identify 3911 intact LTR retrotransposons classified into 790 families. The top 44 most abundant LTR retrotransposon families show patterns of rapid and distinct diversification since the species split over the last ∼4.8 MY (million years). Phylogenetic and read depth analyses of 11 representative retrotransposon families further provide a comprehensive evolutionary landscape of these changes. Compared with Ty1- copia, independent bursts of Ty3- gypsy retrotransposon expansions have occurred with the three largest showing signatures of lineage-specific evolution. The estimated insertion times of 2213 complete retrotransposons from the top 23 most abundant families reveal divergent life histories marked by speedy accumulation, decline, and extinction that differed radically between species. We hypothesize that this rapid evolution of LTR retrotransposons not only divergently shaped the architecture of rice genomes but also contributed to the process of speciation and diversification of rice.

          Most cited references49

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          Repbase update: a database and an electronic journal of repetitive elements.

          J Jurka (2000)
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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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              Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice.

              Retrotransposons are the main components of eukaryotic genomes, representing up to 80% of some large plant genomes. These mobile elements transpose via a "copy and paste" mechanism, thus increasing their copy number while active. Their accumulation is now accepted as the main factor of genome size increase in higher eukaryotes, besides polyploidy. However, the dynamics of this process are poorly understood. In this study, we show that Oryza australiensis, a wild relative of the Asian cultivated rice O. sativa, has undergone recent bursts of three LTR-retrotransposon families. This genome has accumulated more than 90,000 retrotransposon copies during the last three million years, leading to a rapid twofold increase of its size. In addition, phenetic analyses of these retrotransposons clearly confirm that the genomic bursts occurred posterior to the radiation of the species. This provides direct evidence of retrotransposon-mediated variation of genome size within a plant genus.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                14 April 2017
                June 2017
                : 7
                : 6
                : 1875-1885
                Affiliations
                [* ]Plant Germplasm and Genomics Center, Kunming Institute of Botany, the Chinese Academy of Sciences, Kunming 650204 China
                []University of the Chinese Academy of Sciences, Beijing 100039, China
                []Agrobiological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
                Author notes
                [1 ]Corresponding author: Kunming Institute of Botany, the Chinese Academy of Sciences, 132 Lanhei Road, Kunming 650204, China. E-mail: lgao@ 123456mail.kib.ac.cn
                Article
                GGG_037572
                10.1534/g3.116.037572
                5473765
                28413161
                91e0a878-4b02-4d70-8c0a-e883f63b2a9d
                Copyright © 2017 Zhang and Gao

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 November 2016
                : 09 April 2017
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 64, Pages: 11
                Categories
                Investigations

                Genetics
                ltr retrotransposons,oryza,aa-genome,rice speciation,comparative genomics
                Genetics
                ltr retrotransposons, oryza, aa-genome, rice speciation, comparative genomics

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