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      Rapid amplification of four retrotransposon families promoted speciation and genome size expansion in the genus Panax

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          Abstract

          Genome duplication and repeat multiplication contribute to genome evolution in plants. Our previous work identified a recent allotetraploidization event and five high-copy LTR retrotransposon (LTR-RT) families PgDel, PgTat, PgAthila, PgTork, and PgOryco in Panax ginseng. Here, using whole-genome sequences, we quantified major repeats in five Panax species and investigated their role in genome evolution. The diploids P. japonicus, P. vietnamensis, and P. notoginseng and the tetraploids P. ginseng and P. quinquefolius were analyzed alongside their relative Aralia elata. These species possess 0.8–4.9 Gb haploid genomes. The PgDel, PgTat, PgAthila, and PgTork LTR-RT superfamilies accounted for 39–52% of the Panax species genomes and 17% of the A. elata genome. PgDel included six subfamily members, each with a distinct genome distribution. In particular, the PgDel1 subfamily occupied 23–35% of the Panax genomes and accounted for much of their genome size variation. PgDel1 occupied 22.6% (0.8 Gb of 3.6 Gb) and 34.5% (1.7 Gb of 4.9 Gb) of the P. ginseng and P. quinquefolius genomes, respectively. Our findings indicate that the P. quinquefolius genome may have expanded due to rapid PgDel1 amplification over the last million years as a result of environmental adaptation following migration from Asia to North America.

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          Most cited references36

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          Genome evolution in polyploids.

          J Wendel (2000)
          Polyploidy is a prominent process in plants and has been significant in the evolutionary history of vertebrates and other eukaryotes. In plants, interdisciplinary approaches combining phylogenetic and molecular genetic perspectives have enhanced our awareness of the myriad genetic interactions made possible by polyploidy. Here, processes and mechanisms of gene and genome evolution in polyploids are reviewed. Genes duplicated by polyploidy may retain their original or similar function, undergo diversification in protein function or regulation, or one copy may become silenced through mutational or epigenetic means. Duplicated genes also may interact through inter-locus recombination, gene conversion, or concerted evolution. Recent experiments have illuminated important processes in polyploids that operate above the organizational level of duplicated genes. These include inter-genomic chromosomal exchanges, saltational, non-Mendelian genomic evolution in nascent polyploids, inter-genomic invasion, and cytonuclear stabilization. Notwithstanding many recent insights, much remains to be learned about many aspects of polyploid evolution, including: the role of transposable elements in structural and regulatory gene evolution; processes and significance of epigenetic silencing; underlying controls of chromosome pairing; mechanisms and functional significance of rapid genome changes; cytonuclear accommodation; and coordination of regulatory factors contributed by two, sometimes divergent progenitor genomes. Continued application of molecular genetic approaches to questions of polyploid genome evolution holds promise for producing lasting insight into processes by which novel genotypes are generated and ultimately into how polyploidy facilitates evolution and adaptation.
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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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              Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes.

              Autonomous transposable elements, generally considered as junk and selfish, encode transposition proteins that can bind, copy, break, join or degrade nucleic acids as well as process or interact with other proteins. Such a repertoire of activities might be of interest for the host cell. There is indeed substantial evidence that mobile DNA can serve as a dynamic reservoir for new cellular functions. Transposable element genes encoding transposase, integrase, reverse transcriptase as well as structural and envelope proteins have been repeatedly recruited by their host during evolution in most eukaryotic lineages. Such domesticated sequences protect us against infections, are necessary for our reproduction, allow the replication of our chromosomes and control cell proliferation and death; others are essential for plant development. Many new candidates for domesticated sequences have been revealed by sequencing projects. Their functional analysis will uncover new aspects of evolutionary alchemy, the turning of junk into gold within genomes. (c) 2006 Wiley periodicals, Inc.
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                Author and article information

                Contributors
                tjyang@snu.ac.kr
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                22 August 2017
                22 August 2017
                2017
                : 7
                : 9045
                Affiliations
                [1 ]ISNI 0000 0004 0470 5905, GRID grid.31501.36, Department of Plant Science, , Plant Genomics and Breeding Institute, and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, ; Seoul, 08826 Republic of Korea
                [2 ]ISNI 0000 0001 0742 3338, GRID grid.418964.6, Advanced Radiation Technology Institute, , Korea Atomic Energy Research Institute, ; Jeongeup, 56212 Republic of Korea
                [3 ]ISNI 0000 0001 1302 4958, GRID grid.55614.33, , Agriculture and Agri-Food Canada, 107 Science Place, ; Saskatoon, SK S7N 0X2 Canada
                [4 ]ISNI 0000 0000 9546 5767, GRID grid.20561.30, Institution of Genomics and Bioinformatics, , South China Agricultural University, ; Guangzhou, 510642 China
                [5 ]ISNI 0000 0004 0470 5905, GRID grid.31501.36, Crop Biotechnology Institute/GreenBio Science and Technology, , Seoul National University, ; Pyeongchang, 25354 Republic of Korea
                Author information
                http://orcid.org/0000-0002-9676-8801
                Article
                8194
                10.1038/s41598-017-08194-5
                5567358
                28831052
                1980eb1a-e7cf-4493-8309-fd79a4c90208
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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                : 27 March 2017
                : 5 July 2017
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