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      Whole-genome sequence of the Tibetan frog Nanorana parkeri and the comparative evolution of tetrapod genomes.

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          Abstract

          The development of efficient sequencing techniques has resulted in large numbers of genomes being available for evolutionary studies. However, only one genome is available for all amphibians, that of Xenopus tropicalis, which is distantly related from the majority of frogs. More than 96% of frogs belong to the Neobatrachia, and no genome exists for this group. This dearth of amphibian genomes greatly restricts genomic studies of amphibians and, more generally, our understanding of tetrapod genome evolution. To fill this gap, we provide the de novo genome of a Tibetan Plateau frog, Nanorana parkeri, and compare it to that of X. tropicalis and other vertebrates. This genome encodes more than 20,000 protein-coding genes, a number similar to that of Xenopus. Although the genome size of Nanorana is considerably larger than that of Xenopus (2.3 vs. 1.5 Gb), most of the difference is due to the respective number of transposable elements in the two genomes. The two frogs exhibit considerable conserved whole-genome synteny despite having diverged approximately 266 Ma, indicating a slow rate of DNA structural evolution in anurans. Multigenome synteny blocks further show that amphibians have fewer interchromosomal rearrangements than mammals but have a comparable rate of intrachromosomal rearrangements. Our analysis also identifies 11 Mb of anuran-specific highly conserved elements that will be useful for comparative genomic analyses of frogs. The Nanorana genome offers an improved understanding of evolution of tetrapod genomes and also provides a genomic reference for other evolutionary studies.

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          Author and article information

          Journal
          Proc. Natl. Acad. Sci. U.S.A.
          Proceedings of the National Academy of Sciences of the United States of America
          1091-6490
          0027-8424
          Mar 17 2015
          : 112
          : 11
          Affiliations
          [1 ] State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China;
          [2 ] China National GeneBank and Shenzhen Key Laboratory of Transomics Biotechnologies, BGI-Shenzhen, Shenzhen 518083, China;
          [3 ] China National GeneBank and Shenzhen Key Laboratory of Transomics Biotechnologies, BGI-Shenzhen, Shenzhen 518083, China; College of Life Sciences, Sichuan University, Chengdu 610064, China;
          [4 ] China National GeneBank and Shenzhen Key Laboratory of Transomics Biotechnologies, BGI-Shenzhen, Shenzhen 518083, China; School of Bioscience and Biotechnology, South China University of Technology, Guangzhou 510641, China;
          [5 ] State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Kunming College of Life Science, Chinese Academy of Sciences, Kunming 650204, China;
          [6 ] Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, Kunming 650091, China;
          [7 ] State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, Kunming 650091, China;
          [8 ] China National GeneBank and BGI-Shenzhen, Shenzhen 518083, China;
          [9 ] China National GeneBank and BGI-Shenzhen, Shenzhen 518083, China; School of Bioscience and Biotechnology, South China University of Technology, Guangzhou 510641, China;
          [10 ] China National GeneBank and BGI-Shenzhen, Shenzhen 518083, China; Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
          [11 ] State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Department of Laboratory Medicine and Pathobiology and Banting and Best Diabetes Centre, University of Toronto, Toronto, ON, M5S 1A8, Canada;
          [12 ] Department of Integrative Biology and Center for Computational Biology and Bioinformatics, University of Texas at Austin, Austin, TX 78712; dhillis@austin.utexas.edu chej@mail.kiz.ac.cn wangjun30@gmail.com zhangyp@mail.kiz.ac.cn.
          [13 ] State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, Toronto, ON, M5S 2C6, Canada;
          [14 ] BGI-Shenzhen, Shenzhen 518083, China; Princess Al Jawhara Albrahim Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21589, Saudi Arabia; James D. Watson Institute of Genome Science, Hangzhou 310008, China;
          [15 ] State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; dhillis@austin.utexas.edu chej@mail.kiz.ac.cn wangjun30@gmail.com zhangyp@mail.kiz.ac.cn.
          [16 ] BGI-Shenzhen, Shenzhen 518083, China; Princess Al Jawhara Albrahim Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21589, Saudi Arabia; Department of Biology, University of Copenhagen, 2200 Copenhagen, Denmark; Macau University of Science and Technology, Taipa, Macau 999078, China; and Department of Medicine, University of Hong Kong, Hong Kong dhillis@austin.utexas.edu chej@mail.kiz.ac.cn wangjun30@gmail.com zhangyp@mail.kiz.ac.cn.
          [17 ] State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, Kunming 650091, China; dhillis@austin.utexas.edu chej@mail.kiz.ac.cn wangjun30@gmail.com zhangyp@mail.kiz.ac.cn.
          Article
          1501764112
          10.1073/pnas.1501764112
          25733869
          4afa1d39-ef2f-4abe-867b-187d91159df8
          History

          chromosome rearrangement,de novo genome,highly conserved element,transposable elements

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