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      Whole genome-wide chromosome fusion and new gene birth in the Monopterus albus genome

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          Abstract

          Background

          Teleost fishes account for over half of extant vertebrate species. A core question in biology is how genomic changes drive phenotypic diversity that relates to the origin of teleost fishes.

          Results

          Here, we used comparative genomic analyses with chromosome assemblies of diverse lineages of vertebrates and reconstructed an ancestral vertebrate genome, which revealed phylogenomic trajectories in vertebrates. We found that the whole-genome-wide chromosome fission/fusions took place in the Monopterus albus lineage after the 3-round whole-genome duplication. Four times of genomic fission/fusions events resulted in the whole genome-wide chromosome fusions in the genomic history of the lineage. In addition, abundant recently evolved new genes for reproduction emerged in the Monopterus albus after separated from medaka. Notably, we described evolutionary trajectories of conserved blocks related to sex determination genes in teleosts.

          Conclusions

          These data pave the way for a better understanding of genomic evolution in extant teleosts.

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          Most cited references47

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          The zebrafish reference genome sequence and its relationship to the human genome.

          Zebrafish have become a popular organism for the study of vertebrate gene function. The virtually transparent embryos of this species, and the ability to accelerate genetic studies by gene knockdown or overexpression, have led to the widespread use of zebrafish in the detailed investigation of vertebrate gene function and increasingly, the study of human genetic disease. However, for effective modelling of human genetic disease it is important to understand the extent to which zebrafish genes and gene structures are related to orthologous human genes. To examine this, we generated a high-quality sequence assembly of the zebrafish genome, made up of an overlapping set of completely sequenced large-insert clones that were ordered and oriented using a high-resolution high-density meiotic map. Detailed automatic and manual annotation provides evidence of more than 26,000 protein-coding genes, the largest gene set of any vertebrate so far sequenced. Comparison to the human reference genome shows that approximately 70% of human genes have at least one obvious zebrafish orthologue. In addition, the high quality of this genome assembly provides a clearer understanding of key genomic features such as a unique repeat content, a scarcity of pseudogenes, an enrichment of zebrafish-specific genes on chromosome 4 and chromosomal regions that influence sex determination.
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            Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration.

            The human Y chromosome is intriguing not only because it harbours the master-switch gene that determines gender but also because of its unusual evolutionary history. The Y chromosome evolved from an autosome, and its evolution has been characterized by massive gene decay. Recent whole-genome and transcriptome analyses of Y chromosomes in humans and other primates, in Drosophila species and in plants have shed light on the current gene content of the Y chromosome, its origins and its long-term fate. Furthermore, comparative analysis of young and old Y chromosomes has given further insights into the evolutionary and molecular forces triggering Y-chromosome degeneration and into the evolutionary destiny of the Y chromosome.
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              DMY is a Y-specific DM-domain gene required for male development in the medaka fish.

              Although the sex-determining gene Sry has been identified in mammals, no comparable genes have been found in non-mammalian vertebrates. Here, we used recombinant breakpoint analysis to restrict the sex-determining region in medaka fish (Oryzias latipes) to a 530-kilobase (kb) stretch of the Y chromosome. Deletion analysis of the Y chromosome of a congenic XY female further shortened the region to 250 kb. Shotgun sequencing of this region predicted 27 genes. Three of these genes were expressed during sexual differentiation. However, only the DM-related PG17 was Y specific; we thus named it DMY. Two naturally occurring mutations establish DMY's critical role in male development. The first heritable mutant--a single insertion in exon 3 and the subsequent truncation of DMY--resulted in all XY female offspring. Similarly, the second XY mutant female showed reduced DMY expression with a high proportion of XY female offspring. During normal development, DMY is expressed only in somatic cells of XY gonads. These findings strongly suggest that the sex-specific DMY is required for testicular development and is a prime candidate for the medaka sex-determining gene.
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                Author and article information

                Contributors
                hhcheng@whu.edu.cn
                rjzhou@whu.edu.cn
                Journal
                Cell Biosci
                Cell Biosci
                Cell & Bioscience
                BioMed Central (London )
                2045-3701
                20 May 2020
                20 May 2020
                2020
                : 10
                : 67
                Affiliations
                [1 ]GRID grid.49470.3e, ISNI 0000 0001 2331 6153, Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, , Wuhan University, ; Wuhan, 430072 People’s Republic of China
                [2 ]GRID grid.170205.1, ISNI 0000 0004 1936 7822, Department of Ecology and Evolution, , University of Chicago, ; Chicago, 60637 USA
                Author information
                http://orcid.org/0000-0002-9701-8009
                Article
                432
                10.1186/s13578-020-00432-0
                7240998
                32477490
                6b2ec658-3886-4e05-bebe-25fa9d9cf3c3
                © The Author(s) 2020

                Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 25 March 2020
                : 13 May 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31771370
                Award ID: 31771487
                Award ID: 31970539
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Cell biology
                genomics,evolution,chromosome,vertebrates
                Cell biology
                genomics, evolution, chromosome, vertebrates

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