Dynamic chromosome rearrangements of the white-spotted bamboo shark shed light on cartilaginous fish diversification mechanisms

Cartilaginous fishes have a very high phenotypical diversity, a phenomenon for which the mechanisms have been largely unexplored. Here, we report the genome of the white-spotted bamboo shark as the first chromosome-level genome assembly of cartilaginous fish. Using this genome, we illustrated a dynamic chromosome rearrangement process in the bamboo shark, which resulted in the formation of 13 chromosomes, all of which were sparsely distributed with conserved genes and fast-evolving. We found the fast-evolving chromosomes to be enriched in immune-related genes with two chromosomes harboring the major genes for developing the single-chain antibody. We also found chromosome rearrangements to have resulted in the loss of two genes (p2rx3 and p2rx5) which we also showed were involved in cartilage development using a CRISPR/Cas9 approach in zebrafish. Our study highlighted the significance of chromosome rearrangements in the phenotypical evolution of cartilaginous fishes, providing clues to inform further studies on mechanisms for fish diversification.

[1]  M. Kadota,et al.  Shark genomes provide insights into elasmobranch evolution and the origin of vertebrates , 2018, Nature Ecology & Evolution.

[2]  Hyunsook Kim,et al.  The purinergic receptor P2X5 contributes to bone loss in experimental periodontitis , 2018, BMB reports.

[3]  J. Kaufman.  Unfinished Business: Evolution of the MHC and the Adaptive Immune System of Jawed Vertebrates. , 2018, Annual review of immunology.

[4]  Mark Yandell,et al.  The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution , 2018, Nature Genetics.

[5]  Neva C. Durand,et al.  De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds , 2016, Science.

[6]  K. Rock,et al.  Present Yourself! By MHC Class I and MHC Class II Molecules. , 2016, Trends in immunology.

[7]  Jeffrey T Leek,et al.  Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown , 2016, Nature Protocols.

[8]  Neva C. Durand,et al.  Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments. , 2016, Cell systems.

[9]  Daisy E. Pagete.  An end-to-end assembly of the Aedes aegypti genome , 2016, 1605.04619.

[10]  Bronwen L. Aken,et al.  The spotted gar genome illuminates vertebrate evolution and facilitates human-to-teleost comparisons , 2016, Nature Genetics.

[11]  Jean-Philippe Vert,et al.  HiC-Pro: an optimized and flexible pipeline for Hi-C data processing , 2015, Genome Biology.

[12]  Evgeny M. Zdobnov,et al.  BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs , 2015, Bioinform..

[13]  G. Kelsey.  Keeping methylation at bay , 2015, Nature Genetics.

[14]  J. Zwerina,et al.  Acute‐phase protein serum amyloid A3 is a novel paracrine coupling factor that controls bone homeostasis , 2015, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[15]  E. Paredes-Gamero,et al.  Dual Role of P2 Receptors during Osteoblast Differentiation , 2014, Cell Biochemistry and Biophysics.

[16]  R. Marmorstein,et al.  Crystal Structure of the Stress-Inducible Human Heat Shock Protein 70 Substrate-Binding Domain in Complex with Peptide Substrate , 2014, PloS one.

[17]  Michael Sattler,et al.  The structural analysis of shark IgNAR antibodies reveals evolutionary principles of immunoglobulins , 2014, Proceedings of the National Academy of Sciences.

[18]  Tetsuya Hayashi,et al.  Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads , 2014, Genome research.

[19]  Erping Luo,et al.  In situ intracellular calcium oscillations in osteocytes in intact mouse long bones under dynamic mechanical loading , 2014, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[20]  Brian J. Raney,et al.  Elephant shark genome provides unique insights into gnathostome evolution , 2014, Nature.

[21]  Colin N. Dewey,et al.  De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis , 2013, Nature Protocols.

[22]  Dahui Sun,et al.  Shockwaves Induce Osteogenic Differentiation of Human Mesenchymal Stem Cells Through ATP Release and Activation of P2X7 Receptors , 2013, Stem cells.

[23]  Alexander S. Garruss,et al.  Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution , 2013, Nature Genetics.

[24]  I. Chessell,et al.  Genetic Background Strongly Influences the Bone Phenotype of P2X7 Receptor Knockout Mice , 2012, Journal of osteoporosis.

[25]  A. Cope,et al.  Monocytes Induce STAT3 Activation in Human Mesenchymal Stem Cells to Promote Osteoblast Formation , 2012, PloS one.

[26]  G. Burnstock.  Purinergic signalling: Its unpopular beginning, its acceptance and its exciting future , 2012, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  Heng Li,et al.  A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data , 2011, Bioinform..

[28]  Philip C J Donoghue,et al.  The impact of the representation of fossil calibrations on Bayesian estimation of species divergence times. , 2010, Systematic biology.

[29]  Jérôme Salse,et al.  Improved criteria and comparative genomics tool provide new insights into grass paleogenomics , 2009, Briefings Bioinform..

[30]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[31]  Nansheng Chen,et al.  Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences , 2009, Current protocols in bioinformatics.

[32]  S. M. Sims,et al.  Expression, signaling, and function of P2X7 receptors in bone , 2009, Purinergic Signalling.

[33]  Haibao Tang,et al.  Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. , 2008, Genome research.

[34]  S. Kranenbarg,et al.  Retinoic acid and Cyp26b1 are critical regulators of osteogenesis in the axial skeleton , 2008, Development.

[35]  L. Hawkley,et al.  Social regulation of gene expression in human leukocytes , 2007, Genome Biology.

[36]  Fumiko Ohta,et al.  The medaka draft genome and insights into vertebrate genome evolution , 2007, Nature.

[37]  Zhao Xu,et al.  LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons , 2007, Nucleic Acids Res..

[38]  G. Weinstock,et al.  Creating a honey bee consensus gene set , 2007, Genome Biology.

[39]  Burkhard Morgenstern,et al.  AUGUSTUS: ab initio prediction of alternative transcripts , 2006, Nucleic Acids Res..

[40]  Jan-Fang Cheng,et al.  Detection of weakly conserved ancestral mammalian regulatory sequences by primate comparisons , 2006, Genome Biology.

[41]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[42]  R. Durbin,et al.  GeneWise and Genomewise. , 2004, Genome research.

[43]  Nansheng Chen,et al.  Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences , 2009, Current protocols in bioinformatics.

[44]  M. Flajnik,et al.  Which came first, MHC class I or class II? , 2004, Immunogenetics.

[45]  A. Baldwin,et al.  NF-κB mediates inhibition of mesenchymal cell differentiation through a posttranscriptional gene silencing mechanism , 2003 .

[46]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[47]  Beverly H. Koller,et al.  Altered Cytokine Production in Mice Lacking P2X7Receptors* , 2001, The Journal of Biological Chemistry.

[48]  Y. Uezono,et al.  ATP activates DNA synthesis by acting on P2X receptors in human osteoblast-like MG-63 cells. , 2000, American journal of physiology. Cell physiology.

[49]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[50]  T. Martin,et al.  Osteoblastic cells are involved in osteoclast formation. , 1988, Endocrinology.

[51]  M. Mckenna.  The vertebrates updated: vertebrate paleontology and evolution. , 1988, Science.

[52]  J. Kaufman.  Vertebrates and the evolution of the major histocompatibility complex (MHC) class I and class II molecules , 1988 .

[53]  Charles Auffray,et al.  The class II molecules of the human and murine major histocompatibility complex , 1984, Cell.