Domain shuffling and the evolution of vertebrates.

The evolution of vertebrates has included a number of important events: the development of cartilage, the immune system, and complicated craniofacial structures. Here, we examine domain shuffling as one of the mechanisms that contributes novel genetic material required for vertebrate evolution. We mapped domain-shuffling events during the evolution of deuterostomes with a focus on how domain shuffling contributed to the evolution of vertebrate- and chordate-specific characteristics. We identified approximately 1000 new domain pairs in the vertebrate lineage, including approximately 100 that were shared by all seven of the vertebrate species examined. Some of these pairs occur in the protein components of vertebrate-specific structures, such as cartilage and the inner ear, suggesting that domain shuffling made a marked contribution to the evolution of vertebrate-specific characteristics. The evolutionary history of the domain pairs is traceable; for example, the Xlink domain of aggrecan, one of the major components of cartilage, was originally utilized as a functional domain of a surface molecule of blood cells in protochordate ancestors, and it was recruited by the protein of the matrix component of cartilage in the vertebrate ancestor. We also identified genes that were created as a result of domain shuffling in ancestral chordates. Some of these are involved in the functions of chordate structures, such as the endostyle, Reissner's fiber of the neural tube, and the notochord. Our analyses shed new light on the role of domain shuffling, especially in the evolution of vertebrates and chordates.

[1]  A. Xu,et al.  Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. , 2008, Genome research.

[2]  Nicholas H. Putnam,et al.  The amphioxus genome illuminates vertebrate origins and cephalochordate biology. , 2008, Genome research.

[3]  Nicholas H. Putnam,et al.  The amphioxus genome and the evolution of the chordate karyotype , 2008, Nature.

[4]  A. Elofsson,et al.  Quantification of the elevated rate of domain rearrangements in metazoa. , 2007, Journal of molecular biology.

[5]  E. Ostertag,et al.  Current topics in genome evolution: Molecular mechanisms of new gene formation , 2007, Cellular and Molecular Life Sciences.

[6]  Andrew R. Jackson,et al.  The Genome of the Sea Urchin Strongylocentrotus purpuratus , 2006, Science.

[7]  S. Goerdt,et al.  Stabilin-1, a homeostatic scavenger receptor with multiple functions , 2006, Journal of cellular and molecular medicine.

[8]  S. Mohammed,et al.  Identification of ischemia-regulated phosphorylation sites in connexin43: A possible target for the antiarrhythmic peptide analogue rotigaptide (ZP123). , 2006, Journal of molecular and cellular cardiology.

[9]  Robert D. Finn,et al.  Pfam: clans, web tools and services , 2005, Nucleic Acids Res..

[10]  Takeshi Kawashima,et al.  An Integrated Database of the Ascidian, Ciona intestinalis: Towards Functional Genomics , 2005, Zoological science.

[11]  Julian Gough,et al.  Convergent evolution of domain architectures (is rare) , 2005, Bioinform..

[12]  N. Sakabe,et al.  Signs of Ancient and Modern Exon-Shuffling Are Correlated to the Distribution of Ancient and Modern Domains Along Proteins , 2005, Journal of Molecular Evolution.

[13]  A. Grigoriev,et al.  Protein domains correlate strongly with exons in multiple eukaryotic genomes--evidence of exon shuffling? , 2004, Trends in genetics : TIG.

[14]  L. Patthy Modular Assembly of Genes and the Evolution of New Functions , 2003, Genetica.

[15]  I. Rigoutsos,et al.  Genomic analysis of immunity in a Urochordate and the emergence of the vertebrate immune system: “waiting for Godot” , 2003, Immunogenetics.

[16]  J. Guénet,et al.  Mouse SCO-spondin, a gene of the thrombospondin type 1 repeat (TSR) superfamily expressed in the brain. , 2003, Gene.

[17]  J. Aster,et al.  Subcellular localisation, secretion, and post-translational processing of normal cochlin, and of mutants causing the sensorineural deafness and vestibular disorder, DFNA9 , 2003, Journal of medical genetics.

[18]  C. Chothia,et al.  Evolution of the Protein Repertoire , 2003, Science.

[19]  N. Lavidis,et al.  Neuromuscular synapses mediate motor axon branching and motoneuron survival during the embryonic period of programmed cell death. , 2003, Developmental biology.

[20]  Nori Satoh,et al.  The ascidian tadpole larva: comparative molecular development and genomics , 2003, Nature Reviews Genetics.

[21]  R. Malinow,et al.  APP Processing and Synaptic Function , 2003, Neuron.

[22]  Takeshi Kawashima,et al.  Large scale EST analyses in Ciona intestinalis: its application as Northern blot analyses. , 2003, Development genes and evolution.

[23]  P. Herrlich,et al.  CD44: From adhesion molecules to signalling regulators , 2003, Nature Reviews Molecular Cell Biology.

[24]  Paul Richardson,et al.  The Draft Genome of Ciona intestinalis: Insights into Chordate and Vertebrate Origins , 2002, Science.

[25]  A. Valencia,et al.  MARVEL: a conserved domain involved in membrane apposition events. , 2002, Trends in biochemical sciences.

[26]  Anton Nekrutenko,et al.  Signatures of domain shuffling in the human genome. , 2002, Genome research.

[27]  T. Burn,et al.  Characterization of human aggrecanase 2 (ADAM-TS5): substrate specificity studies and comparison with aggrecanase 1 (ADAM-TS4). , 2002, Matrix biology : journal of the International Society for Matrix Biology.

[28]  Takeshi Kawashima,et al.  A cDNA resource from the basal chordate Ciona intestinalis , 2002, Genesis.

[29]  Y. Kohara,et al.  Gene expression profiles in young adult Ciona intestinalis , 2002, Development Genes and Evolution.

[30]  Sean B. Carroll,et al.  Evolution of a transcriptional repression domain in an insect Hox protein , 2002, Nature.

[31]  T. Noda,et al.  Complex phenotype of mice lacking occludin, a component of tight junction strands. , 2000, Molecular biology of the cell.

[32]  L. Patthy Genome evolution and the evolution of exon-shuffling--a review. , 1999, Gene.

[33]  L. Hood,et al.  EST analysis of gene expression in early cleavage-stage sea urchin embryos. , 1999, Development.

[34]  N. Satoh,et al.  Ascidian homologs of mammalian thyroid peroxidase genes are expressed in the thyroid-equivalent region of the endostyle. , 1999, The Journal of experimental zoology.

[35]  Yoshihiko Yamada,et al.  Mice lacking link protein develop dwarfism and craniofacial abnormalities , 1999, Nature Genetics.

[36]  E. Tongiorgi Tenascin-C expression in the trunk of wild-type, cyclops and floating head zebrafish embryos , 1999, Brain Research Bulletin.

[37]  K. Verhoeven Mutations in the human α-tectorin gene cause autosomal dominant non-syndromic hearing impairment , 1999, Nature Genetics.

[38]  G. Freeman,et al.  Attractin (DPPT-L), a member of the CUB family of cell adhesion and guidance proteins, is secreted by activated human T lymphocytes and modulates immune cell interactions. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[39]  C. Wollheim,et al.  Ca2+‐independent insulin exocytosis induced by α‐latrotoxin requires latrophilin, a G protein‐coupled receptor , 1998, The EMBO journal.

[40]  G. Richardson,et al.  Mutations in the human α-tectorin gene cause autosomal dominant non-syndromic hearing impairment , 1998, Nature Genetics.

[41]  Sean R. Eddy,et al.  Profile hidden Markov models , 1998, Bioinform..

[42]  J. Cheng,et al.  Structure of the human aggrecan gene: exon-intron organization and association with the protein domains. , 1995, The Biochemical journal.

[43]  M. Tanzer,et al.  Molecular cloning and analysis of the protein modules of aggrecans. , 1994, EXS.

[44]  A. Sidow,et al.  Gene duplications and the origins of vertebrate development. , 1994, Development (Cambridge, England). Supplement.