Phylogenetics of early vertebrate genomes: an approach to understanding genomic innovations as sources of phenotypic evolution

• Applicant: Dr. Shigehiro Kuraku
• Subject Area: Evolution, Anthropology
• Term: from 2009 to 2014
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 150795574

• Final Report Year: 2015

Final Report Abstract

This research project was conducted in a highly interdisciplinary manner in the interface of molecular phylogenetics, genome informatics, and developmental biology. The goal was to reinforce sequence information for cyclostomes and chondrichthyans and characterize available resources for phylogenetic reconstruction of the process of genome evolution. Achieving these goals was largely supported by the International Sea Lamprey Genome Analysis Project, but the sequence resources derived from that project as well as those for other key species, such as hagfish and Southern Hemisphere lampreys, have remained insufficient. With all these limitations, first, existing information for chondrichthyans was processed to clarify divergence times between the major chondrichthyan lineages, namely, between rays/skates, sharks and chimaeras. Second, lamprey genomes were revealed to have accumulated unique modifications during evolution. This includes massive invasion of Tc1-like transposable elements possibly because of its horizontal transfer from Salmonidae fishes and acquisition of unique patterns of codon usage bias and amino acid composition in protein-coding regions in their genomes. It is of great interest to examine if these genomic characteristics have been maintained in hagfish and Southern Hemisphere lampreys. The whole genome analysis also facilitated an identification of 224 gene families whose members do not exist in any invertebrates but do exist in both sea lamprey and jawed vertebrates. In addition, molecular phylogenetic analyses on individual regulatory gene families were performed to contribute to identification and phylogenetic characterization of developmental regulatory genes to better understand the evolution of morphogenetic and physiological programs at the molecular level. Further investigation on the origin of vertebrates and subsequent evolutionary processes is expected to be performed on the basis of more complete sequence resources covering elasmobranchs, hagfishes and Southern Hemisphere lampreys.

Publications

• The evolution and maintenance of Hox gene clusters in vertebrates and the teleost-specific genome duplication. International Journal of Developmental Biology, 2009. 53: 765-773
  Shigehiro Kuraku and Axel Meyer
  
• Evolution of oropharyngeal patterning mechanisms involving Dlx and endothelins in vertebrates. Developmental Biology, 2010, 341: 315-323
  Shigehiro Kuraku, Yoko Takio, Fumiaki Sugahara, Masaki Takechi, and Shigeru Kuratani
  
• Palaeophylogenomics of the vertebrate ancestor—impact of hidden paralogy in hagfish and lamprey gene phylogeny. Integrative and Comparative Biology, 2010. 50: 124-129
  Shigehiro Kuraku
  
• “Whole Genome Duplications and the Radiation of Vertebrates” in Evolution after Gene Duplication. Pp. 299 - 311. Katharina Dittmar and David Liberles, Eds. Wiley-Blackwell, NY. 2010
  Shigehiro Kuraku and Axel Meyer
  
• Hox gene clusters of early vertebrates: do they serve as reliable markers for genome evolution? Genomics, Proteomics & Bioinformatics, 2011. 9: 97-103
  Shigehiro Kuraku
  
• Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: evolution of regionalization and dorsoventral patterning of the vertebrate forebrain. Development, 2011, 138: 1217-1226
  Fumiaki Sugahara, Shin-ichi Aota, Shigehiro Kuraku, Yasunori Murakami, Yoko Takio-Ogawa, Shigeki Hirano, and Shigeru Kuratani
  
• Unresolved orthology and peculiar coding sequence properties of lamprey genes: the KCNA gene family as test case. BMC Genomics, 2011. 12: 325
  Huan Qiu, Falk Hildebrand, Shigehiro Kuraku, and Axel Meyer
  
• Genomic novelty at the vertebrate ancestor. 2012. In: eLS. John Wiley & Sons Ltd, Chichester
  Kuraku, Shigehiro
  
• Horizontal transfers of Tc1 elements between teleost fishes and their vertebrate parasites, lampreys. Genome Biology and Evolution. 2012. 4: 929-936
  Kuraku, Shigehiro; Qiu, Huan & Meyer, Axel
  
• Revealing less derived nature of cartilaginous fish genomes with their evolutionary time scale inferred with nuclear genes. PLoS One, 2013. 8(6): e66400
  Renz, Adina J.; Meyer, Axel & Kuraku, Shigehiro
  
• Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nature Genetics, 2013. 45: 415-421
  Smith, Jeramiah J; Kuraku, Shigehiro; Holt, Carson; Sauka-Spengler, Tatjana; Jiang, Ning; Campbell, Michael S; Yandell, Mark D; Manousaki, Tereza; Meyer, Axel; Bloom, Ona E; Morgan, Jennifer R; Buxbaum, Joseph D; Sachidanandam, Ravi; Sims, Carrie; Garruss, Alexander S; Cook, Malcolm; Krumlauf, Robb; Wiedemann, Leanne M; Sower, Stacia A; ... & Li, Weiming
  
• Evolution of retinoic acid receptors in chordates: insights from three lamprey species, Lampetra fluviatilis, Petromyzon marinus, and Lethenteron japonicum. EvoDevo, 2015. 6: 18
  Campo-Paysaa, Florent; Jandzik, David; Takio-Ogawa, Yoko; Cattell, Maria V; Neef, Haley C; Langeland, James A; Kuratani, Shigeru; Medeiros, Daniel M; Mazan, Sylvie; Kuraku, Shigehiro; Laudet, Vincent & Schubert, Michael