1932

Abstract

Homeostatic control and reproductive functions of humans are regulated at the molecular levels largely by peptide hormones secreted from endocrine and/or neuroendocrine cells in the central nervous system and peripheral organs. Homologs of those hormones and their receptors function similarly in many vertebrate species distantly related to humans, but the evolutionary history of the endocrine system involving those factors has been obscured by the scarcity of genome DNA sequence information of some taxa that potentially contain their orthologs. Focusing on non-osteichthyan vertebrates, namely jawless and cartilaginous fishes, this article illustrates how investigating genome sequence information assists our understanding of the diversification of vertebrate gene repertoires in four broad themes: () the presence or absence of genes, () multiplication and maintenance of paralogs, () differential fates of duplicated paralogs, and () the evolutionary timing of gene origins.

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2023-02-15
2024-12-06
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Literature Cited

  1. 1.
    Ando H, Ukena K, Nagata S 2021. Handbook of Hormones London: Elsevier
    [Google Scholar]
  2. 2.
    Sanger GJ, Lee K. 2008. Hormones of the gut-brain axis as targets for the treatment of upper gastrointestinal disorders. Nat. Rev. Drug Discov. 7:324154
    [Google Scholar]
  3. 3.
    Hara Y, Yamaguchi K, Onimaru K, Kadota M, Koyanagi M et al. 2018. Shark genomes provide insights into elasmobranch evolution and the origin of vertebrates. Nat. Ecol. Evol. 2:11176171
    [Google Scholar]
  4. 4.
    Borell M. 1978. Setting the standards for a new science: Edward Schäfer and endocrinology. Med. Hist. 22:328290
    [Google Scholar]
  5. 5.
    Tata JR. 2005. One hundred years of hormones. EMBO Rep. 6:649096
    [Google Scholar]
  6. 6.
    Sower SA. 1998. Brain and pituitary hormones of lampreys, recent findings and their evolutionary significance. Am. Zool. 38:11538
    [Google Scholar]
  7. 7.
    Takahashi A, Amemiya Y, Nozaki M, Sower SA, Kawauchi H. 2001. Evolutionary significance of proopiomelanocortin in agnatha and chondrichthyes. Comp. Biochem. Physiol. B 129:2–328389
    [Google Scholar]
  8. 8.
    Krell F-T, Cranston PS. 2004. Which side of the tree is more basal?. Syst. Entomol. 29:327981
    [Google Scholar]
  9. 9.
    Kuraku S, Feiner N, Keeley SD, Hara Y. 2016. Incorporating tree-thinking and evolutionary time scale into developmental biology. Dev. Growth Differ. 58:113142
    [Google Scholar]
  10. 10.
    Takei Y. 2000. Comparative physiology of body fluid regulation in vertebrates with special reference to thirst regulation. Jpn. J. Physiol. 50:217186
    [Google Scholar]
  11. 11.
    Mardis ER. 2011. A decade's perspective on DNA sequencing technology. Nature 470:7333198203
    [Google Scholar]
  12. 12.
    Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N et al. 2013. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat. Genet. 45:41521
    [Google Scholar]
  13. 13.
    Zhu T, Li Y, Pang Y, Han Y, Li J et al. 2021. Chromosome-level genome assembly of Lethenteron reissneri provides insights into lamprey evolution. Mol. Ecol. Resour. 21:244863
    [Google Scholar]
  14. 14.
    Mehta TK, Ravi V, Yamasaki S, Lee AP, Lian MM et al. 2013. Evidence for at least six Hox clusters in the Japanese lamprey (Lethenteron japonicum). PNAS 110:401604449
    [Google Scholar]
  15. 15.
    Marra NJ, Stanhope MJ, Jue NK, Wang M, Sun Q et al. 2019. White shark genome reveals ancient elasmobranch adaptations associated with wound healing and the maintenance of genome stability. PNAS 116:10444655
    [Google Scholar]
  16. 16.
    Zhang Y, Gao H, Li H, Guo J, Ouyang B et al. 2020. The white-spotted bamboo shark genome reveals chromosome rearrangements and fast-evolving immune genes of cartilaginous fish. iScience 23:11101754
    [Google Scholar]
  17. 17.
    Tan M, Redmond AK, Dooley H, Nozu R, Sato K et al. 2021. The whale shark genome reveals patterns of vertebrate gene family evolution. eLife 10:e65394
    [Google Scholar]
  18. 18.
    Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM et al. 2014. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:748217479
    [Google Scholar]
  19. 19.
    Yamaguchi K, Hara Y, Tatsumi K, Nishimura O, Smith JJ et al. 2020. Inference of a genome-wide protein-coding gene set of the inshore hagfish Eptatretus burgeri Work. Pap. RIKEN Jpn.:
    [Google Scholar]
  20. 20.
    Cunningham F, Allen JE, Allen J, Alvarez-Jarreta J, Amode MR et al. 2022. Ensembl 2022. Nucleic Acids Res. 50:D1D98895
    [Google Scholar]
  21. 21.
    Smith JJ, Timoshevskaya N, Ye C, Holt C, Keinath MC et al. 2018. The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution. Nat. Genet. 50:227077
    [Google Scholar]
  22. 22.
    Nakatani Y, Shingate P, Ravi V, Pillai NE, Prasad A et al. 2021. Reconstruction of proto-vertebrate, proto-cyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution. Nat. Commun. 12:14489
    [Google Scholar]
  23. 23.
    Hess JE, Smith JJ, Timoshevskaya N, Baker C, Caudill CC et al. 2020. Genomic islands of divergence infer a phenotypic landscape in Pacific lamprey. Mol. Ecol. 29:20384156
    [Google Scholar]
  24. 24.
    Kuraku S, Qiu H, Meyer A. 2012. Horizontal transfers of Tc1 elements between teleost fishes and their vertebrate parasites, lampreys. Genome Biol. Evol. 4:992936
    [Google Scholar]
  25. 25.
    Kuraku S. 2013. Impact of asymmetric gene repertoire between cyclostomes and gnathostomes. Semin. Cell Dev. Biol. 24:211927
    [Google Scholar]
  26. 26.
    Venkatesh B, Kirkness EF, Loh Y-H, Halpern AL, Lee AP et al. 2007. Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLOS Biol. 5:4e101
    [Google Scholar]
  27. 27.
    Read TD, Petit RA 3rd, Joseph SJ, Alam MT, Weil MR et al. 2017. Draft sequencing and assembly of the genome of the world's largest fish, the whale shark: Rhincodon typus Smith 1828. BMC Genom. 18:1532
    [Google Scholar]
  28. 28.
    Darwin Tree Life Proj. Consort. 2022. Sequence locally, think globally: the Darwin Tree of Life Project. PNAS 119:4e2115642118
    [Google Scholar]
  29. 29.
    Hoencamp C, Dudchenko O, Elbatsh AMO, Brahmachari S, Raaijmakers JA et al. 2021. 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science 372:654598489
    [Google Scholar]
  30. 30.
    Rhie A, McCarthy SA, Fedrigo O, Damas J, Formenti G et al. 2021. Towards complete and error-free genome assemblies of all vertebrate species. Nature 592:785673746
    [Google Scholar]
  31. 31.
    Kuraku S. 2021. Shark and ray genomics for disentangling their morphological diversity and vertebrate evolution. Dev. Biol. 477:26272
    [Google Scholar]
  32. 32.
    Philippe H, Zhou Y, Brinkmann H, Rodrigue N, Delsuc F. 2005. Heterotachy and long-branch attraction in phylogenetics. BMC Evol. Biol. 5:50
    [Google Scholar]
  33. 33.
    Yang Z, Rannala B. 2012. Molecular phylogenetics: principles and practice. Nat. Rev. Genet. 13:530314
    [Google Scholar]
  34. 34.
    Wiemers DO, Shao L-J, Ain R, Dai G, Soares MJ. 2003. The mouse prolactin gene family locus. Endocrinology 144:131325
    [Google Scholar]
  35. 35.
    Simmons DG, Rawn S, Davies A, Hughes M, Cross JC 2008. Spatial and temporal expression of the 23 murine Prolactin/Placental Lactogen-related genes is not associated with their position in the locus. BMC Genom. 9:352
    [Google Scholar]
  36. 36.
    Okada R, Suzuki M, Ito N, Hyodo S, Kikuyama S. 2019. A novel type of prolactin expressed in the bullfrog pituitary specifically during the larval period. Gen. Comp. Endocrinol. 276:7785
    [Google Scholar]
  37. 37.
    Yamaguchi Y, Takagi W, Kuraku S, Moriyama S, Bell JD et al. 2015. Discovery of conventional prolactin from the holocephalan elephant fish, Callorhinchus milii. Gen. Comp. Endocrinol. 224:21627
    [Google Scholar]
  38. 38.
    Hallast P, Nagirnaja L, Margus T, Laan M. 2005. Segmental duplications and gene conversion: human luteinizing hormone/chorionic gonadotropin β gene cluster. Genome Res. 15:11153546
    [Google Scholar]
  39. 39.
    Petronella N, Drouin G 2011. Gene conversions in the growth hormone gene family of primates: stronger homogenizing effects in the Hominidae lineage. Genomics 98:317381
    [Google Scholar]
  40. 40.
    Navarro VM, Tena-Sempere M. 2011. Neuroendocrine control by kisspeptins: role in metabolic regulation of fertility. Nat. Rev. Endocrinol. 8:14053
    [Google Scholar]
  41. 41.
    Freeman ME, Kanyicska B, Lerant A, Nagy G. 2000. Prolactin: structure, function, and regulation of secretion. Physiol. Rev. 80:41523631
    [Google Scholar]
  42. 42.
    Venken K, Movérare-Skrtic S, Kopchick JJ, Coschigano KT, Ohlsson C et al. 2007. Impact of androgens, growth hormone, and IGF-I on bone and muscle in male mice during puberty. J. Bone Miner. Res. 22:17282
    [Google Scholar]
  43. 43.
    Fukamachi S, Meyer A. 2007. Evolution of receptors for growth hormone and somatolactin in fish and land vertebrates: lessons from the lungfish and sturgeon orthologues. J. Mol. Evol. 65:435972
    [Google Scholar]
  44. 44.
    Wan G, Chan KM. 2010. A study of somatolactin actions by ectopic expression in transgenic zebrafish larvae. J. Mol. Endocrinol. 45:530115
    [Google Scholar]
  45. 45.
    Huang X, Hui MNY, Liu Y, Yuen DSH, Zhang Y et al. 2009. Discovery of a novel prolactin in non-mammalian vertebrates: evolutionary perspectives and its involvement in teleost retina development. PLOS ONE 4:7e6163
    [Google Scholar]
  46. 46.
    Moriyama S, Oda M, Takahashi A, Sower SA, Kawauchi H. 2006. Genomic structure of the sea lamprey growth hormone-encoding gene. Gen. Comp. Endocrinol. 148:13340
    [Google Scholar]
  47. 47.
    Ocampo Daza D, Larhammar D. 2018. Evolution of the growth hormone, prolactin, prolactin 2 and somatolactin family. Gen. Comp. Endocrinol. 264:94112
    [Google Scholar]
  48. 48.
    Gong N, Ferreira-Martins D, Norstog JL, McCormick SD, Sheridan MA. 2022. Discovery of prolactin-like in lamprey: role in osmoregulation and new insight into the evolution of the growth hormone/prolactin family. PNAS 119:40e2212196119
    [Google Scholar]
  49. 49.
    Huising MO, Kruiswijk CP, Flik G. 2006. Phylogeny and evolution of class-I helical cytokines. J. Endocrinol. 189:1125
    [Google Scholar]
  50. 50.
    Liongue C, Ward AC. 2007. Evolution of class I cytokine receptors. BMC Evol. Biol. 7:120
    [Google Scholar]
  51. 51.
    Nurk S, Koren S, Rhie A, Rautiainen M, Bzikadze AV et al. 2022. The complete sequence of a human genome. Science 376:65884453
    [Google Scholar]
  52. 52.
    Yamaguchi K, Kadota M, Nishimura O, Ohishi Y, Naito Y, Kuraku S. 2021. Technical considerations in Hi-C scaffolding and evaluation of chromosome-scale genome assemblies. Mol. Ecol. 30:23592334
    [Google Scholar]
  53. 53.
    Pitel F, Faraut T, Bruneau G, Monget P. 2010. Is there a leptin gene in the chicken genome? Lessons from phylogenetics, bioinformatics and genomics. Gen. Comp. Endocrinol. 167:115
    [Google Scholar]
  54. 54.
    Seroussi E, Pitel F, Leroux S, Morisson M, Bornelöv S et al. 2017. Mapping of leptin and its syntenic genes to chicken chromosome 1p. BMC Genet. 18:177
    [Google Scholar]
  55. 55.
    Bankir L. 2001. Antidiuretic action of vasopressin: quantitative aspects and interaction between V1a and V2 receptor-mediated effects. Cardiovasc. Res. 51:337290
    [Google Scholar]
  56. 56.
    Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M. 2011. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat. Rev. Neurosci. 12:952438
    [Google Scholar]
  57. 57.
    Theofanopoulou C, Gedman G, Cahill JA, Boeckx C, Jarvis ED. 2021. Universal nomenclature for oxytocin-vasotocin ligand and receptor families. Nature 592:785674755
    [Google Scholar]
  58. 58.
    Hyodo S. 2021. Neurohypophysial hormone family. See Reference 1 6769
  59. 59.
    Gwee P-C, Tay B-H, Brenner S, Venkatesh B. 2009. Characterization of the neurohypophysial hormone gene loci in elephant shark and the Japanese lamprey: origin of the vertebrate neurohypophysial hormone genes. BMC Evol. Biol. 9:47
    [Google Scholar]
  60. 60.
    Gwee P-C, Amemiya CT, Brenner S, Venkatesh B. 2008. Sequence and organization of coelacanth neurohypophysial hormone genes: evolutionary history of the vertebrate neurohypophysial hormone gene locus. BMC Evol. Biol. 8:93
    [Google Scholar]
  61. 61.
    Acher R, Chauvet J, Chauvet MT, Rouille Y. 1999. Unique evolution of neurohypophysial hormones in cartilaginous fishes: possible implications for urea-based osmoregulation. J. Exp. Zool. 284:547584
    [Google Scholar]
  62. 62.
    Hyodo S, Tsukada T, Takei Y. 2004. Neurohypophysial hormones of dogfish, Triakis scyllium: structures and salinity-dependent secretion. Gen. Comp. Endocrinol. 138:297104
    [Google Scholar]
  63. 63.
    Ruppert S, Scherer G, Schütz G. 1984. Recent gene conversion involving bovine vasopressin and oxytocin precursor genes suggested by nucleotide sequence. Nature 308:595955457
    [Google Scholar]
  64. 64.
    Theofanopoulou C. 2021. Reconstructing the evolutionary history of the oxytocin and vasotocin receptor gene family: insights on whole genome duplication scenarios. Dev. Biol. 479:99106
    [Google Scholar]
  65. 65.
    Ocampo Daza D, Bergqvist CA, Larhammar D. 2021. The evolution of oxytocin and vasotocin receptor genes in jawed vertebrates: a clear case for gene duplications through ancestral whole-genome duplications. Front. Endocrinol. 12:792644
    [Google Scholar]
  66. 66.
    Cañestro C. 2012. Two rounds of whole-genome duplication: evidence and impact on the evolution of vertebrate innovations. Polyploidy and Genome Evolution PS Soltis, DE Soltis 30939. Berlin, Heidelberg: Springer Berlin Heidelberg
    [Google Scholar]
  67. 67.
    Dehal P, Boore JL. 2005. Two rounds of whole genome duplication in the ancestral vertebrate. PLOS Biol. 3:10e314
    [Google Scholar]
  68. 68.
    Larhammar D, Lundin L-G, Hallböök F. 2002. The human Hox-bearing chromosome regions did arise by block or chromosome (or even genome) duplications. Genome Res. 12:12191020
    [Google Scholar]
  69. 69.
    Sacerdot C, Louis A, Bon C, Berthelot C, Roest Crollius H. 2018. Chromosome evolution at the origin of the ancestral vertebrate genome. Genome Biol. 19:166
    [Google Scholar]
  70. 70.
    Simakov O, Marlétaz F, Yue J-X, O'Connell B, Jenkins J et al. 2020. Deeply conserved synteny resolves early events in vertebrate evolution. Nat. Ecol. Evol. 4:682030
    [Google Scholar]
  71. 71.
    Sefideh FA, Moon MJ, Yun S, Hong SI, Hwang J-I, Seong JY. 2014. Local duplication of gonadotropin-releasing hormone (GnRH) receptor before two rounds of whole genome duplication and origin of the mammalian GnRH receptor. PLOS ONE 9:2e87901
    [Google Scholar]
  72. 72.
    Ocampo Daza D, Larhammar D. 2018. Evolution of the receptors for growth hormone, prolactin, erythropoietin and thrombopoietin in relation to the vertebrate tetraploidizations. Gen. Comp. Endocrinol. 257:14360
    [Google Scholar]
  73. 73.
    Cardoso JCR, Félix RC, Bergqvist CA, Larhammar D. 2014. New insights into the evolution of vertebrate CRH (corticotropin-releasing hormone) and invertebrate DH44 (diuretic hormone 44) receptors in metazoans. Gen. Comp. Endocrinol. 209:16270
    [Google Scholar]
  74. 74.
    Kim D-K, Yun S, Son GH, Hwang J-I, Park CR et al. 2014. Coevolution of the spexin/galanin/kisspeptin family: Spexin activates galanin receptor type II and III. Endocrinology 155:5186473
    [Google Scholar]
  75. 75.
    Hara Y, Takeuchi M, Kageyama Y, Tatsumi K, Hibi M et al. 2018. Madagascar ground gecko genome analysis characterizes asymmetric fates of duplicated genes. BMC Biol. 16:40
    [Google Scholar]
  76. 76.
    Pradhan G, Samson SL, Sun Y. 2013. Ghrelin. Curr. Opin. Clin. Nutr. Metab. Care. 16:661924
    [Google Scholar]
  77. 77.
    Peeters TL. 2005. Ghrelin: a new player in the control of gastrointestinal functions. Gut 54:11163849
    [Google Scholar]
  78. 78.
    Kaiya H. 2021. Ghrelin. See Reference 1 32124
  79. 79.
    Kaiya H, Kodama S, Ishiguro K, Matsuda K, Uchiyama M et al. 2009. Ghrelin-like peptide with fatty acid modification and O-glycosylation in the red stingray, Dasyatis akajei. BMC Biochem. 10:30
    [Google Scholar]
  80. 80.
    Kawakoshi A, Kaiya H, Riley LG, Hirano T, Grau EG et al. 2007. Identification of a ghrelin-like peptide in two species of shark, Sphyrna lewini and Carcharhinus melanopterus. Gen. Comp. Endocrinol. 151:325968
    [Google Scholar]
  81. 81.
    Chen C-Y, Tsai C-Y. 2012. Ghrelin and motilin in the gastrointestinal system. Curr. Pharm. Des. 18:31475565
    [Google Scholar]
  82. 82.
    Liu Y, Li S, Huang X, Lu D, Liu X et al. 2013. Identification and characterization of a motilin-like peptide and its receptor in teleost. Gen. Comp. Endocrinol. 186:8593
    [Google Scholar]
  83. 83.
    Kuraku S. 2010. Palaeophylogenomics of the vertebrate ancestor—impact of hidden paralogy on hagfish and lamprey gene phylogeny. Integr. Comp. Biol. 50:112429
    [Google Scholar]
  84. 84.
    Kaiya H, Kangawa K, Miyazato M. 2014. Molecular evolution of GPCRs: ghrelin/ghrelin receptors. J. Mol. Endocrinol. 52:3T87100
    [Google Scholar]
  85. 85.
    Kaiya H, Kangawa K, Miyazato M. 2013. Ghrelin receptors in non-Mammalian vertebrates. Front. Endocrinol. 4:81
    [Google Scholar]
  86. 86.
    Kitazawa T, Kaiya H. 2021. Motilin comparative study: structure, distribution, receptors, and gastrointestinal motility. Front. Endocrinol. 12:700884
    [Google Scholar]
  87. 87.
    Pan WW, Myers MG Jr. 2018. Leptin and the maintenance of elevated body weight. Nat. Rev. Neurosci. 19:295105
    [Google Scholar]
  88. 88.
    Wada N. 2021. Leptin. See Reference 1 57375
  89. 89.
    Wolf G. 1996. Leptin: the weight-reducing plasma protein encoded by the obese gene. Nutr. Rev. 54:39193
    [Google Scholar]
  90. 90.
    Mania M, Maruccio L, Russo F, Abbate F, Castaldo L et al. 2017. Expression and distribution of leptin and its receptors in the digestive tract of DIO (diet-induced obese) zebrafish. Ann. Anat. 212:3747
    [Google Scholar]
  91. 91.
    Audira G, Sarasamma S, Chen J-R, Juniardi S, Sampurna BP et al. 2018. Zebrafish mutants carrying Leptin a (lepa) gene deficiency display obesity, anxiety, less aggression and fear, and circadian rhythm and color preference dysregulation. Int. J. Mol. Sci. 19:124038
    [Google Scholar]
  92. 92.
    Montalbano G, Maugeri A, Guerrera MC, Miceli N, Navarra M et al. 2021. A white grape juice extract reduces fat accumulation through the modulation of ghrelin and leptin expression in an in vivo model of overfed zebrafish. Molecules 26:41119
    [Google Scholar]
  93. 93.
    Gesta S, Tseng Y-H, Kahn CR. 2007. Developmental origin of fat: tracking obesity to its source. Cell 131:224256
    [Google Scholar]
  94. 94.
    Ishida-Takahashi R, Rosario F, Gong Y, Kopp K, Stancheva Z et al. 2006. Phosphorylation of Jak2 on Ser523 inhibits Jak2-dependent Leptin receptor signaling. Mol. Cell. Biol. 26:11406373
    [Google Scholar]
  95. 95.
    Eyckerman S, Broekaert D, Verhee A, Vandekerckhove J, Tavernier J. 2000. Identification of the Y985 and Y1077 motifs as SOCS3 recruitment sites in the murine leptin receptor. FEBS Lett. 486:13337
    [Google Scholar]
  96. 96.
    Mori H, Hanada R, Hanada T, Aki D, Mashima R et al. 2004. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat. Med. 10:773943
    [Google Scholar]
  97. 97.
    Gong Y, Ishida-Takahashi R, Villanueva EC, Fingar DC, Münzberg H, Myers MG Jr. 2007. The long form of the leptin receptor regulates STAT5 and ribosomal protein S6 via alternate mechanisms. J. Biol. Chem. 282:423101927
    [Google Scholar]
  98. 98.
    Bates SH, Stearns WH, Dundon TA, Schubert M, Tso AWK et al. 2003. STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature 421:692585659
    [Google Scholar]
  99. 99.
    Carpenter B, Hemsworth GR, Wu Z, Maamra M, Strasburger CJ et al. 2012. Structure of the human obesity receptor leptin-binding domain reveals the mechanism of leptin antagonism by a monoclonal antibody. Structure 20:348797
    [Google Scholar]
  100. 100.
    Nishimura O, Rozewicki J, Yamaguchi K, Tatsumi K, Ohishi Y et al. 2022. Squalomix: shark and ray genome analysis consortium and its data sharing platform. . F1000Research 11:1077
    [Google Scholar]
  101. 101.
    Uno Y, Nozu R, Kiyatake I, Higashiguchi N, Sodeyama S et al. 2020. Cell culture-based karyotyping of orectolobiform sharks for chromosome-scale genome analysis. Commun. Biol. 3:652
    [Google Scholar]
  102. 102.
    Parra G, Bradnam K, Ning Z, Keane T, Korf I. 2009. Assessing the gene space in draft genomes. Nucleic Acids Res. 37:128997
    [Google Scholar]
  103. 103.
    Hara Y, Tatsumi K, Yoshida M, Kajikawa E, Kiyonari H, Kuraku S 2015. Optimizing and benchmarking de novo transcriptome sequencing: from library preparation to assembly evaluation. BMC Genom. 16:977
    [Google Scholar]
  104. 104.
    Sayers EW, Beck J, Brister JR, Bolton EE, Canese K et al. 2020. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 48:D1D916
    [Google Scholar]
  105. 105.
    Seppey M, Manni M, Zdobnov EM. 2019. BUSCO: assessing genome assembly and annotation completeness. Methods Mol. Biol. 1962:22745
    [Google Scholar]
  106. 106.
    Kikugawa K, Katoh K, Kuraku S, Sakurai H, Ishida O et al. 2004. Basal jawed vertebrate phylogeny inferred from multiple nuclear DNA-coded genes. BMC Biol. 2:3
    [Google Scholar]
  107. 107.
    Putnam NH, Butts T, Ferrier DEK, Furlong RF, Hellsten U et al. 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature 453:7198106471
    [Google Scholar]
  108. 108.
    Smith JJ, Keinath MC. 2015. The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplications. Genome Res. 25:8108190
    [Google Scholar]
  109. 109.
    Kuraku S, Meyer A, Kuratani S. 2009. Timing of genome duplications relative to the origin of the vertebrates: Did cyclostomes diverge before or after?. Mol. Biol. Evol. 26:14759
    [Google Scholar]
  110. 110.
    Escriva H, Manzon L, Youson J, Laudet V. 2002. Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol. Biol. Evol. 19:9144050
    [Google Scholar]
  111. 111.
    Cruz SA, Tseng Y-C, Kaiya H, Hwang PP. 2010. Ghrelin affects carbohydrate-glycogen metabolism via insulin inhibition and glucagon stimulation in the zebrafish (Danio rerio) brain. Comp. Biochem. Physiol. A 156:2190200
    [Google Scholar]
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