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Recent genome duplications facilitate the phenotypic diversity of Hb repertoire in the Cyprinidae

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Abstract

Whole-genome duplications (WGDs) are an important contributor to phenotypic innovations in evolutionary history. The diversity of blood oxygen transport traits is the perfect reflection of physiological versatility for evolutionary success among vertebrates. In this study, the evolutionary changes of hemoglobin (Hb) repertoire driven by the recent genome duplications were detected in representative Cyprinidae fish, including eight diploid and four tetraploid species. Comparative genomic analysis revealed a substantial variation in both membership composition and intragenomic organization of Hb genes in these species. Phylogenetic reconstruction analyses were conducted to characterize the evolutionary history of these genes. Data were integrated with the expression profiles of the genes during ontogeny. Our results indicated that genome duplications facilitated the phenotypic diversity of the Hb gene family; each was associated with species-specific changes in gene content via gene loss and fusion after genome duplications. This led to repeated evolutionary transitions in the ontogenic regulation of Hb gene expression. Our results revealed that genome duplications helped to generate phenotypic changes in Cyprinidae Hb systems.

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References

  • Abi-Rached, L., Gilles, A., Shiina, T., Pontarotti, P., and Inoko, H. (2002). Evidence of en bloc duplication in vertebrate genomes. Nat Genet 31, 100–105.

    CAS  PubMed  Google Scholar 

  • Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J Mol Biol 215, 403–410.

    CAS  PubMed  Google Scholar 

  • Arnegard, M.E., Zwickl, D.J., Lu, Y., and Zakon, H.H. (2010). Old gene duplication facilitates origin and diversification of an innovative communication system—twice. Proc Natl Acad Sci USA 107, 22172–22177.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baalsrud, H.T., Voje, K.L., Tørresen, O.K., Solbakken, M.H., Matschiner, M., Malmstrøm, M., Hanel, R., Salzburger, W., Jakobsen, K.S., and Jentoft, S. (2017). Evolution of hemoglobin genes in codfishes influenced by ocean depth. Sci Rep 7, 1.

    CAS  Google Scholar 

  • Berenbrink, M. (2007). Historical reconstructions ofevolving physiological complexity: O2 secretion in the eye and swimbladder of fishes. J Exp Biol 210, 1641–1652.

    PubMed  Google Scholar 

  • Berenbrink, M., Koldkjaer, P., Kepp, O., and Cossins, A.R. (2005). Evolution of oxygen secretion in fishes and the emergence ofa complex physiological system. Science 307, 1752–1757.

    CAS  PubMed  Google Scholar 

  • Berthelot, C., Brunet, F., Chalopin, D., Juanchich, A., Bernard, M., Noël, B., Bento, P., Da Silva, C., Labadie, K., Alberti, A., et al. (2014). The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5, 1.

    Google Scholar 

  • Birney, E., Clamp, M., and Durbin, R. (2004). GeneWise and genomewise. Genome Res 14, 988–995.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blanc, G., and Wolfe, K.H. (2004). Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679–1691.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Borza, T., Stone, C., Gamperl, A.K., and Bowman, S. (2009). Atlantic cod (Gadus morhua) hemoglobin genes: multiplicity and polymorphism. BMC Genet 10, 51.

    PubMed  PubMed Central  Google Scholar 

  • Braasch, I., Salzburger, W., and Meyer, A. (2006). Asymmetric evolution in two fish-specifically duplicated receptor tyrosine kinase paralogons involved in teleost coloration. Mol Biol Evol 23, 1192–1202.

    CAS  PubMed  Google Scholar 

  • Braasch, I., Schartl, M., and Volff, J.N. (2007). Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol Biol 7, 74.

    PubMed  PubMed Central  Google Scholar 

  • Braasch, I., Brunet, F., Volff, J.N., and Schartl, M. (2009a). Pigmentation pathway evolution after whole-genome duplication in fish. Genome Biol Evol 1, 479–493.

    PubMed  PubMed Central  Google Scholar 

  • Braasch, I., Volff, J.N., and Schartl, M. (2009b). The endothelin system: evolution of vertebrate-specific ligand-receptor interactions by three rounds of genome duplication. Mol Biol Evol 26, 783–799.

    CAS  PubMed  Google Scholar 

  • Brunet, F.G., Volff, J.N., and Schartl, M. (2016). Whole genome duplications shaped the receptor tyrosine kinase repertoire of jawed vertebrates. Genome Biol Evol 8, 1600–1613.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cadiz, L., Desmarais, E., Servili, A., Quazuguel, P., Madec, L., Huelvan, C., Andersen, O., Zambonino-Infante, J., and Mazurais, D. (2017). Genomic organization and spatio-temporal expression of the hemoglobin genes in European sea bass (Dicentrarchus labrax). Mar Biol 164, 95.

    Google Scholar 

  • Chen, S., Zhou, Y., Chen, Y., and Gu, J. (2018). fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890.

    PubMed  PubMed Central  Google Scholar 

  • Chen, Z., Omori, Y., Koren, S., Shirokiya, T., Kuroda, T., Miyamoto, A., Wada, H., Fujiyama, A., Toyoda, A., Zhang, S., et al. (2019). De novo assembly of the goldfish (Carassius auratus) genome and the evolution of genes after whole-genome duplication. Sci Adv 5, eaav0547.

    PubMed  PubMed Central  Google Scholar 

  • Comai, L. (2005). The advantages and disadvantages of being polyploid. Nat Rev Genet 6, 836–846.

    CAS  PubMed  Google Scholar 

  • Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E. (2004). WebLogo: a sequence logo generator. Genome Res 14, 1188–1190.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Czelusniak, J., Goodman, M., Hewett-Emmett, D., Weiss, M.L., Venta, P.J., and Tashian, R.E. (1982). Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes. Nature 298, 297–300.

    CAS  PubMed  Google Scholar 

  • Damsgaard, C., Storz, J.F., Hoffmann, F.G., and Fago, A. (2013). Hemoglobin isoform differentiation and allosteric regulation of oxygen binding in the turtle, Trachemys scripta. Am J Physiol Regul Integr Comp Physiol 305, R961–R967.

    CAS  PubMed  PubMed Central  Google Scholar 

  • David, L., Blum, S., Feldman, M.W., Lavi, U., and Hillel, J. (2003). Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Mol Biol Evol 20, 1425–1434.

    CAS  PubMed  Google Scholar 

  • Dehal, P.S., and Boore, J.L. (2005). Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3.

  • Douard, V., Brunet, F., Boussau, B., Ahrens-Fath, I., Vlaeminck-Guillem, V., Haendler, B., Laudet, V., and Guiguen, Y. (2008). The fate of the duplicated androgen receptor in fishes: a late neofunctionalization event? BMC Evol Biol 8, 336.

    PubMed  PubMed Central  Google Scholar 

  • Fago, A., Forest, E., and Weber, R.E. (2001). Hemoglobin and subunit multiplicity in the rainbow trout (Oncorhynchus mykiss) hemoglobin system. Fish Physiol Biochem 24, 335–342.

    CAS  Google Scholar 

  • Feng, J., Liu, S., Wang, X., Wang, R., Zhang, J., Jiang, Y., Li, C., Kaltenboeck, L., Li, J., and Liu, Z. (2014). Channel catfish hemoglobin genes: identification, phylogenetic and syntenic analysis, and specific induction in response to heat stress. Comp Biochem Physiol Part D Genomics Proteomics 9, 11–22.

    CAS  PubMed  Google Scholar 

  • Flajnik, M.F., and Kasahara, M. (2010). Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 11, 47–59.

    CAS  PubMed  Google Scholar 

  • Giles, M.A., and Vanstone, W.E. (1976). Ontogenetic variation in the multiple hemoglobins of coho salmon (Oncorhynchus kisutch) and effect of environmental factors on their expression. J Fish Res Bd Can 33, 1144–1149.

    CAS  Google Scholar 

  • Giordano, D., Russo, R., Coppola, D., di Prisco, G., and Verde, C. (2010). Molecular adaptations in haemoglobins of notothenioid fishes. J Fish Biol 76, 301–318.

    CAS  PubMed  Google Scholar 

  • Glasauer, S.M.K., and Neuhauss, S.C.F. (2014). Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol Genet Genomics 289, 1045–1060.

    CAS  PubMed  Google Scholar 

  • Goodman, M., Czelusniak, J., Koop, B.F., Tagle, D.A., and Slightom, J.L. (1987). Globins: a case study in molecular phylogeny. Cold Spring Harbor Symp Quant Biol 52, 875–890.

    CAS  PubMed  Google Scholar 

  • Goodman, M., Moore, G.W., and Matsuda, G. (1975). Darwinian evolution in the genealogy of haemoglobin. Nature 253, 603–608.

    CAS  PubMed  Google Scholar 

  • Gribaldo, S., Casane, D., Lopez, P., and Philippe, H. (2003). Functional divergence prediction from evolutionary analysis: a case study of vertebrate hemoglobin. Mol Biol Evol 20, 1754–1759.

    CAS  PubMed  Google Scholar 

  • Grispo, M.T., Natarajan, C., Projecto-Garcia, J., Moriyama, H., Weber, R. E., and Storz, J.F. (2012). Gene duplication and the evolution of hemoglobin isoform differentiation in birds. J Biol Chem 287, 37647–37658.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gu, X., Wang, Y., and Gu, J. (2002). Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat Genet 31, 205–209.

    CAS  PubMed  Google Scholar 

  • Hardison, R.C. (2001). Organisation, evolution and regulation of the globin genes. In: Steinberg, M.H., Forget, B.G., Higgs, D.R., and Nagel, R.L., eds. Disorders of Hemoglobin: Genetics, Pathophysiology, and Clinical Management. Cambridge: Cambridge University Press. 95–115.

    Google Scholar 

  • Hardison, R.C. (2012). Evolution ofhemoglobin and its genes. Cold Spring Harbor Perspect Med 2, a011627.

    Google Scholar 

  • Henkel, C.V., Burgerhout, E., De Wijze, D.L., Dirks, R.P., Minegishi, Y., Jansen, H.J., Spaink, H.P., Dufour, S., Weltzien, F., Tsukamoto, K., etal. (2012). Primitive duplicate hox clusters in the European Eel’s genome. PLoS One 7, 32231.

    Google Scholar 

  • Hirano, M., Das, S., Guo, P., and Cooper, M.D., (2011). The evolution of adaptive immunity in vertebrates. Adv Immunal 109, 125–157.

    CAS  Google Scholar 

  • Hoffmann, F.G., Opazo, J.C., and Storz, J.F. (2012). Whole-genome duplications spurred the functional diversification of the globin gene superfamily in vertebrates. Mol Biol Evol 29, 303–312.

    CAS  PubMed  Google Scholar 

  • Hoffmann, F.G., and Storz, J.F. (2007). The αD-globin gene originated via duplication of an embryonic α-like globin gene in the ancestor of tetrapod vertebrates. Mol Biol Evol 24, 1982–1990.

    CAS  PubMed  Google Scholar 

  • Hoffmann, F.G., Storz, J.F., Gorr, T.A., and Opazo, J.C. (2010). Lineage-specific patterns of functional diversification in thea- and β-globin gene families of tetrapod vertebrates. Mol Biol Evol 27, 1126–1138.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann, F.G., Vandewege, M.W., Storz, J.F., and Opazo, J.C. (2018). Gene turnover and diversification of the α- and β-globin gene families in sauropsid vertebrates. Genome Biol Evol 10, 344–358.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holland, P.W., Garcia-Fernàndez, J., Williams, N.A., and Sidow, A. (1994). Gene duplications and the origins of vertebrate development. Development 1994, 125–133.

    Google Scholar 

  • Huminiecki, L., and Conant, G.C. (2012). Polyploidy and the evolution of complex traits. Int J Evol Biol 2012, 1–12.

    Google Scholar 

  • Hurley, I.A., Mueller, R.L., Dunn, K.A., Schmidt, E.J., Friedman, M., Ho, R.K., Prince, V.E., Yang, Z., Thomas, M.G., and Coates, M.I. (2007). A new time-scale for ray-finned fish evolution. Proc R Soc B 274, 489–498.

    CAS  PubMed  Google Scholar 

  • Iuchi, I., Suzuki, R., and Yamagami, K. (1975). Ontogenetic expression of larval and adult hemoglobin phenotypes in the intergeneric salmonid hybrids. J Exp Zool 192, 57–64.

    CAS  PubMed  Google Scholar 

  • Jaillon, O., Aury, J.M., Brunet, F., Petit, J.L., Stange-Thomann, N., Mauceli, E., Bouneau, L., Fischer, C., Ozouf-Costaz, C., Bernot, A., et al. (2004). Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431, 946–957.

    PubMed  Google Scholar 

  • Katoh, K., and Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30, 772–780.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, D., Langmead, B., and Salzberg, S.L. (2015). HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12, 357–360.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T., and Calcott, B. (2017). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34, 772–773.

    CAS  PubMed  Google Scholar 

  • Lanfranchi, G., Pallavicini, A., Laveder, P., and Valle, G. (1994). Ancestral hemoglobin switching in lampreys. Dev Biol 164, 402–408.

    CAS  PubMed  Google Scholar 

  • Lassmann, T., and Sonnhammer, E.L. (2005). Automatic assessment of alignment quality. Nucleic Acids Res 33, 7120–7128.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., and Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079.

    PubMed  PubMed Central  Google Scholar 

  • Lien, S., Koop, B.F., Sandve, S.R., Miller, J.R., Kent, M.P., Nome, T., Hvidsten, T.R., Leong, J.S., Minkley, D.R., Zimin, A., et al. (2016). The Atlantic salmon genome provides insights into rediploidization. Nature 533, 200–205.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, H.P., **ao, S.J., Wu, N., Wang, D., Liu, Y.C., Zhou, C.W., Liu, Q.Y., Yang, R.B., Jiang, W.K., Liang, Q.Q., et al. (2019). The sequence and de novo assembly of Oxygymnocypris stewartii genome. Sci Data 6, 190009.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Macqueen, D.J., and Johnston, I.A. (2014). Awell-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc R Soc B 281, 20132881.

    PubMed  PubMed Central  Google Scholar 

  • Makova, K.D., and Li, W.H. (2003). Divergence in the spatial pattern of gene expression between human duplicate genes. Genome Res 13, 1638–1645.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marlétaz, F., Firbas, P.N., Maeso, I., Tena, J.J., Bogdanovic, O., Perry, M., Wyatt, C.D.R., de la Calle-Mustienes, E., Bertrand, S., Burguera, D., et al. (2018). Amphioxus functional genomics and the origins ofvertebrate gene regulation. Nature 564, 64–70.

    PubMed  PubMed Central  Google Scholar 

  • Meyer, A., and Van de Peer, Y. (2005). From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27, 937–945.

    CAS  PubMed  Google Scholar 

  • Nakamura, Y., Yasuike, M., Mekuchi, M., Iwasaki, Y., Ojima, N., Fujiwara, A., Chow, S., and Saitoh, K. (2017). Rhodopsin gene copies in Japanese eel originated in a teleost-specific genome duplication. Zool Lett 3, 18.

    Google Scholar 

  • Near, T.J., Parker, S.K., and Detrich III, H.W. (2006). A genomic fossil reveals key steps in hemoglobin loss by the Antarctic icefishes. Mol Biol Evol 23, 2008–2016.

    CAS  PubMed  Google Scholar 

  • Ocampo Daza, D. (2013). Evolution of vertebrate endocrine and neuronal gene families: focus on pituitary and retina. Dissertation for Doctoral Degree. Uppsala: Uppsala University.

    Google Scholar 

  • Opazo, J.C., Butts, G.T., Nery, M.F., Storz, J.F., and Hoffmann, F.G. (2013). Whole-genome duplication and the functional diversification of teleost fish hemoglobins. Mol Biol Evol 30, 140–153.

    CAS  PubMed  Google Scholar 

  • Opazo, J.C., Hoffmann, F.G., Natarajan, C., Witt, C.C., Berenbrink, M., and Storz, J.F. (2015). Gene turnover in the avian globin gene families and evolutionary changes in hemoglobin isoform expression. Mol Biol Evol 32, 871–887.

    CAS  PubMed  Google Scholar 

  • Otto, S.P. (2007). The evolutionary consequences of polyploidy. Cell 131, 452–462.

    CAS  PubMed  Google Scholar 

  • Pan, Y.K., Ern, R., Morrison, P.R., Brauner, C.J., and Esbaugh, A.J. (2017). Acclimation to prolonged hypoxia alters hemoglobin isoform expression and increases hemoglobin oxygen affinity and aerobic performance in a marine fish. Sci Rep 7, 7834.

    PubMed  PubMed Central  Google Scholar 

  • Pebusque, M.J., Coulier, F., Birnbaum, D., and Pontarotti, P. (1998). Ancient large-scale genome duplications: phylogenetic and linkage analyses shed light on chordate genome evolution. Mol Biol Evol 15, 1145–1159.

    CAS  PubMed  Google Scholar 

  • Pertea, M., Pertea, G.M., Antonescu, C.M., Chang, T.C., Mendell, J.T., and Salzberg, S.L. (2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33, 290–295.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Piekarski, N., Gross, J.B., and Hanken, J. (2014). Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull. Nat Commun 5, 5661.

    CAS  PubMed  Google Scholar 

  • Prince, V.E., and Pickett, F.B. (2002). Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3, 827–837.

    CAS  PubMed  Google Scholar 

  • Quinn, N.L., Boroevich, K.A., Lubieniecki, K.P., Chow, W., Davidson, E. A., Phillips, R.B., Koop, B.F., and Davidson, W.S. (2010). Genomic organization and evolution of the Atlantic salmon hemoglobin repertoire. BMC Genomics 11, 539.

    PubMed  PubMed Central  Google Scholar 

  • Randall, D.J., Rummer, J.L., Wilson, J.M., Wang, S., and Brauner, C.J. (2014). A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes. J Exp Biol 217, 1205–1214.

    CAS  PubMed  Google Scholar 

  • Roesner, A., Hankeln, T., and Burmester, T. (2006). Hypoxia induces a complex response of globin expression in zebrafish (Danio rerio). J Exp Biol 209, 2129–2137.

    CAS  PubMed  Google Scholar 

  • Ronquist, F., and Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.

    CAS  PubMed  Google Scholar 

  • Rutjes, H.A., Nieveen, M.C., Weber, R.E., Witte, F., and Van den Thillart, G.E.E.J.M. (2007). Multiple strategies of Lake Victoria cichlids to cope with lifelong hypoxia include hemoglobin switching. Am J Physiol Regul Integr Comp Physiol 293, R1376–R1383.

    CAS  PubMed  Google Scholar 

  • Sandve, S.R., Rohlfs, R.V., and Hvidsten, T.R. (2018). Subfunctionalization versus neofunctionalization after whole-genome duplication. Nat Genet 50, 908–909.

    CAS  PubMed  Google Scholar 

  • Sato, Y., Hashiguchi, Y., and Nishida, M. (2009). Temporal pattern of loss/persistence of duplicate genes involved in signal transduction and metabolic pathways after teleost-specific genome duplication. BMC Evol Biol 9, 127.

    PubMed  PubMed Central  Google Scholar 

  • Shimeld, S.M., and Holland, P.W.H. (2000). Vertebrate innovations. Proc Natl Acad Sci USA 97, 4449–4452.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Solovyev, V., Kosarev, P., Seledsov, I., and Vorobyev, D. (2006). Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7, S10.

    PubMed  PubMed Central  Google Scholar 

  • Song, X., Wang, Y., and Tang, Y. (2013). Rapid diversification of FoxP2 in teleosts through gene duplication in the teleost-specific whole genome duplication event. PLoS ONE 8, e83858.

    PubMed  PubMed Central  Google Scholar 

  • Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Storz, J.F. (2016). Gene duplication and evolutionary innovations in hemoglobin-oxygen transport. Physiology 31, 223–232.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Storz, J.F., Natarajan, C., Grouleff, M.K., Vandewege, M., Hoffmann, F.G., You, X., Venkatesh, B., and Fago, A. (2020). Oxygenation properties of hemoglobin and the evolutionary origins of isoform multiplicity in an amphibious air-breathing fish, the blue-spotted mudskipper (Boleophthalmus pectinirostris). J Exp Biol 223, jeb217307.

    PubMed  PubMed Central  Google Scholar 

  • Storz, J.F., Opazo, J.C., and Hoffmann, F.G. (2011). Phylogenetic diversification of the globin gene superfamily in chordates. IUBMB Life 63, 313–322.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Storz, J.F., Opazo, J.C., and Hoffmann, F.G. (2013). Gene duplication, genome duplication, and the functional diversification of vertebrate globins. Mol Phylogenet Evol 66, 469–478.

    CAS  PubMed  Google Scholar 

  • Tiedke, J., Gerlach, F., Mitz, S.A., Hankeln, T., and Burmester, T. (2011). Ontogeny of globin expression in zebrafish (Danio rerio). J Comp Physiol B 181, 1011–1021.

    CAS  PubMed  Google Scholar 

  • Van de Peer, Y., Maere, S., and Meyer, A. (2009). The evolutionary significance of ancient genome duplications. Nat Rev Genet 10, 725–732.

    CAS  PubMed  Google Scholar 

  • Van de Peer, Y., Mizrachi, E., and Marchal, K. (2017). The evolutionary significance of polyploidy. Nat Rev Genet 18, 411–424.

    CAS  PubMed  Google Scholar 

  • Wada, H. (2001). Origin and evolution of the neural crest: a hypothetical reconstruction of its evolutionary history. Dev Growth Differ 43, 509–520.

    CAS  PubMed  Google Scholar 

  • Wada, H., and Makabe, K. (2006). Genome duplications of early vertebrates as a possible chronicle of the evolutionary history of the neural crest. Int J Biol Sci 2, 133–141.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, J.T., Li, J.T., Zhang, X.F., and Sun, X.W. (2012). Transcriptome analysis reveals the time of the fourth round of genome duplication in common carp (Cyprinus carpio). BMC Genomics 13, 96.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, X., Gan, X., Li, J., Chen, Y., and He, S. (2016). Cyprininae phylogeny revealed independent origins of the Tibetan Plateau endemic polyploid cyprinids and their diversifications related to the Neogene uplift of the plateau. Sci China Life Sci 59, 1149–1165.

    PubMed  Google Scholar 

  • Weber, R.E. (2000). Adaptations for oxygen transport: lessons from fish hemoglobins. In: Di Prisco, G., Giardina, B., and Weber, R.E., eds. Hemoglobin Function in Vertebrates: Molecular Adaptation in Extreme and Temperate Environments. New York: Springer. 23–37.

    Google Scholar 

  • Weber, R.E., Fago, A., Malte, H., Storz, J.F., and Gorr, T.A. (2013). Lack of conventional oxygen-linked proton and anion binding sites does not impair allosteric regulation of oxygen binding in dwarf caiman hemoglobin. Am J Physiol Regul Integr Comp Physiol 305, R300–R312.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weber, R.E., and White, F.N. (1994). Chloride-dependent organic phosphate sensitivity of the oxygenation reaction in crocodilian hemoglobins. J Exp Biol 192, 1–11.

    CAS  PubMed  Google Scholar 

  • Wells, P.R., and Pinder, A.W. (1996). The respiratory development of Atlantic salmon. II. Partitioning of oxygen uptake among gills, yolk sac and body surfaces. J Exp Biol 199, 2737–2744.

    CAS  PubMed  Google Scholar 

  • Wells, R.M., (2009). Blood-gas transport and hemoglobin function: adaptations for functional and environmental hypoxia. In: Richards, J.G., Farrell, A.P., and Brauner, C.J., eds. Fish Physiology. New York: Elsevier. 255–299.

    Google Scholar 

  • Wheeler, D., Hope, R.M., Cooper, S.J.B., Gooley, A.A., and Holland, R.A.B. (2004). Linkage of the β-like ω-globin gene to a-like globin genes in an Australian marsupial supports the chromosome duplication model for separation of globin gene clusters. J Mol Evol 58, 642–652.

    CAS  PubMed  Google Scholar 

  • Wolf, U., Ritter, H., Atkin, N.B., and Ohno, S. (1969). Polyploidization in the fish family Cyprinidae, order Cypriniformes. Hum Genet 7, 240–244.

    CAS  Google Scholar 

  • **a, M., Chao, Y., Jia, J., Li, C., Kong, Q., Zhao, Y., Guo, S., and Qi, D. (2016). Changes of hemoglobin expression in response to hypoxia in a Tibetan schizothoracine fish, Schizopygopsis pylzovi. J Comp Physiol B 186, 1033–1043.

    CAS  PubMed  Google Scholar 

  • Xu, P., Xu, J., Liu, G., Chen, L., Zhou, Z., Peng, W., Jiang, Y., Zhao, Z., Jia, Z., Sun, Y., et al. (2019). The allotetraploid origin and asymmetrical genome evolution of the common carp Cyprinus carpio. Nat Commun 10, 4625.

    PubMed  PubMed Central  Google Scholar 

  • Zhu, X., Guan, Y., Signore, A.V., Natarajan, C., DuBay, S.G., Cheng, Y., Han, N., Song, G., Qu, Y., Moriyama, H., et al. (2018). Divergent and parallel routes ofbiochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau. Proc Natl Acad Sci USA 115, 1865–1870.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmer, E.A., Martin, S.L., Beverley, S.M., Kan, Y.W., and Wilson, A.C. (1980). Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. Proc Natl Acad Sci USA 77, 2158–2162.

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31972866), the Strategic Priority Research Program (XDB31000000). The research was supported by the Wuhan Branch, Supercomputing Center, Chinese Academy of Sciences, China. We thank Yu Zhou for revising the manuscript.

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Authors and Affiliations

  1. The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Yi Lei, Liandong Yang, Haifeng Jiang, Juan Chen, Ning Sun, Wenqi Lv & Shun** He

  2. University of Chinese Academy of Sciences, Bei**g, 100049, China

    Yi Lei, Liandong Yang, Haifeng Jiang, Juan Chen, Ning Sun & Wenqi Lv

  3. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China

    Shun** He

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  1. Yi Lei
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  2. Liandong Yang
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  3. Haifeng Jiang
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  4. Juan Chen
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  5. Ning Sun
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  6. Wenqi Lv
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  7. Shun** He
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Correspondence to Shun** He.

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Lei, Y., Yang, L., Jiang, H. et al. Recent genome duplications facilitate the phenotypic diversity of Hb repertoire in the Cyprinidae. Sci. China Life Sci. 64, 1149–1164 (2021). https://doi.org/10.1007/s11427-020-1809-0

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  • DOI: https://doi.org/10.1007/s11427-020-1809-0

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