Abstract
The haemoglobin protein, required for oxygen transportation in the body, is encoded by α- and β-globin genes that are arranged in clusters. The transpositional model for the evolution of distinct α-globin and β-globin clusters in amniotes is much simpler than the previously proposed whole genome duplication model. According to this model, all jawed vertebrates share one ancient region containing α- and β-globin genes and several flanking genes in the order MPG-C16orf35-(α-β)-GBY-LUC7L that has been conserved for more than 410 million years, whereas amniotes evolved a distinct β-globin cluster by insertion of a transposed β-globin gene from this ancient region into a cluster of olfactory receptors flanked by CCKBR and RRM1. It could not be determined whether this organisation is conserved in all amniotes because of the paucity of information from non-avian reptiles. To fill in this gap, we examined globin gene organisation in a squamate reptile, the Australian bearded dragon lizard, Pogona vitticeps (Agamidae). We report here that the α-globin cluster (HBK, HBA) is flanked by C16orf35 and GBY and is located on a pair of microchromosomes, whereas the β-globin cluster is flanked by RRM1 on the 3′ end and is located on the long arm of chromosome 3. However, the CCKBR gene that flanks the β-globin cluster on the 5′ end in other amniotes is located on the short arm of chromosome 5 in P. vitticeps, indicating that a chromosomal break between the β-globin cluster and CCKBR occurred at least in the agamid lineage. Our data from a reptile species provide further evidence to support the transpositional model for the evolution of β-globin gene cluster in amniotes.
Similar content being viewed by others
Abbreviations
- α:
-
Cluster of α-like globin genes
- β:
-
Cluster of β-like globin genes
- BAC:
-
Bacterial artificial chromosome
- Blastn:
-
Basic local alignment search tool nucleotide
- Blastp:
-
Basic local alignment search tool protein
- BLAT:
-
Blast-like alignment tool
- bp:
-
Base pairs
- C16orf35 :
-
Chromosome 16 open read frame 35
- CCKBR :
-
Cholecystokinin B receptor
- dUTP:
-
2′-Deoxyuridine 5′-triphosphate
- FISH:
-
Fluorescence in situ hybridisation
- FTSJ1 :
-
FtsJ homolog 1 (E. coli)
- GBY :
-
Globin Y
- HBA :
-
αA-Globin gene
- HBA-T3 :
-
αA-Globin gene subunit 3
- HBB :
-
β-Globin gene
- HBE :
-
ε-Globin gene
- HBK :
-
αD- Or μ- Globin gene
- HBP :
-
π-Globin gene
- HBQ :
-
θ-Globin gene
- HBW :
-
ω-Globin gene
- HBZ :
-
ζ-Globin gene
- kb:
-
Kilobase
- MPG :
-
N-methylpurine-DNA glycosylase
- MY:
-
Million years
- MYA:
-
Million years ago
- NS:
-
No sequences
- nr/nt:
-
Non-redundant nucleotide
- ORs :
-
Cluster of olfactory receptor genes
- overgo:
-
Overlapping oligonucleotides
- LUC7L :
-
LUC7-like
- RPS11 :
-
Ribosomal protein S11
- RRM1 :
-
Ribonucleotide reductase M1
References
Aguileta G, Bielawski JP, Yang Z (2006) Evolutionary rate variation among vertebrate beta globin genes: implications for dating gene family duplication events. Gene 380:21–29
Bulger M, van Doorninck JH, Saitoh N et al (1999) Conservation of sequence and structure flanking the mouse and human beta-globin loci: the beta-globin genes are embedded within an array of odorant receptor genes. Proc Natl Acad Sci USA 96:5129–5134
Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94
Burmester T, Ebner B, Weich B et al (2002) Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol Biol Evol 19:416–421
Chan FY, Robinson J, Brownlie A et al (1997) Characterization of adult alpha- and beta-globin genes in the zebrafish. Blood 89:688–700
Cooper SJ, Wheeler D, De Leo A et al (2006) The mammalian alphaD-globin gene lineage and a new model for the molecular evolution of alpha-globin gene clusters at the stem of the mammalian radiation. Mol Phylogenet Evol 38:439–448
Czelusniak J, Goodman M, Hewett-Emmett D et al (1982) Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes. Nature 298:297–300
De Leo AA, Wheeler D, Lefevre C et al (2005) Sequencing and mapping hemoglobin gene clusters in the Australian model dasyurid marsupial Sminthopsis macroura. Cytogenet Genome Res 108:333–341
Deakin JE, Koina E, Waters PD et al (2008) Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals. Chromosome Res 16:1159–1175
Ezaz T, Quinn AE, Miura I et al (2005) The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Res 13:763–776
Ezaz T, Moritz B, Waters P et al (2009) The ZW sex microchromosomes of an Australian dragon lizard share no homology with those of other reptiles or birds. Chromosome Res 17:965–973
Flint J, Tufarelli C, Peden J et al (2001) Comparative genome analysis delimits a chromosomal domain and identifies key regulatory elements in the alpha globin cluster. Hum Mol Genet 10:371–382
Fuchs C, Burmester T, Hankeln T (2006) The amphibian globin gene repertoire as revealed by the Xenopus genome. Cytogenet Genome Res 112:296–306
Gillemans N, McMorrow T, Tewari R et al (2003) Functional and comparative analysis of globin loci in pufferfish and humans. Blood 101:2842–2849
Goodman M, Moore GW, Matsuda G (1975) Darwinian evolution in the genealogy of haemoglobin. Nature 253:603–608
Goodman M, Czelusniak J, Koop BF et al (1987) Globins: a case study in molecular phylogeny. Cold Spring Harb Symp Quant Biol 52:875–890
Gorr TA, Mable BK, Kleinschmidt T (1998) Phylogenetic analysis of reptilian hemoglobins: trees, rates, and divergences. J Mol Evol 47:471–485
Hardison RC (2001) New views of evolution and regulation of vertebrate beta-like globin gene clusters from an orphaned gene in marsupials. Proc Natl Acad Sci USA 98:1327–1329
Hardison RC (2005) Globin genes: evolution. Encylcopedia of life sciences. Wiley, Chichester. doi:10.1038/npg.els.0005134, http://www.els.net/
Hardison RC (2008) Globin genes on the move. J Biol 7:35
Hedges SB, Vidal N (2009) Lizards, snakes, and amphisbaenians (Squamata). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, pp 383–389
Hoffmann FG, Storz JF (2007) The {alpha}D-globin gene originated via duplication of an embryonic {alpha}-like globin gene in the ancestor of tetrapod vertebrates. Mol Biol Evol 24:1982–1990
Hoffmann FG, Opazo JC, Storz JF (2008) Rapid rates of lineage-specific gene duplication and deletion in the alpha-globin gene family. Mol Biol Evol 25:591–602
Hoffmann FG, Opazo JC, Storz JF (2010a) Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates. Proc Natl Acad Sci USA 107:14274–14279
Hoffmann FG, Storz JF, Gorr TA et al (2010b) Lineage-specific patterns of functional diversification in the {alpha}- and {beta}-globin gene families of tetrapod vertebrates. Mol Biol Evol 27:1126–1138
Holland RA, Gooley AA 2nd (1997) Characterization of the embryonic globin chains of the marsupial Tammar Wallaby, Macropus eugenii. Eur J Biochem 248:864–871
Holland RA, Gooley AA, Hope RM (1998) Embryonic globins of the marsupial the Tammar Wallaby (Macropus eugenii): bird like and mammal like. Clin Exp Pharmacol Physiol 25:740–744
Hosbach HA, Wyler T, Weber R (1983) The Xenopus laevis globin gene family: chromosomal arrangement and gene structure. Cell 32:45–53
Hughes JR, Cheng JF, Ventress N et al (2005) Annotation of cis-regulatory elements by identification, subclassification, and functional assessment of multispecies conserved sequences. Proc Natl Acad Sci USA 102:9830–9835
Jeffreys AJ, Wilson V, Wood D et al (1980) Linkage of adult alpha- and beta-globin genes in X. laevis and gene duplication by tetraploidization. Cell 21:555–564
Opazo JC, Hoffmann FG, Storz JF (2008) Genomic evidence for independent origins of beta-like globin genes in monotremes and therian mammals. Proc Natl Acad Sci USA 105:1590–1595
Opazo JC, Sloan AM, Campbell KL et al (2009) Origin and ascendancy of a chimeric fusion gene: the beta/delta-globin gene of paenungulate mammals. Mol Biol Evol 26:1469–1478
Patel VS, Cooper SJ, Deakin JE et al (2008) Platypus globin genes and flanking loci suggest a new insertional model for beta-globin evolution in birds and mammals. BMC Biol 6:34
Pisano E, Cocca E, Mazzei F et al (2003) Mapping of alpha- and beta-globin genes on Antarctic fish chromosomes by fluorescence in-situ hybridization. Chromosome Res 11:633–640
Washington University Genome Sequencing Center (2010) Internet reference. Retrieved from http://genome.wustl.edu/tools/software/overgo.cgi Accessed 15 April 2010
Wheeler D, Hope R, Cooper SB et al (2001) An orphaned mammalian beta-globin gene of ancient evolutionary origin. Proc Natl Acad Sci USA 98:1101–1106
Wheeler D, Hope RM, Cooper SJ et al (2004) Linkage of the beta-like omega-globin gene to alpha-like globin genes in an Australian marsupial supports the chromosome duplication model for separation of globin gene clusters. J Mol Evol 58:642–652
Yeh RF, Lim LP, Burge CB (2001) Computational inference of homologous gene structures in the human genome. Genome Res 11:803–816
Acknowledgements
This study was partially supported by an Australian Research Council Discovery grant (ARC DP0881196) awarded to Stephen Sarre, Arthur Georges and Scott Edwards, and a block grant from the Research School of Biology at the Australian National University (ANU). VSP is supported by ANU PhD Gradate School Scholarship.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Wendy Bickmore.
Rights and permissions
About this article
Cite this article
Patel, V.S., Ezaz, T., Deakin, J.E. et al. Globin gene structure in a reptile supports the transpositional model for amniote α- and β-globin gene evolution. Chromosome Res 18, 897–907 (2010). https://doi.org/10.1007/s10577-010-9164-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-010-9164-5