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Globin gene structure in a reptile supports the transpositional model for amniote α- and β-globin gene evolution

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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.

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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

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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.

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Authors and Affiliations

  1. Research School of Biology, The Australian National University, Canberra, ACT, 0200, Australia

    Vidushi S. Patel, Janine E. Deakin & Jennifer A. Marshall Graves

  2. Institute for Applied Ecology, University of Canberra, Bruce, ACT, 2616, Australia

    Tariq Ezaz

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  1. Vidushi S. Patel
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  2. Tariq Ezaz
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  3. Janine E. Deakin
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  4. Jennifer A. Marshall Graves
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Correspondence to Vidushi S. Patel.

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Responsible Editor: Wendy Bickmore.

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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

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  • DOI: https://doi.org/10.1007/s10577-010-9164-5

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