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Mol Biol Evol. 2014 Oct;31(10):2708-21. doi: 10.1093/molbev/msu216. Epub 2014 Jul 23.

The globin gene repertoire of lampreys: convergent evolution of hemoglobin and myoglobin in jawed and jawless vertebrates.

Author information

1
Institute of Zoology and Zoological Museum, University of Hamburg, Hamburg, Germany.
2
Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada.
3
Institute of Molecular Genetics, Johannes Gutenberg University of Mainz, Mainz, Germany.
4
School of Biological Sciences, University of Nebraska, Lincoln.
5
Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University.
6
Institute of Zoology and Zoological Museum, University of Hamburg, Hamburg, Germany thorsten.burmester@uni-hamburg.de.

Abstract

Agnathans (jawless vertebrates) occupy a key phylogenetic position for illuminating the evolution of vertebrate anatomy and physiology. Evaluation of the agnathan globin gene repertoire can thus aid efforts to reconstruct the origin and evolution of the globin genes of vertebrates, a superfamily that includes the well-known model proteins hemoglobin and myoglobin. Here, we report a comprehensive analysis of the genome of the sea lamprey (Petromyzon marinus) which revealed 23 intact globin genes and two hemoglobin pseudogenes. Analyses of the genome of the Arctic lamprey (Lethenteron camtschaticum) identified 18 full length and five partial globin gene sequences. The majority of the globin genes in both lamprey species correspond to the known agnathan hemoglobins. Both genomes harbor two copies of globin X, an ancient globin gene that has a broad phylogenetic distribution in the animal kingdom. Surprisingly, we found no evidence for an ortholog of neuroglobin in the lamprey genomes. Expression and phylogenetic analyses identified an ortholog of cytoglobin in the lampreys; in fact, our results indicate that cytoglobin is the only orthologous vertebrate-specific globin that has been retained in both gnathostomes and agnathans. Notably, we also found two globins that are highly expressed in the heart of P. marinus, thus representing functional myoglobins. Both genes have orthologs in L. camtschaticum. Phylogenetic analyses indicate that these heart-expressed globins are not orthologous to the myoglobins of jawed vertebrates (Gnathostomata), but originated independently within the agnathans. The agnathan myoglobin and hemoglobin proteins form a monophyletic group to the exclusion of functionally analogous myoglobins and hemoglobins of gnathostomes, indicating that specialized respiratory proteins for O2 transport in the blood and O2 storage in the striated muscles evolved independently in both lineages. This dual convergence of O2-transport and O2-storage proteins in agnathans and gnathostomes involved the convergent co-option of different precursor proteins in the ancestral globin repertoire of vertebrates.

KEYWORDS:

Agnatha; convergent evolution; cytoglobin; gene duplication; hemoglobin; myoglobin

PMID:
25061084
PMCID:
PMC4166926
DOI:
10.1093/molbev/msu216
[Indexed for MEDLINE]
Free PMC Article

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