Ancient Duplications and Expression Divergence in the Globin Gene Superfamily of Vertebrates: Insights from the Elephant Shark Genome and Transcriptome.
Comparative analyses of vertebrate genomes continue to uncover a surprising diversity of genes in the globin gene superfamily, some of which have very restricted phyletic distributions despite their antiquity. Genomic analysis of the globin gene repertoire of cartilaginous fish (Chondrichthyes) should be especially informative about the duplicative origins and ancestral functions of vertebrate globins, as divergence between Chondrichthyes and bony vertebrates represents the most basal split within the jawed vertebrates. Here, we report a comparative genomic analysis of the vertebrate globin gene family that includes the complete globin gene repertoire of the elephant shark (Callorhinchus milii). Using genomic sequence data from representatives of all major vertebrate classes, integrated analyses of conserved synteny and phylogenetic relationships revealed that the last common ancestor of vertebrates possessed a repertoire of at least seven globin genes: single copies of androglobin and neuroglobin, four paralogous copies of globin X, and the single-copy progenitor of the entire set of vertebrate-specific globins. Combined with expression data, the genomic inventory of elephant shark globins yielded four especially surprising findings: 1) there is no trace of the neuroglobin gene (a highly conserved gene that is present in all other jawed vertebrates that have been examined to date), 2) myoglobin is highly expressed in heart, but not in skeletal muscle (reflecting a possible ancestral condition in vertebrates with single-circuit circulatory systems), 3) elephant shark possesses two highly divergent globin X paralogs, one of which is preferentially expressed in gonads, and 4) elephant shark possesses two structurally distinct α-globin paralogs, one of which is preferentially expressed in the brain. Expression profiles of elephant shark globin genes reveal distinct specializations of function relative to orthologs in bony vertebrates and suggest hypotheses about ancestral functions of vertebrate globins.
Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile jopazo@gmail.com mcbbv@imcb.a-star.edu.sg jstorz2@unl.edu.
Juan C
JC
Opazo
Institute of Molecular and Cell Biology, Comparative and Medical Genomics Laboratory, Agency for Science, Technology, and Research Biopolis, Singapore jopazo@gmail.com mcbbv@imcb.a-star.edu.sg jstorz2@unl.edu.
Alison P
AP
Lee
Department of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State University Institute for Genomics, Biocomputing, and Biotechnology, Mississippi State University jopazo@gmail.com mcbbv@imcb.a-star.edu.sg jstorz2@unl.edu.
Federico G
FG
Hoffmann
Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.
Jessica
J
Toloza-Villalobos
Institute of Zoology, University of Hamburg, Hamburg, Germany.
Thorsten
T
Burmester
Institute of Molecular and Cell Biology, Comparative and Medical Genomics Laboratory, Agency for Science, Technology, and Research Biopolis, Singapore Departments of Paediatrics, Yong Loo Lin School of Medicine, National University of Singapore, Singapore jopazo@gmail.com mcbbv@imcb.a-star.edu.sg jstorz2@unl.edu.
Byrappa
B
Venkatesh
School of Biological Sciences, University of Nebraska, Lincoln jopazo@gmail.com mcbbv@imcb.a-star.edu.sg jstorz2@unl.edu.
Jay F
JF
Storz
D000818:Animals; D001499:Bayes Theorem; D019143:Evolution, Molecular; D020440:Gene Duplication; D020869:Gene Expression Profiling; D005786:Gene Expression Regulation; D016678:Genome; D005914:Globins / Q000235:genetics; D005810:Multigene Family; D009928:Organ Specificity / Q000235:genetics; D010802:Phylogeny; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D012754:Sharks / Q000235:genetics*; D026801:Synteny; D059467:Transcriptome / Q000235:genetics*; D014714:Vertebrates / Q000235:genetics*
D012333:RNA, Messenger; D005914:Globins
Chondrichthyes; gene duplication; gene family evolution; globin; myoglobin; neuroglobin