Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Evolution of the globin gene family in deuterostomes: lineage-specific patterns of diversification and attrition.
Hoffmann FG
,
Opazo JC
,
Hoogewijs D
,
Hankeln T
,
Ebner B
,
Vinogradov SN
,
Bailly X
,
Storz JF
.
???displayArticle.abstract???
In the Metazoa, globin proteins display an underlying unity in tertiary structure that belies an extraordinary diversity in primary structures, biochemical properties, and physiological functions. Phylogenetic reconstructions can reveal which of these functions represent novel, lineage-specific innovations, and which represent ancestral functions that are shared with homologous globin proteins in other eukaryotes and even prokaryotes. To date, our understanding of globin diversity in deuterostomes has been hindered by a dearth of genomic sequence data from the Ambulacraria (echinoderms + hemichordates), the sister group of chordates, and the phylum Xenacoelomorpha, which includes xenoturbellids, acoelomorphs, and nemertodermatids. Here, we report the results of a phylogenetic and comparative genomic analysis of the globin gene repertoire of deuterostomes. We first characterized the globin genes of the acorn worm, Saccoglossus kowalevskii, a representative of the phylum Hemichordata. We then integrated genomic sequence data from the acorn worm into a comprehensive analysis of conserved synteny and phylogenetic relationships among globin genes from representatives of the eight lineages that comprise the superphylum Deuterostomia. The primary aims were 1) to unravel the evolutionary history of the globin gene superfamily in deuterostomes and 2) to use the estimated phylogeny to gain insights into the functional evolution of deuterostome globins. Results of our analyses indicate that the deuterostome common ancestor possessed a repertoire of at least four distinct globin paralogs and that different subsets of these ancestral genes have been retained in each of the descendant organismal lineages. In each major deuterostome group, a different subset of ancestral precursor genes underwent lineage-specific expansions of functional diversity through repeated rounds of gene duplication and divergence. By integrating results of the phylogenetic analysis with available functional data, we discovered that circulating oxygen-transport hemoglobins evolved independently in several deuterostome lineages and that intracellular nerve globins evolved independently in chordates and acoelomorph worms.
Altschul,
Basic local alignment search tool.
1990, Pubmed
Altschul,
Basic local alignment search tool.
1990,
Pubmed
Altschul,
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
1997,
Pubmed
Anderson,
SuiteMSA: visual tools for multiple sequence alignment comparison and molecular sequence simulation.
2011,
Pubmed
Baker,
Hemoglobin Structure and Function in the Rat-Tailed Sea Cucumber, Paracaudina chilensis.
1993,
Pubmed
,
Echinobase
Berenbrink,
Historical reconstructions of evolving physiological complexity: O2 secretion in the eye and swimbladder of fishes.
2007,
Pubmed
Berenbrink,
Evolution of oxygen secretion in fishes and the emergence of a complex physiological system.
2005,
Pubmed
Blank,
A membrane-bound vertebrate globin.
2011,
Pubmed
Bologna,
N-Terminal myristoylation predictions by ensembles of neural networks.
2004,
Pubmed
Bonaventura,
Functional consequences of ligand-linked dissociation in hemoglobin from the sea cucumber Molpadia arenicola.
1976,
Pubmed
,
Echinobase
Bourlat,
Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida.
2006,
Pubmed
,
Echinobase
Brittain,
Characterization of the changes in the state of aggregation induced by ligand binding in the hemoglobin system of a primitive vertebrate, the hagfish Eptatretus cirrhatus.
1986,
Pubmed
Burmester,
Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues.
2002,
Pubmed
Burmester,
What is the function of neuroglobin?
2009,
Pubmed
Burmester,
The hemoglobin genes of Drosophila.
2006,
Pubmed
Christensen,
Functional and biochemical properties of the hemoglobins of the burrowing brittle star Hemipholis elongata say (Echinodermata, Ophiuroidea).
2003,
Pubmed
,
Echinobase
Dewilde,
The nerve hemoglobin of the bivalve mollusc Spisula solidissima: molecular cloning, ligand binding studies, and phylogenetic analysis.
2006,
Pubmed
Dröge,
Phylogenetic analysis reveals wide distribution of globin X.
2011,
Pubmed
Ebner,
Globin genes are present in Ciona intestinalis.
2003,
Pubmed
Ebner,
The globin gene family of the cephalochordate amphioxus: implications for chordate globin evolution.
2010,
Pubmed
Edgar,
MUSCLE: multiple sequence alignment with high accuracy and high throughput.
2004,
Pubmed
Fago,
Hagfish hemoglobins: structure, function, and oxygen-linked association.
2001,
Pubmed
Fago,
Functional properties of neuroglobin and cytoglobin. Insights into the ancestral physiological roles of globins.
2004,
Pubmed
Fago,
The hemoglobin system of the hagfish Myxine glutinosa: aggregation state and functional properties.
1995,
Pubmed
Farazi,
The biology and enzymology of protein N-myristoylation.
2001,
Pubmed
Goodman,
Globins: a case study in molecular phylogeny.
1987,
Pubmed
Goodman,
Darwinian evolution in the genealogy of haemoglobin.
1975,
Pubmed
Hankeln,
Neuroglobin and cytoglobin in search of their role in the vertebrate globin family.
2005,
Pubmed
Hardison,
A brief history of hemoglobins: plant, animal, protist, and bacteria.
1996,
Pubmed
Hardison,
Hemoglobins from bacteria to man: evolution of different patterns of gene expression.
1998,
Pubmed
Hoffmann,
Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates.
2010,
Pubmed
Hoffmann,
Differential loss and retention of cytoglobin, myoglobin, and globin-E during the radiation of vertebrates.
2011,
Pubmed
Hoffmann,
Whole-genome duplications spurred the functional diversification of the globin gene superfamily in vertebrates.
2012,
Pubmed
Hoffmann,
Lineage-specific patterns of functional diversification in the alpha- and beta-globin gene families of tetrapod vertebrates.
2010,
Pubmed
Hoogewijs,
The Caenorhabditis globin gene family reveals extensive nematode-specific radiation and diversification.
2008,
Pubmed
Hoogewijs,
Androglobin: a chimeric globin in metazoans that is preferentially expressed in Mammalian testes.
2012,
Pubmed
Kakar,
Structure and reactivity of hexacoordinate hemoglobins.
2010,
Pubmed
Katoh,
Multiple alignment of DNA sequences with MAFFT.
2009,
Pubmed
Katoh,
Recent developments in the MAFFT multiple sequence alignment program.
2008,
Pubmed
Kitto,
Evolution of cooperativity in hemoglobins: what can invertebrate hemoglobins tell us?
NULL,
Pubmed
,
Echinobase
Lamy,
Giant Hexagonal Bilayer Hemoglobins.
1996,
Pubmed
Lassmann,
Kalign2: high-performance multiple alignment of protein and nucleotide sequences allowing external features.
2009,
Pubmed
Lassmann,
Automatic assessment of alignment quality.
2005,
Pubmed
Lassmann,
Kalign, Kalignvu and Mumsa: web servers for multiple sequence alignment.
2006,
Pubmed
Lecomte,
Structural divergence and distant relationships in proteins: evolution of the globins.
2005,
Pubmed
Lesk,
How different amino acid sequences determine similar protein structures: the structure and evolutionary dynamics of the globins.
1980,
Pubmed
Linder,
Palmitoylation: policing protein stability and traffic.
2007,
Pubmed
Maurer-Stroh,
N-terminal N-myristoylation of proteins: prediction of substrate proteins from amino acid sequence.
2002,
Pubmed
Mauri,
Amino acid sequence of a globin from the sea cucumber Caudina (Molpadia) arenicola.
1991,
Pubmed
,
Echinobase
McDonald,
Amino acid sequence of the coelomic C globin from the sea cucumber Caudina (Molpadia) arenicola.
1992,
Pubmed
,
Echinobase
Mitchell,
Three-dimensional structure of a hemichrome hemoglobin from Caudina arenicola.
1995,
Pubmed
,
Echinobase
Notredame,
T-Coffee: A novel method for fast and accurate multiple sequence alignment.
2000,
Pubmed
Opazo,
Genomic evidence for independent origins of beta-like globin genes in monotremes and therian mammals.
2008,
Pubmed
Pei,
PROMALS3D web server for accurate multiple protein sequence and structure alignments.
2008,
Pubmed
Perutz,
Stereochemistry of cooperative mechanisms in hemoglobin.
1987,
Pubmed
Pesce,
Neuroglobin and cytoglobin. Fresh blood for the vertebrate globin family.
2002,
Pubmed
Philippe,
Acoelomorph flatworms are deuterostomes related to Xenoturbella.
2011,
Pubmed
,
Echinobase
Projecto-Garcia,
Origin and evolution of the unique tetra-domain hemoglobin from the hydrothermal vent scale worm Branchipolynoe.
2010,
Pubmed
Qiu,
Lamprey hemoglobin. Structural basis of the bohr effect.
2000,
Pubmed
Ren,
CSS-Palm 2.0: an updated software for palmitoylation sites prediction.
2008,
Pubmed
Resh,
Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins.
1999,
Pubmed
Riggs,
Self-association, cooperativity and supercooperativity of oxygen binding by hemoglobins.
1998,
Pubmed
,
Echinobase
Roesner,
A globin gene of ancient evolutionary origin in lower vertebrates: evidence for two distinct globin families in animals.
2005,
Pubmed
Ronquist,
MrBayes 3: Bayesian phylogenetic inference under mixed models.
2003,
Pubmed
Storz,
Phylogenetic diversification of the globin gene superfamily in chordates.
2011,
Pubmed
Suzuki,
Amino acid sequence of a major globin from the sea cucumber Paracaudina chilensis.
1989,
Pubmed
,
Echinobase
Tamura,
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
2011,
Pubmed
Terwilliger,
Functional adaptations of oxygen-transport proteins.
1998,
Pubmed
Terwilliger,
Oxygen binding domains of a clam (Cardita borealis) extracellular hemoglobin.
1978,
Pubmed
Terwilliger,
The hemoglobin of the holothurian echinoderm, Molpadia oölitica Pourtales.
1972,
Pubmed
,
Echinobase
Vinogradov,
The structure of invertebrate extracellular hemoglobins (erythrocruorins and chlorocruorins).
1985,
Pubmed
Vinogradov,
A phylogenomic profile of globins.
2006,
Pubmed
Vinogradov,
Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life.
2005,
Pubmed
Vinogradov,
A model of globin evolution.
2007,
Pubmed
Vinogradov,
Diversity of globin function: enzymatic, transport, storage, and sensing.
2008,
Pubmed
Vinogradov,
Adventitious variability? The amino acid sequences of nonvertebrate globins.
1993,
Pubmed
,
Echinobase
Weber,
Nonvertebrate hemoglobins: functions and molecular adaptations.
2001,
Pubmed
