Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates

Abstract

Natural selection often promotes evolutionary innovation by coopting preexisting genes for new functions, and this process may be greatly facilitated by gene duplication. Here we report an example of cooptive convergence where paralogous members of the globin gene superfamily independently evolved a specialized O 2 transport function in the two deepest branches of the vertebrate family tree. Specifically, phylogenetic evidence demonstrates that erythroidspecific O 2 transport hemoglobins evolved independently from different ancestral precursor proteins in jawed vertebrates (gnathostomes) and jawless fish (cyclostomes, represented by lamprey and hagfish). A comprehensive phylogenetic analysis of the vertebrate globin gene superfamily revealed that the erythroid hemoglobins of cyclostomes are orthologous to the cytoglobin protein of gnathostome vertebrates, a hexacoordinate globin that has no O 2 transport function and that is predominantly expressed in fibroblasts and related cell types. The phylogeny reconstruction also revealed that vertebrate-specific globins are grouped into four main clades: (i) cyclostome hemoglobin + cytoglobin, (ii) myoglobin + globin E, (iii) globin Y, and (iv) the α-and β-chain hemoglobins of gnathostomes. In the hemoglobins of gnathostomes and cyclostomes, multisubunit quaternary structures provide the basis for cooperative O 2 binding and allosteric regulation by coupling the effects of ligand binding at individual subunits with interactions between subunits. However, differences in numerous structural details belie their independent origins. This example of convergent evolution of protein function provides an impressive demonstration of the ability of natural selection to cobble together complex design solutions by tinkering with different variations of the same basic protein scaffold.cytoglobin | gene family evolution | globin | hagfish | lamprey

Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana

“…While it is not known what evolutionary events underlie such network co-option events, it is tempting to speculate that novel developmental or stress-related functions could be created by for instance the evolution of novel expression patterns of just one or few upstream regulatory genes and hence require a minimal number of evolutionary changes. Previously reported cases of network or pathway co-option (e.g., Shimeld et al, 2005;Werner et al, 2010) usually relate to existing gene sets being used in a new setting, but some examples exist of pathway co-option following gene duplication (Rosin and Kramer, 2009;Hoffmann et al, 2010). The latter has the advantage of producing template pathways that can be molded by evolution while simultaneously limiting possible interference with the ancestral function.…”

Characterisation of Duplicated Haemoglobin Genes in Bivalves

“…A recent phylogenetic analysis of the vertebrate Hbs by Hoffmann et al, (2010a) (Hoffmann et al, 2010a). Findings such as these are in contrast to the prevailing paradigm that the current vertebrate Hbs have evolved from an ancestral Mb gene.…”

“…Structural variations in Hbs can be observed even among vertebrate lineages, where jawless vertebrates (agnathans) have weakly cooperative dimers compared to the canonical tetrameric Hbs of jawed vertebrates (gnathostomes) (Hoffmann et al, 2010a).…”

“…The globin gene superfamily includes genes encoding Hbs, neuroglobins (Ngbs), cytoglobins (Cygbs), globin X (GbX), androglobins (Angbs), Mbs, globin E (GbE) and globin Y (GbY) among others (Hoffmann et al, 2010a;Storz et al, 2013;Opazo et al, 2015). This diverse group of genes is thought to have evolved from a common ancestral gene through repeated rounds of gene and genome duplication, some 1.8 billion years ago (Efstratiadis et al, 1980;Wajcman et al, 2009).…”

“…The globins are an ancient gene superfamily, thought to have been present in the last universal common ancestor (LUCA) of the three domains of life (Hoffmann et al, 2010a). Globin genes encode for small iron metalloproteins, typically ~ 150 amino acids in length.…”