The Globin Gene Family in Arthropods: Evolution and Functional Diversity

Prothmann, Andreas; Hoffmann, Federico G.; Opazo, Juan C.; Herbener, Peter; Storz, Jay F.; Burmester, Thorsten; Hankeln, Thomas

doi:10.3389/fgene.2020.00858

Cited by 11 publications

(11 citation statements)

References 91 publications

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“…This paradigm change came with an increased interest in deciphering its evolutionary history and its still elusive functional role ( Burmester and Hankeln 2014 ; Keppner et al 2020 ). We have recently documented the presence of GbX paralogs in arthropods ( Prothmann et al 2020 ), confirming phylogenetic predictions that indicate that the origin of GbX predates the split between deuterostomes and protostomes ( Burmester et al 2002 ; Roesner et al 2005 ; Dröge and Makałowski 2011 ; Blank and Burmester 2012 ; Hoffmann, Opazo, Hoogewijs, et al 2012 ; Opazo et al 2015 ), which is estimated to have occurred ∼ 730 million years ago ( Kumar et al 2017 ).…”

Section: Discussionsupporting

confidence: 77%

“…In the case of GbX , recently released genomes from key vertebrate taxa provide an excellent opportunity to address questions about its evolution. Globin-X is an especially enigmatic globin because it is predicted to be bound to the cell membrane ( Blank et al 2011 ), and because it has a very wide phyletic distribution that spans protostomes and deuterostomes ( Blank and Burmester 2012 ; Hoffmann, Opazo, Hoogewijs, et al 2012 ; Prothmann et al 2020 ). There are GbX genes present in the genomes of insects, crustaceans, platyhelminthes, myriapods, spiders, hemichordates, and vertebrates among others, indicating that its origin predates the split between protostome and deuterostomes ( Dröge and Makałowski 2011 ).…”

Section: Introductionmentioning

confidence: 99%

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Whole-Genome Duplications and the Diversification of the Globin-X Genes of Vertebrates

Hoffmann

Storz

Kuraku

et al. 2021

Genome Biology and Evolution

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Globin-X (GbX) is an enigmatic member of the vertebrate globin gene family with a wide phyletic distribution that spans protostomes and deuterostomes. Unlike canonical globins such as hemoglobins and myoglobins, functional data suggest that GbX does not have a primary respiratory function. Instead, evidence suggests that the monomeric, membrane-bound GbX may play a role in cellular signaling or protection against the oxidation of membrane lipids. Recently released genomes from key vertebrates provide an excellent opportunity to address questions about the early stages of the evolution of GbX in vertebrates. We integrate bioinformatics, synteny, and phylogenetic analyses to characterize the diversity of GbX genes in non-teleost ray-finned fishes, resolve relationships between the GbX genes of cartilaginous fish and bony vertebrates, and demonstrate that the GbX genes of cyclostomes and gnathostomes derive from independent duplications. Our study highlights the role that whole-genome duplications (WGDs) have played in expanding the repertoire of genes in vertebrate genomes. Our results indicate that GbX paralogs have a remarkably high rate of retention following WGDs relative to other globin genes, and provide an evolutionary framework for interpreting results of experiments that examine functional properties of GbX and patterns of tissue-specific expression. By identifying GbX paralogs that are products of different WGDs, our results can guide the design of experimental work to explore whether gene duplicates that originate via WGDs have evolved novel functional properties or expression profiles relative to singleton or tandemly duplicated copies of GbX.

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Section: Discussionsupporting

confidence: 77%

Section: Introductionmentioning

confidence: 99%

Whole-Genome Duplications and the Diversification of the Globin-X Genes of Vertebrates

Hoffmann

Storz

Kuraku

et al. 2021

Genome Biology and Evolution

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show abstract

“…This change in paradigm came with an increased interest in deciphering its evolutionary history and its still elusive functional role (Burmester and Hankeln, 2014; Keppner et al, 2020). We have recently documented the presence of GbX paralogs in arthropods (Prothmann et al, 2020), confirming phylogenetic predictions that indicate that the origin of GbX predates the split between deuterostomes and protostomes (Burmester et al, 2002; Roesner et al, 2005; Dröge and Makałowski, 2011; Blank and Burmester, 2012; Hoffmann et al, 2012a)(Opazo et al, 2015), which is estimated to have occurred ~ 730 million years ago (Kumar et al, 2017).…”

Section: Discussionsupporting

confidence: 76%

“…Because some of the sequences retrieved were annotated as neuroglobins or cytoglobins, and our searches potentially yielded redundant results, we first performed a phylogenetic analysis with all GbX candidates, to confirm the GbX identity of all retrieved sequences, to identify redundant sequences, and to detect potential annotation problems as evidenced by unusually long branches. Thus, for the second round of analyses, we removed all acorn worm globins other than 7, 8, 9,10, and 16, which had already been shown to be the most closely related to GbX (Hoffmann et al, 2012a; Prothmann et al, 2020). We removed redundant records and retained a single representative species per genus, with the exception of the carp, where we kept two separate assemblies that include two separate duplications.…”

Section: Methodsmentioning

confidence: 99%

“…In the case of GbX, recently released genomes from key vertebrate taxa provide an excellent opportunity to address questions about its evolution. Globin-X is an especially enigmatic globin because it is predicted to be bound to the cell membrane (Blank et al, 2011), and because it has a very wide phyletic distribution that spans protostomes and deuterostomes (Blank and Burmester, 2012; Hoffmann et al, 2012a; Prothmann et al, 2020). There are GbX genes present in the genomes of insects, crustaceans, platyhelminthes, myriapods, spiders, hemichordates, and vertebrates among others, indicating that its origin predates the split between protostome and deuterostomes (Dröge and Makałowski, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Whole genome duplications and the diversification of the Globin-X genes of vertebrates

Hoffmann

Storz²,

Kuraku

et al. 2021

Preprint

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The globin superfamily of vertebrate genes is a textbook example of how the interplay between local gene duplications, whole-genome duplications, and regulatory changes can facilitate the evolution of novel protein functions. Almost every vertebrate examined possesses copies of hemoglobin and myoglobin in their genomes, and both cytoglobin and neuroglobin are present in the vast majority of vertebrate genomes surveyed as well. The phylogenetic distribution of globin-E, globin-Y and globin-X (GbX), however, is more spotty, suggesting multiple independent gene losses. Globin-X is an enigmatic globin with a wide phyletic distribution that spans protostomes and deuterostomes. Unlike canonical globins such as hemoglobins and myoglobins, functional data suggest that GbX does not have a primary respiratory function. Instead, available evidence suggests that GbX may play a role in protecting cells from oxidative damage and in reducing nitrite and it is predicted to be bound to the cell membrane. Recently released genomes from key vertebrate taxa provide an excellent opportunity to address questions about the early stages of evolution of these genes in vertebrates. In the current study, we integrate bioinformatic, synteny and phylogenetic analyses to characterize the diversity of GbX genes in non-teleost ray-finned fishes, resolve relationships between the GbX genes of cartilaginous fish and the GbX genes of bony vertebrates, and demonstrate that the GbX genes of cyclostomes and gnathostomes have independent duplicative histories. Our study highlights the role that whole genome duplications (WGDs) have played in expanding the repertoire of genes in vertebrate genomes. Our results indicate that GbX paralogs have a remarkably high rate of retention following WGDs in comparison to other globin genes, and also provide an evolutionary framework for interpreting results of experiments that examine functional properties of GbX and patterns of tissue-specific expression. By identifying GbX genes products of different WGDs in the vertebrate tree of life, our results can guide the design of experimental work to explore whether gene duplicates that originate via WGDs have evolved novel functional properties or expression profiles relative to singleton or tandemly duplicated copies of GbX.

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Globin phylogeny, evolution and function, the newest update

Schuster,

Salvatore,

Moens

et al. 2024

Proteins

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Our globin census update allows us to refine our vision of globin origin, evolution, and structure to function relationship in the context of the currently accepted tree of life. The modern globin domain originates as a single domain, three‐over‐three α‐helical folded structure before the diversification of the kingdoms of life (Bacteria, Archaea, Eukarya). Together with the diversification of prokaryotes, three monophyletic globin families (M, S, and T) emerged, most likely in Proteobacteria and Actinobacteria, displaying specific sequence and structural features, and spread by vertical and horizontal gene transfer, most probably already present in the last universal common ancestor (LUCA). Non‐globin domains were added, and eventually lost again, creating multi‐domain structures in key branches of M‐ (FHb and Adgb) and the vast majority of S globins, which with their coevolved multi‐domain architectures, have predominantly “sensor” functions. Single domain T‐family globins diverged into four major groups and most likely display functions related to reactive nitrogen and oxygen species (RNOS) chemistry, as well as oxygen storage/transport which drives the evolution of its major branches with their characteristic key distal residues (B10, E11, E7, and G8). M‐family evolution also lead to distinctive major types (FHb and Fgb, Ngb, Adgb, GbX vertebrate Gbs), and shows the shift from high oxygen affinity controlled by TyrB10‐Gln/AsnE11 likely related to RNOS chemistry in microorganisms, to a moderate oxygen affinity storage/transport function controlled by hydrophobic B10/E11–HisE7 in multicellular animals.

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The Globin Gene Family in Arthropods: Evolution and Functional Diversity

Abstract: Prothmann et al. Arthropod Globin Diversity evolutionary stability of some globin variants is contrasted by occasional dynamic gene multiplication or even loss of otherwise strongly conserved globin lineages in arthropod phylogeny.

Cited by 11 publications

References 91 publications

Whole-Genome Duplications and the Diversification of the Globin-X Genes of Vertebrates

Whole-Genome Duplications and the Diversification of the Globin-X Genes of Vertebrates

Whole genome duplications and the diversification of the Globin-X genes of vertebrates

Globin phylogeny, evolution and function, the newest update

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