Dataset Information

Gene content evolution in the arthropods.

ABSTRACT: BACKGROUND:Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. RESULTS:Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. CONCLUSIONS:These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

SUBMITTER: Thomas GWC

PROVIDER: S-EPMC6977273 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Gene content evolution in the arthropods.

Thomas Gregg W C GWC Dohmen Elias E Hughes Daniel S T DST Murali Shwetha C SC Poelchau Monica M Glastad Karl K Anstead Clare A CA Ayoub Nadia A NA Batterham Phillip P Bellair Michelle M Binford Greta J GJ Chao Hsu H Chen Yolanda H YH Childers Christopher C Dinh Huyen H Doddapaneni Harsha Vardhan HV Duan Jian J JJ Dugan Shannon S Esposito Lauren A LA Friedrich Markus M Garb Jessica J Gasser Robin B RB Goodisman Michael A D MAD Gundersen-Rindal Dawn E DE Han Yi Y Handler Alfred M AM Hatakeyama Masatsugu M Hering Lars L Hunter Wayne B WB Ioannidis Panagiotis P Jayaseelan Joy C JC Kalra Divya D Khila Abderrahman A Korhonen Pasi K PK Lee Carol Eunmi CE Lee Sandra L SL Li Yiyuan Y Lindsey Amelia R I ARI Mayer Georg G McGregor Alistair P AP McKenna Duane D DD Misof Bernhard B Munidasa Mala M Munoz-Torres Monica M Muzny Donna M DM Niehuis Oliver O Osuji-Lacy Nkechinyere N Palli Subba R SR Panfilio Kristen A KA Pechmann Matthias M Perry Trent T Peters Ralph S RS Poynton Helen C HC Prpic Nikola-Michael NM Qu Jiaxin J Rotenberg Dorith D Schal Coby C Schoville Sean D SD Scully Erin D ED Skinner Evette E Sloan Daniel B DB Stouthamer Richard R Strand Michael R MR Szucsich Nikolaus U NU Wijeratne Asela A Young Neil D ND Zattara Eduardo E EE Benoit Joshua B JB Zdobnov Evgeny M EM Pfrender Michael E ME Hackett Kevin J KJ Werren John H JH Worley Kim C KC Gibbs Richard A RA Chipman Ariel D AD Waterhouse Robert M RM Bornberg-Bauer Erich E Hahn Matthew W MW Richards Stephen S

Genome biology 20200123 1

<h4>Background</h4>Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.<h4>Results</h4>Using 76 whole genome sequences representing 21 ...[more]

PMID: 31969194

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Project description:Globins are small heme-proteins that reversibly bind oxygen. Their most prominent roles in vertebrates are the transport and storage of O2 for oxidative energy metabolism, but recent research has suggested alternative, non-respiratory globin functions. In the species-rich and ecologically highly diverse taxon of arthropods, the copper-containing hemocyanin is considered the main respiratory protein. However, recent studies have suggested the presence of globin genes and their proteins in arthropod taxa, including model species like Drosophila. To systematically assess the taxonomic distribution, evolution and diversity of globins in arthropods, we systematically searched transcriptome and genome sequence data and found a conserved, widespread occurrence of three globin classes in arthropods: hemoglobin-like (HbL), globin X (GbX), and globin X-like (GbXL) protein lineages. These globin types were previously identified in protostome and deuterostome animals including vertebrates, suggesting their early ancestry in Metazoa. The HbL genes show multiple, lineage-specific gene duplications in all major arthropod clades. Some HbL genes (e.g., Glob2 and 3 of Drosophila) display particularly fast substitution rates, possibly indicating the evolution of novel functions, e.g., in spermatogenesis. In contrast, arthropod GbX and GbXL globin genes show high evolutionary stability: GbXL is represented by a single-copy gene in all arthropod groups except Brachycera, and representatives of the GbX clade are present in all examined taxa except holometabolan insects. GbX and GbXL both show a brain-specific expression. Most arthropod GbX and GbXL proteins, but also some HbL variants, include sequence motifs indicative of potential N-terminal acylation (i.e., N-myristoylation, 3C-palmitoylation). All arthropods except for the brachyceran Diptera harbor at least one such potentially acylated globin copy, confirming the hypothesis of an essential, conserved globin function associated with the cell membrane. In contrast to other animals, the fourth ancient globin lineage, represented by neuroglobin, appears to be absent in arthropods, and the putative arthropod orthologs of the fifth metazoan globin lineage, androglobin, lack a recognizable globin domain. Thus, the remarkable 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.

Project description:BACKGROUND: One way of creating phenotypic diversity is through alternative splicing of precursor mRNAs. A gene that has evolved a hypervariable form is Down syndrome cell adhesion molecule (Dscam-hv), which in Drosophila melanogaster can produce thousands of isoforms via mutually exclusive alternative splicing. The extracellular region of this protein is encoded by three variable exon clusters, each containing multiple exon variants. The protein is vital for neuronal wiring where the extreme variability at the somatic level is required for axonal guidance, and it plays a role in immunity where the variability has been hypothesised to relate to recognition of different antigens. Dscam-hv has been found across the Pancrustacea. Additionally, three paralogous non-hypervariable Dscam-like genes have also been described for D. melanogaster. Here we took a bioinformatics approach, building profile Hidden Markov Models to search across species for putative orthologs to the Dscam genes and for hypervariable alternatively spliced exons, and inferring the phylogenetic relationships among them. Our aims were to examine whether Dscam orthologs exist outside the Bilateria, whether the origin of Dscam-hv could lie outside the Pancrustacea, when the Dscam-like orthologs arose, how many alternatively spliced exons of each exon cluster were present in the most common recent ancestor, and how these clusters evolved. RESULTS: Our results suggest that the origin of Dscam genes may lie after the split between the Cnidaria and the Bilateria and supports the hypothesis that Dscam-hv originated in the common ancestor of the Pancrustacea. Our phylogeny of Dscam gene family members shows six well-supported clades: five containing Dscam-like genes and one containing all the Dscam-hv genes, a seventh clade contains arachnid putative Dscam genes. Furthermore, the exon clusters appear to have experienced different evolutionary histories. CONCLUSIONS: Dscam genes have undergone independent duplication events in the insects and in an arachnid genome, which adds to the more well-known tandem duplications that have taken place within Dscam-hv genes. Therefore, two forms of gene expansion seem to be active within this gene family. The evolutionary history of this dynamic gene family will be further unfolded as genomes of species from more disparate groups become available.

Dataset Information

Gene content evolution in the arthropods.

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Gene content evolution in the arthropods.

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