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Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans.

ABSTRACT: The phylum Rotifera consists of minuscule, nonsegmented animals with a unique body plan and an unresolved phylogenetic position. The presence of pharyngeal articulated jaws supports an inclusion in Gnathifera nested in the Spiralia. Comparison of Hox genes, involved in animal body plan patterning, can be used to infer phylogenetic relationships. Here, we report the expression of five Hox genes during embryogenesis of the rotifer Brachionus manjavacas and show how these genes define different functional components of the nervous system and not the usual bilaterian staggered expression along the anteroposterior axis. Sequence analysis revealed that the lox5-parapeptide, a key signature in lophotrochozoan and platyhelminthean Hox6/lox5 genes, is absent and replaced by different signatures in Rotifera and Chaetognatha, and that the MedPost gene, until now unique to Chaetognatha, is also present in rotifers. Collectively, our results support an inclusion of chaetognaths in gnathiferans and Gnathifera as sister group to the remaining spiralians.Rotifers are microscopic animals with an unusual, nonsegmented body plan consisting of a head, trunk and foot. Here, Fröbius and Funch investigate the role of Hox genes-which are widely used in animal body plan patterning-in rotifer embryogenesis and find non-canonical expression in the nervous system.

SUBMITTER: Frobius AC

PROVIDER: S-EPMC5431905 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans.

Fröbius Andreas C AC Funch Peter P

Nature communications 20170404 1

The phylum Rotifera consists of minuscule, nonsegmented animals with a unique body plan and an unresolved phylogenetic position. The presence of pharyngeal articulated jaws supports an inclusion in Gnathifera nested in the Spiralia. Comparison of Hox genes, involved in animal body plan patterning, can be used to infer phylogenetic relationships. Here, we report the expression of five Hox genes during embryogenesis of the rotifer Brachionus manjavacas and show how these genes define different fun ...[more]

PMID: 28377584

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Project description:BACKGROUND: Hox and the closely-related ParaHox genes, which emerged prior to the divergence between cnidarians and bilaterians, are the most well-known members of the ancient genetic toolkit that controls embryonic development across all metazoans. Fundamental questions relative to their origin and evolutionary relationships remain however unresolved. We investigate here the evolution of metazoan Hox and ParaHox genes using the HoxPred program that allows the identification of Hox genes without the need of phylogenetic tree reconstructions. RESULTS: We show that HoxPred provides an efficient and accurate classification of Hox and ParaHox genes in their respective homology groups, including Hox paralogous groups (PGs). We analyzed more than 10,000 sequences from 310 metazoan species, from 6 genome projects and the complete UniProtKB database. The HoxPred program and all results arranged in the Datab'Hox database are freely available at http://cege.vub.ac.be/hoxpred/. Results for the genome-scale studies are coherent with previous studies, and also brings knowledge on the Hox repertoire and clusters for newly-sequenced species. The unprecedented scale of this study and the use of a non-tree-based approach allows unresolved key questions about Hox and ParaHox genes evolution to be addressed. CONCLUSIONS: Our analysis suggests that the presence of a single type of Posterior Hox genes (PG9-like) is ancestral to bilaterians, and that new Posterior PGs would have arisen in deuterostomes through independent gene duplications. Four types of Central genes would also be ancestral to bilaterians, with two of them, PG6- and PG7-like that gave rise, in protostomes, to the UbdA- and ftz/Antp/Lox5-type genes, respectively. A fifth type of Central genes (PG8) would have emerged in the vertebrate lineage. Our results also suggest the presence of Anterior (PG1 and PG3), Central and Posterior Hox genes in the cnidarians, supporting an ancestral four-gene Hox cluster. In addition, our data support the relationship of the bilaterian ParaHox genes Gsx and Xlox with PG3, and Cdx with the Central genes. Our study therefore indicates three possible models for the origin of Hox and ParaHox in early metazoans, a two-gene (Anterior/PG3--Central/Posterior), a three-gene (Anterior/PG1, Anterior/PG3 and Central/Posterior), or a four-gene (Anterior/PG1--Anterior/PG3--Central--Posterior) ProtoHox cluster.

Project description:BACKGROUND: Alvinella pompejana is a representative of Annelids, a key phylum for evo-devo studies that is still poorly studied at the sequence level. A. pompejana inhabits deep-sea hydrothermal vents and is currently known as one of the most thermotolerant Eukaryotes in marine environments, withstanding the largest known chemical and thermal ranges (from 5 to 105°C). This tube-dwelling worm forms dense colonies on the surface of hydrothermal chimneys and can withstand long periods of hypo/anoxia and long phases of exposure to hydrogen sulphides. A. pompejana specifically inhabits chimney walls of hydrothermal vents on the East Pacific Rise. To survive, Alvinella has developed numerous adaptations at the physiological and molecular levels, such as an increase in the thermostability of proteins and protein complexes. It represents an outstanding model organism for studying adaptation to harsh physicochemical conditions and for isolating stable macromolecules resistant to high temperatures. RESULTS: We have constructed four full length enriched cDNA libraries to investigate the biology and evolution of this intriguing animal. Analysis of more than 75,000 high quality reads led to the identification of 15,858 transcripts and 9,221 putative protein sequences. Our annotation reveals a good coverage of most animal pathways and networks with a prevalence of transcripts involved in oxidative stress resistance, detoxification, anti-bacterial defence, and heat shock protection. Alvinella proteins seem to show a slow evolutionary rate and a higher similarity with proteins from Vertebrates compared to proteins from Arthropods or Nematodes. Their composition shows enrichment in positively charged amino acids that might contribute to their thermostability. The gene content of Alvinella reveals that an important pool of genes previously considered to be specific to Deuterostomes were in fact already present in the last common ancestor of the Bilaterian animals, but have been secondarily lost in model invertebrates. This pool is enriched in glycoproteins that play a key role in intercellular communication, hormonal regulation and immunity. CONCLUSIONS: Our study starts to unravel the gene content and sequence evolution of a deep-sea annelid, revealing key features in eukaryote adaptation to extreme environmental conditions and highlighting the proximity of Annelids and Vertebrates.

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Project description:BackgroundGerm lines are the cell lineages that give rise to the sperm and eggs in animals. The germ lines first arise from primordial germ cells (PGCs) during embryogenesis: these form from either a presumed derived mode of preformed germ plasm (inheritance) or from an ancestral mechanism of inductive cell-cell signalling (induction). Numerous genes involved in germ line specification and development have been identified and functionally studied. However, little is known about the molecular evolutionary dynamics of germ line genes in metazoan model systems.ResultsHere, we studied the molecular evolution of germ line genes within three metazoan model systems. These include the genus Drosophila (N=34 genes, inheritance), the fellow insect Apis (N=30, induction), and their more distant relative Caenorhabditis (N=23, inheritance). Using multiple species and established phylogenies in each genus, we report that germ line genes exhibited marked variation in the constraint on protein sequence divergence (dN/dS) and codon usage bias (CUB) within each genus. Importantly, we found that de novo lineage-specific inheritance (LSI) genes in Drosophila (osk, pgc) and in Caenorhabditis (pie-1, pgl-1), which are essential to germ plasm functions under the derived inheritance mode, displayed rapid protein sequence divergence relative to the other germ line genes within each respective genus. We show this may reflect the evolution of specialized germ plasm functions and/or low pleiotropy of LSI genes, features not shared with other germ line genes. In addition, we observed that the relative ranking of dN/dS and of CUB between genera were each more strongly correlated between Drosophila and Caenorhabditis, from different phyla, than between Drosophila and its insect relative Apis, suggesting taxonomic differences in how germ line genes have evolved.ConclusionsTaken together, the present results advance our understanding of the evolution of animal germ line genes within three well-known metazoan models. Further, the findings provide insights to the molecular evolution of germ line genes with respect to LSI status, pleiotropy, adaptive evolution as well as PGC-specification mode.

Dataset Information

Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans.

Publications

Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans.

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