Embryonic expression patterns and phylogenetic analysis of panarthropod sox genes: insight into nervous system development, segmentation and gonadogenesis

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Abstract

Background

Sox ( Sry-related high-mobility-group b ox) genes represent important factors in animal development. Relatively little, however, is known about the embryonic expression patterns and thus possible function(s) of Sox genes during ontogenesis in panarthropods (Arthropoda+Tardigrada+Onychophora). To date, studies have been restricted exclusively to higher insects, including the model system Drosophila melanogaster, with no comprehensive data available for any other arthropod group, or any tardigrade or onychophoran.

Results

This study provides a phylogenetic analysis of panarthropod Sox genes and presents the first comprehensive analysis of embryonic expression patterns in the flour beetle Tribolium castaneum (Hexapoda), the pill millipede Glomeris marginata (Myriapoda), and the velvet worm, Euperipatoides kanangrensis (Onychophora). 24 Sox genes were identified and investigated: 7 in Euperipatoides, 8 in Glomeris, and 9 in Tribolium. Each species possesses at least one ortholog of each of the five expected Sox gene families, B, C, D, E, and F, many of which are differentially expressed during ontogenesis.

Conclusion

Sox gene expression (and potentially function) is highly conserved in arthropods and their closest relatives, the onychophorans. Sox B, C and D class genes appear to be crucial for nervous system development, while the Sox B genes Dichaete ( D) and Sox21b likely play an additional conserved role in panarthropod segmentation. The Sox B gene Sox21a likely has a conserved function in foregut and Malpighian tubule development, at least in Hexapoda. The data further suggest that Sox D and E genes are involved in mesoderm differentiation, and that Sox E genes are involved in gonadal development.

The new data expand our knowledge about the expression and implied function of Sox genes to Mandibulata (Myriapoda+Pancrustacea) and Panarthropoda (Arthropoda+Onychophora).

Electronic supplementary material

The online version of this article (10.1186/s12862-018-1196-z) contains supplementary material, which is available to authorized users.

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Most cited references 87

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Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators.

Josephine Bowles, Goslik E. Schepers, Peter Koopman (2000)

Members of the SOX family of transcription factors are found throughout the animal kingdom, are characterized by the presence of a DNA-binding HMG domain, and are involved in a diverse range of developmental processes. Previous attempts to group SOX genes and deduce their structural, functional, and evolutionary relationships have relied largely on complete or partial HMG box sequence of a limited number of genes. In this study, we have used complete HMG domain sequence, full-length protein structure, and gene organization data to study the pattern of evolution within the family. For the first time, a substantial number of invertebrate SOX sequences have been included in the analysis. We find support for subdivision of the family into groups A-H, as has been suggested in some previous studies, and for the assignment of two new groups, I and J. For vertebrate genes, it appears that relatedness as suggested by HMG domain sequence is congruent with relatedness as indicated by overall structure of the full-length protein and intron-exon structure of the genes. Most of the SOX groups identified in vertebrates were represented by a single SOX sequence in each invertebrate species studied. We have named anonymous sequences and, where appropriate, have suggested systematic names for some previously identified sequences. In addition, we identify an HMG domain signature motif which may be considered representative of the SOX family. Based on our data, we propose a robust phylogeny of SOX genes that reflects their evolutionary history in metazoans. Copyright 2000 Academic Press.

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Genomic data do not support comb jellies as the sister group to all other animals.

Davide Pisani, Walker Pett, Martin Dohrmann … (2015)

Understanding how complex traits, such as epithelia, nervous systems, muscles, or guts, originated depends on a well-supported hypothesis about the phylogenetic relationships among major animal lineages. Traditionally, sponges (Porifera) have been interpreted as the sister group to the remaining animals, a hypothesis consistent with the conventional view that the last common animal ancestor was relatively simple and more complex body plans arose later in evolution. However, this premise has recently been challenged by analyses of the genomes of comb jellies (Ctenophora), which, instead, found ctenophores as the sister group to the remaining animals (the "Ctenophora-sister" hypothesis). Because ctenophores are morphologically complex predators with true epithelia, nervous systems, muscles, and guts, this scenario implies these traits were either present in the last common ancestor of all animals and were lost secondarily in sponges and placozoans (Trichoplax) or, alternatively, evolved convergently in comb jellies. Here, we analyze representative datasets from recent studies supporting Ctenophora-sister, including genome-scale alignments of concatenated protein sequences, as well as a genomic gene content dataset. We found no support for Ctenophora-sister and conclude it is an artifact resulting from inadequate methodology, especially the use of simplistic evolutionary models and inappropriate choice of species to root the metazoan tree. Our results reinforce a traditional scenario for the evolution of complexity in animals, and indicate that inferences about the evolution of Metazoa based on the Ctenophora-sister hypothesis are not supported by the currently available data.

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The house spider genome reveals an ancient whole-genome duplication during arachnid evolution

Evelyn E. Schwager, Prashant Sharma, Thomas E Clarke … (2017)

Background The duplication of genes can occur through various mechanisms and is thought to make a major contribution to the evolutionary diversification of organisms. There is increasing evidence for a large-scale duplication of genes in some chelicerate lineages including two rounds of whole genome duplication (WGD) in horseshoe crabs. To investigate this further, we sequenced and analyzed the genome of the common house spider Parasteatoda tepidariorum. Results We found pervasive duplication of both coding and non-coding genes in this spider, including two clusters of Hox genes. Analysis of synteny conservation across the P. tepidariorum genome suggests that there has been an ancient WGD in spiders. Comparison with the genomes of other chelicerates, including that of the newly sequenced bark scorpion Centruroides sculpturatus, suggests that this event occurred in the common ancestor of spiders and scorpions, and is probably independent of the WGDs in horseshoe crabs. Furthermore, characterization of the sequence and expression of the Hox paralogs in P. tepidariorum suggests that many have been subject to neo-functionalization and/or sub-functionalization since their duplication. Conclusions Our results reveal that spiders and scorpions are likely the descendants of a polyploid ancestor that lived more than 450 MYA. Given the extensive morphological diversity and ecological adaptations found among these animals, rivaling those of vertebrates, our study of the ancient WGD event in Arachnopulmonata provides a new comparative platform to explore common and divergent evolutionary outcomes of polyploidization events across eukaryotes. Electronic supplementary material The online version of this article (doi:10.1186/s12915-017-0399-x) contains supplementary material, which is available to authorized users.

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Author and article information

Contributors

Ralf Janssen:

ORCID: http://orcid.org/0000-0002-4026-4129

(+46) 18 471 2763 , ralf.janssen@geo.uu.se

Emil Andersson: emil.andersson.2836@student.uu.se

Ellinor Betnér: ellinor.betner@gmail.com

Sifra Bijl: sifrabijl@gmail.com

Will Fowler: william.fowler.9356@student.uu.se

Lars Höök: larsfredrikhook@hotmail.com

Jake Leyhr: jakeleyhr535@gmail.com

Alexander Mannelqvist: Stupelgard@outlook.com

Virginia Panara: virginia.panara@fastwebnet.it

Kate Smith: kateflorencesmith@gmail.com

Sydney Tiemann: sftiemann@gmail.com

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2148

Publication date (Electronic): 8 June 2018

Publication date PMC-release: 8 June 2018

Publication date Collection: 2018

Volume: 18

Electronic Location Identifier: 88

Affiliations

ISNI 0000 0004 1936 9457, GRID grid.8993.b, Uppsala University, Department of Earth Sciences, Palaeobiology, ; Villavägen 16, 75236 Uppsala, Sweden

Author information

Ralf Janssen http://orcid.org/0000-0002-4026-4129

Article

Publisher ID: 1196

DOI: 10.1186/s12862-018-1196-z

PMC ID: 5994082

PubMed ID: 29884143

SO-VID: d6342618-cb10-42bb-97ec-1794db7fd79a

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 2 November 2017

Date accepted : 18 May 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;

Award ID: 621-2011-4703

Award Recipient : Ralf Janssen

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ScienceOpen disciplines: Evolutionary Biology

Keywords: sry,germ cells,vasa,arthropoda,onychophora,development

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ScienceOpen disciplines: Evolutionary Biology

Keywords: sry, germ cells, vasa, arthropoda, onychophora, development

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Embryonic expression patterns and phylogenetic analysis of panarthropod sox genes: insight into nervous system development, segmentation and gonadogenesis

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Most cited references 87

Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators.

Genomic data do not support comb jellies as the sister group to all other animals.

The house spider genome reveals an ancient whole-genome duplication during arachnid evolution

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