Duplication and divergence of Sox genes in spiders

AbstractBackgroundThe Sox family of transcription factors are present and conserved in the genomes of all metazoans examined to data and are known to play important developmental roles in vertebrates and insects. However, outside the commonly studied Drosophila model little is known about the extent or conservation of the Sox family in other arthropod species. Here we characterise the Sox family in two chelicerate species, the spiders Parasteatoda tepidariorum and Stegodyphus mimosarum, which have experienced a whole genome duplication (WGD) in their evolutionary history.ResultsWe find that virtually all of the duplicate Sox genes have been retained in these spiders after the WGD. Analysis of the expression of Sox genes in P. tepidariorum embryos indicates that it is likely that some of these genes have neofunctionalised after duplication. Our expression analysis also strengthens the view that an orthologue of vertebrate Group B1 genes, SoxNeuro, is implicated in the earliest events of CNS specification in both vertebrates and invertebrates. In addition, a gene in the Dichaete/Sox21b class is dynamically expressed in the spider segment addition zone, suggestive of an ancient regulatory mechanism controlling arthropod segmentation as recently suggested for flies and beetles. Together with the recent analysis of Sox gene expression in the embryos of other arthropods, our findings are also indicative of conserved functions for some of these genes, including a role for SoxC and SoxD genes in CNS development, SoxF in limb development and a tantalising suggestion that SoxE genes may be involved in gonadogenesis across the metazoa.ConclusionsOur study provides a new chelicerate perspective to understanding the evolution and function of Sox genes and how the retention of duplicates of such important tool-box genes after WGD has contributed to different aspects of spider embryogenesis. Future characterisation of the function of these genes in spiders will help us to better understand the evolution of the regulation of important developmental processes in arthropods and other metazoans including neurogenesis and segmentation.

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The evolution of Sox gene repertoires and regulation of segmentation in arachnids

10.1101/2020.06.04.133389 ◽

2020 ◽

Cited By ~ 1

Author(s):

Luis Baudouin-Gonzalez ◽

Anna Schoenauer ◽

Amber Harper ◽

Grace Blakeley ◽

Michael Seiter ◽

...

Keyword(s):

Regulatory Networks ◽

Close Relative ◽

System Specification ◽

Germline Development ◽

Simultaneous Formation ◽

Parasteatoda Tepidariorum ◽

Stem Cell Maintenance ◽

Arthropod Species ◽

Anterior Segments ◽

Sox Genes

AbstractThe Sox family of transcription factors regulate many different processes during metazoan development, including stem cell maintenance, nervous system specification and germline development. In addition, it has recently become apparent that SoxB genes are involved in embryonic segmentation in several arthropod species. Segmentation in arthropods occurs in two main ways: long germ animals form all segments at once, best exemplified in the well-studied Drosophila melanogaster system, and short germ animals form anterior segments simultaneously, with posterior segments added sequentially from a segment addition zone. In both D. melanogaster and the short germ beetle Tribolium castaneum, the SoxB gene Dichaete is required for correct segmentation and, more recently, we showed that a close relative of Dichaete, Sox21b-1, is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in the spider Parasteatoda tepidariorum. Here we further analysed the function and expression of Sox21b-1 in P. tepidariorum. We found that while this gene regulates the generation of both prosomal and opisthosomal segments, it plays different roles in the formation of these tagma reflecting their contrasting modes of segmentation and deployment of gene regulatory networks with different architectures. To further investigate the evolution of Sox genes and their roles we characterised the repertoire of the gene family across several arachnid species with and without an ancestral whole genome duplication, and compared Sox expression between P. tepidariorum and the harvestman Phalangium opilio. The results suggest that Sox21b-1 was likely involved in segmentation ancestrally in arachnids, but that other Sox genes could also regulate this process in these animals. We also found that most Sox families have been retained as duplicates or ohnologs after WGD and evidence for potential subfunctionalisation and/or neofunctionalization events.

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A SoxB gene acts as an anterior gap gene and regulates posterior segment addition in a spider

eLife ◽

10.7554/elife.37567 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 13

Author(s):

Christian Louis Bonatto Paese ◽

Anna Schoenauer ◽

Daniel J Leite ◽

Steven Russell ◽

Alistair P McGregor

Keyword(s):

Posterior Segment ◽

Parasteatoda Tepidariorum ◽

Gap Gene ◽

Sequential Addition ◽

Soxb Gene ◽

Sox Gene ◽

Anterior Segments ◽

Conserved Gene ◽

Sox Genes

Sox genes encode a set of highly conserved transcription factors that regulate many developmental processes. In insects, the SoxB gene Dichaete is the only Sox gene known to be involved in segmentation. To determine if similar mechanisms are used in other arthropods, we investigated the role of Sox genes during segmentation in the spider Parasteatoda tepidariorum. While Dichaete does not appear to be involved in spider segmentation, we found that the closely related Sox21b-1 gene acts as a gap gene during formation of anterior segments and is also part of the segmentation clock for development of the segment addition zone and sequential addition of opisthosomal segments. Thus, we have found that two different mechanisms of segmentation in a non-mandibulate arthropod are regulated by a SoxB gene. Our work provides new insights into the function of an important and conserved gene family, and the evolution of the regulation of segmentation in arthropods.

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The Evolution of Sox Gene Repertoires and Regulation of Segmentation in Arachnids

Molecular Biology and Evolution ◽

10.1093/molbev/msab088 ◽

2021 ◽

Author(s):

Luis Baudouin-Gonzalez ◽

Anna Schoenauer ◽

Amber Harper ◽

Grace Blakeley ◽

Michael Seiter ◽

...

Keyword(s):

Whole Genome Duplication ◽

Regulatory Networks ◽

Genome Duplication ◽

Whole Genome ◽

System Specification ◽

Animal Evolution ◽

Simultaneous Formation ◽

Parasteatoda Tepidariorum ◽

Stem Cell Maintenance ◽

And Function

Abstract The Sox family of transcription factors regulates many processes during metazoan development, including stem cell maintenance and nervous system specification. Characterizing the repertoires and roles of these genes can therefore provide important insights into animal evolution and development. We further characterized the Sox repertoires of several arachnid species with and without an ancestral whole-genome duplication and compared their expression between the spider Parasteatoda tepidariorum and the harvestman Phalangium opilio. We found that most Sox families have been retained as ohnologs after whole-genome duplication and evidence for potential subfunctionalization and/or neofunctionalization events. Our results also suggest that Sox21b-1 likely regulated segmentation ancestrally in arachnids, playing a similar role to the closely related SoxB gene, Dichaete, in insects. We previously showed that Sox21b-1 is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in P. tepidariorum. We studied the expression and function of Sox21b-1 further in this spider and found that although this gene regulates the generation of both prosomal and opisthosomal segments, it plays different roles in the formation of these tagmata reflecting their contrasting modes of segmentation and deployment of gene regulatory networks with different architectures.

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Matrix Metalloproteinases in Invertebrates

Protein and Peptide Letters ◽

10.2174/0929866527666200429110945 ◽

2020 ◽

Vol 27 (11) ◽

pp. 1068-1081

Author(s):

Xi Liu ◽

Dongwu Liu ◽

Yangyang Shen ◽

Mujie Huang ◽

Lili Gao ◽

...

Keyword(s):

Matrix Metalloproteinases ◽

Immune Responses ◽

Theoretical Basis ◽

Regulatory Mechanism ◽

Structure And Function ◽

Catalytic Domains ◽

Physiological Processes ◽

Disease Occurrence ◽

Complex Functions ◽

And Function

Matrix Metalloproteinases (MMPs) belong to a family of metal-dependent endopeptidases which contain a series of conserved pro-peptide domains and catalytic domains. MMPs have been widely found in plants, animals, and microorganisms. MMPs are involved in regulating numerous physiological processes, pathological processes, and immune responses. In addition, MMPs play a key role in disease occurrence, including tumors, cardiovascular diseases, and other diseases. Compared with invertebrate MMPs, vertebrate MMPs have diverse subtypes and complex functions. Therefore, it is difficult to study the function of MMPs in vertebrates. However, it is relatively easy to study invertebrate MMPs because there are fewer subtypes of MMPs in invertebrates. In the present review, the structure and function of MMPs in invertebrates were summarized, which will provide a theoretical basis for investigating the regulatory mechanism of MMPs in invertebrates.

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A Family of Genes Clustered at the Triplo-lethal Locus of Drosophila melanogaster Has an Unusual Evolutionary History and Significant Synteny With Anopheles gambiae

Genetics ◽

10.1093/genetics/165.2.613 ◽

2003 ◽

Vol 165 (2) ◽

pp. 613-621 ◽

Cited By ~ 2

Author(s):

Douglas R Dorer ◽

Jamie A Rudnick ◽

Etsuko N Moriyama ◽

Alan C Christensen

Keyword(s):

Phylogenetic Analysis ◽

Drosophila Melanogaster ◽

Anopheles Gambiae ◽

Evolutionary History ◽

Codon Bias ◽

Good Target ◽

The Family ◽

Genes Encoding ◽

And Function ◽

Gambiae Genome

Abstract Within the unique Triplo-lethal region (Tpl) of the Drosophila melanogaster genome we have found a cluster of 20 genes encoding a novel family of proteins. This family is also present in the Anopheles gambiae genome and displays remarkable synteny and sequence conservation with the Drosophila cluster. The family is also present in the sequenced genome of D. pseudoobscura, and homologs have been found in Aedes aegypti mosquitoes and in four other insect orders, but it is not present in the sequenced genome of any noninsect species. Phylogenetic analysis suggests that the cluster evolved prior to the divergence of Drosophila and Anopheles (250 MYA) and has been highly conserved since. The ratio of synonymous to nonsynonymous substitutions and the high codon bias suggest that there has been selection on this family both for expression level and function. We hypothesize that this gene family is Tpl, name it the Osiris family, and consider possible functions. We also predict that this family of proteins, due to the unique dosage sensitivity and the lack of homologs in noninsect species, would be a good target for genetic engineering or novel insecticides.

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The Pleiotropic Intricacies of Hedgehog Signaling: From Craniofacial Patterning to Carcinogenesis

FACE ◽

10.1177/27325016211024326 ◽

2021 ◽

pp. 273250162110243

Author(s):

Mikhail Pakvasa ◽

Andrew B. Tucker ◽

Timothy Shen ◽

Tong-Chuan He ◽

Russell R. Reid

Keyword(s):

Intracellular Signaling ◽

Limb Development ◽

Hedgehog Signaling ◽

Target Genes ◽

Craniofacial Development ◽

Signaling Cascade ◽

Signaling Mechanisms ◽

Intracellular Signaling Cascade ◽

And Function

Hedgehog signaling was discovered more than 40 years ago in experiments demonstrating that it is a fundamental mediator of limb development. Since that time, it has been shown to be important in development, homeostasis, and disease. The hedgehog pathway proceeds through a pathway highly conserved throughout animals beginning with the extracellular diffusion of hedgehog ligands, proceeding through an intracellular signaling cascade, and ending with the activation of specific target genes. A vast amount of research has been done elucidating hedgehog signaling mechanisms and regulation. This research has found a complex system of genetics and signaling that helps determine how organisms develop and function. This review provides an overview of what is known about hedgehog genetics and signaling, followed by an in-depth discussion of the role of hedgehog signaling in craniofacial development and carcinogenesis.

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Limb deformity proteins: role in mesodermal induction of the apical ectodermal ridge

Development ◽

10.1242/dev.124.1.133 ◽

1997 ◽

Vol 124 (1) ◽

pp. 133-139 ◽

Cited By ~ 6

Author(s):

J. Kuhlman ◽

L. Niswander

Keyword(s):

Sonic Hedgehog ◽

Limb Development ◽

Apical Ectodermal Ridge ◽

Primary Defect ◽

Limb Deformity ◽

Normal Morphology ◽

Fibroblast Growth Factor 8 ◽

Skeletal Pattern ◽

Two Phases ◽

And Function

During early limb development, distal tip ectoderm is induced by the underlying mesenchyme to form the apical ectodermal ridge. Subsequent limb growth and patterning depend on reciprocal signaling between the mesenchyme and ridge. Mice that are homozygous for mutations at the limb deformity (ld) locus do not form a proper ridge and the anteroposterior axis of the limb is shortened. Skeletal analyses reveal shortened limbs that involve loss and fusion of distal bones and digits, defects in both anteroposterior and proximodistal patterning. Using molecular markers and mouse-chick chimeras we examined the ridge-mesenchymal interactions to determine the origin of the ld patterning defects. In the ld ridge, fibroblast growth factor 8 (Fgf8) RNA is decreased and Fgf4 RNA is not detected. In the ld mesenchyme, Sonic hedgehog (Shh), Evx1 and Wnt5a expression is decreased. In chimeras between ld ectoderm and wild-type mesenchyme, a ridge of normal morphology and function is restored, Fgf8 and Shh are expressed normally, Fgf4 is induced and a normal skeletal pattern arises. These results suggest that the ld mesenchyme is unable to induce the formation of a completely functional ridge. This primary defect causes a disruption of ridge function and subsequently leads to the patterning defects observed in ld limbs. We propose a model in which ridge induction requires at least two phases: an early competence phase, which includes induction of Fgf8 expression, and a later differentiation phase in which Fgf4 is induced and a morphological ridge is formed. Ld proteins appear to act during the differentiation phase.

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K6-linked SUMOylation of BAF regulates nuclear integrity and DNA replication in mammalian cells

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1912984117 ◽

2020 ◽

Vol 117 (19) ◽

pp. 10378-10387 ◽

Cited By ~ 1

Author(s):

Qiaoyu Lin ◽

Bin Yu ◽

Xiangyang Wang ◽

Shicong Zhu ◽

Gan Zhao ◽

...

Keyword(s):

Dna Replication ◽

Nuclear Localization ◽

Proliferating Cell Nuclear Antigen ◽

Mammalian Cells ◽

Regulatory Mechanism ◽

Nuclear Antigen ◽

Multiple Functions ◽

And Function ◽

Proliferating Cell ◽

Replication Failure

Barrier-to-autointegration factor (BAF) is a highly conserved protein in metazoans that has multiple functions during the cell cycle. We found that BAF is SUMOylated at K6, and that this modification is essential for its nuclear localization and function, including nuclear integrity maintenance and DNA replication. K6-linked SUMOylation of BAF promotes binding and interaction with lamin A/C to regulate nuclear integrity. K6-linked SUMOylation of BAF also supports BAF binding to DNA and proliferating cell nuclear antigen and regulates DNA replication. SENP1 and SENP2 catalyze the de-SUMOylation of BAF at K6. Disrupting the SUMOylation and de-SUMOylation cycle of BAF at K6 not only disturbs nuclear integrity, but also induces DNA replication failure. Taken together, our findings demonstrate that SUMOylation at K6 is an important regulatory mechanism that governs the nuclear functions of BAF in mammalian cells.

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Melatonin Synthesis and Function: Evolutionary History in Animals and Plants

Frontiers in Endocrinology ◽

10.3389/fendo.2019.00249 ◽

2019 ◽

Vol 10 ◽

Cited By ~ 95

Author(s):

Dake Zhao ◽

Yang Yu ◽

Yong Shen ◽

Qin Liu ◽

Zhiwei Zhao ◽

...

Keyword(s):

Evolutionary History ◽

Melatonin Synthesis ◽

And Function

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Myxosporea (Myxozoa, Cnidaria) Lack DNA Cytosine Methylation

Molecular Biology and Evolution ◽

10.1093/molbev/msaa214 ◽

2020 ◽

Author(s):

Ryan Kyger ◽

Agusto Luzuriaga-Neira ◽

Thomas Layman ◽

Tatiana Orli Milkewitz Sandberg ◽

Devika Singh ◽

...

Keyword(s):

Evolutionary History ◽

Cytosine Methylation ◽

Bisulfite Sequencing ◽

Regulatory Mechanism ◽

Regulation Of Gene Expression ◽

Biological Processes ◽

Free Living ◽

Genome Bisulfite Sequencing ◽

History Of ◽

Dna Cytosine Methylation

Abstract DNA cytosine methylation is central to many biological processes, including regulation of gene expression, cellular differentiation, and development. This DNA modification is conserved across animals, having been found in representatives of sponges, ctenophores, cnidarians, and bilaterians, and with very few known instances of secondary loss in animals. Myxozoans are a group of microscopic, obligate endoparasitic cnidarians that have lost many genes over the course of their evolution from free-living ancestors. Here, we investigated the evolution of the key enzymes involved in DNA cytosine methylation in 29 cnidarians and found that these enzymes were lost in an ancestor of Myxosporea (the most speciose class of Myxozoa). Additionally, using whole-genome bisulfite sequencing, we confirmed that the genomes of two distant species of myxosporeans, Ceratonova shasta and Henneguya salminicola, completely lack DNA cytosine methylation. Our results add a notable and novel taxonomic group, the Myxosporea, to the very short list of animal taxa lacking DNA cytosine methylation, further illuminating the complex evolutionary history of this epigenetic regulatory mechanism.

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