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

Author(s):  
Luis Baudouin-Gonzalez ◽  
Anna Schoenauer ◽  
Amber Harper ◽  
Grace Blakeley ◽  
Michael Seiter ◽  
...  

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.

Author(s):  
Luis Baudouin-Gonzalez ◽  
Anna Schoenauer ◽  
Amber Harper ◽  
Grace Blakeley ◽  
Michael Seiter ◽  
...  

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.


2015 ◽  
Vol 35 (13) ◽  
pp. 2242-2253 ◽  
Author(s):  
Chia-Pei Chang ◽  
Chih-Yao Chang ◽  
Yi-Hsueh Lee ◽  
Yeong-Shin Lin ◽  
Chien-Chia Wang

Cytoplasmic and mitochondrial forms of a eukaryotic aminoacyl-tRNA synthetase (aaRS) are generally encoded by two distinct nuclear genes, one of eukaryotic origin and the other of mitochondrial origin. However, in most known yeasts, only the mitochondrial-origin alanyl-tRNA synthetase (AlaRS) gene is retained and plays a dual-functional role. Here, we present a novel scenario of AlaRS evolution in the yeastVanderwaltozyma polyspora.V. polysporapossesses two significantly diverged AlaRS gene homologues, one encoding the cytoplasmic form and the other its mitochondrial counterpart. Clever selection of transcription and translation initiation sites enables the two isoforms to be localized and thus functional in their respective cellular compartments. However, the two isoforms can also be stably expressed and function in the reciprocal compartments by insertion or removal of a mitochondrial targeting signal. Synteny and phylogeny analyses revealed that the AlaRS homologues ofV. polysporaarose from a dual-functional common ancestor through whole-genome duplication (WGD). Moreover, the mitochondrial form had higher synonymous (1.6-fold) and nonsynonymous (2.8-fold) substitution rates than did its cytoplasmic counterpart, presumably due to a lesser constraint imposed on components of the mitochondrial translational apparatus. Our study suggests that asymmetric evolution confers the divergence between the AlaRS paralogues ofV. polyspora.


Author(s):  
Amber Harper ◽  
Luis Baudouin Gonzalez ◽  
Anna Schönauer ◽  
Ralf Janssen ◽  
Michael Seiter ◽  
...  

Abstract Whole genome duplications have occurred multiple times during animal evolution, including in lineages leading to vertebrates, teleosts, horseshoe crabs and arachnopulmonates. These dramatic events initially produce a wealth of new genetic material, generally followed by extensive gene loss. It appears, however, that developmental genes such as homeobox genes, signalling pathway components and microRNAs are frequently retained as duplicates (so called ohnologs) following whole-genome duplication. These not only provide the best evidence for whole-genome duplication, but an opportunity to study its evolutionary consequences. Although these genes are well studied in the context of vertebrate whole-genome duplication, similar comparisons across the extant arachnopulmonate orders are patchy. We sequenced embryonic transcriptomes from two spider species and two amblypygid species and surveyed three important gene families, Hox, Wnt and frizzled, across these and twelve existing transcriptomic and genomic resources for chelicerates. We report extensive retention of putative ohnologs, further supporting the ancestral arachnopulmonate whole-genome duplication. We also found evidence of consistent evolutionary trajectories in Hox and Wnt gene repertoires across three of the six arachnopulmonate orders, with inter-order variation in the retention of specific paralogs. We identified variation between major clades in spiders and are better able to reconstruct the chronology of gene duplications and losses in spiders, amblypygids, and scorpions. These insights shed light on the evolution of the developmental toolkit in arachnopulmonates, highlight the importance of the comparative approach within lineages, and provide substantial new transcriptomic data for future study.


2017 ◽  
Author(s):  
Evelyn E. Schwager ◽  
Prashant P. Sharma ◽  
Thomas Clarke ◽  
Daniel J. Leite ◽  
Torsten Wierschin ◽  
...  

AbstractThe 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. 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 neofunctionalization and/or subfunctionalization since their duplication, and therefore may have contributed to the diversification of spiders and other pulmonate arachnids.


Genetics ◽  
2000 ◽  
Vol 156 (3) ◽  
pp. 1249-1257
Author(s):  
Ilya Ruvinsky ◽  
Lee M Silver ◽  
Jeremy J Gibson-Brown

Abstract The duplication of preexisting genes has played a major role in evolution. To understand the evolution of genetic complexity it is important to reconstruct the phylogenetic history of the genome. A widely held view suggests that the vertebrate genome evolved via two successive rounds of whole-genome duplication. To test this model we have isolated seven new T-box genes from the primitive chordate amphioxus. We find that each amphioxus gene generally corresponds to two or three vertebrate counterparts. A phylogenetic analysis of these genes supports the idea that a single whole-genome duplication took place early in vertebrate evolution, but cannot exclude the possibility that a second duplication later took place. The origin of additional paralogs evident in this and other gene families could be the result of subsequent, smaller-scale chromosomal duplications. Our findings highlight the importance of amphioxus as a key organism for understanding evolution of the vertebrate genome.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Gareth B. Gillard ◽  
Lars Grønvold ◽  
Line L. Røsæg ◽  
Matilde Mengkrog Holen ◽  
Øystein Monsen ◽  
...  

Abstract Background Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap, we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80–100 million years ago. Results We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards lower expression and possible pseudogenization. Loss of expression in one ohnolog is significantly associated with transposable element insertions in promoters and likely driven by selection on gene dosage including selection on stoichiometric balance. We also find symmetric expression shifts, and these are associated with genes under strong evolutionary constraints such as ribosome subunit genes. This possibly reflects selection operating to achieve a gene dose reduction while avoiding accumulation of “toxic mutations”. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one likely source of novel binding sites driving tissue-specific gains in expression. Conclusions Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Amit Rai ◽  
Hideki Hirakawa ◽  
Ryo Nakabayashi ◽  
Shinji Kikuchi ◽  
Koki Hayashi ◽  
...  

AbstractPlant genomes remain highly fragmented and are often characterized by hundreds to thousands of assembly gaps. Here, we report chromosome-level reference and phased genome assembly of Ophiorrhiza pumila, a camptothecin-producing medicinal plant, through an ordered multi-scaffolding and experimental validation approach. With 21 assembly gaps and a contig N50 of 18.49 Mb, Ophiorrhiza genome is one of the most complete plant genomes assembled to date. We also report 273 nitrogen-containing metabolites, including diverse monoterpene indole alkaloids (MIAs). A comparative genomics approach identifies strictosidine biogenesis as the origin of MIA evolution. The emergence of strictosidine biosynthesis-catalyzing enzymes precede downstream enzymes’ evolution post γ whole-genome triplication, which occurred approximately 110 Mya in O. pumila, and before the whole-genome duplication in Camptotheca acuminata identified here. Combining comparative genome analysis, multi-omics analysis, and metabolic gene-cluster analysis, we propose a working model for MIA evolution, and a pangenome for MIA biosynthesis, which will help in establishing a sustainable supply of camptothecin.


Sign in / Sign up

Export Citation Format

Share Document