scholarly journals Widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates

2021 ◽  
Author(s):  
Amber Harper ◽  
Luis Baudouin Gonzalez ◽  
Anna Schönauer ◽  
Ralf Janssen ◽  
Michael Seiter ◽  
...  
Keyword(s):  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Genetic Material ◽  
Gene Families ◽  
Comparative Approach ◽  
Whole Genome ◽  
Animal Evolution ◽  
Whole Genome Duplications ◽  
Genome Duplications ◽  
Horseshoe Crabs

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.

scholarly journals Widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates

2020 ◽  
Author(s):  
Amber Harper ◽  
Luis Baudouin Gonzalez ◽  
Anna Schönauer ◽  
Michael Seiter ◽  
Michaela Holzem ◽  
...  
Keyword(s):  
Genetic Material ◽  
Gene Families ◽  
Comparative Approach ◽  
Whole Genome ◽  
Developmental Gene ◽  
Spider Species ◽  
Transcriptomic Data ◽  
Whole Genome Duplications ◽  
Genome Duplications ◽  
Horseshoe Crabs

AbstractWhole genome duplications (WGD) have occurred multiple times in the evolution of animals, including in the lineages leading to vertebrates, teleosts, horseshoe crabs and arachnopulmonates. These dramatic genomic events initially produce a wealth of new genetic material, which is generally followed by extensive gene loss. It appears that developmental genes such as homeobox genes, signalling pathway components and microRNAs, however, tend to be more frequently retained in duplicate following WGD (ohnologs). These not only provide the best evidence for the occurrence of WGD, but an opportunity to study its evolutionary implications. Although these genes are relatively well studied in the context of vertebrate WGD, genomic and transcriptomic data for independent comparison in other groups are scarce, with patchy sampling of only two of the five extant arachnopulmonate orders. To improve our knowledge of developmental gene repertoires, and their evolution since the arachnopulmonate WGD, we sequenced embryonic transcriptomes from two additional spider species and two whip spider species and surveyed them for three important gene families: Hox, Wnt and frizzled. We report extensive retention of ohnologs in all four species, further supporting the arachnopulmonate WGD hypothesis. Thanks to improved sampling we were able to identify patterns of likely ohnolog retention and loss within spiders, including apparent differences between major clades. The two amblypygid species have larger ohnolog repertoires of these genes than both spiders and scorpions; including the first reported duplicated Wnt1/wg, the first Wnt10 recovered in an arachnid, and broad retention of frizzled genes. These insights shed light on the evolution of the enigmatic whip spiders, highlight the importance of the comparative approach within lineages, and provide substantial new transcriptomic data for future study.

scholarly journals Horseshoe crab genomes reveal the evolution of genes and microRNAs after three rounds of whole genome duplication

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Wenyan Nong ◽  
Zhe Qu ◽  
Yiqian Li ◽  
Tom Barton-Owen ◽  
Annette Y. P. Wong ◽  
...  
Keyword(s):  
Whole Genome Duplication ◽  
Horseshoe Crab ◽  
Genome Duplication ◽  
Population Level ◽  
Gene Families ◽  
Whole Genome ◽  
Horseshoe Crabs ◽  
The Individual ◽  
Evolutionary Consequences ◽  
High Quality Genome

AbstractWhole genome duplication (WGD) has occurred in relatively few sexually reproducing invertebrates. Consequently, the WGD that occurred in the common ancestor of horseshoe crabs ~135 million years ago provides a rare opportunity to decipher the evolutionary consequences of a duplicated invertebrate genome. Here, we present a high-quality genome assembly for the mangrove horseshoe crab Carcinoscorpius rotundicauda (1.7 Gb, N50 = 90.2 Mb, with 89.8% sequences anchored to 16 pseudomolecules, 2n = 32), and a resequenced genome of the tri-spine horseshoe crab Tachypleus tridentatus (1.7 Gb, N50 = 109.7 Mb). Analyses of gene families, microRNAs, and synteny show that horseshoe crabs have undergone three rounds (3R) of WGD. Comparison of C. rotundicauda and T. tridentatus genomes from populations from several geographic locations further elucidates the diverse fates of both coding and noncoding genes. Together, the present study represents a cornerstone for improving our understanding of invertebrate WGD events on the evolutionary fates of genes and microRNAs, at both the individual and population level. We also provide improved genomic resources for horseshoe crabs, of applied value for breeding programs and conservation of this fascinating and unusual invertebrate lineage.

scholarly journals Genetic drift dominates genome-wide regulatory evolution following an ancient whole genome duplication in Atlantic salmon

2020 ◽  
Author(s):  
Jukka-Pekka Verta ◽  
Henry Barton ◽  
Victoria Pritchard ◽  
Craig Primmer
Keyword(s):  
Atlantic Salmon ◽  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Regulatory Elements ◽  
Functional Redundancy ◽  
Neutral Evolution ◽  
Whole Genome ◽  
Regulatory Evolution ◽  
Whole Genome Duplications ◽  
Genome Duplications

AbstractWhole genome duplications (WGD) have been considered as springboards that potentiate lineage diversification through increasing functional redundancy. Divergence in gene regulatory elements is a central mechanism for evolutionary diversification, yet the patterns and processes governing regulatory divergence following events that lead to massive functional redundancy, such as WGD, remain largely unknown. We studied the patterns of divergence and strength of natural selection on regulatory elements in the Atlantic salmon (Salmo salar) genome, which has undergone WGD 100-80 Mya. Using ChIPmentation, we first show that H3K27ac, a histone modification typical to enhancers and promoters, is associated with genic regions, tissue specific transcription factor binding motifs, and with gene transcription levels in immature testes. Divergence in transcription between duplicated genes from WGD (ohnologs) correlated with difference in the number of proximal regulatory elements, but not with promoter elements, suggesting that functional divergence between ohnologs after WGD is mainly driven by enhancers. By comparing H3K27ac regions between duplicated genome blocks, we further show that a longer polyploid state post-WGD has constrained asymmetric regulatory evolution. Patterns of genetic diversity across natural populations inferred from re-sequencing indicate that recent evolutionary pressures on H3K27ac regions are dominated by largely neutral evolution. In sum, our results suggest that post-WGD functional redundancy in regulatory elements continues to have an impact on the evolution of the salmon genome, promoting largely neutral evolution of regulatory elements despite their association with transcription levels. These results highlight a case where genome-wide regulatory evolution following an ancient WGD is dominated by genetic drift.Significance statementRegulatory evolution following whole genome duplications (WGD) has been investigated at the gene expression level, but studies of the regulatory elements that control expression have been lacking. By investigating regulatory elements in the Atlantic salmon genome, which has undergone a whole genome duplication 100-80 million years ago, we discovered patterns suggesting that neutral divergence is the prevalent mode of regulatory element evolution post-WGD. Our results suggest mechanisms for explaining the prevalence of asymmetric gene expression evolution following whole genome duplication, as well as the mismatch between evolutionary rates in enhancers versus that of promoters.

scholarly journals Selective constraints on coding sequences of nervous system genes are a major determinant of duplicate gene retention in vertebrates

2016 ◽  
Author(s):  
Julien Roux ◽  
Jialin Liu ◽  
Marc Robinson-Rechavi
Keyword(s):  
Nervous System ◽  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Expression Patterns ◽  
Enrichment Analysis ◽  
Duplicate Genes ◽  
Whole Genome ◽  
Coding Sequences ◽  
Whole Genome Duplications ◽  
Genome Duplications

AbstractThe evolutionary history of vertebrates is marked by three ancient whole-genome duplications: two successive rounds in the ancestor of vertebrates, and a third one specific to teleost fishes. Biased loss of most duplicates enriched the genome for specific genes, such as slow evolving genes, but this selective retention process is not well understood. To understand what drives the long-term preservation of duplicate genes, we characterized duplicated genes in terms of their expression patterns. We used a new method of expression enrichment analysis, TopAnat, applied to in situ hybridization data from thousands of genes from zebrafish and mouse. We showed that the presence of expression in the nervous system is a good predictor of a higher rate of retention of duplicate genes after whole-genome duplication. Further analyses suggest that purifying selection against the toxic effects of misfolded or misinteracting proteins, which is particularly strong in non-renewing neural tissues, likely constrains the evolution of coding sequences of nervous system genes, leading indirectly to the preservation of duplicate genes after whole-genome duplication. Whole-genome duplications thus greatly contributed to the expansion of the toolkit of genes available for the evolution of profound novelties of the nervous system at the base of the vertebrate radiation.

scholarly journals Horseshoe crab genomes reveal the evolutionary fates of genes and microRNAs after three rounds (3R) of whole genome duplication

2020 ◽  
Author(s):  
Wenyan Nong ◽  
Zhe Qu ◽  
Yiqian Li ◽  
Tom Barton-Owen ◽  
Annette Y.P. Wong ◽  
...  
Keyword(s):  
Whole Genome Duplication ◽  
Horseshoe Crab ◽  
Genome Duplication ◽  
Gene Families ◽  
Whole Genome ◽  
Breeding Programs ◽  
Horseshoe Crabs ◽  
The Common ◽  
Evolutionary Consequences ◽  
High Quality Genome

AbstractWhole genome duplication (WGD) has occurred in relatively few sexually reproducing invertebrates. Consequently, the WGD that occurred in the common ancestor of horseshoe crabs ~135 million years ago provides a rare opportunity to decipher the evolutionary consequences of a duplicated invertebrate genome. Here, we present a high-quality genome assembly for the mangrove horseshoe crab Carcinoscorpius rotundicauda (1.7Gb, N50 = 90.2Mb, with 89.8% sequences anchored to 16 pseudomolecules, 2n = 32), and a resequenced genome of the tri-spine horseshoe crab Tachypleus tridentatus (1.7Gb, N50 = 109.7Mb). Analyses of gene families, microRNAs, and synteny show that horseshoe crabs have undergone three rounds (3R) of WGD, and that these WGD events are shared with spiders. Comparison of the genomes of C. rotundicauda and T. tridentatus populations from several geographic locations further elucidates the diverse fates of both coding and noncoding genes. Together, the present study represents a cornerstone for a better understanding of the consequences of invertebrate WGD events on evolutionary fates of genes and microRNAs at individual and population levels, and highlights the genetic diversity with practical values for breeding programs and conservation of horseshoe crabs.

Phylogenetic Analysis of T-Box Genes Demonstrates the Importance of Amphioxus for Understanding Evolution of the Vertebrate Genome

Genetics ◽  
2000 ◽  
Vol 156 (3) ◽  
pp. 1249-1257
Author(s):  
Ilya Ruvinsky ◽  
Lee M Silver ◽  
Jeremy J Gibson-Brown
Keyword(s):  
Phylogenetic Analysis ◽  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Gene Families ◽  
Vertebrate Evolution ◽  
Whole Genome ◽  
Vertebrate Genome ◽  
T Box ◽  
Genetic Complexity ◽  
History Of

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.

scholarly journals Giant African snail genomes provide insights into molluscan whole-genome duplication and aquatic-terrestrial transition

2020 ◽  
Author(s):  
Conghui Liu ◽  
Yuwei Ren ◽  
Zaiyuan Li ◽  
Qi Hu ◽  
Lijuan Yin ◽  
...  
Keyword(s):  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Terrestrial Ecosystems ◽  
Gene Families ◽  
Gene Clusters ◽  
Immune Defense ◽  
Whole Genome ◽  
Genomic Plasticity ◽  
Ecological Adaptability ◽  
Chromosome Level

AbstractWhole-genome duplication (WGD) has been observed across a wide variety of eukaryotic groups, contributing to evolutionary diversity and environmental adaptability. Mollusks are the second largest group of animals, and are among the organisms that have successfully adapted to the nonmarine realm through aquatic-terrestrial (A-T) transition, and no comprehensive research on WGD has been reported in this group. To explore WGD and the A-T transition in Mollusca, we assembled a chromosome-level reference genome for the giant African snail Achatina immaculata, a global invasive species, and compared the genomes of two giant African snails (A. immaculata and Achatina fulica) to the other available mollusk genomes. The chromosome-level macrosynteny, colinearity blocks, Ks peak and Hox gene clusters collectively suggested the occurrence of a WGD event shared by A. immaculata and A. fulica. The estimated timing of this WGD event (∼70 MYA) was close to the speciation age of the Sigmurethra-Orthurethra (within Stylommatophora) lineage and the Cretaceous-Tertiary (K-T) mass extinction, indicating that the WGD reported herein may have been a common event shared by all Sigmurethra-Orthurethra species and could have conferred ecological adaptability and genomic plasticity allowing the survival of the K-T extinction. Based on macrosynteny, we deduced an ancestral karyotype containing 8 conserved clusters for the Gastropoda-Bivalvia lineage. To reveal the mechanism of WGD in shaping adaptability to terrestrial ecosystems, we investigated gene families related to the respiration, aestivation and immune defense of giant African snails. Several mucus-related gene families expanded early in the Stylommatophora lineage, functioning in water retention, immune defense and wound healing. The hemocyanins, PCK and FBP families were doubled and retained after WGD, enhancing the capacity for gas exchange and glucose homeostasis in aestivation. After the WGD, zinc metalloproteinase genes were highly tandemly duplicated to protect tissue against ROS damage. This evidence collectively suggests that although the WGD may not have been the direct driver of the A-T transition, it provided an important legacy for the terrestrial adaptation of the giant African snail.

scholarly journals Synteny-Guided Resolution of Gene Trees Clarifies the Functional Impact of Whole-Genome Duplications

2020 ◽  
Vol 37 (11) ◽  
pp. 3324-3337
Author(s):  
Elise Parey ◽  
Alexandra Louis ◽  
Cédric Cabau ◽  
Yann Guiguen ◽  
Hugues Roest Crollius ◽  
...  
Keyword(s):  
Gene Families ◽  
Sequence Evolution ◽  
Whole Genome ◽  
Gene Trees ◽  
Ensembl Database ◽  
Whole Genome Duplications ◽  
Gene Copies ◽  
Genome Duplications ◽  
Phenotypic Robustness ◽  
New Gene

Abstract Whole-genome duplications (WGDs) have major impacts on the evolution of species, as they produce new gene copies contributing substantially to adaptation, isolation, phenotypic robustness, and evolvability. They result in large, complex gene families with recurrent gene losses in descendant species that sequence-based phylogenetic methods fail to reconstruct accurately. As a result, orthologs and paralogs are difficult to identify reliably in WGD-descended species, which hinders the exploration of functional consequences of WGDs. Here, we present Synteny-guided CORrection of Paralogies and Orthologies (SCORPiOs), a novel method to reconstruct gene phylogenies in the context of a known WGD event. WGDs generate large duplicated syntenic regions, which SCORPiOs systematically leverages as a complement to sequence evolution to infer the evolutionary history of genes. We applied SCORPiOs to the 320-My-old WGD at the origin of teleost fish. We find that almost one in four teleost gene phylogenies in the Ensembl database (3,394) are inconsistent with their syntenic contexts. For 70% of these gene families (2,387), we were able to propose an improved phylogenetic tree consistent with both the molecular substitution distances and the local syntenic information. We show that these synteny-guided phylogenies are more congruent with the species tree, with sequence evolution and with expected expression conservation patterns than those produced by state-of-the-art methods. Finally, we show that synteny-guided gene trees emphasize contributions of WGD paralogs to evolutionary innovations in the teleost clade.

scholarly journals OHNOLOGS v2: a comprehensive resource for the genes retained from whole genome duplication in vertebrates

2019 ◽  
Author(s):  
Param Priya Singh ◽  
Hervé Isambert
Keyword(s):  
Teleost Fish ◽  
Whole Genome Duplication ◽  
Genome Duplication ◽  
Genetic Diseases ◽  
Genomic Analysis ◽  
Biased Sampling ◽  
Whole Genome ◽  
Genome Duplications ◽  
Evolutionary Genomic ◽  
The Impact

Abstract All vertebrates including human have evolved from an ancestor that underwent two rounds of whole genome duplication (2R-WGD). In addition, teleost fish underwent an additional third round of genome duplication (3R-WGD). The genes retained from these genome duplications, so-called ohnologs, have been instrumental in the evolution of vertebrate complexity, development and susceptibility to genetic diseases. However, the identification of vertebrate ohnologs has been challenging, due to lineage specific genome rearrangements since 2R- and 3R-WGD. We previously identified vertebrate ohnologs using a novel synteny comparison across multiple genomes. Here, we refine and apply this approach on 27 vertebrate genomes to identify ohnologs from both 2R- and 3R-WGD, while taking into account the phylogenetically biased sampling of available species. We assemble vertebrate ohnolog pairs and families in an expanded OHNOLOGS v2 database. We find that teleost fish have retained more 2R-WGD ohnologs than mammals and sauropsids, and that these 2R-ohnologs have retained significantly more ohnologs from the subsequent 3R-WGD than genes without 2R-ohnologs. Interestingly, species with fewer extant genes, such as sauropsids, have retained similar or higher proportions of ohnologs. OHNOLOGS v2 should allow deeper evolutionary genomic analysis of the impact of WGD on vertebrates and can be freely accessed at http://ohnologs.curie.fr.

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