Evolution of the Parvalbumin Genes in Teleost Fishes after the Whole-Genome Duplication

Parvalbumin is considered a major fish allergen. Here, we report the molecular evolution of the parvalbumin genes in bony fishes based on 19 whole genomes and 70 transcriptomes. We found unexpectedly high parvalbumin diversity in teleosts; three main gene types (pvalb-α, pvalb-β1, and pvalb-β2, including oncomodulins) originated at the onset of vertebrates. Teleosts have further multiplied the parvalbumin gene repertoire up to nine ancestral copies—two copies of pvalb-α, two copies of pvalb-β1, and five copies of pvalb-β2. This gene diversity is a result of teleost-specific whole-genome duplication. Two conserved parvalbumin genomic clusters carry pvalb-β1 and β2 copies, whereas pvalb-α genes are located separately in different linkage groups. Further, we investigated parvalbumin gene expression in 17 tissues of the common carp (Cyprinus carpio), a species with 21 parvalbumin genes in its genome. Two pvalb-α and eight pvalb-β2 copies are highly expressed in the muscle, while two alternative pvalb-α copies show expression in the brain and the testes, and pvalb-β1 is dominant in the retina and the kidney. The recent pairs of muscular pvalb-β2 genes show differential expression in this species. We provide robust genomic evidence of the complex evolution of the parvalbumin genes in fishes.

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Evolution and Expression of the Immune System of a Facultatively Anadromous Salmonid

Frontiers in Immunology ◽

10.3389/fimmu.2021.568729 ◽

2021 ◽

Vol 12 ◽

Author(s):

Thomas J. Colgan ◽

Peter A. Moran ◽

Louise C. Archer ◽

Robert Wynne ◽

Stephen A. Hutton ◽

...

Keyword(s):

Life Cycle ◽

Immune System ◽

Brown Trout ◽

Salmo Trutta ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Immune Gene ◽

Whole Genome ◽

Gene Repertoire ◽

Immune Genes

Vertebrates have evolved a complex immune system required for the identification of and coordinated response to harmful pathogens. Migratory species spend periods of their life-cycle in more than one environment, and their immune system consequently faces a greater diversity of pathogens residing in different environments. In facultatively anadromous salmonids, individuals may spend parts of their life-cycle in freshwater and marine environments. For species such as the brown trout Salmo trutta, sexes differ in their life-histories with females more likely to migrate to sea while males are more likely to stay and complete their life-cycle in their natal river. Salmonids have also undergone a lineage-specific whole genome duplication event, which may provide novel immune innovations but our current understanding of the differences in salmonid immune expression between the sexes is limited. We characterized the brown trout immune gene repertoire, identifying a number of canonical immune genes in non-salmonid teleosts to be duplicated in S. trutta, with genes involved in innate and adaptive immunity. Through genome-wide transcriptional profiling (“RNA-seq”) of male and female livers to investigate sex differences in gene expression amplitude and alternative splicing, we identified immune genes as being generally male-biased in expression. Our study provides important insights into the evolutionary consequences of whole genome duplication events on the salmonid immune gene repertoire and how the sexes differ in constitutive immune expression.

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An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth

PLoS ONE ◽

10.1371/journal.pone.0255006 ◽

2021 ◽

Vol 16 (7) ◽

pp. e0255006

Author(s):

Bruno Oliveira Silva Duran ◽

Daniel Garcia de la serrana ◽

Bruna Tereza Thomazini Zanella ◽

Erika Stefani Perez ◽

Edson Assunção Mareco ◽

...

Keyword(s):

Skeletal Muscle ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Muscle Growth ◽

Great Majority ◽

Molecular Networks ◽

Whole Genome ◽

Gene Repertoire ◽

Duplicated Genes ◽

The Impact

Fish muscle growth is a complex process regulated by multiple pathways, resulting on the net accumulation of proteins and the activation of myogenic progenitor cells. Around 350–320 million years ago, teleost fish went through a specific whole genome duplication (WGD) that expanded the existent gene repertoire. Duplicated genes can be retained by different molecular mechanisms such as subfunctionalization, neofunctionalization or redundancy, each one with different functional implications. While the great majority of ohnolog genes have been identified in the teleost genomes, the effect of gene duplication in the fish physiology is still not well characterized. In the present study we studied the effect of WGD on the transcription of the duplicated components controlling muscle growth. We compared the expression of lineage-specific ohnologs related to myogenesis and protein balance in the fast-skeletal muscle of pacus (Piaractus mesopotamicus—Ostariophysi) and Nile tilapias (Oreochromis niloticus—Acanthopterygii) fasted for 4 days and refed for 3 days. We studied the expression of 20 ohnologs and found that in the great majority of cases, duplicated genes had similar expression profiles in response to fasting and refeeding, indicating that their functions during growth have been conserved during the period after the WGD. Our results suggest that redundancy might play a more important role in the retention of ohnologs of regulatory pathways than initially thought. Also, comparison to non-duplicated orthologs showed that it might not be uncommon for the duplicated genes to gain or loss new regulatory elements simultaneously. Overall, several of duplicated ohnologs have similar transcription profiles in response to pro-growth signals suggesting that evolution tends to conserve ohnolog regulation during muscle development and that in the majority of ohnologs related to muscle growth their functions might be very similar.

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Visual pigment evolution in Characiformes: the dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning

10.1101/695544 ◽

2019 ◽

Cited By ~ 1

Author(s):

Daniel Escobar-Camacho ◽

Karen L. Carleton ◽

Devika W. Narain ◽

Michele E.R. Pierotti

Keyword(s):

Visual System ◽

Gene Conversion ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Opsin Gene ◽

Whole Genome ◽

Gene Repertoire ◽

Spectral Tuning ◽

Diverse Range ◽

System Evolution

AbstractVision represents an excellent model for studying adaptation, given the genotype-to-phenotype-map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we characterized the visual system of Neotropical Characiformes, which is the result of several spectral tuning mechanisms acting in concert including gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1/A2-chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform’s entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS- and RH1-duplicates originated from a teleost specific whole-genome duplication as well as characiform-specific duplication events. Both LWS-opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS-paralogs has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. In addition, characiforms exhibited species-specific differences in opsin expression. Finally, we found interspecific and intraspecific variation in the use of A1/A2-chromophores correlating with the light environment. These multiple mechanisms may be a result of the highly diverse visual environments where Characiformes have evolved.

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Faculty Opinions recommendation of Reciprocal gene loss following experimental whole-genome duplication causes reproductive isolation in yeast.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.10069956.10824063 ◽

2011 ◽

Author(s):

Santiago F Elena ◽

Stéphanie Bedhomme

Keyword(s):

Reproductive Isolation ◽

Whole Genome Duplication ◽

Gene Loss ◽

Genome Duplication ◽

Whole Genome

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

Genetics ◽

10.1093/genetics/156.3.1249 ◽

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.

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Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

G3 Genes|Genome|Genetics ◽

10.1534/g3.114.012294 ◽

2014 ◽

Vol 4 (9) ◽

pp. 1717-1730 ◽

Cited By ~ 37

Author(s):

M. Kodama ◽

M. S. O. Brieuc ◽

R. H. Devlin ◽

J. J. Hard ◽

K. A. Naish

Keyword(s):

Comparative Mapping ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Coho Salmon ◽

Chromosomal Rearrangements ◽

Oncorhynchus Kisutch ◽

Duplication Event ◽

Whole Genome ◽

Genome Duplication Event ◽

Whole Genome Duplication Event

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Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication

Genome Biology ◽

10.1186/s13059-021-02323-0 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Gareth B. Gillard ◽

Lars Grønvold ◽

Line L. Røsæg ◽

Matilde Mengkrog Holen ◽

Øystein Monsen ◽

...

Keyword(s):

Genome Evolution ◽

Whole Genome Duplication ◽

Genome Stability ◽

Genome Duplication ◽

Gene Dosage ◽

Whole Genome ◽

Specific Expression ◽

Tissue Specific ◽

Genome Doubling ◽

Expression Evolution

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.

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Chromosome-level genome assembly of Ophiorrhiza pumila reveals the evolution of camptothecin biosynthesis

Nature Communications ◽

10.1038/s41467-020-20508-2 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Amit Rai ◽

Hideki Hirakawa ◽

Ryo Nakabayashi ◽

Shinji Kikuchi ◽

Koki Hayashi ◽

...

Keyword(s):

Genome Assembly ◽

Whole Genome Duplication ◽

Experimental Validation ◽

Genome Duplication ◽

Indole Alkaloids ◽

Whole Genome ◽

Comparative Genome Analysis ◽

Plant Genomes ◽

Genome Triplication ◽

Chromosome Level

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.

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