scholarly journals The grayling genome reveals selection on gene expression regulation after whole genome duplication

2017 ◽  
Author(s):  
Srinidhi Varadharajan ◽  
Simen R. Sandve ◽  
Gareth B. Gillard ◽  
Ole K. Tørresen ◽  
Teshome D. Mulugeta ◽  
...  

AbstractWhole genome duplication (WGD) has been a major evolutionary driver of increased genomic complexity in vertebrates. One such event occurred in the salmonid family ~80 million years ago (Ss4R) giving rise to a plethora of structural and regulatory duplicate-driven divergence, making salmonids an exemplary system to investigate the evolutionary consequences of WGD. Here, we present a draft genome assembly of European grayling (Thymallus thymallus) and use this in a comparative framework to study evolution of gene regulation following WGD. Among the Ss4R duplicates identified in European grayling and Atlantic salmon (Salmo salar), one third reflect non-neutral tissue expression evolution, with strong purifying selection, maintained over ~50 million years. Of these, the majority reflect conserved tissue regulation under strong selective constraints related to brain and neural-related functions, as well as higher-order protein-protein interactions. A small subset of the duplicates has evolved tissue regulatory expression divergence in a common ancestor, which have been subsequently conserved in both lineages, suggestive of adaptive divergence following WGD. These candidates for adaptive tissue expression divergence have elevated rates of protein coding- and promoter-sequence evolution and are enriched for immune- and lipid metabolism ontology terms. Lastly, lineage-specific duplicate divergence points towards underlying differences in adaptive pressures on expression regulation in the non-anadromous grayling versus the anadromous Atlantic salmon.Our findings enhance our understanding of the role of WGD in genome evolution and highlights cases of regulatory divergence of Ss4R duplicates, possibly related to a niche shift in early salmonid evolution.

2017 ◽  
Author(s):  
Simen R. Sandve ◽  
Rori V. Rohlfs ◽  
Torgeir R. Hvidsten

The question of what is the predominant evolutionary fate of genes after duplication events has been hotly debated for decades1,2. Two recently published articles in Nature (Lien et al.3) and Nature Genetics (Braasch et al.4) investigated the regulatory fate of gene duplicates after the salmonid-specific (Ss4R) and teleost specific (Ts3R) whole genome duplication (WGD) events, respectively. Both studies relied on tissue expression atlases for estimating regulatory divergence and used closely related unduplicated sister taxa (i.e. Northern pike and the spotted gar, respectively) as proxies for the ancestral expression state. Surprisingly, the two studies reach very different conclusions about the evolutionary mechanisms impacting gene expression after WGD. Braasch et al.4 concluded that the expression divergence was consistent with partitioning of tissue regulation between duplicates (subfunctionalization), while Lien et al.3 concluded that most divergence in tissue regulation were consistent with one copy maintaining ancestral tissue regulation while the other having diverged (in line with neofunctionalization). Here we show that this striking discrepancy in the conclusions of the two studies is a consequence of the data analysis approaches used, and is not related to underlying differences in the data.


Gene ◽  
2016 ◽  
Vol 591 (1) ◽  
pp. 34-42 ◽  
Author(s):  
Greta Carmona-Antoñanzas ◽  
Xiaozhong Zheng ◽  
Douglas R. Tocher ◽  
Michael J. Leaver

2020 ◽  
Author(s):  
Jukka-Pekka Verta ◽  
Henry Barton ◽  
Victoria Pritchard ◽  
Craig Primmer

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.


2021 ◽  
Author(s):  
Guilherme Gainett ◽  
Vanessa L. González ◽  
Jesús A. Ballesteros ◽  
Emily V. W. Setton ◽  
Caitlin M. Baker ◽  
...  

AbstractChelicerates exhibit dynamic evolution of genome architecture, with multiple whole genome duplication events affecting groups like spiders, scorpions, and horseshoe crabs. Yet, genomes remain unavailable for several chelicerate orders, such as Opiliones (harvestmen), which has hindered comparative genomics and developmental genetics across arachnids. We assembled a draft genome of the daddy-long-legs Phalangium opilio, which revealed no signal of whole genome duplication. To test the hypothesis that single-copy Hox genes of the harvestman exhibit broader functions than subfunctionalized spider paralogs, we performed RNA interference against Deformed in P. opilio. Knockdown of Deformed incurred homeotic transformation of the two anterior pairs of walking legs into pedipalpal identity; by comparison, knockdown of the spatially restricted paralog Deformed-A in the spider affects only the first walking leg. To investigate the genetic basis for leg elongation and tarsomere patterning, we identified and interrogated the function of an Epidermal growth factor receptor (Egfr) homolog. Knockdown of Egfr incurred shortened appendages and the loss of distal leg structures. The overlapping phenotypic spectra of Egfr knockdown experiments in the harvestman and multiple insect models are striking because tarsomeres have evolved independently in these groups. Our results suggest a conserved role for Egfr in patterning distal leg structures across arthropods, as well as cooption of EGFR signaling in tarsomere patterning in both insects and arachnids. The establishment of genomic resources for P. opilio, together with functional investigations of appendage fate specification and distal patterning mechanisms, are key steps in understanding how daddy-long-legs make their long legs.


2021 ◽  
Vol 8 (1) ◽  
Author(s):  
Jinfang Zheng ◽  
Lyndel W. Meinhardt ◽  
Ricardo Goenaga ◽  
Dapeng Zhang ◽  
Yanbin Yin

AbstractDragon fruits are tropical fruits economically important for agricultural industries. As members of the family of Cactaceae, they have evolved to adapt to the arid environment. Here we report the draft genome of Hylocereus undatus, commercially known as the white-fleshed dragon fruit. The chromosomal level genome assembly contains 11 longest scaffolds corresponding to the 11 chromosomes of H. undatus. Genome annotation of H. undatus found ~29,000 protein-coding genes, similar to Carnegiea gigantea (saguaro). Whole-genome duplication (WGD) analysis revealed a WGD event in the last common ancestor of Cactaceae followed by extensive genome rearrangements. The divergence time between H. undatus and C. gigantea was estimated to be 9.18 MYA. Functional enrichment analysis of orthologous gene clusters (OGCs) in six Cactaceae plants found significantly enriched OGCs in drought resistance. Fruit flavor-related functions were overrepresented in OGCs that are significantly expanded in H. undatus. The H. undatus draft genome also enabled the discovery of carbohydrate and plant cell wall-related functional enrichment in dragon fruits treated with trypsin for a longer storage time. Lastly, genes of the betacyanin (a red-violet pigment and antioxidant with a very high concentration in dragon fruits) biosynthetic pathway were found to be co-localized on a 12 Mb region of one chromosome. The consequence may be a higher efficiency of betacyanin biosynthesis, which will need experimental validation in the future. The H. undatus draft genome will be a great resource to study various cactus plants.


2018 ◽  
Vol 10 (10) ◽  
pp. 2785-2800 ◽  
Author(s):  
Srinidhi Varadharajan ◽  
Simen R Sandve ◽  
Gareth B Gillard ◽  
Ole K Tørresen ◽  
Teshome D Mulugeta ◽  
...  

Author(s):  
Yann Guiguen ◽  
Jeremy Pasquier ◽  
Alexis Fostier ◽  
Julien Bobe

AbstractSex hormone-binding globulin (Shbg) is an important vertebrate blood carrier protein synthetized in the liver and involved in the transport and local regulation of sex steroids in target tissues. A novel shbg gene (shbgb) with a predominant ovarian expression was recently characterized. Being initially found only in salmonids, this shbgb was originally thought to result from the Salmonid-specific whole genome duplication. Using updated transcriptomic and genomic resources we identified Shbgb orthologs in non-salmonid teleosts (European eel, arowana), holosteans (spotted gar, bowfin), polypteriformes (reedfish), agnatha (sea lamprey) and in amphibians, and found that the classical Shbg gene (Shbga) displays a predominant hepatic expression whereas Shbgb has a predominant gonadal expression. Together, these results indicate that these two Shgb genes most likely originate from a whole genome duplication event at the root of vertebrate evolution, followed by numerous and independent losses and by tissue expression specialization of Shbga and Shbgb paralogs.HighlightsPhylogeny, synteny and expression analyses shed new light on Shbg evolution in vertebrates.Shbg diversity originates from a duplication event at the root of vertebrate evolution.This duplication was followed by many independent losses of Shbg paralogs in vertebrates.Shbg paralogs have acquired different tissue expression patterns.


2017 ◽  
Author(s):  
Yang Jin ◽  
Rolf Erik Olsen ◽  
Mari-Ann Østensen ◽  
Gareth Benjamin Gillard ◽  
Sven Arild Korsvoll ◽  
...  

AbstractBackgroundIt has been suggested that the high phospholipid (PL) requirement in Atlantic salmon (Salmo salar) fry is due to insufficient intestinal de-novo synthesis causing low lipoprotein (LP) production and reduced transport capacity of dietary lipids. However, there has not been performed any in-depth ontological analysis of intestinal PL and LP synthesis with development of salmon. Therefore in this paper we used RNA-seq technology to test the hypothesis that the high PL requirement in salmon fry was associated with undeveloped PL synthesis and LP formation pathways in intestine. There was a special focus on the understanding homologous genes, especially from salmonid-specific fourth vertebrate whole-genome duplication (Ss4R), contribution to salmonid specific features of regulation of PL metabolic pathways. The study was performed in stomach, pyloric caeca and hindgut at 0.16g (1 day before first-feeding), 2.5g and 10g of salmon.ResultsIn general, we found an up-regulation of de-novo phosphatidylcholine (PtdCho) synthesis, phosphatidylethanolamine (PtdEtn) and LP formation pathways in pyloric caeca of salmon between 0.16g and 10g. Thirteen genes in these pathways were highly (q<0.05) up-regulated in 2.5g salmon compared to 0.16g, while only five more significant (q<0.05) genes were found when the fish grew up to 10g. Different homologous genes were found dominating in stomach, pyloric caeca and hindgut. However, the expression of dominating genes in PL and LP synthesis pathways was much higher in pyloric caeca than stomach and hindgut. Salmon-specific homologous (Ss4R) genes had similar expression during development, while other homologs had more diverged expression.ConclusionsAn increasing capacity for PL synthesis and LP formation was confirmed in pyloric caeca. The up-regulation of the de-novo PtdCho pathway confirms that the salmon fry have increasing requirement for dietary PtdCho compared to adult. The similar expressions between Ss4R homologous genes suggest that the functional divergence of these genes was incomplete compared to homologs derived from other whole genome duplication. The results of the present study have provided new information on the molecular mechanisms of phospholipid synthesis and lipoprotein formation in fish.


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