scholarly journals Sex chromosome dosage compensation in Heliconius butterflies: global yet still incomplete?

2015 ◽  
Author(s):  
James R Walters ◽  
Thomas J Hardcastle ◽  
Chris Jiggins
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosome ◽  
Gene Dosage ◽  
Dosage Effect ◽  
Epigenetic Mechanism ◽  
Z Chromosome ◽  
Specific Gene ◽  
Dosage Effects ◽  
Heliconius Butterflies ◽  
The Impact

The evolution of heterogametic sex chromosome is often ? but not always ? accompanied by the evolution of dosage compensating mechanisms that mitigate the impact of sex-specific gene dosage on levels of gene expression. One emerging view of this process is that such mechanisms may only evolve in male-heterogametic (XY) species but not in female-heterogametic (ZW) species, which will consequently exhibit ?incomplete? sex chromosome dosage compensation. However, some recent results from moths suggest that Lepidoptera (moths and butterflies) may prove to be an exception to this prediction. Here we report an analysis of sex chromosome dosage compensation in Heliconius butterflies, sampling multiple individuals for several different adult tissues (head, abdomen, leg, mouth, and antennae). Methodologically, we introduce a novel application of linear mixed-effects models to assess dosage compensation, offering a unified statistical framework that can estimate effects specific to chromosome, to sex, and their interactions (i.e., a dosage effect). Our results show substantially reduced Z-linked expression relative to autosomes in both sexes, as previously observed in bombycoid moths. This observation is consistent with an increasing body of evidence that at least some species of moths and butterflies possess an epigenetic sex chromosome dosage compensating mechanism that operates by reducing Z chromosome expression in males. However, this mechanism appears to be imperfect in Heliconius, resulting in a modest dosage effect that produces an average 5-20% male-bias on the Z chromosome, depending on the tissue. Strong sex chromosome dosage effects have been previously in a pyralid moth. Thus our results reflect a mixture of previous patterns reported for Lepidoptera and bisect the emerging view that female-heterogametic ZW taxa have incomplete dosage compensation because they lack a chromosome-wide epigenetic mechanism mediating sex chromosome dosage compensation. In the case of Heliconius, sex chromosome dosage effects persist apparently despite such a mechanism. We also analyze chromosomal distributions of sex-biased genes and show an excess of male-biased and a dearth of female-biased genes on the Z chromosome relative to autosomes, consistent with predictions of sexually antagonistic evolution.

scholarly journals Clinical Epigenetic Therapies Disrupt Sex Chromosome Dosage Compensation in Human Female Cells

2018 ◽  
Vol 2 (1) ◽  
pp. 2-7 ◽  
Author(s):  
Agnieszka I. Laskowski ◽  
Danielle A. Fanslow ◽  
Erica D. Smith ◽  
Steven T. Kosak
Keyword(s):  
Small Molecule ◽  
X Chromosome ◽  
Dosage Compensation ◽  
Sex Chromosome ◽  
Gene Dosage ◽  
X Inactivation ◽  
Epigenetic Mechanism ◽  
Human Female ◽  
Healthy Human ◽  
Inactivation Center

Sex chromosome gene dosage compensation is required to ensure equivalent levels of X-linked gene expression between males (46, XY) and females (46, XX). To achieve similar expression, X-chromosome inactivation (XCI) is initiated in female cells during early stages of embryogenesis. Within each cell, either the maternal or paternal X chromosome is selected for whole chromosome transcriptional silencing, which is initiated and maintained by epigenetic and chromatin conformation mechanisms. With the emergence of small-molecule epigenetic inhibitors for the treatment of disease, such as cancer, the epigenetic mechanism underlying XCI may be inadvertently targeted. Here, we test 2 small-molecule epigenetic inhibitors being used clinically, GSK126 (a histone H3 lysine 27 methyltransferase inhibitor) and suberoylanilide hydroxamic acid (a histone deacetylase inhibitor), on their effects of the inactive X (Xi) in healthy human female fibroblasts. The combination of these modifiers, at subcancer therapeutic levels, leads to the inability to detect the repressive H3K27me3 modification characteristic of XCI in the majority of the cells. Importantly, genes positioned near the X-inactivation center ( Xic), where inactivation is initiated, exhibit robust expression with treatment of the inhibitors, while genes located near the distal ends of the X chromosome intriguingly exhibit significant downregulation. These results demonstrate that small-molecule epigenetic inhibitors can have profound consequences on XCI in human cells, and they underscore the importance of considering gender when developing and clinically testing small-molecule epigenetic inhibitors, in particular those that target the well-characterized mechanisms of X inactivation.

scholarly journals Epigenetic mechanisms of partial dosage compensation in an avian, female heterogametic system

2021 ◽  
Author(s):  
Ana Catalan ◽  
Jochen Wolf ◽  
Justin Merondun ◽  
Ulrich Knief
Keyword(s):  
Gene Expression ◽  
Dosage Compensation ◽  
Sex Chromosome ◽  
Gene Dosage ◽  
Common Garden ◽  
Underlying Mechanism ◽  
Chromatin Accessibility ◽  
Z Chromosome ◽  
Open Chromatin ◽  
Epigenetic Mechanisms

The evolution of genetic sex determination is often accompanied by degradation of one of the proto sex chromosomes. Male heterogametic systems have evolved convergent, epigenetic mechanisms restoring the resulting imbalance in gene dosage between diploid autosomes (AA) and the hemizygous sex chromosome (X). Female heterogametic systems (AAf ZWf, AAm ZZm) tend to only show partial dosage compensation (0.5 < Zf:AAf < 1) and dosage balance (0.5<Zf:ZZm<1). The underlying mechanism remains largely elusive. Here, we quantified gene expression for a total of 15 male and female Eurasian crows (Corvus (corone) spp.) raised under common garden conditions. In addition, we characterized aspects of the regulatory landscape quantifying genome-wide ATAC-seq and 5mC methylation profiles. Partial dosage compensation was explained by female upregulation of Z-linked genes accompanied by increased chromatin accessibility on the female Z chromosome. 5mC methylation was strongly reduced in open chromatin-regions and GC islands and showed chromosome-, but no sex-specific variation. With the exception of the pseudo-autosomal region (PAR), female upregulation of gene expression was evenly spread across the Z chromosome without evidence for regional epigenetic regulation, as has for example been suggested for the male hypermethylated region (MHM) in chicken. Our results support the hypothesis that partial dosage compensation in female heterogametic systems is subject to chromosome-wide, epigenetic control mediated by differential chromatin accessibility between the sexes.

scholarly journals THE GENETIC BASIS OF DOSAGE COMPENSATION OF ALCOHOL DEHYDROGENASE-1 IN MAIZE

Genetics ◽  
1981 ◽  
Vol 97 (3-4) ◽  
pp. 625-637 ◽  
Author(s):  
James A Birchler
Keyword(s):  
Alcohol Dehydrogenase ◽  
Structural Gene ◽  
Dosage Compensation ◽  
Genetic Basis ◽  
Gene Dosage ◽  
Dosage Effect ◽  
Gene Dosage Effect ◽  
Negative Effect ◽  
Higher Eukaryotes ◽  
Alcohol Dehydrogenase 1

ABSTRACT The levels of alcohol dehydrogenase (ADH) do not exhibit a structural gene-dosage effect in a one to four dosage series of the long arm of chromosome one (1L) (BIRCHLER19 79). This phenomenon, termed dosage compensation, has been studied in more detail. Experiments are described in which individuals aneuploid for shorter segments were examined for the level of ADH in order to characterize the genetic nature of the compensation. The relative ADH expression in segmental trisomics and tetrasomics of region IL 0.72–0.90, which includes the Adh locus, approaches the level expected from a strict gene dosage effect. Region IL 0.20–0.72 produces a negative effect upon ADH in a similar manner to that observed with other enzyme levels when IL as a whole is varied (BIRCHLEF1I9 79). These and other comparisons have led to the concept that the compensation of ADH results from the cancellation of the structural gene effect by the negative aneuploid effect. The example of ADH is discussed as a model for certain other cases of dosage compensation in higher eukaryotes.

scholarly journals Evolutionary Variability of W-Linked Repetitive Content in Lacertid Lizards

Genes ◽  
2020 ◽  
Vol 11 (5) ◽  
pp. 531
Author(s):  
Grzegorz Suwala ◽  
Marie Altmanová ◽  
Sofia Mazzoleni ◽  
Emmanouela Karameta ◽  
Panayiotis Pafilis ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Phylogenetic Signal ◽  
Z Chromosome ◽  
Specific Gene ◽  
W Chromosome ◽  
Squamate Reptiles ◽  
Lacertid Lizards ◽  
Species Specific

Lacertid lizards are a widely radiated group of squamate reptiles with long-term stable ZZ/ZW sex chromosomes. Despite their family-wide homology of Z-specific gene content, previous cytogenetic studies revealed significant variability in the size, morphology, and heterochromatin distribution of their W chromosome. However, there is little evidence about the accumulation and distribution of repetitive content on lacertid chromosomes, especially on their W chromosome. In order to expand our knowledge of the evolution of sex chromosome repetitive content, we examined the topology of telomeric and microsatellite motifs that tend to often accumulate on the sex chromosomes of reptiles in the karyotypes of 15 species of lacertids by fluorescence in situ hybridization (FISH). The topology of the above-mentioned motifs was compared to the pattern of heterochromatin distribution, as revealed by C-banding. Our results show that the topologies of the examined motifs on the W chromosome do not seem to follow a strong phylogenetic signal, indicating independent and species-specific accumulations. In addition, the degeneration of the W chromosome can also affect the Z chromosome and potentially also other parts of the genome. Our study provides solid evidence that the repetitive content of the degenerated sex chromosomes is one of the most evolutionary dynamic parts of the genome.

scholarly journals Evolution of gene dosage on the Z-chromosome of schistosome parasites

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Marion A L Picard ◽  
Celine Cosseau ◽  
Sabrina Ferré ◽  
Thomas Quack ◽  
Christoph G Grevelding ◽  
...  
Keyword(s):  
Gene Expression ◽  
Comparative Genomics ◽  
Schistosoma Mansoni ◽  
Dosage Compensation ◽  
Quantitative Proteomics ◽  
Gene Dosage ◽  
Z Chromosome ◽  
Sex Linkage ◽  
Expression Evolution ◽  
Gene Expression Evolution

XY systems usually show chromosome-wide compensation of X-linked genes, while in many ZW systems, compensation is restricted to a minority of dosage-sensitive genes. Why such differences arose is still unclear. Here, we combine comparative genomics, transcriptomics and proteomics to obtain a complete overview of the evolution of gene dosage on the Z-chromosome of Schistosoma parasites. We compare the Z-chromosome gene content of African (Schistosoma mansoni and S. haematobium) and Asian (S. japonicum) schistosomes and describe lineage-specific evolutionary strata. We use these to assess gene expression evolution following sex-linkage. The resulting patterns suggest a reduction in expression of Z-linked genes in females, combined with upregulation of the Z in both sexes, in line with the first step of Ohno's classic model of dosage compensation evolution. Quantitative proteomics suggest that post-transcriptional mechanisms do not play a major role in balancing the expression of Z-linked genes.

scholarly journals Multilayered Tuning of Dosage Compensation and Z-Chromosome Masculinization in the Wood White (Leptidea sinapis) Butterfly

2019 ◽  
Vol 11 (9) ◽  
pp. 2633-2652
Author(s):  
Lars Höök ◽  
Luis Leal ◽  
Venkat Talla ◽  
Niclas Backström
Keyword(s):  
Dosage Compensation ◽  
Developmental Stages ◽  
Current Knowledge ◽  
Gene Dosage ◽  
Model Organisms ◽  
Z Chromosome ◽  
Xy Model ◽  
Expression Levels ◽  
Male Specific Lethal ◽  
Male Specific

AbstractIn species with genetic sex determination, dosage compensation can evolve to equal expression levels of sex-linked and autosomal genes. Current knowledge about dosage compensation has mainly been derived from male-heterogametic (XX/XY) model organisms, whereas less is understood about the process in female-heterogametic systems (ZZ/ZW). In moths and butterflies, downregulation of Z-linked expression in males (ZZ) to match the expression level in females (ZW) is often observed. However, little is known about the underlying regulatory mechanisms, or if dosage compensation patterns vary across ontogenetic stages. In this study, we assessed dynamics of Z-linked and autosomal expression levels across developmental stages in the wood white (Leptidea sinapis). We found that although expression of Z-linked genes in general was reduced compared with autosomal genes, dosage compensation was actually complete for some categories of genes, in particular sex-biased genes, but equalization in females was constrained to a narrower gene set. We also observed a noticeable convergence in Z-linked expression between males and females after correcting for sex-biased genes. Sex-biased expression increased successively across developmental stages, and male-biased genes were enriched on the Z-chromosome. Finally, all five core genes associated with the ribonucleoprotein dosage compensation complex male-specific lethal were detected in adult females, in correspondence with a reduction in the expression difference between autosomes and the single Z-chromosome. We show that tuning of gene dosage is multilayered in Lepidoptera and argue that expression balance across chromosomal classes may predominantly be driven by enrichment of male-biased genes on the Z-chromosome and cooption of available dosage regulators.

scholarly journals Genomic Characterization of the Fruity Aroma Gene, FaFAD1, Reveals a Gene Dosage Effect on γ-Decalactone Production in Strawberry (Fragaria × ananassa)

2021 ◽  
Vol 12 ◽  
Author(s):  
Youngjae Oh ◽  
Christopher R. Barbey ◽  
Saket Chandra ◽  
Jinhe Bai ◽  
Zhen Fan ◽  
...  
Keyword(s):  
Gene Dosage ◽  
Association Studies ◽  
Genomic Structure ◽  
Dosage Effect ◽  
Genome Wide Association Studies ◽  
Sequencing Analysis ◽  
Strawberry Fruit ◽  
Gene Dosage Effect ◽  
Allele Dosage ◽  
The Impact

Strawberries produce numerous volatile compounds that contribute to the unique flavors of fruits. Among the many volatiles, γ-decalactone (γ-D) has the greatest contribution to the characteristic fruity aroma in strawberry fruit. The presence or absence of γ-D is controlled by a single locus, FaFAD1. However, this locus has not yet been systematically characterized in the octoploid strawberry genome. It has also been reported that the volatile content greatly varies among the strawberry varieties possessing FaFAD1, suggesting that another genetic factor could be responsible for the different levels of γ-D in fruit. In this study, we explored the genomic structure of FaFAD1 and determined the allele dosage of FaFAD1 that regulates variations of γ-D production in cultivated octoploid strawberry. The genome-wide association studies confirmed the major locus FaFAD1 that regulates the γ-D production in cultivated strawberry. With the hybrid capture-based next-generation sequencing analysis, a major presence–absence variation of FaFAD1 was discovered among γ-D producers and non-producers. To explore the genomic structure of FaFAD1 in the octoploid strawberry, three bacterial artificial chromosome (BAC) libraries were developed. A deletion of 8,262 bp was consistently found in the FaFAD1 region of γ-D non-producing varieties. With the newly developed InDel-based codominant marker genotyping, along with γ-D metabolite profiling data, we revealed the impact of gene dosage effect for the production of γ-D in the octoploid strawberry varieties. Altogether, this study provides systematic information of the prominent role of FaFAD1 presence and absence polymorphism in producing γ-D and proposes that both alleles of FaFAD1 are required to produce the highest content of fruity aroma in strawberry fruit.

Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation

2013 ◽  
Vol 29 (7) ◽  
pp. 385-393 ◽  
Author(s):  
Reiner A. Veitia ◽  
Samuel Bottani ◽  
James A. Birchler
Keyword(s):  
Dosage Compensation ◽  
Gene Dosage ◽  
Genetic Interactions ◽  
Gene Dosage Effects ◽  
Dosage Effects

scholarly journals Convergent patterns of sex chromosome dosage compensation between lepidopteran species (WZ/ZZ) and eutherian mammals (XX/XY): insights from a moth neo-Z chromosome

2015 ◽  
Author(s):  
Liuqi Gu ◽  
James Walters ◽  
Douglas Knipple
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosome ◽  
De Novo ◽  
Cydia Pomonella ◽  
Codling Moth ◽  
Z Chromosome ◽  
De Novo Transcriptome ◽  
Insect Order ◽  
Lepidopteran Species ◽  
Different Levels

In contrast to XX/XY species, Z-linked expression is overall reduced in female WZ/ZZ species compared to males or the autosomal expression. This pattern (Z<ZZ≈AA) has been consistently reported in all the WZ/ZZ taxa examined so far, with the singular exception of the insect order of Lepidoptera (moths and butterflies). However, conflicting results linger in this taxon due to discrepancies in data analyses and tissues sampled. To address this issue, we analyzed dosage compensation in the codling moth Cydia pomonella (Tortricidae) using tissues that represent different levels of sexual divergence. C. pomonella is the most basal lepidopteran species yet examined for dosage compensation and has a neo-Z chromosome resulting from an ancient Z:autosome translocation. We based our analyses on RNAseq and de novo transcriptome data from C. pomonella, as well as scrutiny into investigations of other lepidopteran species. Our evidence supports that the lepidopterans share a pattern (Z≈ZZ<AA) of dosage compensation that mirrors the eutherian mammals (X≈XX<AA). In particular, reproductive tissues appear to be exempt from dosage compensation, which helps explain the incongruence in prior reports. Furthermore, C. pomonella ancestral-Z segment exhibited a greater expression reduction than genes on the neo-Z segment, which intriguingly also reflects the differential up-regulation between the ancestral and newly-acquired X-linked genes in mammals. The insect order of Lepidoptera challenges both the classic theories regarding evolution of sex chromosome dosage compensation and the emerging view on association of dosage compensation with sexual heterogamety.

Sign in / Sign up

Export Citation Format

Share Document