scholarly journals Ancestral chromatin configuration constrains chromatin evolution on differentiating sex chromosomes in Drosophila

2015 ◽  
Author(s):  
Qi Zhou ◽  
Doris Bachtrog
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Functional Expression ◽  
Pericentric Heterochromatin ◽  
Evolutionary Trajectory ◽  
Normal Expression ◽  
Chromatin Configuration ◽  
Y Degeneration ◽  
Canonical Histone ◽  
Histone Modification Mark

Sex chromosomes evolve distinctive types of chromatin from a pair of ancestral autosomes that are usually euchromatic. In Drosophila, the dosage-compensated X becomes enriched for hyperactive chromatin in males (mediated by H4K16ac), while the Y chromosome acquires silencing heterochromatin (enriched for H3K9me2/3). Drosophila autosomes are typically mostly euchromatic but the small dot chromosome has evolved a heterochromatin-like milieu (enriched for H3K9me2/3) that permits the normal expression of dot-linked genes, but which is different from typical pericentric heterochromatin. In Drosophila busckii, the dot chromosomes have fused to the ancestral sex chromosomes, creating a pair of ‘neo-sex’ chromosomes. Here we collect genomic, transcriptomic and epigenomic data from D. busckii, to investigate the evolutionary trajectory of sex chromosomes from a largely heterochromatic ancestor. We show that the neo-sex chromosomes formed <1 million years ago, but nearly 60% of neo-Y linked genes have already become non-functional. Expression levels are generally lower for the neo-Y alleles relative to their neo-X homologs, and the silencing heterochromatin mark H3K9me2, but not H3K9me3, is significantly enriched on silenced neo-Y genes. Despite rampant neo-Y degeneration, we find that the neo-X is deficient for the canonical histone modification mark of dosage compensation (H4K16ac), relative to autosomes or the compensated ancestral X chromosome, possibly reflecting constraints imposed on evolving hyperactive chromatin in an originally heterochromatic environment. Yet, neo-X genes are transcriptionally more active in males, relative to females, suggesting the evolution of incipient dosage compensation on the neo-X. Our data show that Y degeneration proceeds quickly after sex chromosomes become established through genomic and epigenetic changes, and are consistent with the idea that the evolution of sex-linked chromatin is influenced by its ancestral configuration.

scholarly journals Evolutionary trajectories of three independent neo-sex chromosomes inDrosophila

2021 ◽  
Author(s):  
Masafumi Nozawa ◽  
Yohei Minakuchi ◽  
Kazuhiro Satomura ◽  
Shu Kondo ◽  
Atsushi Toyoda ◽  
...  
Keyword(s):  
X Chromosome ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Gene Loss ◽  
Comparative Genomic ◽  
Functional Constraints ◽  
Evolutionary Trajectory ◽  
Y Chromosomes ◽  
Dead End ◽  
Evolutionary Trajectories

ABSTRACTDosage compensation (DC) on the X chromosome is a mechanism to counteract the deleterious effects by gene loss from the Y chromosome. However, DC cannot work efficiently if the X chromosome also degenerates. This indeed occurs in the neo-sex chromosomes inDrosophila miranda, where neo-X as well as neo-Y chromosomes are under accelerated pseudogenization. To examine the generality of this pattern, we investigated the evolution of two additional neo-sex chromosomes that independently emerged inD. albomicansandD. americanaand compared their evolutionary processes with that inD. miranda. Comparative genomic and transcriptomic analyses revealed that the pseudogenization rate on neo-X is also accelerated in the two species (though lesser extent inD. americana). We also found that neo-X-linked genes whose neo-Y homologs are pseudogenized tend to be upregulated more stringently than those whose neo-Y homologs remain functional. Moreover, the genes under strong functional constraints and highly expressed in the testis tended to remain functional on neo-X and neo-Y, respectively. Focusing on theD. mirandaandD. albomicansneo-sex chromosomes that independently emerged from the same autosome, we further found that the same genes tend to have been pseudogenized in parallel on neo-Y. Those genes includeIdgf6andJhI-26whose functions seem to be unnecessary or could be even harmful for males. These results indicate that neo-sex chromosomes inDrosophilashare a common evolutionary trajectory after their emergence, which may be applicable to other sex chromosomes in a variety of organisms to avoid being an evolutionary dead-end.

scholarly journals Evolution of dosage compensation does not depend on genomic background

2020 ◽  
Author(s):  
Michail Rovatsos ◽  
Lukáš Kratochvíl
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Genomic Region ◽  
Gene Copy ◽  
Gene Dose ◽  
Copy Numbers ◽  
Compensation Mechanisms ◽  
Gene Copy Numbers ◽  
Softshell Turtles

AbstractOrganisms evolved various mechanisms to cope with the differences in the gene copy numbers between sexes caused by degeneration of Y and W sex chromosomes. Complete dosage compensation or at least expression balance between sexes was reported predominantly in XX/XY, but rarely in ZZ/ZW systems. However, this often-reported pattern is based on comparisons of lineages where sex chromosomes evolved from non-homologous genomic regions, potentially differing in sensitivity to differences in gene copy numbers. Here we document that two reptilian lineages (XX/XY iguanas and ZZ/ZW softshell turtles), which independently co-opted the same ancestral genomic region for the function of sex chromosomes, evolved different gene dose regulatory mechanisms. The independent co-option of the same genomic region for the role of sex chromosome as in the iguanas and the softshell turtles offers a great opportunity for testing evolutionary scenarios on the sex chromosome evolution under the explicit control for the genomic background and for gene identity. We showed that the parallel loss of functional genes from the Y chromosome of the green anole and the W chromosome of the Florida softshell turtle led to different dosage compensation mechanisms. Our approach controlling for genetic background thus does not support that the variability in the regulation of the gene dose differences is a consequence of ancestral autosomal gene content.

scholarly journals Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila

2018 ◽  
Author(s):  
Doris Bachtrog ◽  
Chris Ellison
Keyword(s):  
Transposable Element ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Binding Sites ◽  
Evolutionary Biology ◽  
De Novo ◽  
Binding Motif ◽  
Sequence Motif ◽  
X Chromosomes ◽  
Msl Complex

The repeatability or predictability of evolution is a central question in evolutionary biology, and most often addressed in experimental evolution studies. Here, we infer how genetically heterogeneous natural systems acquire the same molecular changes, to address how genomic background affects adaptation in natural populations. In particular, we take advantage of independently formed neo-sex chromosomes in Drosophila species that have evolved dosage compensation by co-opting the dosage compensation (MSL) complex, to study the mutational paths that have led to the acquisition of 100s of novel binding sites for the MSL complex in different species. This complex recognizes a conserved 21-bp GA-rich sequence motif that is enriched on the X chromosome, and newly formed X chromosomes recruit the MSL complex by de novo acquisition of this binding motif. We identify recently formed sex chromosomes in the Drosophila repleta and robusta species groups by genome sequencing, and generate genomic occupancy maps of the MSL complex to infer the location of novel binding sites. We find that diverse mutational paths were utilized in each species to evolve 100s of de novo binding motifs along the neo-X, including expansions of microsatellites and transposable element insertions. However, the propensity to utilize a particular mutational path differs between independently formed X chromosomes, and appears to be contingent on genomic properties of that species, such as simple repeat or transposable element density. This establishes the “genomic environment” as an important determinant in predicting the outcome of evolutionary adaptations.

scholarly journals Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

2019 ◽  
Vol 116 (38) ◽  
pp. 19031-19036 ◽  
Author(s):  
Iulia Darolti ◽  
Alison E. Wright ◽  
Benjamin A. Sandkam ◽  
Jake Morris ◽  
Natasha I. Bloch ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Poecilia Reticulata ◽  
Sex Chromosome ◽  
Sequencing Data ◽  
Chromosome Differentiation ◽  
Y Chromosomes ◽  
Shared Ancestry ◽  
Suppressed Recombination

Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

scholarly journals Rapid Y degeneration and dosage compensation in plant sex chromosomes

2015 ◽  
Vol 112 (42) ◽  
pp. 13021-13026 ◽  
Author(s):  
Alexander S. T. Papadopulos ◽  
Michael Chester ◽  
Kate Ridout ◽  
Dmitry A. Filatov
Keyword(s):  
Sex Chromosomes ◽  
Large Scale ◽  
De Novo ◽  
Silene Latifolia ◽  
Stop Codons ◽  
Y Chromosomes ◽  
Evolutionary Trajectories ◽  
Plant Sex Chromosomes ◽  
Two Kingdoms ◽  
Y Degeneration

The nonrecombining regions of animal Y chromosomes are known to undergo genetic degeneration, but previous work has failed to reveal large-scale gene degeneration on plant Y chromosomes. Here, we uncover rapid and extensive degeneration of Y-linked genes in a plant species, Silene latifolia, that evolved sex chromosomes de novo in the last 10 million years. Previous transcriptome-based studies of this species missed unexpressed, degenerate Y-linked genes. To identify sex-linked genes, regardless of their expression, we sequenced male and female genomes of S. latifolia and integrated the genomic contigs with a high-density genetic map. This revealed that 45% of Y-linked genes are not expressed, and 23% are interrupted by premature stop codons. This contrasts with X-linked genes, in which only 1.3% of genes contained stop codons and 4.3% of genes were not expressed in males. Loss of functional Y-linked genes is partly compensated for by gene-specific up-regulation of X-linked genes. Our results demonstrate that the rate of genetic degeneration of Y-linked genes in S. latifolia is as fast as in animals, and that the evolutionary trajectories of sex chromosomes are similar in the two kingdoms.

scholarly journals Finding a Balance: How Diverse Dosage Compensation Strategies Modify Histone H4 to Regulate Transcription

2012 ◽  
Vol 2012 ◽  
pp. 1-12
Author(s):  
Michael B. Wells ◽  
Györgyi Csankovszki ◽  
Laura M. Custer
Keyword(s):  
Gene Expression ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Current Understanding ◽  
Histone H4 ◽  
Linked Gene ◽  
Expression Levels ◽  
Gene Expression Levels

Dosage compensation balances gene expression levels between the sex chromosomes and autosomes and sex-chromosome-linked gene expression levels between the sexes. Different dosage compensation strategies evolved in different lineages, but all involve changes in chromatin. This paper discusses our current understanding of how modifications of the histone H4 tail, particularly changes in levels of H4 lysine 16 acetylation and H4 lysine 20 methylation, can be used in different contexts to either modulate gene expression levels twofold or to completely inhibit transcription.

Dosage compensation, the origin and the afterlife of sex chromosomes

2006 ◽  
Vol 14 (4) ◽  
pp. 417-431 ◽  
Author(s):  
Jan Larsson ◽  
Victoria H. Meller
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosomes

scholarly journals Avian sex chromosomes: dosage compensation matters

2009 ◽  
Vol 17 (5) ◽  
pp. 687-697 ◽  
Author(s):  
Heather A. McQueen ◽  
Michael Clinton
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosomes

scholarly journals Drosophila CLAMP is an essential protein with sex-specific roles in males and females

2016 ◽  
Author(s):  
Jennifer A. Urban ◽  
Caroline A. Doherty ◽  
William T. Jordan ◽  
Jacob E. Bliss ◽  
Jessica Feng ◽  
...  
Keyword(s):  
X Chromosome ◽  
Dosage Compensation ◽  
Zinc Finger Protein ◽  
Pericentric Heterochromatin ◽  
Single Male ◽  
Essential Protein ◽  
Msl Complex ◽  
Males And Females ◽  
Male Specific

AbstractDosage compensation is a fundamental mechanism in many species that corrects for the inherent imbalance in X-chromosome copy number between XY males and XX females. In Drosophila melanogaster, transcriptional output from the single male X-chromosome is equalized to that of XX females by recruitment of the Male Specific Lethal (MSL) complex to specific sequences along the length of the X-chromosome. The initial recruitment of MSL complex to the X-chromosome is dependent on a recently discovered zinc finger protein called Chromatin-Linked Adapter for MSL Proteins (CLAMP). However, further studies on the in vivo function of CLAMP remained difficult because the location of the gene in pericentric heterochromatin made it challenging to create null mutations or deficiencies. Using the CRISPR/Cas9 genome editing system, we generated the first null mutant in the clamp gene that eliminates expression of CLAMP protein. We show that CLAMP is necessary for both male and female viability. While females die at the third instar larval stage, males die earlier, likely due to the essential role of CLAMP in male dosage compensation. Moreover, we demonstrate that CLAMP promotes dosage compensation in males and represses key male-specific transcripts involved in sex-determination in females. Our results reveal that CLAMP is an essential protein with dual roles in males and females, which together assure that dosage compensation is a sex-specific process.

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