The Epigenome of Evolving Drosophila Neo-Sex Chromosomes: Dosage Compensation and Heterochromatin Formation

Organisms with highly differentiated sex chromosomes face an imbalance in X-linked gene dosage. Male Drosophila solve this problem by increasing expression from virtually every gene on their single X chromosome, a process known as dosage compensation. This involves a ribonucleoprotein complex that is recruited to active, X-linked genes to remodel chromatin and increase expression. Interestingly, the male X chromosome is also enriched for several proteins associated with heterochromatin. Furthermore, the polytenized male X is selectively disrupted by the loss of factors involved in repression, silencing, heterochromatin formation or chromatin remodeling. Mutations in many of these factors preferentially reduce male survival or enhance the lethality of mutations that prevent normal recognition of the X chromosome. The involvement of primarily repressive factors in a process that elevates expression has long been puzzling. Interestingly, recent work suggests that the siRNA pathway, often associated with heterochromatin formation and repression, also helps the dosage compensation machinery identify the X chromosome. In light of this finding, we revisit the evidence that links nuclear organization and heterochromatin to regulation of the male X chromosome.

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Evolution of dosage compensation does not depend on genomic background

10.1101/2020.08.14.251801 ◽

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.

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

10.1101/488569 ◽

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.

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Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1905298116 ◽

2019 ◽

Vol 116 (38) ◽

pp. 19031-19036 ◽

Cited By ~ 20

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.

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

Genetics Research International ◽

10.1155/2012/795069 ◽

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.

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Dosage compensation, the origin and the afterlife of sex chromosomes

Chromosome Research ◽

10.1007/s10577-006-1064-3 ◽

2006 ◽

Vol 14 (4) ◽

pp. 417-431 ◽

Cited By ~ 38

Author(s):

Jan Larsson ◽

Victoria H. Meller

Keyword(s):

Dosage Compensation ◽

Sex Chromosomes

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Avian sex chromosomes: dosage compensation matters

Chromosome Research ◽

10.1007/s10577-009-9056-8 ◽

2009 ◽

Vol 17 (5) ◽

pp. 687-697 ◽

Cited By ~ 18

Author(s):

Heather A. McQueen ◽

Michael Clinton

Keyword(s):

Dosage Compensation ◽

Sex Chromosomes

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Dosage compensation in sciarids is achieved by hypertranscription of the single X chromosome in males.

Genetics ◽

10.1093/genetics/138.3.787 ◽

1994 ◽

Vol 138 (3) ◽

pp. 787-790

Author(s):

P R da Cunha ◽

B Granadino ◽

A L Perondini ◽

L Sánchez

Keyword(s):

X Chromosome ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Sex Chromosome ◽

X Chromosomes ◽

Different Doses

Abstract Dosage compensation refers to the process whereby females and males with different doses of sex chromosomes have similar amounts of products from sex chromosome-linked genes. We analyzed the process of dosage compensation in Sciara ocellaris, Diptera of the suborder Nematocera. By autoradiography and measurements of X-linked rRNA in females (XX) and males (XO), we found that the rate of transcription of the single X chromosome in males is similar to that of the two X chromosomes in females. This, together with the bloated appearance of the X chromosome in males, support the idea that in sciarids dosage compensation is accomplished by hypertranscription of the X chromosome in males.

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

10.1101/019786 ◽

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.

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Genomic imprinting mediates dosage compensation in a young plant XY system

10.1101/179044 ◽

2017 ◽

Cited By ~ 2

Author(s):

Aline Muyle ◽

Niklaus Zemp ◽

Cécile Fruchard ◽

Radim Cegan ◽

Jan Vrana ◽

...

Keyword(s):

Gene Expression ◽

Genomic Imprinting ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Evolutionary Biology ◽

Early Stage ◽

Silene Latifolia ◽

Negative Effects ◽

Y Chromosomes ◽

Sex Determination System

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100044).Sex chromosomes have repeatedly evolved from a pair of autosomes1. Consequently, X and Y chromosomes initially have similar gene content, but ongoing Y degeneration leads to reduced Y gene expression and eventual Y gene loss. The resulting imbalance in gene expression between Y genes and the rest of the genome is expected to reduce male fitness, especially when protein networks have components from both autosomes and sex chromosomes. A diverse set of dosage compensating mechanisms that alleviates these negative effects has been described in animals2–4. However, the early steps in the evolution of dosage compensation remain unknown and dosage compensation is poorly understood in plants5. Here we show a novel dosage compensation mechanism in the evolutionarily young XY sex determination system of the plant Silene latifolia. Genomic imprinting results in higher expression from the maternal X chromosome in both males and females. This compensates for reduced Y expression in males but results in X overexpression in females and may be detrimental. It could represent a transient early stage in the evolution of dosage compensation. Our finding has striking resemblance to the first stage proposed by Ohno for the evolution of X inactivation in mammals.

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