Genomic imprinting mediates dosage compensation in a young plant XY 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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Rapid evolution of complete dosage compensation in Poecilia

10.1101/2021.02.12.431036 ◽

2021 ◽

Author(s):

David C.H. Metzger ◽

Benjamin A. Sandkam ◽

Iulia Darolti ◽

Judith E. Mank

Keyword(s):

Gene Expression ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Evolutionary Dynamics ◽

Common Ancestor ◽

Sex Chromosome ◽

Close Relative ◽

Y Chromosomes ◽

Compensation Mechanisms ◽

The Common

ABSTRACTDosage compensation balances gene expression between the sexes in systems with diverged heterogametic sex chromosomes. Theory predicts that dosage compensation should rapidly evolve in parallel with the divergence of sex chromosomes to prevent the deleterious effects of dosage imbalances that occur as a result of sex chromosome divergence. Examples of complete dosage compensation, where gene expression of the entire sex chromosome is compensated, are rare and have only been found in relatively ancient sex chromosome systems. Consequently, very little is known about the evolutionary dynamics of complete dosage compensation systems. We recently found the first example of complete dosage compensation in a fish, Poecilia picta. We also found that the Y chromosome degraded substantially in the common ancestor of P. picta and their close relative Poecilia parae. In this study we find that P. parae also have complete dosage compensation, thus complete dosage compensation likely evolved in the short (∼3.7 my) interval after the split of the ancestor of these two species from P. reticulata, but before they diverged from each other. These data suggest that novel dosage compensation mechanisms can evolve rapidly, thus supporting the longstanding theoretical prediction that such mechanisms arise in parallel with rapidly diverging sex chromosomes.SIGNIFICANCE STATEMENTIn species with XY sex chromosomes, females (XX) have as many copies of X-linked genes compared to males (XY), leading to unbalanced expression between the sexes. Theory predicts that dosage compensation mechanisms should evolve rapidly as X and Y chromosomes diverge, but examples of complete dosage compensation in recently diverged sex chromosomes are scarce, making this theory difficult to test. Across Poeciliid species the X and Y chromosomes have recently diversified. Here we find complete dosage compensation evolved rapidly as the X and Y diverged in the common ancestor of Poecilia parae and P. picta, supporting that novel dosage compensation mechanisms can evolve rapidly in tandem with diverging sex chromosomes. These data confirm longstanding theoretical predictions of sex chromosome evolution.

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Dosage-sensitive functions in embryonic development drove the survival of genes on sex-specific chromosomes in snakes, birds, and mammals

10.1101/2020.07.09.196279 ◽

2020 ◽

Cited By ~ 3

Author(s):

Daniel W. Bellott ◽

David C. Page

Keyword(s):

Gene Expression ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Meta Analysis ◽

Purifying Selection ◽

Y Chromosomes ◽

The Face ◽

Heterogametic Sex ◽

Additional Constraints ◽

Insight Into

AbstractDifferent ancestral autosomes independently evolved into sex chromosomes in snakes, birds, and mammals. In snakes and birds, females are ZW, while males are ZZ; in mammals, females are XX and males are XY. While X and Z chromosomes retain nearly all ancestral genes, sex-specific W and Y chromosomes suffered extensive genetic decay. In both birds and mammals, the genes that survived on sex-specific chromosomes are enriched for broadly expressed, dosage sensitive regulators of gene expression, subject to strong purifying selection. To gain deeper insight into the processes that govern survival on sex-specific chromosomes, we carried out a meta-analysis of survival across 41 species — three snakes, 24 birds and 14 mammals — doubling the number of ancestral genes under investigation and increasing our power to detect enrichments among survivors relative to non-survivors. Out of 2573 ancestral genes, representing an eighth of the ancestral amniote genome, only 322 survive on present-day sex-specific chromosomes. Survivors are enriched for dosage sensitive developmental processes, particularly development of the face. However, there was no enrichment for expression in sex-specific tissues, involvement in sex-determination or gonadogenesis pathways, or conserved sex-biased expression. Broad expression and dosage sensitivity contributed independently to gene survival, suggesting that pleiotropy imposes additional constraints on the evolution of dosage compensation. We propose that maintaining the viability of the heterogametic sex drove gene survival on amniote sex-specific chromosomes, and that subtle modulation of the expression of survivor genes and their autosomal orthologs has disproportionately large effects on development and disease.

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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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Rapid Y degeneration and dosage compensation in plant sex chromosomes

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1508454112 ◽

2015 ◽

Vol 112 (42) ◽

pp. 13021-13026 ◽

Cited By ~ 80

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.

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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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LTR retrotransposons in the dioecious plant Silene latifolia

Genome ◽

10.1139/g02-026 ◽

2002 ◽

Vol 45 (4) ◽

pp. 745-751 ◽

Cited By ~ 28

Author(s):

Sachihiro Matsunaga ◽

Fumi Yagisawa ◽

Maki Yamamoto ◽

Wakana Uchida ◽

Shunsuke Nakao ◽

...

Keyword(s):

Sex Chromosomes ◽

Evolutionary Dynamics ◽

Sex Chromosome ◽

Silene Latifolia ◽

Ltr Retrotransposons ◽

Dioecious Plant ◽

Dioecious Species ◽

Y Chromosomes ◽

Genus Silene ◽

Silene Species

Conserved domains of two types of LTR retrotransposons, Ty1copia- and Ty3gypsy-like retrotransposons, were isolated from the dioecious plant Silene latifolia, whose sex is determined by X and Y chromosomes. Southern hybridization analyses using these retrotransposons as probes resulted in identical patterns from male and female genomes. Fluorescence in situ hybridization indicated that these retrotransposons do not accumulate specifically in the sex chromosomes. These results suggest that recombination between the sex chromosomes of S. latifolia has not been severely reduced. Conserved reverse transcriptase regions of Ty1copia-like retrotransposons were isolated from 13 different Silene species and classified into two major families. Their categorization suggests that parallel divergence of the Ty1copia-like retrotransposons occurred during the differentiation of Silene species. Most functional retrotransposons from three dioecious species, S. latifolia, S. dioica, and S. diclinis, fell into two clusters. The evolutionary dynamics of retrotransposons implies that, in the genus Silene, dioecious species evolved recently from gynodioecious species.Key words: retrotransposon, dioecious plant, sex chromosome.

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Y chromosome specific markers and the evolution of dioecy in the genus Silene

Genome ◽

10.1139/g97-094 ◽

1998 ◽

Vol 41 (2) ◽

pp. 141-147 ◽

Cited By ~ 17

Author(s):

Y Hi Zhang ◽

Veronica S Stilio ◽

Farah Rehman ◽

Amy Avery ◽

David Mulcahy ◽

...

Keyword(s):

Y Chromosome ◽

Sex Chromosomes ◽

Silene Latifolia ◽

Dioecious Species ◽

Sequence Characterized Amplified Region ◽

Y Chromosomes ◽

Heteromorphic Sex Chromosomes ◽

Males And Females ◽

Genus Silene ◽

Evolution Of Dioecy

Sex determination in plants has been most thoroughly investigated in Silene latifolia, a dioecious species possessing heteromorphic sex chromosomes. We have identified several new Y chromosome linked RAPD markers and converted these to more reliable sequence characterized amplified region (SCAR) markers by cloning the RAPD fragments and developing longer primers. Of the primer pairs for seven SCARs, five amplify a single, unique fragment from the DNA of male S. latifolia. Two sets of primers also amplify additional fragments common to males and females. Homology between the X and Y chromosomes is sufficient to allow the amplification of fragments from females under less stringent PCR conditions. Five of the SCARs also distinguish between the sexes of closely related dioecious taxa of the section Elisanthe, but not between the sexes of distantly related dioecious species. These markers will be useful for continued investigations into the evolution of sex, phylogenetic relationships among taxa, and population dynamics of sex ratios in the genus Silene.Key words: Melandrium, RAPDs, sex chromosomes, SCARs.

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Temperature-dependent effects of house fly proto-Y chromosomes on gene expression act independently of the sex determination pathway

10.1101/2020.08.05.238378 ◽

2020 ◽

Author(s):

Kiran Adhikari ◽

Jae Hak Son ◽

Anna H. Rensink ◽

Jaweria Jaweria ◽

Daniel Bopp ◽

...

Keyword(s):

Gene Expression ◽

Sex Determination ◽

Sex Chromosomes ◽

Developmental Process ◽

Natural Populations ◽

House Fly ◽

Sexually Dimorphic ◽

Temperature Dependent ◽

Y Chromosomes ◽

Polygenic Sex Determination

AbstractSex determination, the developmental process by which sexually dimorphic phenotypes are established, evolves fast. Species with polygenic sex determination, in which master regulatory genes are found on multiple different proto-sex chromosomes, are informative models to study the evolution of sex determination. House flies are such a model system, with male determining loci possible on all six chromosomes and a female-determiner on one of the chromosomes as well. The distributions of the two most common male-determining proto-Y chromosomes across natural populations suggests that temperature variation is an important selection pressure responsible for maintaining polygenic sex determination in this species. To test that hypothesis, we used RNA-seq to identify temperature-dependent effects of the proto-Y chromosomes on gene expression. We find no evidence for ecologically meaningful temperature-dependent expression of sex determining genes between male genotypes, but we identified hundreds of other genes whose expression depends on the interaction between proto-Y chromosome genotype and temperature. Notably, genes with genotype-by-temperature interactions on expression are not enriched on the proto-sex chromosomes. Moreover, there is no evidence that temperature-dependent expression is driven by chromosome-wide expression divergence between the proto-Y and proto-X alleles. Therefore, if temperature-dependent gene expression is responsible for differences in phenotypes and fitness of proto-Y genotypes across house fly populations, these effects are driven by a small number of temperature-dependent alleles on the proto-Y chromosomes.

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Sexually dimorphic gene expression and transcriptome evolution provides mixed evidence for a fast-Z effect in Heliconius

10.1101/380030 ◽

2018 ◽

Author(s):

A Pinharanda ◽

M Rousselle ◽

SH Martin ◽

JJ Hanly ◽

JW Davey ◽

...

Keyword(s):

Gene Expression ◽

Molecular Evolution ◽

Adaptive Evolution ◽

Sex Chromosomes ◽

Expression Profiles ◽

Sequence Divergence ◽

Gene Expression Profiles ◽

Purifying Selection ◽

Specific Gene ◽

Sex Determination System

AbstractSex chromosomes have different evolutionary properties as compared to the autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution in the sex chromosomes of a group of tropical butterflies. We first improved the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then we sequenced RNA from male and female whole abdomens and female ovary and gut tissue to identify sex and tissue specific gene expression profiles in H. melpomene. Using these expression profiles we compare sequence divergence and polymorphism, the strength of positive and negative selection and rates of adaptive evolution for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato.We show that the rate of adaptive substitutions is higher for Z as compared to autosomal genes, but contrary to expectation it is also higher for male as compared to female biased genes. There is therefore mixed evidence that hemizygosity influences the rate of adaptive substitutions. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic specific tissue. Together our results provide limited support for fast-Z evolution. This contributes to a growing body of literature from other ZW systems that also provide mixed evidence for a fast-Z effect.

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