Homomorphic ZW chromosomes 1 in a wild strawberry show distinctive recombination heterogeneity but a small sex-determining region

SummaryRecombination in ancient, heteromorphic sex chromosomes is typically suppressed at the sex-determining region (SDR) and proportionally elevated in the pseudoautosomal region (PAR). However, little is known about recombination dynamics of young, homomorphic plant sex chromosomes.We examine male and female function in crosses and unrelated samples of the dioecious octoploid strawberry Fragaria chiloensis in order to map the small and recently evolved SDR controlling both traits and to examine recombination patterns on the incipient ZW chromosome.The SDR of this ZW system is located within a 280kb window, in which the maternal recombination rate is lower than the paternal. In contrast to the SDR, the maternal PAR recombination rate is much higher than the rates of the paternal PAR or autosomes, culminating in an elevated chromosome-wide rate. W-specific divergence is elevated within the SDR and a single polymorphism is observed in high species-wide linkage disequilibrium with sex.Selection for recombination suppression within the small SDR may be weak, but fluctuating sex ratios could favor elevated recombination in the PAR to remove deleterious mutations on the W. The recombination dynamics of this nascent sex chromosome with a modestly diverged SDR may be typical of other dioecious plants.

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Evolutionary stasis of the pseudoautosomal boundary in strepsirrhine primates

10.1101/445072 ◽

2018 ◽

Cited By ~ 1

Author(s):

Rylan Shearn ◽

Alison E. Wright ◽

Sylvain Mousset ◽

Corinne Régis ◽

Simon Penel ◽

...

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Relative Size ◽

Pseudoautosomal Region ◽

Recombination Suppression ◽

Males And Females ◽

Work Supports ◽

Y Degeneration ◽

Female Genome ◽

Pseudoautosomal Boundary

AbstractSex chromosomes are typically comprised of a non-recombining region and a recombining pseudoautosomal region. Accurately quantifying the relative size of these regions is critical for sex chromosome biology both from a functional (i.e. number of sex-linked genes) and evolutionary perspective (i.e. extent of Y degeneration and X-Y heteromorphy). The evolution of the pseudoautosomal boundary (PAB) - the limit between the recombining and the non-recombining regions of the sex chromosomes - is well documented in haplorrhines (apes and monkeys) but not in strepsirrhines (lemurs and lorises), which represent almost 30% of all primates. Here we studied the PAB of seven species representing the main strepsirrhine lineages by sequencing a male and a female genome in each species and using sex differences in coverage to identify the PAB. We found that during primate evolution, the PAB has remained unchanged in strepsirrhines whereas several recombination suppression events moved the PAB and shortened the pseudoautosomal region in haplorrhines. Strepsirrhines are well known to have much lower sexual dimorphism than haplorrhines. We suggest that mutations with antagonistic effects between males and females have driven recombination suppression and PAB evolution in haplorrhines. Our work supports the view that sexually antagonistic mutations have influenced the evolution of sex chromosomes in primates.

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Plant genera Cannabis and Humulus share the same pair of well-differentiated sex chromosomes

10.1101/2021.03.11.434957 ◽

2021 ◽

Author(s):

D Prentout ◽

N Stajner ◽

A Cerenak ◽

T Tricou ◽

C Brochier-Armanet ◽

...

Keyword(s):

Sex Chromosomes ◽

Cannabis Sativa ◽

Sex Chromosome ◽

Probabilistic Method ◽

List Type ◽

Recombination Suppression ◽

Sex Chromosome System ◽

The Common ◽

Well Differentiated ◽

First Time

SummaryWe recently described, in Cannabis sativa, the oldest sex chromosome system documented so far in plants. Based on our estimate of its age, we predicted that it should be shared by its sister genus Humulus, which is known to also possess XY sex chromosomes.Here, we used transcriptome sequencing of a F1 family of Humulus lupulus to identify and study the sex chromosomes in this species using the probabilistic method SEX-DETector.We identified 265 sex-linked genes in H. lupulus, located on the chromosome that is also the C. sativa sex chromosome pair. Using phylogenies of sex-linked genes, we show that a region of these chromosomes had already stopped recombining in the common ancestor of the two species. Furthermore, as in C. sativa, Y gene expression was reduced in correlation to the position on the X chromosome, and strongly Y degenerated genes showed dosage compensation.Here we report, for the first time in the Angiosperms, a sex chromosome system that is shared by two different genera. Recombination suppression started at least 21-25 My ago, and then (either gradually or step-wise) spread to a large part of the sex chromosomes, leading to a strongly degenerated Y.

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Extreme variation in recombination rate and genetic variation along the Sylvioidea neo-sex chromosome

10.1101/2020.09.25.314054 ◽

2020 ◽

Author(s):

Suvi Ponnikas ◽

Hanna Sigeman ◽

Max Lundberg ◽

Bengt Hansson

Keyword(s):

Sex Chromosomes ◽

Recombination Rate ◽

Sex Chromosome ◽

Bird Species ◽

Pseudoautosomal Region ◽

Z Chromosome ◽

Strong Impact ◽

Sequence Evolution ◽

Apparent Lack ◽

Extreme Variation

In the majority of bird species, recombination between the sex chromosome pairs in heterogametic females (ZW) is restricted to a small pseudoautosomal region (PAR), whereas recombination is ongoing along the entire Z chromosome in the homogametic males (ZZ). Recombination has a strong impact on the sequence evolution by affecting the extent of linkage, level of genetic diversity and efficacy of selection. Species within the Sylvioidea superfamily are unique among birds in having extended Z and W chromosomes (neo-sex chromosomes) formed by a fusion between the ancestral sex chromosomes and a part of chromosome 4A. So far the recombination landscape of the Sylvioidea neo-sex chromosomes remains unknown, despite its importance for understanding sequence evolution. Here, we use linkage mapping in a multi-generation pedigree to assemble, and assess the recombination rate along the entire Z chromosome of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). This resulted in an 87.54 Mbp and 90.19 cM large Z including the ancestral-Z, where the small PAR (0.89 Mbp) is located, and the added-Z. A striking result was an extreme variation in recombination rate along the Z in male great reed warblers with high rates at both telomeric ends, but an apparent lack of recombination over a substantial central section, covering 77% of the chromosome. This region showed a drastic loss of nucleotide diversity and accumulation of repeats compared to the highly recombining regions. Nonetheless, the evolutionary rate of genes (measured by dN/dS) did not differ between these regions, suggesting that the efficacy of selection on protein-coding sequences is not reduced by lack of recombination.

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Differential Gene Expression between Fungal Mating Types Is Associated with Sequence Degeneration

Genome Biology and Evolution ◽

10.1093/gbe/evaa028 ◽

2020 ◽

Vol 12 (4) ◽

pp. 243-258 ◽

Cited By ~ 3

Author(s):

Wen-Juan Ma ◽

Fantin Carpentier ◽

Tatiana Giraud ◽

Michael E Hood

Keyword(s):

Differential Expression ◽

Differentially Expressed Genes ◽

Mating Type ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Gc Content ◽

Differentially Expressed ◽

Mating Types ◽

Sexual Antagonism ◽

Recombination Suppression

Abstract Degenerative mutations in non-recombining regions, such as in sex chromosomes, may lead to differential expression between alleles if mutations occur stochastically in one or the other allele. Reduced allelic expression due to degeneration has indeed been suggested to occur in various sex-chromosome systems. However, whether an association occurs between specific signatures of degeneration and differential expression between alleles has not been extensively tested, and sexual antagonism can also cause differential expression on sex chromosomes. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal for testing associations between specific degenerative signatures and differential expression because 1) there are multiple evolutionary strata on the mating-type chromosomes, reflecting successive recombination suppression linked to mating-type loci; 2) separate haploid cultures of opposite mating types help identify differential expression between alleles; and 3) there is no sexual antagonism as a confounding factor accounting for differential expression. We found that differentially expressed genes were enriched in the four oldest evolutionary strata compared with other genomic compartments, and that, within compartments, several signatures of sequence degeneration were greater for differentially expressed than non-differentially expressed genes. Two particular degenerative signatures were significantly associated with lower expression levels within differentially expressed allele pairs: upstream insertion of transposable elements and mutations truncating the protein length. Other degenerative mutations associated with differential expression included nonsynonymous substitutions and altered intron or GC content. The association between differential expression and allele degeneration is relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions where recombination is suppressed.

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Telomere-to-telomere assembly of a fish Y chromosome reveals the origin of a young sex chromosome pair

Genome Biology ◽

10.1186/s13059-021-02430-y ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Lingzhan Xue ◽

Yu Gao ◽

Meiying Wu ◽

Tian Tian ◽

Haiping Fan ◽

...

Keyword(s):

Y Chromosome ◽

Sex Chromosomes ◽

Chromosome Pair ◽

Sex Chromosome ◽

Structural Variations ◽

Recombination Suppression ◽

Chromosome Differentiation ◽

Y Chromosomes ◽

Recent Origin ◽

Mastacembelus Armatus

Abstract Background The origin of sex chromosomes requires the establishment of recombination suppression between the proto-sex chromosomes. In many fish species, the sex chromosome pair is homomorphic with a recent origin, providing species for studying how and why recombination suppression evolved in the initial stages of sex chromosome differentiation, but this requires accurate sequence assembly of the X and Y (or Z and W) chromosomes, which may be difficult if they are recently diverged. Results Here we produce a haplotype-resolved genome assembly of zig-zag eel (Mastacembelus armatus), an aquaculture fish, at the chromosomal scale. The diploid assembly is nearly gap-free, and in most chromosomes, we resolve the centromeric and subtelomeric heterochromatic sequences. In particular, the Y chromosome, including its highly repetitive short arm, has zero gaps. Using resequencing data, we identify a ~7 Mb fully sex-linked region (SLR), spanning the sex chromosome centromere and almost entirely embedded in the pericentromeric heterochromatin. The SLRs on the X and Y chromosomes are almost identical in sequence and gene content, but both are repetitive and heterochromatic, consistent with zero or low recombination. We further identify an HMG-domain containing gene HMGN6 in the SLR as a candidate sex-determining gene that is expressed at the onset of testis development. Conclusions Our study supports the idea that preexisting regions of low recombination, such as pericentromeric regions, can give rise to SLR in the absence of structural variations between the proto-sex chromosomes.

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Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals

Genes ◽

10.3390/genes12091434 ◽

2021 ◽

Vol 12 (9) ◽

pp. 1434

Author(s):

Ana Gil-Fernández ◽

Marta Ribagorda ◽

Marta Martín-Ruiz ◽

Pablo López-Jiménez ◽

Tamara Laguna ◽

...

Keyword(s):

Dna Repair ◽

Y Chromosome ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Mammalian Species ◽

Evolutionary Process ◽

Small Region ◽

Pseudoautosomal Region ◽

Evolution Of Sex ◽

African Pygmy Mouse

X and Y chromosomes in mammals are different in size and gene content due to an evolutionary process of differentiation and degeneration of the Y chromosome. Nevertheless, these chromosomes usually share a small region of homology, the pseudoautosomal region (PAR), which allows them to perform a partial synapsis and undergo reciprocal recombination during meiosis, which ensures their segregation. However, in some mammalian species the PAR has been lost, which challenges the pairing and segregation of sex chromosomes in meiosis. The African pygmy mouse Mus mattheyi shows completely differentiated sex chromosomes, representing an uncommon evolutionary situation among mouse species. We have performed a detailed analysis of the location of proteins involved in synaptonemal complex assembly (SYCP3), recombination (RPA, RAD51 and MLH1) and sex chromosome inactivation (γH2AX) in this species. We found that neither synapsis nor chiasmata are found between sex chromosomes and their pairing is notably delayed compared to autosomes. Interestingly, the Y chromosome only incorporates RPA and RAD51 in a reduced fraction of spermatocytes, indicating a particular DNA repair dynamic on this chromosome. The analysis of segregation revealed that sex chromosomes are associated until metaphase-I just by a chromatin contact. Unexpectedly, both sex chromosomes remain labelled with γH2AX during first meiotic division. This chromatin contact is probably enough to maintain sex chromosome association up to anaphase-I and, therefore, could be relevant to ensure their reductional segregation. The results presented suggest that the regulation of both DNA repair and epigenetic modifications in the sex chromosomes can have a great impact on the divergence of sex chromosomes and their proper transmission, widening our understanding on the relationship between meiosis and the evolution of sex chromosomes in mammals.

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Evolutionary Dynamics of Sex Chromosomes of Paleognathous Birds

Genome Biology and Evolution ◽

10.1093/gbe/evz154 ◽

2019 ◽

Vol 11 (8) ◽

pp. 2376-2390 ◽

Cited By ~ 13

Author(s):

Luohao Xu ◽

Simon Yung Wa Sin ◽

Phil Grayson ◽

Scott V Edwards ◽

Timothy B Sackton

Keyword(s):

Sex Chromosomes ◽

Evolutionary Dynamics ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Z Chromosome ◽

Recombination Suppression ◽

Evolutionary Forces ◽

Genomic Level ◽

Standard Models ◽

Pseudoautosomal Regions

Abstract Standard models of sex chromosome evolution propose that recombination suppression leads to the degeneration of the heterogametic chromosome, as is seen for the Y chromosome in mammals and the W chromosome in most birds. Unlike other birds, paleognaths (ratites and tinamous) possess large nondegenerate regions on their sex chromosomes (PARs or pseudoautosomal regions). It remains unclear why these large PARs are retained over >100 Myr, and how this retention impacts the evolution of sex chromosomes within this system. To address this puzzle, we analyzed Z chromosome evolution and gene expression across 12 paleognaths, several of whose genomes have recently been sequenced. We confirm at the genomic level that most paleognaths retain large PARs. As in other birds, we find that all paleognaths have incomplete dosage compensation on the regions of the Z chromosome homologous to degenerated portions of the W (differentiated regions), but we find no evidence for enrichments of male-biased genes in PARs. We find limited evidence for increased evolutionary rates (faster-Z) either across the chromosome or in differentiated regions for most paleognaths with large PARs, but do recover signals of faster-Z evolution in tinamou species with mostly degenerated W chromosomes, similar to the pattern seen in neognaths. Unexpectedly, in some species, PAR-linked genes evolve faster on average than genes on autosomes, suggested by diverse genomic features to be due to reduced efficacy of selection in paleognath PARs. Our analysis shows that paleognath Z chromosomes are atypical at the genomic level, but the evolutionary forces maintaining largely homomorphic sex chromosomes in these species remain elusive.

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Evolutionary dynamics of sex chromosomes of paleognathous birds

10.1101/295089 ◽

2018 ◽

Cited By ~ 3

Author(s):

Luohao Xu ◽

Simon Yung Wa Sin ◽

Phil Grayson ◽

Scott V. Edwards ◽

Timothy B. Sackton

Keyword(s):

Sex Chromosomes ◽

Evolutionary Dynamics ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Z Chromosome ◽

Recombination Suppression ◽

Evolutionary Forces ◽

Genomic Level ◽

Standard Models ◽

Pseudoautosomal Regions

AbstractStandard models of sex chromosome evolution propose that recombination suppression leads to the degeneration of the heterogametic chromosome, as is seen for the Y chromosome in mammals and the W chromosome in most birds. Unlike other birds, paleognaths (ratites and tinamous) possess large non-degenerate regions on their sex chromosomes (PARs or pseudoautosomal regions). It remains unclear why these large PARs are retained over more than 100 MY, and how this retention impacts the evolution of sex chromosomes within this system. To address this puzzle, we analysed Z chromosome evolution and gene expression across 12 paleognaths, several of whose genomes have recently been sequenced. We confirm at the genomic level that most paleognaths retain large PARs. As in other birds, we find that all paleognaths have incomplete dosage compensation on the regions of the Z chromosome homologous to degenerated portions of the W (differentiated regions or DRs), but we find no evidence for enrichments of male-biased genes in PARs. We find limited evidence for increased evolutionary rates (faster-Z) either across the chromosome or in DRs for most paleognaths with large PARs, but do recover signals of faster-Z evolution in tinamou species with mostly degenerated W chromosomes, similar to the pattern seen in neognaths. Unexpectedly, in some species PAR-linked genes evolve faster on average than genes on autosomes, suggested by diverse genomic features to be due to reduced efficacy of selection in paleognath PARs. Our analysis shows that paleognath Z chromosomes are atypical at the genomic level, but the evolutionary forces maintaining largely homomorphic sex chromosomes in these species remain elusive.

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Sexually dimorphic recombination can facilitate the establishment of sexually antagonistic polymorphisms in guppies

10.1101/365114 ◽

2018 ◽

Cited By ~ 1

Author(s):

Roberta Bergero ◽

Jim Gardner ◽

Beth Bader ◽

Lengxob Yong ◽

Deborah Charlesworth

Keyword(s):

Sex Chromosomes ◽

Poecilia Reticulata ◽

Common Ancestor ◽

Sex Chromosome ◽

Empirical Support ◽

Male Meiosis ◽

Sexually Dimorphic ◽

Sex Linkage ◽

Recombination Suppression ◽

Males And Females

Summary/AbstractRecombination suppression between sex chromosomes is often stated to evolve in response to polymorphisms for mutations that affect fitness of males and females in opposite directions (sexually antagonistic, or SA, mutations), but direct empirical support is lacking. The sex chromosomes of the fish Poecilia reticulata (the guppy) carry SA polymorphisms, making them excellent for testing this hypothesis for the evolution of sex linkage. We resequenced genomes of male and female guppies and, unexpectedly, found that variants on the sex chromosome indicate no extensive region with fully sex-linked genotypes, though many variants show strong evidence for partial sex linkage. We present genetic mapping results that help understand the evolution of the guppy sex chromosome pair. We find very different distributions of crossing over in the two sexes, with recombination events in male meiosis detected only at the tips of the chromosomes. The guppy may exemplify a route for sex chromosome evolution in which low recombination in males, likely evolved in a common ancestor, has facilitated the establishment of sexually antagonistic polymorphisms.

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A comparison of methodological approaches to the study of young sex chromosomes: A case study in Poecilia

10.1101/2021.11.29.470452 ◽

2021 ◽

Author(s):

Iulia Darolti ◽

Pedro Almeida ◽

Alison E Wright ◽

Judith E Mank

Keyword(s):

Sex Chromosomes ◽

Reference Genome ◽

Sex Chromosome ◽

De Novo ◽

Sequence Similarity ◽

Sequence Evolution ◽

Structural Variations ◽

Recombination Suppression ◽

Custom Made ◽

Methodological Approaches

Studies of sex chromosome systems at early stages of divergence are key to understanding the initial process and underlying causes of recombination suppression. However, identifying signatures of divergence in homomorphic sex chromosomes can be challenging due to high levels of sequence similarity between the X and the Y. Variations in methodological precision and underlying data can make all the difference between detecting subtle divergence patterns or missing them entirely. Recent efforts to test for X-Y sequence differentiation in the guppy have led to contradictory results. Here we apply different analytical methodologies to the same dataset to test for the accuracy of different approaches in identifying patterns of sex chromosome divergence in the guppy. Our comparative analysis reveals that the most substantial source of variation in the results of the different analyses lies in the reference genome used. Analyses using custom-made de novo genome assemblies for the focal species successfully recover a signal of divergence across different methodological approaches. By contrast, using the distantly related Xiphophorus reference genome results in variable patterns, due to both sequence evolution and structural variations on the sex chromosomes between the guppy and Xiphophorus. Changes in mapping and filtering parameters can additionally introduce noise and obscure the signal. Our results illustrate how analytical differences can alter perceived results and we highlight best practices for the study of nascent sex chromosomes.

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