Sex Chromosomes In Animals Research Articles

Evolution and regulation of animal sex chromosomes.

Animal sex chromosomes typically carry the upstream sex-determining gene that triggers testis or ovary development and, in some species, are regulated by global dosage compensation in response to functional decay of the Y chromosome. Despite the importance of these pathways, they exhibit striking differences across species, raising fundamental questions regarding the mechanisms underlying their evolutionary turnover. Recent studies of non-model organisms, including insects, reptiles and teleosts, have yielded a broad view of the diversity of sex chromosomes that challenges established theories. Moreover, continued studies in model organisms with recently developed technologies have characterized the dynamics of sex determination and dosage compensation in three-dimensional nuclear space and at single-cell resolution. Here, we synthesize recent insights into sex chromosomes from a variety of species to review their evolutionary dynamics with respect to the canonical model, as well as their diverse mechanisms of regulation.

Why should we study plant sex chromosomes?

Understanding plant sex chromosomes involves studying interactions between developmental and physiological genetics, genome evolution, and evolutionary ecology. We focus on areas of overlap between these. Ideas about how species with separate sexes (dioecious species, in plant terminology) can evolve are even more relevant to plants than to most animal taxa because dioecy has evolved many times from ancestral functionally hermaphroditic populations, often recently. One aim of studying plant sex chromosomes is to discover how separate males and females evolved from ancestors with no such genetic sex-determining polymorphism, and the diversity in the genetic control of maleness vs femaleness. Different systems share some interesting features, and their differences help to understand why completely sex-linked regions may evolve. In some dioecious plants, the sex-determining genome regions are physically small. In others, regions without crossing over have evolved sometimes extensive regions with properties very similar to those of the familiar animal sex chromosomes. The differences also affect the evolutionary changes possible when the environment (or pollination environment, for angiosperms) changes, as dioecy is an ecologically risky strategy for sessile organisms. Dioecious plants have repeatedly reverted to cosexuality, and hermaphroditic strains of fruit crops such as papaya and grapes are desired by plant breeders. Sex-linked regions are predicted to become enriched in genes with sex differences in expression, especially when higher expression benefits one sex function but harms the other. Such trade-offs may be important for understanding other plant developmental and physiological processes and have direct applications in plant breeding.

Are plant and animal sex chromosomes really all that different?

Sex chromosomes in plants have often been contrasted with those in animals with the goal of identifying key differences that can be used to elucidate fundamental evolutionary properties. For example, the often homomorphic sex chromosomes in plants have been compared to the highly divergent systems in some animal model systems, such as birds, Drosophila and therian mammals, with many hypotheses offered to explain the apparent dissimilarities, including the younger age of plant sex chromosomes, the lesser prevalence of sexual dimorphism, or the greater extent of haploid selection. Furthermore, many plant sex chromosomes lack complete sex chromosome dosage compensation observed in some animals, including therian mammals, Drosophila, some poeciliids, and Anolis, and plant dosage compensation, where it exists, appears to be incomplete. Even the canonical theoretical models of sex chromosome formation differ somewhat between plants and animals. However, the highly divergent sex chromosomes observed in some animal groups are actually the exception, not the norm, and many animal clades are far more similar to plants in their sex chromosome patterns. This begs the question of how different are plant and animal sex chromosomes, and which of the many unique properties of plants would be expected to affect sex chromosome evolution differently than animals? In fact, plant and animal sex chromosomes exhibit more similarities than differences, and it is not at all clear that they differ in terms of sexual conflict, dosage compensation, or even degree of divergence. Overall, the largest difference between these two groups is the greater potential for haploid selection in plants compared to animals. This may act to accelerate the expansion of the non-recombining region at the same time that it maintains gene function within it. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.

Epigenetics drive the evolution of sex chromosomes in animals and plants.

We review how epigenetics affect sex chromosome evolution in animals and plants. In a few species, sex is determined epigenetically through the action of Y-encoded small RNAs. Epigenetics is also responsible for changing the sex of individuals through time, even in species that carry sex chromosomes, and could favour species adaptation through breeding system plasticity. The Y chromosome accumulates repeats that become epigenetically silenced which leads to an epigenetic conflict with the expression of Y genes and could accelerate Y degeneration. Y heterochromatin can be lost through ageing, which activates transposable elements and lowers male longevity. Y chromosome degeneration has led to the evolution of meiotic sex chromosome inactivation in eutherians (placentals) and marsupials, and dosage compensation mechanisms in animals and plants. X-inactivation convergently evolved in eutherians and marsupials via two independently evolved non-coding RNAs. In Drosophila, male X upregulation by the male specific lethal (MSL) complex can spread to neo-X chromosomes through the transposition of transposable elements that carry an MSL-binding motif. We discuss similarities and possible differences between plants and animals and suggest future directions for this dynamic field of research. This article is part of the theme issue 'How does epigenetics influence the course of evolution?'

The Mutation Rate and the Age of the Sex Chromosomes in Silene latifolia

Many aspects of sex chromosome evolution are common to both plants and animals [1], but the process of Y chromosome degeneration, where genes on the Y become non-functional over time, may be much slower in plants due to purifying selection against deleterious mutations in the haploid gametophyte [2, 3]. Testing for differences in Y degeneration between the kingdoms has been hindered by the absence of accurate age estimates for plant sex chromosomes. Here, we used genome resequencing to estimate the spontaneous mutation rate and theage of the sex chromosomes in white campion (Silene latifolia). Screening of single nucleotide polymorphisms (SNPs) in parents and 10 F1 progeny identified 39 de novo mutations and yielded a rate of 7.31× 10-9 (95% confidence interval: 5.20× 10-9 - 8.00× 10-9) mutations per site per haploid genome per generation. Applying this mutation rate to the synonymous divergence between homologous X- and Y-linked genes (gametologs) gave age estimates of 11.00 and 6.32 million years for the old and young strata, respectively. Based on SNP segregation patterns, we inferred which genes were Y-linked and found that at least 47% are already dysfunctional. Applying our new estimates for the age of the sex chromosomes indicates that the rate of Y degeneration in S.latifolia is nearly 2-fold slower when compared to animal sex chromosomes of a similar age. Our revised estimates support Y degeneration taking place more slowly in plants, a discrepancy that may be explained by differences in the life cycles of animals and plants.

Shared and Species-Specific Patterns of Nascent Y Chromosome Evolution in Two Guppy Species.

Sex chromosomes form once recombination is halted around the sex-determining locus between a homologous pair of chromosomes, resulting in a male-limited Y chromosome. We recently characterized the nascent sex chromosome system in the Trinidadian guppy (Poecilia reticulata). The guppy Y is one of the youngest animal sex chromosomes yet identified, and therefore offers a unique window into the early evolutionary forces shaping sex chromosome formation, particularly the rate of accumulation of repetitive elements and Y-specific sequence. We used comparisons between male and female genomes in P. reticulata and its sister species, Endler’s guppy (P. wingei), which share an ancestral sex chromosome, to identify male-specific sequences and to characterize the degree of differentiation between the X and Y chromosomes. We identified male-specific sequence shared between P. reticulata and P. wingei consistent with a small ancestral non-recombining region. Our assembly of this Y-specific sequence shows substantial homology to the X chromosome, and appears to be significantly enriched for genes implicated in pigmentation. We also found two plausible candidates that may be involved in sex determination. Furthermore, we found that the P. wingei Y chromosome exhibits a greater signature of repetitive element accumulation than the P. reticulata Y chromosome. This suggests that Y chromosome divergence does not necessarily correlate with the time since recombination suppression. Overall, our results reveal the early stages of Y chromosome divergence in the guppy.

Evolutionary Significance of Wolbachia-to-Animal Horizontal Gene Transfer: Female Sex Determination and the f Element in the Isopod Armadillidium vulgare.

An increasing number of horizontal gene transfer (HGT) events from bacteria to animals have been reported in the past years, many of which involve Wolbachia bacterial endosymbionts and their invertebrate hosts. Most transferred Wolbachia genes are neutrally-evolving fossils embedded in host genomes. A remarkable case of Wolbachia HGT for which a clear evolutionary significance has been demonstrated is the “f element”, a nuclear Wolbachia insert involved in female sex determination in the terrestrial isopod Armadillidium vulgare. The f element represents an instance of bacteria-to-animal HGT that has occurred so recently that it was possible to infer the donor (feminizing Wolbachia closely related to the wVulC Wolbachia strain of A. vulgare) and the mechanism of integration (a nearly complete genome inserted by micro-homology-mediated recombination). In this review, we summarize our current knowledge of the f element and discuss arising perspectives regarding female sex determination, unstable inheritance, population dynamics and the molecular evolution of the f element. Overall, the f element unifies three major areas in evolutionary biology: symbiosis, HGT and sex determination. Its characterization highlights the tremendous impact sex ratio distorters can have on the evolution of sex determination mechanisms and sex chromosomes in animals and plants.

Plant Sex Chromosomes

Although individuals in most flowering plant species, and in many haploid plants, have both sex functions, dioecious species-in which individuals have either male or female functions only-are scattered across many taxonomic groups, and many species have genetic sex determination. Among these, some have visibly heteromorphic sex chromosomes, and molecular genetic studies are starting to uncover sex-linked markers in others, showing that they too have fully sex-linked regions that are either too small or are located in chromosomes that are too small to be cytologically detectable from lack of pairing, lack of visible crossovers, or accumulation of heterochromatin. Detailed study is revealing that, like animal sex chromosomes, plant sex-linked regions show evidence for accumulation of repetitive sequences and genetic degeneration. Estimating when recombination stopped confirms the view that many plants have young sex-linked regions, making plants of great interest for studying the timescale of these changes.

Genomics and Transcriptomics Analyses of the Oil-Accumulating Basidiomycete Yeast Trichosporon oleaginosus: Insights into Substrate Utilization and Alternative Evolutionary Trajectories of Fungal Mating Systems.

ABSTRACTMicrobial fermentation of agro-industrial waste holds great potential for reducing the environmental impact associated with the production of lipids for industrial purposes from plant biomass. However, the chemical complexity of many residues currently prevents efficient conversion into lipids, creating a high demand for strains with the ability to utilize all energy-rich components of agricultural residues. Here, we present results of genome and transcriptome analyses of Trichosporon oleaginosus. This oil-accumulating yeast is able to grow on a wide variety of substrates, including pentoses and N-acetylglucosamine, making it an interesting candidate for biotechnological applications. Transcriptomics shows specific changes in gene expression patterns under lipid-accumulating conditions. Furthermore, gene content and expression analyses indicate that T. oleaginosus is well-adapted for the utilization of chitin-rich biomass. We also focused on the T. oleaginosus mating type, because this species is a member of the Tremellomycetes, a group that has been intensively analyzed as a model for the evolution of sexual development, the best-studied member being Cryptococcus neoformans. The structure of the T. oleaginosus mating-type regions differs significantly from that of other Tremellomycetes and reveals a new evolutionary trajectory paradigm. Comparative analysis shows that recruitment of developmental genes to the ancestral tetrapolar mating-type loci occurred independently in the Trichosporon and Cryptococcus lineages, supporting the hypothesis of a trend toward larger mating-type regions in fungi.

Rapid De Novo Evolution of X Chromosome Dosage Compensation in Silene latifolia, a Plant with Young Sex Chromosomes

Author SummaryThe mammalian sex chromosomes originated from an ancestral pair of autosomes about 150 million years ago and the Y chromosome subsequently degenerated, losing most of its genes. During this process, a phenomenon called dosage compensation evolved to compensate for the gene loss on the Y chromosome and to equalize expression of X-linked genes in the two sexes. In humans, this is achieved by inactivating one of the two X chromosomes in females. Dosage compensation has also been reported in other animal XY systems such as fruit flies and worms, each 100 million years old or more. Here we studied dosage compensation in plants. We used high-throughput RNA sequencing in male and female Silene latifolia (white campion)—a dioecious plant whose XY chromosomes originated only about 10 million years ago—to identify hundreds of sex-linked genes. Analysis of their expression patterns in males and females revealed equal doses of sex-linked transcripts in both sexes, regardless of the degree of reduction of Y expression due to degeneration. Our results thus show that dosage compensation occurs in plants and is thus not an animal-specific phenomenon. They also reveal that proportionate dosage compensation can evolve rapidly de novo after the origin of sex chromosomes.

Sex Chromosome Equality in Plants

Sex Chromosome Equality in Plants

Contrasted Patterns of Molecular Evolution in Dominant and Recessive Self-Incompatibility Haplotypes in Arabidopsis

Self-incompatibility has been considered by geneticists a model system for reproductive biology and balancing selection, but our understanding of the genetic basis and evolution of this molecular lock-and-key system has remained limited by the extreme level of sequence divergence among haplotypes, resulting in a lack of appropriate genomic sequences. In this study, we report and analyze the full sequence of eleven distinct haplotypes of the self-incompatibility locus (S-locus) in two closely related Arabidopsis species, obtained from individual BAC libraries. We use this extensive dataset to highlight sharply contrasted patterns of molecular evolution of each of the two genes controlling self-incompatibility themselves, as well as of the genomic region surrounding them. We find strong collinearity of the flanking regions among haplotypes on each side of the S-locus together with high levels of sequence similarity. In contrast, the S-locus region itself shows spectacularly deep gene genealogies, high variability in size and gene organization, as well as complete absence of sequence similarity in intergenic sequences and striking accumulation of transposable elements. Of particular interest, we demonstrate that dominant and recessive S-haplotypes experience sharply contrasted patterns of molecular evolution. Indeed, dominant haplotypes exhibit larger size and a much higher density of transposable elements, being matched only by that in the centromere. Overall, these properties highlight that the S-locus presents many striking similarities with other regions involved in the determination of mating-types, such as sex chromosomes in animals or in plants, or the mating-type locus in fungi and green algae.

The sex-specific region of sex chromosomes in animals and plants

Our understanding of the evolution of sex chromosomes has increased greatly in recent years due to a number of molecular evolutionary investigations in divergent sex chromosome systems, and these findings are reshaping theories of sex chromosome evolution. In particular, the dynamics of the sex-determining region (SDR) have been demonstrated by recent findings in ancient and incipient sex chromosomes. Radical changes in genomic structure and gene content in the male specific region of the Y chromosome between human and chimpanzee indicated rapid evolution in the past 6 million years, defying the notion that the pace of evolution in the SDR was fast at early stages but slowed down overtime. The chicken Z and the human X chromosomes appeared to have acquired testis-expressed genes and expanded in intergenic regions. Transposable elements greatly contributed to SDR expansion and aided the trafficking of genes in the SDR and its X or Z counterpart through retrotransposition. Dosage compensation is not a destined consequence of sex chromosomes as once thought. Most X-linked microRNA genes escape silencing and are expressed in testis. Collectively, these findings are challenging many of our preconceived ideas of the evolutionary trajectory and fates of sex chromosomes.

Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the Filamentous FungusNeurospora tetrasperma

A large region of suppressed recombination surrounds the sex-determining locus of the self-fertile fungus Neurospora tetrasperma. This region encompasses nearly one-fifth of the N. tetrasperma genome and suppression of recombination is necessary for self-fertility. The similarity of the N. tetrasperma mating chromosome to plant and animal sex chromosomes and its recent origin (<5 MYA), combined with a long history of genetic and cytological research, make this fungus an ideal model for studying the evolutionary consequences of suppressed recombination. Here we compare genome sequences from two N. tetrasperma strains of opposite mating type to determine whether structural rearrangements are associated with the nonrecombining region and to examine the effect of suppressed recombination for the evolution of the genes within it. We find a series of three inversions encompassing the majority of the region of suppressed recombination and provide evidence for two different types of rearrangement mechanisms: the recently proposed mechanism of inversion via staggered single-strand breaks as well as ectopic recombination between transposable elements. In addition, we show that the N. tetrasperma mat a mating-type region appears to be accumulating deleterious substitutions at a faster rate than the other mating type (mat A) and thus may be in the early stages of degeneration.

Drosophila MUS312 and the Vertebrate Ortholog BTBD12 Interact with DNA Structure-Specific Endonucleases in DNA Repair and Recombination

DNA recombination and repair pathways require structure-specific endonucleases to process DNA structures that include forks, flaps, and Holliday junctions. Previously, we determined that the Drosophila MEI-9-ERCC1 endonuclease interacts with the MUS312 protein to produce meiotic crossovers, and that MUS312 has a MEI-9-independent role in interstrand crosslink (ICL) repair. The importance of MUS312 to pathways crucial for maintaining genomic stability in Drosophila prompted us to search for orthologs in other organisms. Based on sequence, expression pattern, conserved protein-protein interactions, and ICL repair function, we determined that the mammalian ortholog of MUS312 is BTBD12. Orthology between these proteins and S. cerevisiae Slx4 helped identify a conserved interaction with a second structure-specific endonuclease, SLX1. Genetic and biochemical evidence described here and in related papers suggest that MUS312 and BTBD12 direct Holliday junction resolution by at least two distinct endonucleases in different recombination and repair contexts.

Chromosomal location and gene paucity of the male specific region on papaya Y chromosome

Sex chromosomes in flowering plants evolved recently and many of them remain homomorphic, including those in papaya. We investigated the chromosomal location of papaya's small male specific region of the hermaphrodite Y (Yh) chromosome (MSY) and its genomic features. We conducted chromosome fluorescence in situ hybridization mapping of Yh-specific bacterial artificial chromosomes (BACs) and placed the MSY near the centromere of the papaya Y chromosome. Then we sequenced five MSY BACs to examine the genomic features of this specialized region, which resulted in the largest collection of contiguous genomic DNA sequences of a Y chromosome in flowering plants. Extreme gene paucity was observed in the papaya MSY with no functional gene identified in 715 kb MSY sequences. A high density of retroelements and local sequence duplications were detected in the MSY that is suppressed for recombination. Location of the papaya MSY near the centromere might have provided recombination suppression and fostered paucity of genes in the male specific region of the Y chromosome. Our findings provide critical information for deciphering the sex chromosomes in papaya and reference information for comparative studies of other sex chromosomes in animals and plants.

Suppressed recombination and a pairing anomaly on the mating-type chromosome of Neurospora tetrasperma.

Neurospora crassa and related heterothallic ascomycetes produce eight homokaryotic self-sterile ascospores per ascus. In contrast, asci of N. tetrasperma contain four self-fertile ascospores each with nuclei of both mating types (matA and mata). The self-fertile ascospores of N. tetrasperma result from first-division segregation of mating type and nuclear spindle overlap at the second meiotic division and at a subsequent mitotic division. Recently, Merino et al. presented population-genetic evidence that crossing over is suppressed on the mating-type chromosome of N. tetrasperma, thereby preventing second-division segregation of mating type and the formation of self-sterile ascospores. The present study experimentally confirmed suppressed crossing over for a large segment of the mating-type chromosome by examining segregation of markers in crosses of wild strains. Surprisingly, our study also revealed a region on the far left arm where recombination is obligatory. In cytological studies, we demonstrated that suppressed recombination correlates with an extensive unpaired region at pachytene. Taken together, these results suggest an unpaired region adjacent to one or more paired regions, analogous to the nonpairing and pseudoautosomal regions of animal sex chromosomes. The observed pairing and obligate crossover likely reflect mechanisms to ensure chromosome disjunction.