Special Issue "Sex Chromosome Evolution and Meiosis"

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Molecular Genetics and Genomics".

Deadline for manuscript submissions: closed (20 September 2021).

Special Issue Editors

Dr. Frederic Veyrunes
E-Mail Website
Guest Editor
Institut des Sciences de l’Évolution de Montpellier (ISEM), Université de Montpellier, Place Eugène Bataillon, 34095 Montpellier CEDEX 05, France
Interests: sex chromosome; sex determination; chromosomal evolution; genomics; transcriptomics; behavior
Dr. Frederic Baudat
E-Mail Website
Guest Editor
Institut de Génétique Humaine (IGH), CNRS, Université de Montpellier, 141 rue de la Cardonille, Montpellier, France
Interests: meiosis; homologous recombination; DNA repair; evolution of recombination
Dr. Jesús Page
E-Mail Website
Guest Editor
Department of Biology, Universidad Autónoma de Madrid, 28049 Madrid, Spain
Interests: sex Chromosomes; meiosis; homologous recombination; chromosome segregation; chromosome evolution; chromatin; cytogenetics

Special Issue Information

Dear Colleagues,

From the early days of study of genetics and – with ever refined research tools – up to the present time, sex chromosomes have always been a source of fascination. At least three features set sex chromosomes apart from the rest of the genome and drive their unique evolution: the unusual pattern of transmission, the lack of recombination on sex-specific regions, and the absence of synapsis once the two sex chromosomes become divergent enough.

All these three features take place during meiosis, which makes this process the key component to understanding the evolution and differentiation of sex chromosomes. Surprisingly, however, the meiotic behaviour of sex chromosomes and the cellular context in which it happens have received little attention so far.

In this Special Issue, we aim to fill this gap by exploring the large diversity of sex chromosome systems and how the tightly choreographed process of meiosis copes with this. We hope that the table of contents will illustrate this diversity, and that multiple model systems, meiotic processes, and disciplines will be covered. We also seek to provide an overview of the advancements in our understanding of the meiotic contexts in which sex chromosomes arise and evolve.

Dr. Frederic Veyrunes
Dr. Frederic Baudat
Dr. Jesús Page
Guest Editors

Manuscript Submission Information

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Keywords

  • Meiosis
  • Sex chromosome
  • Synapsis
  • Recombination
  • Meiotic sex chromosome inactivation
  • Chromatin
  • Evolution

Published Papers (6 papers)

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Research

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Article
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 2021, 12(9), 1434; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12091434 - 17 Sep 2021
Viewed by 595
Abstract
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue Sex Chromosome Evolution and Meiosis)
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Article
Highly Conservative Pattern of Sex Chromosome Synapsis and Recombination in Neognathae Birds
Genes 2021, 12(9), 1358; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12091358 - 29 Aug 2021
Cited by 1 | Viewed by 866
Abstract
We analyzed the synapsis and recombination between Z and W chromosomes in the oocytes of nine neognath species: domestic chicken Gallus gallus domesticus, grey goose Anser anser, black tern Chlidonias niger, common tern Sterna hirundo, pale martin Riparia diluta [...] Read more.
We analyzed the synapsis and recombination between Z and W chromosomes in the oocytes of nine neognath species: domestic chicken Gallus gallus domesticus, grey goose Anser anser, black tern Chlidonias niger, common tern Sterna hirundo, pale martin Riparia diluta, barn swallow Hirundo rustica, European pied flycatcher Ficedula hypoleuca, great tit Parus major and white wagtail Motacilla alba using immunolocalization of SYCP3, the main protein of the lateral elements of the synaptonemal complex, and MLH1, the mismatch repair protein marking mature recombination nodules. In all species examined, homologous synapsis occurs in a short region of variable size at the ends of Z and W chromosomes, where a single recombination nodule is located. The remaining parts of the sex chromosomes undergo synaptic adjustment and synapse non-homologously. In 25% of ZW bivalents of white wagtail, synapsis and recombination also occur at the secondary pairing region, which probably resulted from autosome−sex chromosome translocation. Using FISH with a paint probe specific to the germline-restricted chromosome (GRC) of the pale martin on the oocytes of the pale martin, barn swallow and great tit, we showed that both maternally inherited songbird chromosomes (GRC and W) share common sequences. Full article
(This article belongs to the Special Issue Sex Chromosome Evolution and Meiosis)
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Article
Evolution, Expression and Meiotic Behavior of Genes Involved in Chromosome Segregation of Monotremes
Genes 2021, 12(9), 1320; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12091320 - 26 Aug 2021
Viewed by 650
Abstract
Chromosome segregation at mitosis and meiosis is a highly dynamic and tightly regulated process that involves a large number of components. Due to the fundamental nature of chromosome segregation, many genes involved in this process are evolutionarily highly conserved, but duplications and functional [...] Read more.
Chromosome segregation at mitosis and meiosis is a highly dynamic and tightly regulated process that involves a large number of components. Due to the fundamental nature of chromosome segregation, many genes involved in this process are evolutionarily highly conserved, but duplications and functional diversification has occurred in various lineages. In order to better understand the evolution of genes involved in chromosome segregation in mammals, we analyzed some of the key components in the basal mammalian lineage of egg-laying mammals. The chromosome passenger complex is a multiprotein complex central to chromosome segregation during both mitosis and meiosis. It consists of survivin, borealin, inner centromere protein, and Aurora kinase B or C. We confirm the absence of Aurora kinase C in marsupials and show its absence in both platypus and echidna, which supports the current model of the evolution of Aurora kinases. High expression of AURKBC, an ancestor of AURKB and AURKC present in monotremes, suggests that this gene is performing all necessary meiotic functions in monotremes. Other genes of the chromosome passenger complex complex are present and conserved in monotremes, suggesting that their function has been preserved in mammals. Cohesins are another family of genes that are of vital importance for chromosome cohesion and segregation at mitosis and meiosis. Previous work has demonstrated an accumulation and differential loading of structural maintenance of chromosomes 3 (SMC3) on the platypus sex chromosome complex at meiotic prophase I. We investigated if a similar accumulation occurs in the echidna during meiosis I. In contrast to platypus, SMC3 was only found on the synaptonemal complex in echidna. This indicates that the specific distribution of SMC3 on the sex chromosome complex may have evolved specifically in platypus. Full article
(This article belongs to the Special Issue Sex Chromosome Evolution and Meiosis)
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Article
Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom Agaricus bisporus
Genes 2021, 12(7), 1079; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12071079 - 16 Jul 2021
Viewed by 676
Abstract
In heterothallic basidiomycete fungi, sexual compatibility is restricted by mating types, typically controlled by two loci: PR, encoding pheromone precursors and pheromone receptors, and HD, encoding two types of homeodomain transcription factors. We analysed the single mating-type locus of the commercial [...] Read more.
In heterothallic basidiomycete fungi, sexual compatibility is restricted by mating types, typically controlled by two loci: PR, encoding pheromone precursors and pheromone receptors, and HD, encoding two types of homeodomain transcription factors. We analysed the single mating-type locus of the commercial button mushroom variety, Agaricus bisporus var. bisporus, and of the related variety burnettii. We identified the location of the mating-type locus using genetic map and genome information, corresponding to the HD locus, the PR locus having lost its mating-type role. We found the mip1 and β-fg genes flanking the HD genes as in several Agaricomycetes, two copies of the β-fg gene, an additional HD2 copy in the reference genome of A. bisporus var. bisporus and an additional HD1 copy in the reference genome of A. bisporus var. burnettii. We detected a 140 kb-long inversion between mating types in an A. bisporus var. burnettii heterokaryon, trapping the HD genes, the mip1 gene and fragments of additional genes. The two varieties had islands of transposable elements at the mating-type locus, spanning 35 kb in the A. bisporus var. burnettii reference genome. Linkage analyses showed a region with low recombination in the mating-type locus region in the A. bisporus var. burnettii variety. We found high differentiation between β-fg alleles in both varieties, indicating an ancient event of recombination suppression, followed more recently by a suppression of recombination at the mip1 gene through the inversion in A. bisporus var. burnettii and a suppression of recombination across whole chromosomes in A. bisporus var. bisporus, constituting stepwise recombination suppression as in many other mating-type chromosomes and sex chromosomes. Full article
(This article belongs to the Special Issue Sex Chromosome Evolution and Meiosis)
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Review

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Review
Lizards as Model Organisms of Sex Chromosome Evolution: What We Really Know from a Systematic Distribution of Available Data?
Genes 2021, 12(9), 1341; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12091341 - 28 Aug 2021
Viewed by 469
Abstract
Lizards represent unique model organisms in the study of sex determination and sex chromosome evolution. Among tetrapods, they are characterized by an unparalleled diversity of sex determination systems, including temperature-dependent sex determination (TSD) and genetic sex determination (GSD) under either male or female [...] Read more.
Lizards represent unique model organisms in the study of sex determination and sex chromosome evolution. Among tetrapods, they are characterized by an unparalleled diversity of sex determination systems, including temperature-dependent sex determination (TSD) and genetic sex determination (GSD) under either male or female heterogamety. Sex chromosome systems are also extremely variable in lizards. They include simple (XY and ZW) and multiple (X1X2Y and Z1Z2W) sex chromosome systems and encompass all the different hypothesized stages of diversification of heterogametic chromosomes, from homomorphic to heteromorphic and completely heterochromatic sex chromosomes. The co-occurrence of TSD, GSD and different sex chromosome systems also characterizes different lizard taxa, which represent ideal models to study the emergence and the evolutionary drivers of sex reversal and sex chromosome turnover. In this review, we present a synthesis of general genome and karyotype features of non-snakes squamates and discuss the main theories and evidences on the evolution and diversification of their different sex determination and sex chromosome systems. We here provide a systematic assessment of the available data on lizard sex chromosome systems and an overview of the main cytogenetic and molecular methods used for their identification, using a qualitative and quantitative approach. Full article
(This article belongs to the Special Issue Sex Chromosome Evolution and Meiosis)
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Review
Flavors of Non-Random Meiotic Segregation of Autosomes and Sex Chromosomes
Genes 2021, 12(9), 1338; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12091338 - 28 Aug 2021
Cited by 1 | Viewed by 589
Abstract
Segregation of chromosomes is a multistep process occurring both at mitosis and meiosis to ensure that daughter cells receive a complete set of genetic information. Critical components in the chromosome segregation include centromeres, kinetochores, components of sister chromatid and homologous chromosomes cohesion, microtubule [...] Read more.
Segregation of chromosomes is a multistep process occurring both at mitosis and meiosis to ensure that daughter cells receive a complete set of genetic information. Critical components in the chromosome segregation include centromeres, kinetochores, components of sister chromatid and homologous chromosomes cohesion, microtubule organizing centres, and spindles. Based on the cytological work in the grasshopper Brachystola, it has been accepted for decades that segregation of homologs at meiosis is fundamentally random. This ensures that alleles on chromosomes have equal chance to be transmitted to progeny. At the same time mechanisms of meiotic drive and an increasing number of other examples of non-random segregation of autosomes and sex chromosomes provide insights into the underlying mechanisms of chromosome segregation but also question the textbook dogma of random chromosome segregation. Recent advances provide a better understanding of meiotic drive as a prominent force where cellular and chromosomal changes allow autosomes to bias their segregation. Less understood are mechanisms explaining observations that autosomal heteromorphism may cause biased segregation and regulate alternating segregation of multiple sex chromosome systems or translocation heterozygotes as an extreme case of non-random segregation. We speculate that molecular and cytological mechanisms of non-random segregation might be common in these cases and that there might be a continuous transition between random and non-random segregation which may play a role in the evolution of sexually antagonistic genes and sex chromosome evolution. Full article
(This article belongs to the Special Issue Sex Chromosome Evolution and Meiosis)
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