Plant sex determination and sex chromosomes

Sex determination systems in plants have evolved many times from hermaphroditic ancestors (including monoecious plants with separate male and female flowers on the same individual), and sex chromosome systems have arisen several times in flowering plant evolution. Consistent with theoretical models for the evolutionary transition from hermaphroditism to monoecy, multiple sex determining genes are involved, including male-sterility and female-sterility factors. The requirement that recombination should be rare between these different loci is probably the chief reason for the genetic degeneration of Y chromosomes. Theories for Y chromosome degeneration are reviewed in the light of recent results from genes on plant sex chromosomes.     

The evolution of sex chromosomes

Mammalian sex chromosomes appear, behave and function differently than the autosomes, passing on their genes in a unique sex-linked manner. The publishing of Ohno's hypothesis provided a framework for discussion of sex chromosome evolution, allowing it to be developed and challenged numerous times. In this report we discuss the pressures that drove the evolution of sex and the mechanisms by which it occurred. We concentrate on how the sex chromosomes evolved in mammals, discussing the various hypotheses proposed and the evidence supporting them.     

Plant sex chromosomes: molecular structure and function

Recent molecular and genomic studies carried out in a number of model dioecious plant species, including Asparagus officinalis, Carica papaya, Silene latifolia, Rumex acetosa and Marchantia polymorpha, have shed light on the molecular structure of both homomorphic and heteromorphic sex chromosomes, and also on the gene functions they have maintained since their evolution from a pair of autosomes. The molecular structure of sex chromosomes in species from different plant families represents the evolutionary pathway followed by sex chromosomes during their evolution. The degree of Y chromosome degeneration that accompanies the suppression of recombination between the Xs and Ys differs among species. The primitive Ys of A. officinalis and C. papaya have only diverged from their homomorphic Xs in a short male-specific and non-recombining region (MSY), while the heteromorphic Ys of S. latifolia, R. acetosa and M. polymorpha have diverged from their respective Xs. As in the Y chromosomes of mammals and Drosophila, the accumulation of repetitive DNA, including both transposable elements and satellite DNA, has played an important role in the divergence and size enlargement of plant Ys, and consequently in reducing gene density. Nevertheless, the degeneration process in plants does not appear to have reached the Y-linked genes. Although a low gene density has been found in the sequenced Y chromosome of M. polymorpha, most of its genes are essential and are expressed in the vegetative and reproductive organs in both male and females. Similarly, most of the Y-linked genes that have been isolated and characterized up to now in S. latifolia are housekeeping genes that have X-linked homologues, and are therefore expressed in both males and females. Only one of them seems to be degenerate with respect to its homologous region in the X. Sequence analysis of larger regions in the homomorphic X and Y chromosomes of papaya and asparagus, and also in the heteromorphic sex chromosomes of S. latifolia and R. acetosa, will reveal the degenerative changes that the Y-linked gene functions have experienced during sex chromosome evolution.     

Origin and evolution of mammalian sex chromosomes

Mammals present an XX/XY system of chromosomal sex determination, males being the heterogametic sex. Comparative studies of the gene content of sex chromosomes from the major groups of mammals reveal that most Y genes have X-linked homologues and that X and Y share homologous pseudoautosomal regions. These observations, together with the presence of the two homologous regions (pseudoautosomal regions) at the tips of the sex chromosomes, suggest that these chromosomes began as an ordinary pair of homologous autosomes. Birds present a ZW/ZZ system of chromosomal sex determination where females are the heterogametic sex. In this case, avian sex chromosomes are derived from different pairs of autosomes than mammals. The evolutionary pathway from the autosomal homomorphic departure to the present-day heteromorphic sex chromosomes in mammals includes suppression of X-Y recombination, differentiation of the nascent non-recombining regions, and progressive autosomal addition and attrition of the sex chromosomes. Recent results indicate that the event marking the beginning of the differentiation between the extant X and Y chromosomes occurred about 300 million years ago.     

Satellite DNA and evolution of sex chromosomes

The satellite DNA (satellite III) which is mainly represented in the female of Elaphe radiata (Ophidia, Colubridae) has been isolated and its buoyant density has been determined (=1.700 g cm^–3). In situ hybridisation of radioactive complementary RNA of this satellite DNA with the chromosomes of different species has revealed that it is mainly concentrated on the W sex chromosome and its sequences are conserved throughout the sub-order Ophidia. From hybridisation studies these sequences are absent from the primitive family Boidae which represents a primitive state of differentiation of sex chromosomes. Chromosome analysis and C-banding have also revealed the absence of heteromorphism and of an entirely heterochromatic chromosome in the species belonging to the primitive family and their presence in the species of highly evolved families. It is suggested that the origin of satellite DNA (satellite III) in the W chromosome is the first step in differentiation of W from the Z in snakes by generating asynchrony in the DNA replication pattern of Z and W chromosomes and thus conceivably reducing the frequency of crossing-over between them which is the prerequisite of differentiation of sex chromosomes. Presence of similar sex chromosome associated satellite DNA in domestic chicken suggests its existence in a wider range of vertebrates than just the snakes.     

Steps in the evolution of heteromorphic sex chromosomes

We review some recently published results on sex chromosomes in a diversity of species. We focus on several fish and some plants whose sex chromosomes appear to be 'young', as only parts of the chromosome are nonrecombining, while the rest is pseudoautosomal. However, the age of these systems is not yet very clear. Even without knowing what proportions of their genes are genetically degenerate, these cases are of great interest, as they may offer opportunities to study in detail how sex chromosomes evolve. In particular, we review evidence that recombination suppression occurs progressively in evolutionarily independent cases, suggesting that selection drives loss of recombination over increasingly large regions. We discuss how selection during the period when a chromosome is adapting to its role as a Y chromosome might drive such a process.     

Sex from W to Z: evolution of vertebrate sex chromosomes and sex determining genes

Sex determination in major vertebrate groups appears to be very variable, including systems of male heterogamety, female heterogamety and a variety of genetic and environmental sex determining systems. Yet comparative studies of sex chromosomes and sex determining genes now suggest that these differences are more apparent than real. The sex chromosomes of even widely divergent groups now appear to have changed very little over the last 300+ million years, and even independently derived sex chromosomes seem to have followed the same set of evolutionary rules. The sex determining pathway seems to be extremely conserved, although the control of the genes in this pathway is vested in different elements. We present a scenario for the independent evolution of XY male heterogamety in mammals and ZW female heterogamety in birds and some reptiles. We suggest that sex determining genes can be made redundant, and replaced by control at another step of a conserved sex determining pathway, and how choice of a gene as a sex switch has led to the evolution of new sex chromosome systems. J. Exp. Zool. 290:449-462, 2001.     

Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes

Background  

The regular mammalian X and Y chromosomes diverged from each other at least 166 to 148 million years ago, leaving few traces of their early evolution, including degeneration of the Y chromosome and evolution of dosage compensation.     

A new look at the evolution of avian sex chromosomes

Birds have a ubiquitous, female heterogametic, ZW sex chromosome system. The current model suggests that the Z chromosome and its degraded partner, the W chromosome, evolved from an ancestral pair of autosomes independently from the mammalian XY male heteromorphic sex chromosomes--which are similar in size, but not gene content (Graves, 1995; Fridolfsson et al., 1998). Furthermore the degradation of the W has been proposed to be progressive, with the basal clade of birds (the ratites) possessing virtually homomorphic sex chromosomes and the more recently derived birds (the carinates) possessing highly heteromorphic sex chromosomes (Ohno, 1967; Solari, 1993). Recent findings have suggested an alternative to independent evolution of bird and mammal chromosomes, in which an XY system took over directly from an ancestral ZW system. Here we examine recent research into avian sex chromosomes and offer alternative suggestions as to their evolution.     

The origin and evolution of vertebrate sex chromosomes and dosage compensation

In mammals, birds, snakes and many lizards and fish, sex is determined genetically (either male XY heterogamy or female ZW heterogamy), whereas in alligators, and in many reptiles and turtles, the temperature at which eggs are incubated determines sex. Evidently, different sex-determining systems (and sex chromosome pairs) have evolved independently in different vertebrate lineages. Homology shared by Xs and Ys (and Zs and Ws) within species demonstrates that differentiated sex chromosomes were once homologous, and that the sex-specific non-recombining Y (or W) was progressively degraded. Consequently, genes are left in single copy in the heterogametic sex, which results in an imbalance of the dosage of genes on the sex chromosomes between the sexes, and also relative to the autosomes. Dosage compensation has evolved in diverse species to compensate for these dose differences, with the stringency of compensation apparently differing greatly between lineages, perhaps reflecting the concentration of genes on the original autosome pair that required dosage compensation. We discuss the organization and evolution of amniote sex chromosomes, and hypothesize that dosage insensitivity might predispose an autosome to evolving function as a sex chromosome.     

Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes

The sexual development and virulence of the fungal pathogen Cryptococcus neoformans is controlled by a bipolar mating system determined by a single locus that exists in two alleles, α and a. The α and a mating-type alleles from two divergent varieties were cloned and sequenced. The C. neoformans mating-type locus is unique, spans >100 kb, and contains more than 20 genes. MAT-encoded products include homologs of regulators of sexual development in other fungi, pheromone and pheromone receptors, divergent components of a MAP kinase cascade, and other proteins with no obvious function in mating. The α and a alleles of the mating-type locus have extensively rearranged during evolution and strain divergence but are stable during genetic crosses and in the population. The C. neoformans mating-type locus is strikingly different from the other known fungal mating-type loci, sharing features with the self-incompatibility systems and sex chromosomes of algae, plants, and animals. Our study establishes a new paradigm for mating-type loci in fungi with implications for the evolution of cell identity and self/nonself recognition.     

Mammalian sex chromosomes

The X and Y chromosomes of the musk shrew are the two largest in the complement and they regularly form a single chiasma during meiosis. This chiasma is located in the short arms of the X and Y, both of which show partial C-banding at meiosis. The in vitro incorporation of 5-bromodeoxyuridine/tritiated thymidine during late S reveals that the non-C-band region of the Y finishes replication later than the C-band positive heterochromatin. During meiosis, the sex bivalent opens out early in pachytene to reveal a single chiasma which persists until late metaphase-I. In surface-spread, silver-stained meiocytes, the sex bivalent morphology changes from a phase of extensive pairing to one which includes a visible chiasma through a brief diffuse stage. Observations on C-banded meiocytes show a shift in the sex pair from a C-band positive to a negative state as compared to their corresponding somatic pattern. Comparable changes are also observed in the sex bivalents of other mammals which undergo a chiasmatic exchange. This suggests that in addition to pairing homology, an alteration in the chromatin configuration may be necessary for crossing over to occur between the sex chromosomes.     

Insect sex chromosomes

The two X chromosomes in tetraploid spermatogonial cells from Gryllotalpa fossor respond differentially to the production of chromatid aberrations by ³H-uridine (³H-U). As in diploid female somatic cells, only the euchromatic arm of one X shows such aberrations. The equivalent arm of the other X and the constitutive arms of both Xs are not affected. This differential response of the homologous arms of the two Xs appears to be due to a facultative heterochromatinization of one of them. It is suggested that an imprinting process, which has been assumed to occur during fertilization in other cases of X-inactivation, may not be necessary for the differential regulation of two X chromosomes in this case.     

Insect sex chromosomes

A presumptive mechanism of X inactivation has been investigated by using tritiated uridine-induced chromosome aberrations to distinguish active from inactive X chromosome arms in the insect Gryllotalpa fossor. Previous work on therian mammals has shown that constitutive and facultative heterochromatin are less susceptible to breakage by ³H-Urd than euchromatin (active). The present study indicates that, irrespective of the presence of two X chromosomes in females, only one of these is affected as in males and that the total number of aberrations induced by ³H-Urd in both male and female Gryllotalpa is the same. This suggests that in the female only one arm of one X chromosome is active and that a facultative heterochromatinization of the homologous arm of the other X is operative coupled with the presence of constitutive heterochromatin in the second arm of both X chromosomes.