Independent origin of sex chromosomes in two species of the genus Silene

Here we introduce a new model species, Silene colpophylla, that could facilitate research of sex chromosome evolution and sex-determining systems. This species is related to the well-established dioecious plant model Silene latifolia. Our results show that S. colpophylla is, similarly to S. latifolia, a male heterogametic species, but its sex chromosomes have evolved from a different pair of autosomes than in S. latifolia. The results of our phylogenetic study and mapping of homologs of S. latifolia X-linked genes indicate that the sex determination system in S. colpophylla evolved independently from that in S. latifolia. We assert that this model species pair will make it possible to study two independent patterns of sex chromosome evolution in related species.     

Genetics of dioecy and causal sex chromosomes in plants

Dioecy (separate male and female individuals) ensures outcrossing and is more prevalent in animals than in plants. Although it is common in bryophytes and gymnosperms, only 5% of angiosperms are dioecious. In dioecious higher plants, flowers borne on male and female individuals are, respectively deficient in functional gynoecium and roecium. Dioecy is inherited via three sex chromosome systems: XX/XY, XX/X0 and WZ/ZZ, such that XX or WZ is female and XY, X0 or ZZ are males. The XX/XY system generates the rarer XX/X0 and WZ/ZZ systems. An autosome pair begets XY chromosomes. A recessive loss-of-androecium mutation (ana) creates X chromosome and a dominant gynoecium-suppressing (GYS) mutation creates Y chromosome. The ana/ANA and gys/GYS loci are in the sex-determining region (SDR) of the XY pair. Accumulation of inversions, deleterious mutations and repeat elements, especially transposons, in the SDR of Y suppresses recombination between X and Y in SDR, making Y labile and increasingly degenerate and heteromorphic from X. Continued recombination between X and Y in their pseudoautosomal region located at the ends of chromosomal arms allows survival of the degenerated Y and of the species. Dioecy is presumably a component of the evolutionary cycle for the origin of new species. Inbred hermaphrodite species assume dioecy. Later they suffer degenerate-Y-led population regression. Cross-hybridization between such extinguishing species and heterologous species, followed by genome duplication of segregants from hybrids, give rise to new species.     

Multiple nuclear genes stabilize the phylogenetic backbone of the genus Quercus

Phylogenetic relationships among 108 oak species (genus Quercus L.) were inferred using DNA sequences of six nuclear genes selected from the existing genomic resources of the genus. Previous phylogenetic reconstructions based on traditional molecular markers are inconclusive at the deeper nodes. Overall, weak phylogenetic signals were obtained for each individual gene analysis, but stronger signals were obtained when gene sequences were concatenated. Our data support the recognition of six major intrageneric groups Cyclobalanopsis, Cerris, Ilex, Quercus, Lobatae and Protobalanus. Our analyses provide resolution at deeper nodes but with moderate support and a more robust infrageneric classification within the two major clades, the ‘Old World Oaks’ (Cyclobalanopsis, Cerris, Ilex) and ‘New World Oaks’ (Quercus, Lobatae, Protobalanus). However, depending on outgroup choice, our analysis yielded two alternative placements of the Cyclobalanopsis clade within the genus Quercus. When Castanea Mill. was chosen as outgroup, our data suggested that the genus Quercus comprised two clades corresponding to two subgenera as traditionally recognized by Camus: subgenus Euquercus Hickel and Camus and subgenus Cyclobalanopsis Øersted (Schneider). However, when Notholithocarpus Manos, Cannon and S. Oh was chosen as an outgroup subgenus Cyclobalanopsis clustered with Cerris and Ilex groups to form the Old World clade. To assess the placement of the root, we complemented our dataset with published data of ITS and CRC sequences. Based on the concatenated eight gene sequences, the most likely root position is at the split between the ‘Old World Oaks’ and the ‘New World Oaks’, which is one of the alternative positions suggested by our six gene analysis. Using a dating approach, we inferred an Eocene age for the primary divergences in Quercus and a root age of about 50–55 Ma, which agrees with palaeobotanical evidence. Finally, irrespective of the outgroup choice, our data boost the topology within the New World clade, where (Protobalanus + Quercus) is a sister clade of Lobatae. Inferred divergence ages within this clade and the Cerris–Ilex clade are generally younger than could be expected from the fossil record, indicating that morphological differentiation pre-dates genetic isolation in this clade.     

The sex chromosomes of Silene latifolia revisited and revised

Classical studies have established that, during meiosis, the X and Y chromosomes of the model dioecious plant Silene latifolia pair over a region at the ends of their q arms. We used fluorescence in situ hybridization of two molecular markers to demonstrate that this widely accepted model is incorrect. From these data we conclude that the homologous arm of the X chromosome is the p arm and that of the Y chromosome is the q arm. The establishment of the proper orientation of the pseudoautosomal region is essential for mapping and evolutionary studies.     

The origin and evolution of sex chromosomes,revealed by sequencing of the Silene latifolia female genome

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Ultrastructure,meiotic behavior,and evolution of sex chromosomes of the genus Ellobius

The whole-mount SC preparations from males of three species of the genus Ellobius (Ellobius fuscocapillus, Ellobius lutescens), and Ellobius tancrei were studied by electron microscopy. In the males of Ellobius fuscocapillus, behavioral peculiarities of the sex bivalent (viz. the normal male heterozygosity) are characterized by early complete desynapsis of sex chromosomes (X, Y), occurring at late pachytene-early diplotene. The karyotype of species Ellobius lutescens is unique for mammals. In both sexes it is characterized by an odd number of chromosomes (2n=17). At prophase I the unpaired chromosome 9 is not involved in synapsis with other chromosomes and forms a sex body at the end of pachytene.The complete Robertsonian fan has been described for superspecies Ellobius tancrei. As shown on the basis of G-band patterns the male and female sex chromosomes are cytologically indistinguishable.Analysis of whole-mount SC preparations revealed the formation of a closed sex SC bivalent and showed some morphological differences in the axes of sex chromosomes at meiotic prophase I. A number of assumptions are made about the relationship between the behavior of sex chromosomes, their evolution and the sex determination system in the studied species of genus Ellobius.

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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.     

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.     

The evolution of dioecy, heterodichogamy, and labile sex expression in Acer

The northern hemisphere tree genus Acer comprises 124 species, most of them monoecious, but 13 dioecious. The monoecious species flower dichogamously, duodichogamously (male, female, male), or in some species heterodichogamously (two morphs that each produce male and female flowers but at reciprocal times). Dioecious species cannot engage in these temporal strategies. Using a phylogeny for 66 species and subspecies obtained from 6600 nucleotides of chloroplast introns, spacers, and a protein-coding gene, we address the hypothesis (Pannell and Verdú, Evolution 60: 660-673. 2006) that dioecy evolved from heterodichogamy. This hypothesis was based on phylogenetic analyses (Gleiser and Verdú, New Phytol. 165: 633-640. 2005) that included 29-39 species of Acer coded for five sexual strategies (duodichogamous monoecy, heterodichogamous androdioecy, heterodichogamous trioecy, dichogamous subdioecy, and dioecy) treated as ordered states or as a single continuous variable. When reviewing the basis for these scorings, we found errors that together with the small taxon sample, cast doubt on the earlier inferences. Based on published studies, we coded 56 species of Acer for four sexual strategies, dioecy, monoecy with dichogamous or duodichogamous flowering, monoecy with heterodichogamous flowering, or labile sex expression, in which individuals reverse their sex allocation depending on environment-phenotype interactions. Using Bayesian character mapping, we infer an average of 15 transformations, a third of them involving changes from monoecy-cum-duodichogamy to dioecy; less frequent were changes from this strategy to heterodichogamy; dioecy rarely reverts to other sexual systems. Contra the earlier inferences, we found no switches between heterodichogamy and dioecy. Unexpectedly, most of the species with labile sex expression are grouped together, suggesting that phenotypic plasticity in Acer may be a heritable sexual strategy. Because of the complex flowering phenologies, however, a concern remains that monoecy in Acer might not always be distinguishable from labile sex expression, which needs to be addressed by long-term monitoring of monoecious trees. The 13 dioecious species occur in phylogenetically disparate clades that date back to the Late Eocene and Oligocene, judging from a fossil-calibrated relaxed molecular clock.     

Androdioecy and the evolution of dioecy

The likelihood that dioecy could evolve via androdioecy is examined. It is concluded that female-sterility mutations are unlikely to be able to invade populations of self-compatible hermaphrodite species, even if the resources that an hermaphrodite devotes to seed production can be diverted to yield increased survival and also to increase male fertility. These findings are in agreement with the great rarity of androdioecy. Claimed cases of androdioecy are reviewed. All of the species in question appear to be functionally dioecious, with females retaining substantial anther vestiges. It is argued that this morphological androdioecy is in no way indicative of a previous functionally androdioecious state. The details of the reproductive biology of many of these species seem rather to be consistent with their having evolved dioecy via gynodioecy.
The rarity of androdioecy, as a route to the evolution of dioecy, suggests that re-allocation of reproductive resources is unlikely to be the sole factor of importance, and supports an important role for inbreeding avoidance. The fact that females in some dioecious species retain anthers of substantial size, containing considerable quantities of pollen, gives further support to the view that male-sterility mutations can sometimes be favoured even when little or no resources are re-allocated to male functions. This is impossible without substantial selfing and inbreeding. It is therefore concluded that inbreeding avoidance is generally important in the evolution of dioecy, though reallocation of reproductive resources is also necessary.     

C-banded karyotypes of two Silene species with heteromorphic sex chromosomes.

Mitotic metaphase chromosomes of Silene latifolia (white campion) and Silene dioica (red campion) were studied and no substantial differences between the conventional karyotypes of these two species were detected. The classification of chromosomes into three distinct groups proposed for S. latifolia by Ciupercescu and colleagues was considered and discussed. Additionally, a new small satellite on the shorter arm of homobrachial chromosome 5 was found. Giemsa C-banded chromosomes of the two analysed species show many fixed and polymorphic heterochromatic bands, mainly distally and centromerically located. Our C-banding studies provided an opportunity to better characterize the sex chromosomes and some autosome types, and to detect differences between the two Silene karyotypes. It was shown that S. latifolia possesses a larger amount of polymorphic heterochromatin, especially of the centromeric type. The two Silene sex chromosomes are easily distinguishable not only by length or DNA amount differences but also by their Giemsa C-banding patterns. All Y chromosomes invariably show only one distally located band, and no other fixed or polymorphic bands on this chromosome were observed in either species. The X chromosomes possess two terminally located fixed bands, and some S. latifolia X chromosomes also have an extra-centric segment of variable length. The heterochromatin amount and distribution revealed by our Giemsa C-banding studies provide a clue to the problem of sex chromosome and karyotype evolution in these two closely related dioecious Silene species.     

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.     

Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes

Silene latifolia is a dioecious plant with heteromorphic sex chromosomes that have originated only ～10 million years ago and is a promising model organism to study sex chromosome evolution in plants. Previous work suggests that S. latifolia XY chromosomes have gradually stopped recombining and the Y chromosome is undergoing degeneration as in animal sex chromosomes. However, this work has been limited by the paucity of sex-linked genes available. Here, we used 35 Gb of RNA-seq data from multiple males (XY) and females (XX) of an S. latifolia inbred line to detect sex-linked SNPs and identified more than 1,700 sex-linked contigs (with X-linked and Y-linked alleles). Analyses using known sex-linked and autosomal genes, together with simulations indicate that these newly identified sex-linked contigs are reliable. Using read numbers, we then estimated expression levels of X-linked and Y-linked alleles in males and found an overall trend of reduced expression of Y-linked alleles, consistent with a widespread ongoing degeneration of the S. latifolia Y chromosome. By comparing expression intensities of X-linked alleles in males and females, we found that X-linked allele expression increases as Y-linked allele expression decreases in males, which makes expression of sex-linked contigs similar in both sexes. This phenomenon is known as dosage compensation and has so far only been observed in evolutionary old animal sex chromosome systems. Our results suggest that dosage compensation has evolved in plants and that it can quickly evolve de novo after the origin of sex chromosomes.     

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.     

用matK序列分析探讨木兰属植物的系统发育关系

用木兰科Magnoliaceae 57种植物的matK基因序列构建了该科的系统发育分支图。结果表明: (1)木兰属Magnolia L.是一个因为性状的趋同演化而建立的多系类群; (2)木兰亚属subgen. Magnolia和玉兰亚属subgen. Yulania (Spach) Reichenb.亲缘关系较远, 支持将后者从该属中分出建立玉兰属Yulania Spach, 木兰亚属作为木兰属保留; (3)木兰亚属的sect. Splendentes Dandy ex Vazquez组与皱种组sect. Rytidospermum Spach的两个美洲种M. macrophylla Michaux和M. dealbata Zucc.亲缘关系较近, 荷花玉兰组sect. Theorhodon Spach与常绿组sect. Gwillimia DC.的亲缘关系较近; (4)盖裂木属Talauma Juss.可以成立, 而其分布于亚洲的Blumiana Blume组可归入木兰属; (5)拟单性木兰属Parakmeria Hu &; Cheng、华盖木属Manglietiastrum Law以及单性木兰属Kmeria (Pierre) Dandy形成一个单系群, 与玉兰亚属和含笑属Michelia L.的亲缘关系较近。花的着生位置不足以作为木兰科的分族依据, 含笑族Michelieae和木兰族Magnolieae的特征及其界定应做修改。将玉兰亚属从木兰属分出后, 木兰属与含笑属无性状交叉,成为两个区别明显的属。