The role of chromosomal rearrangements in the evolution of Silene latifolia sex chromosomes

Silene latifolia is a model plant for studies of the early steps of sex chromosome evolution. In comparison to mammalian sex chromosomes that evolved 300mya, sex chromosomes of S. latifolia appeared approximately 20mya. Here, we combine results from physical mapping of sex-linked genes using polymerase chain reaction on microdissected arms of the S. latifolia X chromosome, and fluorescence in situ hybridization analysis of a new cytogenetic marker, Silene tandem repeat accumulated on the Y chromosome. The data are interpreted in the light of current genetic linkage maps of the X chromosome and a physical map of the Y chromosome. Our results identify the position of the centromere relative to the mapped genes on the X chromosome. We suggest that the evolution of the S. latifolia Y chromosome has been accompanied by at least one paracentric and one pericentric inversion. These results indicate that large chromosomal rearrangements have played an important role in Y chromosome evolution in S. latifolia and that chromosomal rearrangements are an integral part of sex chromosome evolutio

Structure and evolution of Apetala3, a sex-linked gene in Silene latifolia

<p>Abstract</p> <p>Background</p> <p>The evolution of sex chromosomes is often accompanied by gene or chromosome rearrangements. Recently, the gene <it>AP3 </it>was characterized in the dioecious plant species <it>Silene latifolia</it>. It was suggested that this gene had been transferred from an autosome to the Y chromosome.</p> <p>Results</p> <p>In the present study we provide evidence for the existence of an X linked copy of the <it>AP3 </it>gene. We further show that the Y copy is probably located in a chromosomal region where recombination restriction occurred during the first steps of sex chromosome evolution. A comparison of X and Y copies did not reveal any clear signs of degenerative processes in exon regions. Instead, both X and Y copies show evidence for relaxed selection compared to the autosomal orthologues in <it>S. vulgaris </it>and <it>S. conica</it>. We further found that promoter sequences differ significantly. Comparison of the genic region of <it>AP3 </it>between the X and Y alleles and the corresponding autosomal copies in the gynodioecious species <it>S. vulgaris </it>revealed a massive accumulation of retrotransposons within one intron of the Y copy of <it>AP3</it>. Analysis of the genomic distribution of these repetitive elements does not indicate that these elements played an important role in the size increase characteristic of the Y chromosome. However, <it>in silico </it>expression analysis shows biased expression of individual domains of the identified retroelements in male plants.</p> <p>Conclusions</p> <p>We characterized the structure and evolution of <it>AP3</it>, a sex linked gene with copies on the X and Y chromosomes in the dioecious plant <it>S. latifolia</it>. These copies showed complementary expression patterns and relaxed evolution at protein level compared to autosomal orthologues, which suggests subfunctionalization. One intron of the Y-linked allele was invaded by retrotransposons that display sex-specific expression patterns that are similar to the expression pattern of the corresponding allele, which suggests that these transposable elements may have influenced evolution of expression patterns of the Y copy. These data could help researchers decipher the role of transposable elements in degenerative processes during sex chromosome evolution.</p

Genomic imprinting mediates dosage compensation in a young plant XY system.: An article peer-reviewed and recommended by Peer Community In Evolutionary Biology (PCI Evol Biol)

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100044). Sex chromosomes have repeatedly evolved from a pair of autosomes. Consequently, X and Y chromosomes initially have similar gene content, but ongoing Y degeneration leads to reduced Y gene expression and eventual Y gene loss. The resulting imbalance in gene expression between Y genes and the rest of the genome is expected to reduce male fitness, especially when protein networks have components from both autosomes and sex chromosomes. A diverse set of dosage compensating mechanisms that alleviates these negative effects has been described in animals. However, the early steps in the evolution of dosage compensation remain unknown and dosage compensation is poorly understood in plants. Here we show a novel dosage compensation mechanism in the evolutionarily young XY sex determination system of the plant Silene latifolia. Genomic imprinting results in higher expression from the maternal X chromosome in both males and females. This compensates for reduced Y expression in males but results in X overexpression in females and may be detrimental. It could represent a transient early stage in the evolution of dosage compensation. Our finding has striking resemblance to the first stage proposed by Ohno for the evolution of X inactivation in mammals

Genomic Diversity in Two Related Plant Species with and without Sex Chromosomes - Silene latifolia and S. vulgaris

Genome size evolution is a complex process influenced by polyploidization, satellite DNA accumulation, and expansion of retroelements. How this process could be affected by different reproductive strategies is still poorly understood.We analyzed differences in the number and distribution of major repetitive DNA elements in two closely related species, Silene latifolia and S. vulgaris. Both species are diploid and possess the same chromosome number (2n = 24), but differ in their genome size and mode of reproduction. The dioecious S. latifolia (1C = 2.70 pg DNA) possesses sex chromosomes and its genome is 2.5× larger than that of the gynodioecious S. vulgaris (1C = 1.13 pg DNA), which does not possess sex chromosomes. We discovered that the genome of S. latifolia is larger mainly due to the expansion of Ogre retrotransposons. Surprisingly, the centromeric STAR-C and TR1 tandem repeats were found to be more abundant in S. vulgaris, the species with the smaller genome. We further examined the distribution of major repetitive sequences in related species in the Caryophyllaceae family. The results of FISH (fluorescence in situ hybridization) on mitotic chromosomes with the Retand element indicate that large rearrangements occurred during the evolution of the Caryophyllaceae family.Our data demonstrate that the evolution of genome size in the genus Silene is accompanied by the expansion of different repetitive elements with specific patterns in the dioecious species possessing the sex chromosomes

De novo transcriptome assembly of heavy metal tolerant Silene dioica

Silene dioica is a dioecious plant of the family Caryophyllaceae. In the present study, we used Illumina sequencing technology (MiSeq) to sequence, de novo assembly and annotate the transcriptomes of male and female copper tolerant S. dioica individuals. We sequenced the normalized mRNA of roots, shoots, flower buds and flowers for each sex. Raw reads of the transcriptome assembly project for S. dioica male and female individual have been deposited in NCBI's Sequence Read Archive (SRA) database with the accession number SRP094611. The Trinity and Detonate program was used to de novo assembly 92,347 transcripts for male and 94,757 transcripts for female transcriptome. The assembled transcriptome sequences for S. dioica male and female individuals can be accessed at NCBI with the following accession numbers: GFCG00000000 (male); GFCH00000000 (female). The obtained transcriptomic data will be useful for further studies focusing on copper tolerance, comparative transcriptome analysis with other Silene species and sex chromosomes evolution

The Sister Chromatid Division of the Heteromorphic Sex Chromosomes in Silene Species and Their Transmissibility towards the Mitosis

Young sex chromosomes possess unique and ongoing dynamics that allow us to understand processes that have an impact on their evolution and divergence. The genus Silene includes species with evolutionarily young sex chromosomes, and two species of section Melandrium, namely Silene latifolia (24, XY) and Silene dioica (24, XY), are well-established models of sex chromosome evolution, Y chromosome degeneration, and sex determination. In both species, the X and Y chromosomes are strongly heteromorphic and differ in the genomic composition compared to the autosomes. It is generally accepted that for proper cell division, the longest chromosomal arm must not exceed half of the average length of the spindle axis at telophase. Yet, it is not clear what are the dynamics between males and females during mitosis and how the cell compensates for the presence of the large Y chromosome in one sex. Using hydroxyurea cell synchronization and 2D/3D microscopy, we determined the position of the sex chromosomes during the mitotic cell cycle and determined the upper limit for the expansion of sex chromosome non-recombining region. Using 3D specimen preparations, we found that the velocity of the large chromosomes is compensated by the distant positioning from the central interpolar axis, confirming previous mathematical modulations

Transcriptome of barley under three different heavy metal stress reaction

In the present study, we used Illumina sequencing technology (HiSeq 2000) to sequence the transcriptome of barley (Hordeum vulgare L., cv. Morex) under three different heavy metal stress conditions: copper, zinc and cadmium. For each of those metals, the concentration causing a 50% inhibitory effect for root growth (EC50) was determined. We sequenced the total RNA of both roots and shoots from barley with and without heavy metal treatments in three replicates. Raw reads of the transcriptome project have been deposited in NCBI's BioProject accession number PRJNA382490. The obtained transcriptomic data will be useful for further studies focusing on heavy metal tolerance and comparative transcriptome analysis in barley

DNA methylation and genetic degeneration of the Y chromosome in the dioecious plant Silene latifolia

Abstract Background S. latifolia is a model organism for the study of sex chromosome evolution in plants. Its sex chromosomes include large regions in which recombination became gradually suppressed. The regions tend to expand over time resulting in the formation of evolutionary strata. Non-recombination and later accumulation of repetitive sequences is a putative cause of the size increase in the Y chromosome. Gene decay and accumulation of repetitive DNA are identified as key evolutionary events. Transposons in the X and Y chromosomes are distributed differently and there is a regulation of transposon insertion by DNA methylation of the target sequences, this points to an important role of DNA methylation during sex chromosome evolution in Silene latifolia. The aim of this study was to elucidate whether the reduced expression of the Y allele in S. latifolia is caused by genetic degeneration or if the cause is methylation triggered by transposons and repetitive sequences. Results Gene expression analysis in S. latifolia males has shown expression bias in both X and Y alleles. To determine whether these differences are caused by genetic degeneration or methylation spread by transposons and repetitive sequences, we selected several sex-linked genes with varying degrees of degeneration and from different evolutionary strata. Immunoprecipitation of methylated DNA (MeDIP) from promoter, exon and intron regions was used and validated through bisulfite sequencing. We found DNA methylation in males, and only in the promoter of genes of stratum I (older). The Y alleles in genes of stratum I were methylation enriched compared to X alleles. There was also abundant and high percentage methylation in the CHH context in most sequences, indicating de novo methylation through the RdDM pathway. Conclusions We speculate that TE accumulation and not gene decay is the cause of DNA methylation in the S. latifolia Y sex chromosome with influence on the process of heterochromatinization

The role of chromosomal rearrangements in the evolution of Silene latifolia sex chromosomes

ISSN:1617-4615ISSN:1617-462

Dosage compensation evolution in plants: theories, controversies and mechanisms

International audienceIn a minority of flowering plants, separate sexes are genetically determined by sex chromosomes. The Y chromosome has a non-recombining region that degenerates, causing a reduced expression of Y genes. In some species, the lower Y expression is accompanied by dosage compensation, a mechanism that re-equalizes male and female expression and/or brings XY male expression back to its ancestral level. Here, we review work on dosage compensation in plants, which started as early as the late 60s with cytological approaches. The use of transcriptomics fired a controversy as to whether dosage compensation existed in plants. Further work revealed that various plants exhibit partial dosage compensation, including a few species with young and homomorphic sex chromosomes. We are starting to understand the mechanisms responsible for DC in some plants, but in most species we lack the data to differentiate between global and gene-by-gene dosage compensation. Also, it is unknown why some species evolve many dosage compensated genes while others do not. Finally, the forces that drive DC evolution remain mysterious, both in plants and animals. We review the multiple evolutionary theories that have been proposed to explain DC patterns in eukaryotes with XY or ZW sex chromosomes