Most cited article - PubMed ID 18853265
Survey of repetitive sequences in Silene latifolia with respect to their distribution on sex chromosomes
Transposable elements (TEs) constitute a significant part of plant genomes and shape their genomic landscape. While some TEs are ubiquitously dispersed, other elements specifically occupy discrete genomic loci. The evolutionary forces behind the chromosomal localization of TEs are poorly understood. Therefore, we first review specific chromosomal niches where TEs are often localized including (i) centromeres, (ii) (sub)telomeres, (iii) genes, and (iv) sex chromosomes. In the second part of this review, we focus on the processes standing behind non-equal distribution of various TEs in genomes including (i) purifying selection, (ii) insertion site preference or targeting of TEs, (iii) post-insertion ectopic recombination between TEs, and (iv) spatiotemporal regulation of TE jumping. Using the combination of the above processes, we explain the distribution of TEs on sex chromosomes. We also describe the phenomena of mutual nesting of TEs, epigenetic mark silencing in TEs, and TE interactions in the 3D interphase nucleus concerning TE localization. We summarize the functional consequences of TE distribution and relate them to cell functioning and genome evolution.
- Keywords
- Centromere, chromosomes, plant genome, recombination, transcription factor, transposable elements,
- MeSH
- Centromere genetics MeSH
- Chromosomes, Plant * genetics MeSH
- Genome, Plant genetics MeSH
- Evolution, Molecular MeSH
- Plants * genetics MeSH
- DNA Transposable Elements * genetics MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- DNA Transposable Elements * MeSH
BACKGROUND: Long terminal repeats (LTRs) represent important parts of LTR retrotransposons and retroviruses found in high copy numbers in a majority of eukaryotic genomes. LTRs contain regulatory sequences essential for the life cycle of the retrotransposon. Previous experimental and sequence studies have provided only limited information about LTR structure and composition, mostly from model systems. To enhance our understanding of these key sequence modules, we focused on the contrasts between LTRs of various retrotransposon families and other genomic regions. Furthermore, this approach can be utilized for the classification and prediction of LTRs. RESULTS: We used machine learning methods suitable for DNA sequence classification and applied them to a large dataset of plant LTR retrotransposon sequences. We trained three machine learning models using (i) traditional model ensembles (Gradient Boosting), (ii) hybrid convolutional/long and short memory network models, and (iii) a DNA pre-trained transformer-based model using k-mer sequence representation. All three approaches were successful in classifying and isolating LTRs in this data, as well as providing valuable insights into LTR sequence composition. The best classification (expressed as F1 score) achieved for LTR detection was 0.85 using the hybrid network model. The most accurate classification task was superfamily classification (F1=0.89) while the least accurate was family classification (F1=0.74). The trained models were subjected to explainability analysis. Positional analysis identified a mixture of interesting features, many of which had a preferred absolute position within the LTR and/or were biologically relevant, such as a centrally positioned TATA-box regulatory sequence, and TG..CA nucleotide patterns around both LTR edges. CONCLUSIONS: Our results show that the models used here recognized biologically relevant motifs, such as core promoter elements in the LTR detection task, and a development and stress-related subclass of transcription factor binding sites in the family classification task. Explainability analysis also highlighted the importance of 5'- and 3'- edges in LTR identity and revealed need to analyze more than just dinucleotides at these ends. Our work shows the applicability of machine learning models to regulatory sequence analysis and classification, and demonstrates the important role of the identified motifs in LTR detection.
- Keywords
- CNN-LSTM, DNABERT, Deep learning, Eukaryote, Regulatory mechanisms, Repeat, SHAP score, Sequence analysis, TFBS, Transcription factor binding sites, Transposable elements,
- Publication type
- Journal Article MeSH
Sex chromosomes have evolved in many plant species with separate sexes. Current plant research is shifting from examining the structure of sex chromosomes to exploring their functional aspects. New studies are progressively unveiling the specific genetic and epigenetic mechanisms responsible for shaping distinct sexes in plants. While the fundamental methods of molecular biology and genomics are generally employed for the analysis of sex chromosomes, it is often necessary to modify classical procedures not only to simplify and expedite analyses but sometimes to make them possible at all. In this review, we demonstrate how, at the level of structural and functional genetics, cytogenetics, and bioinformatics, it is essential to adapt established procedures for sex chromosome analysis.
- Keywords
- Bioinformatics, chromosome dissection, cytogenetics, dioecious plants, epigenetics, functional genetics, sex chromosomes, tandem repeats, transposable elements,
- MeSH
- Chromosomes, Plant * genetics MeSH
- Sex Chromosomes * genetics MeSH
- Plants genetics MeSH
- Computational Biology methods MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
The oxidation of 5-methylcytosine (5mC) to 5-hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC), and 5-carboxylcytosine (5caC), known as oxi-mCs, garners significant interest in plants as potential epigenetic marks. While research in mammals has established a role in cell reprogramming, carcinogenesis, and gene regulation, their functions in plants remain unclear. In rice, 5hmC has been associated with transposable elements (TEs) and heterochromatin. This study utilizes Silene latifolia, a dioecious plant with heteromorphic sex chromosomes and a genome with a large proportion of TEs, which provides a favourable environment for the study of oxi-mCs in individual sexes. Notably, we detected surprisingly high levels of oxi-mCs in S. latifolia comparable with mammals. Nuclei showed enrichment in heterochromatic regions, except for 5hmC whose signal was homogeneously distributed. Intriguingly, the same X chromosome in females displayed overall enrichment of 5hmC and 5fC compared with its counterpart. This fact is shared with 5mC, resembling dosage compensation. Co-localization showed higher correlation between 5mC and 5fC than with 5hmC, indicating no potential relationship between 5hmC and 5fC. Additionally, the promoter of several sex-linked genes and sex-biased TEs clustered in a clear sex-dependent way. Together, these findings unveil a hypothetical role for oxi-mCs in S. latifolia sex chromosome development, warranting further exploration.
- Keywords
- Silene latifolia, Cytosine modifications, dosage compensation, oxi-mCs, sex chromosomes, transposable elements,
- MeSH
- 5-Methylcytosine metabolism analogs & derivatives MeSH
- Chromosomes, Plant * genetics MeSH
- Epigenesis, Genetic MeSH
- Sex Chromosomes * genetics MeSH
- Silene * genetics MeSH
- DNA Transposable Elements genetics MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- 5-Methylcytosine MeSH
- DNA Transposable Elements MeSH
In 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 (DC), 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 DC in plants, which started as early as the late 1960s with cytological approaches. The use of transcriptomics fired a controversy as to whether DC existed in plants. Further work revealed that various plants exhibit partial DC, 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 DC. 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. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.
- Keywords
- Y degeneration, cis-regulatory sequence divergence, dosage balance, dosage-sensitive genes, imprinting, sex chromosomes,
- MeSH
- Dosage Compensation, Genetic * MeSH
- Evolution, Molecular MeSH
- Sex Chromosomes * genetics MeSH
- Plants genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
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.
- Keywords
- Silene, central interpolar axis, chromosome velocity, sex chromosomes, sister chromatid division,
- MeSH
- Chromatids physiology MeSH
- Chromosomes, Plant physiology MeSH
- In Situ Hybridization, Fluorescence MeSH
- Hydroxyurea pharmacology MeSH
- Microscopy, Confocal MeSH
- Mitosis MeSH
- Evolution, Molecular MeSH
- Sex Chromosomes physiology MeSH
- Silene genetics physiology MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Hydroxyurea MeSH
BACKGROUND AND AIMS: Dioecious species with well-established sex chromosomes are rare in the plant kingdom. Most sex chromosomes increase in size but no comprehensive analysis of the kind of sequences that drive this expansion has been presented. Here we analyse sex chromosome structure in common sorrel (Rumex acetosa), a dioecious plant with XY1Y2 sex determination, and we provide the first chromosome-specific repeatome analysis for a plant species possessing sex chromosomes. METHODS: We flow-sorted and separately sequenced sex chromosomes and autosomes in R. acetosa using the two-dimensional fluorescence in situ hybridization in suspension (FISHIS) method and Illumina sequencing. We identified and quantified individual repeats using RepeatExplorer, Tandem Repeat Finder and the Tandem Repeats Analysis Program. We employed fluorescence in situ hybridization (FISH) to analyse the chromosomal localization of satellites and transposons. KEY RESULTS: We identified a number of novel satellites, which have, in a fashion similar to previously known satellites, significantly expanded on the Y chromosome but not as much on the X or on autosomes. Additionally, the size increase of Y chromosomes is caused by non-long terminal repeat (LTR) and LTR retrotransposons, while only the latter contribute to the enlargement of the X chromosome. However, the X chromosome is populated by different LTR retrotransposon lineages than those on Y chromosomes. CONCLUSIONS: The X and Y chromosomes have significantly diverged in terms of repeat composition. The lack of recombination probably contributed to the expansion of diverse satellites and microsatellites and faster fixation of newly inserted transposable elements (TEs) on the Y chromosomes. In addition, the X and Y chromosomes, despite similar total counts of TEs, differ significantly in the representation of individual TE lineages, which indicates that transposons proliferate preferentially in either the paternal or the maternal lineage.
- Keywords
- Rumex acetosa, genome dynamics, satellites, sex chromosomes, transposable elements,
- MeSH
- Chromosomes, Plant MeSH
- In Situ Hybridization, Fluorescence MeSH
- Evolution, Molecular MeSH
- Sex Chromosomes MeSH
- Retroelements MeSH
- Rumex * genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Retroelements MeSH
The genus Silene includes a plethora of dioecious and gynodioecious species. Two species, Silene latifolia (white campion) and Silene dioica (red campion), are dioecious plants, having heteromorphic sex chromosomes with an XX/XY sex determination system. The X and Y chromosomes differ mainly in size, DNA content and posttranslational histone modifications. Although it is generally assumed that the sex chromosomes evolved from a single pair of autosomes, it is difficult to distinguish the ancestral pair of chromosomes in related gynodioecious and hermaphroditic plants. We designed an oligo painting probe enriched for X-linked scaffolds from currently available genomic data and used this probe on metaphase chromosomes of S. latifolia (2n = 24, XY), S. dioica (2n = 24, XY), and two gynodioecious species, S. vulgaris (2n = 24) and S. maritima (2n = 24). The X chromosome-specific oligo probe produces a signal specifically on the X and Y chromosomes in S. latifolia and S. dioica, mainly in the subtelomeric regions. Surprisingly, in S. vulgaris and S. maritima, the probe hybridized to three pairs of autosomes labeling their p-arms. This distribution suggests that sex chromosome evolution was accompanied by extensive chromosomal rearrangements in studied dioecious plants.
- Keywords
- Silene, Y chromosome, chromosome painting, double-translocation, pseudo-autosomal region,
- Publication type
- Journal Article MeSH
Contrasting patterns of histone modifications between the X and Y chromosome in Silene latifolia show euchromatic histone mark depletion on the Y chromosome and indicate hyperactivation of one X chromosome in females. Silene latifolia (white campion) is a dioecious plant with heteromorphic sex chromosomes (24, XX in females and 24, XY in males), and a genetically degenerated Y chromosome that is 1.4 times larger than the X chromosome. Although the two sex chromosomes differ in their DNA content, information about epigenetic histone marks and evidence of their function are scarce. We performed immunolabeling experiments using antibodies specific for active and suppressive histone modifications as well as pericentromere-specific histone modifications. We show that the Y chromosome is partially depleted of histone modifications important for transcriptionally active chromatin, and carries these marks only in the pseudo-autosomal region, but that it is not enriched for suppressive and pericentromere histone marks. We also show that two of the active marks are specifically enriched in one of the X chromosomes in females and in the X chromosome in males. Our data support recent findings that genetic imprinting mediates dosage compensation of sex chromosomes in S. latifolia.
- Keywords
- Posttranslational histone modifications, Pseudo-autosomal region, Sex chromosomes,
- MeSH
- Chromosomes, Plant genetics MeSH
- Epigenesis, Genetic * MeSH
- Histone Code genetics MeSH
- Silene genetics MeSH
- Publication type
- Journal Article MeSH
BACKGROUND: The evolution of dioecious plants is occasionally accompanied by the establishment of sex chromosomes: both XY and ZW systems have been found in plants. Structural studies of sex chromosomes are now being followed up by functional studies that are gradually shedding light on the specific genetic and epigenetic processes that shape the development of separate sexes in plants. SCOPE: This review describes sex determination diversity in plants and the genetic background of dioecy, summarizes recent progress in the investigation of both classical and emerging model dioecious plants and discusses novel findings. The advantages of interspecies hybrids in studies focused on sex determination and the role of epigenetic processes in sexual development are also overviewed. CONCLUSIONS: We integrate the genic, genomic and epigenetic levels of sex determination and stress the impact of sex chromosome evolution on structural and functional aspects of plant sexual development. We also discuss the impact of dioecy and sex chromosomes on genome structure and expression.
