Nejvíce citovaný článek - PubMed ID 15879508
Comparison of the X and Y chromosome organization in Silene latifolia
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.
- Klíčová slova
- Silene, Y chromosome, chromosome painting, double-translocation, pseudo-autosomal region,
- Publikační typ
- časopisecké články MeSH
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.
- Klíčová slova
- DNA methylation, Epigenetics, Immunoprecipitation, Sex chromosomes, Sex-linked genes, Silene latifolia, Sodium bisulfite, Y degeneration,
- MeSH
- chromozomy rostlin * MeSH
- DNA rostlinná chemie MeSH
- exprese genu MeSH
- listy rostlin metabolismus MeSH
- metylace DNA * MeSH
- molekulární evoluce * MeSH
- sekvenční homologie nukleových kyselin MeSH
- Silene genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- DNA rostlinná MeSH
BACKGROUND: The evolution of sex chromosomes is often accompanied by gene or chromosome rearrangements. Recently, the gene AP3 was characterized in the dioecious plant species Silene latifolia. It was suggested that this gene had been transferred from an autosome to the Y chromosome. RESULTS: In the present study we provide evidence for the existence of an X linked copy of the AP3 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 S. vulgaris and S. conica. We further found that promoter sequences differ significantly. Comparison of the genic region of AP3 between the X and Y alleles and the corresponding autosomal copies in the gynodioecious species S. vulgaris revealed a massive accumulation of retrotransposons within one intron of the Y copy of AP3. 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, in silico expression analysis shows biased expression of individual domains of the identified retroelements in male plants. CONCLUSIONS: We characterized the structure and evolution of AP3, a sex linked gene with copies on the X and Y chromosomes in the dioecious plant S. latifolia. 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.
- MeSH
- alely MeSH
- chromozomy rostlin genetika MeSH
- DNA rostlinná genetika MeSH
- exony MeSH
- introny MeSH
- molekulární evoluce * MeSH
- promotorové oblasti (genetika) MeSH
- regulace genové exprese u rostlin MeSH
- repetitivní sekvence nukleových kyselin MeSH
- retroelementy MeSH
- rostlinné geny MeSH
- rostlinné proteiny genetika MeSH
- sekvenční analýza DNA MeSH
- Silene genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA rostlinná MeSH
- retroelementy MeSH
- rostlinné proteiny MeSH
Understanding the origin and evolution of sex chromosomes requires studying recently evolved X-Y chromosome systems such as those in some flowering plants. We describe Y chromosome deletion mutants of Silene latifolia, a dioecious plant with heteromorphic sex chromosomes. The combination of results from new and previously described deletions with histological descriptions of their stamen development defects indicates the presence of two distinct Y regions containing loci with indispensable roles in male reproduction. We determined their positions relative to the two main sex determination functions (female suppressing and the other male promoting). A region proximal to the centromere on the Y p arm containing the putative stamen promoting sex determination locus includes additional early stamen developmental factors. A medial region of the Y q arm carries late pollen fertility factors. Cytological analysis of meiotic X-Y pairing in one of the male-sterile mutants indicates that the Y carries sequences or functions specifically affecting sex chromosome pairing.
- MeSH
- biologická evoluce * MeSH
- DNA rostlinná genetika MeSH
- druhová specificita MeSH
- genetická variace MeSH
- mutace MeSH
- pohlavní chromozomy genetika MeSH
- rekombinace genetická * MeSH
- rostlinné geny genetika MeSH
- rozmnožování genetika MeSH
- selekce (genetika) MeSH
- Silene genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA rostlinná MeSH
Sex chromosomes in mammals are about 300 million years old and typically have a highly degenerated Y chromosome. The sex chromosomes in the dioecious plant Silene latifolia in contrast, represent an early stage of evolution in which functional X-Y gene pairs are still frequent. In this study, we characterize a novel tandem repeat called TRAYC, which has accumulated on the Y chromosome in S. latifolia. Its presence demonstrates that processes of satellite accumulation are at work even in this early stage of sex chromosome evolution. The presence of TRAYC in other species of the Elisanthe section suggests that this repeat had spread after the sex chromosomes evolved but before speciation within this section. TRAYC possesses a palindromic character and a strong potential to form secondary structures, which could play a role in satellite evolution. TRAYC accumulation is most prominent near the centromere of the Y chromosome. We propose a role for the centromere as a starting point for the cessation of recombination between the X and Y chromosomes.
- MeSH
- chromozom Y genetika MeSH
- DNA primery genetika MeSH
- DNA rostlinná chemie genetika MeSH
- druhová specificita MeSH
- hybridizace in situ fluorescenční MeSH
- konformace nukleové kyseliny MeSH
- molekulární evoluce * MeSH
- molekulární sekvence - údaje MeSH
- pohlavní chromozomy genetika MeSH
- sekvence nukleotidů MeSH
- sekvenční homologie nukleových kyselin MeSH
- Silene klasifikace genetika MeSH
- tandemové repetitivní sekvence MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA primery MeSH
- DNA rostlinná MeSH
The aim of this work was to isolate new DNA markers linked to the Silene latifolia Y chromosome. To do this we created a chromosome-specific plasmid library after DOP-PCR amplification of laser-microdissected Y-chromosomes. The library screening led to the isolation of several clones yielding mostly to exclusive male specific hybridization signals. Subsequent PCR confirmed the Y-unique linkage for one of the sequences. This DNA sequence called MK17 has no homology to any known DNA sequence and it is not expressed. Based on PCR and Southern analyses, MK17 is present only in dioecious species of the Elisanthe section of the genus Silene (S. latifolia, S. dioica, and S. diclinis) and it is absent in related gynodioecious and hermaphroditic species. The mapping analysis using a panel of deletion mutants showed that MK17 is closely linked to the region controlling suppression of gynoecium development. Hence MK17 represents a valuable marker to isolate genes controlling the gynoecium development suppression on the Y chromosome of S. latifolia.
