Nejvíce citovaný článek - PubMed ID 37198485
Cycles of satellite and transposon evolution in Arabidopsis centromeres
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.
- Klíčová slova
- Centromere, chromosomes, plant genome, recombination, transcription factor, transposable elements,
- MeSH
- centromera genetika MeSH
- chromozomy rostlin * genetika MeSH
- genom rostlinný genetika MeSH
- molekulární evoluce MeSH
- rostliny * genetika MeSH
- transpozibilní elementy DNA * genetika MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- transpozibilní elementy DNA * MeSH
The centromere has a conserved function across eukaryotes; however, the associated DNA sequences exhibit remarkable diversity in both size and structure. In plants, some species possess well-defined centromeres dominated by tandem satellite repeats and centromeric retrotransposons, while others have centromeric regions composed almost entirely of retrotransposons. Using a combination of bioinformatic, molecular, and cytogenetic approaches, we analyzed the centromeric landscape of Humulus lupulus. We identified novel centromeric repeats and characterized two types of centromeric organization. Cytogenetic localization on metaphase chromosomes confirmed the genomic distribution of the major repeats and revealed unique centromeric organization specifically on chromosomes 2, 8, and Y. Two centromeric types are composed of the major repeats SaazCEN and SaazCRM1 (Ty3/Gypsy) which are further accompanied by chromosome-specific centromeric satellites, Saaz40, Saaz293, Saaz85, and HuluTR120. Chromosome 2 displays unbalanced segregation during mitosis and meiosis, implicating an important role for its centromere structure in segregation patterns. Moreover, chromosome 2-specific centromeric repeat Saaz293 is a new marker for studying aneuploidy in hops. Our findings provide new insights into chromosome segregation in hops and highlight the diversity and complexity of the centromere organization in H. lupulus.
- Klíčová slova
- Cannabaceae, asymmetric cell division, centromere, retrotransposons, sex chromosomes,
- MeSH
- centromera * genetika MeSH
- chromozomy rostlin genetika MeSH
- Humulus * genetika MeSH
- meióza genetika MeSH
- repetitivní sekvence nukleových kyselin * genetika MeSH
- retroelementy * genetika MeSH
- segregace chromozomů genetika MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- retroelementy * MeSH
Matthiola incana, commonly known as stock and gillyflower, is a widely grown ornamental plant whose genome is significantly larger than that of other species in the mustard family. However, the evolutionary history behind such a large genome (~2 Gb) is still unknown. Here, we have succeeded in obtaining a high-quality chromosome-scale genome assembly of M. incana by integrating PacBio HiFi reads, Illumina short reads and Hi-C data. The resulting genome consists of seven pseudochromosomes with a length of 1965 Mb and 38 245 gene models. Phylogenetic analysis indicates that M. incana and other taxa of the supertribe Hesperodae represent an early-diverging lineage in the evolutionary history of the Brassicaceae. Through a comparative analysis, we revisited the ancestral Hesperodae karyotype (AHK, n = 7) and found several differences from the well-established ancestral crucifer karyotype (ACK, n = 8) model, including extensive inter- and intra-chromosomal rearrangements. Our results suggest that the primary reason for genome obesity in M. incana is the massive expansion of long terminal repeat retrotransposons (LTR-RTs), particularly from the Angela, Athila and Retand families. CHG methylation modification is obviously reduced in the regions where the highest density of Copia-type LTR-RTs and the lowest density of Gypsy-type LTR-RTs overlap, corresponding to the putative centromeres. Based on insertion times and methylation profiling, recently inserted LTR-RTs were found to have a significantly different methylation pattern compared to older ones.
- Klíčová slova
- Cruciferae, Hesperodae, Lineage III, genome assembly, genome obesity, retrotransposons,
- MeSH
- Brassicaceae * genetika MeSH
- chromozomy rostlin genetika MeSH
- fylogeneze MeSH
- genom rostlinný * genetika MeSH
- karyotyp MeSH
- molekulární evoluce * MeSH
- retroelementy * genetika MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- retroelementy * MeSH
Sexual reproduction relies on meiotic chromosome pairing to form bivalents, a process that is complicated in polyploids owing to the presence of multiple subgenomes1. Uneven ploidy mostly results in sterility due to unbalanced chromosome pairing and segregation during meiosis. However, pentaploid dogroses (Rosa sect. Caninae; 2n = 5x = 35) achieve stable sexual reproduction through a unique mechanism: 14 chromosomes form bivalents and are transmitted biparentally, while the remaining 21 chromosomes are maternally inherited as univalents2,3. Despite being studied for over a century, the role of centromeres in this process has remained unclear. Here we analyse haplotype-resolved chromosome-level genome assemblies for three pentaploid dogroses. Subgenome phasing revealed a bivalent-forming subgenome with two highly homozygous chromosome sets and three divergent subgenomes lacking homologous partners, therefore explaining their meiotic behaviour. Comparative analyses of chromosome synteny, phylogenetic relationships and centromere composition indicate that the subgenomes originated from two divergent clades of the genus Rosa. Pollen genome analysis shows that subgenomes from different evolutionary origins form bivalents, supporting multiple origins of dogroses and highlighting variation in subgenome contributions. We reveal that bivalent-forming centromeres are enriched with ATHILA retrotransposons, contrasting with larger tandem-repeat-based centromeres mainly found in univalents. This centromere structural bimodality possibly contributes to univalent drive during female meiosis. Our findings provide insights into the unique reproductive strategies of dogroses, advancing our understanding of genome evolution, centromere diversity and meiotic mechanisms in organisms with asymmetrical inheritance systems.
- MeSH
- centromera * genetika metabolismus MeSH
- chromozomy rostlin genetika MeSH
- fylogeneze MeSH
- genom rostlinný genetika MeSH
- haplotypy genetika MeSH
- meióza * genetika MeSH
- polyploidie * MeSH
- pyl genetika cytologie MeSH
- retroelementy genetika MeSH
- syntenie genetika MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- retroelementy MeSH
BACKGROUND: The centromere is one of the key regions of the eukaryotic chromosome. While maintaining its function, centromeric DNA may differ among closely related species. Here, we explored the composition and structure of the pericentromeres (a chromosomal region including a functional centromere) of Hieracium alpinum (Asteraceae), a member of one of the most diverse genera in the plant kingdom. Previously, we identified a pericentromere-specific tandem repeat that made it possible to distinguish reads within the Oxford Nanopore library attributed to the pericentromeres, separating them into a discrete subset and allowing comparison of the repeatome composition of this subset with the remaining genome. RESULTS: We found that the main satellite DNA (satDNA) monomer forms long arrays of linear and block types in the pericentromeric heterochromatin of H. alpinum, and very often, single reads contain forward and reverse arrays and mirror each other. Beside the major, two new minor satDNA families were discovered. In addition to satDNAs, high amounts of LTR retrotransposons (TEs) with dominant of Tekay lineage, were detected in the pericentromeres. We were able to reconstruct four main TEs of the Ty3-gypsy and Ty1-copia superfamilies and compare their relative positions with satDNAs. The latter showed that the conserved domains (CDs) of the TE proteins are located between the newly discovered satDNAs, which appear to be parts of ancient Tekay LTRs that we were able to reconstruct. The dominant satDNA monomer shows a certain similarity to the GAG CD of the Angela retrotransposon. CONCLUSIONS: The species-specific pericentromeric arrays of the H. alpinum genome are heterogeneous, exhibiting both linear and block type structures. High amounts of forward and reverse arrays of the main satDNA monomer point to multiple microinversions that could be the main mechanism for rapid structural evolution stochastically creating the uniqueness of an individual pericentromeric structure. The traces of TEs insertion waves remain in pericentromeres for a long time, thus "keeping memories" of past genomic events. We counted at least four waves of TEs insertions. In pericentromeres, TEs particles can be transformed into satDNA, which constitutes a background pool of minor families that, under certain conditions, can replace the dominant one(s).
- Klíčová slova
- Asteraceae, Hieracium, Oxford Nanopore Technology sequencing, Pericentromeres, Plants, Satellite DNA, Transposable elements,
- Publikační typ
- časopisecké články MeSH
In most studied eukaryotes, chromosomes are monocentric, with centromere activity confined to a single region. However, the rush family (Juncaceae) includes species with both monocentric (Juncus) and holocentric (Luzula) chromosomes, where centromere activity is distributed along the entire chromosome length. Here, we combine chromosome-scale genome assembly, epigenetic analysis, immuno-FISH and super-resolution microscopy to study the transition to holocentricity in Luzula sylvatica. We report repeat-based holocentromeres with an irregular distribution of features along the chromosomes. Luzula sylvatica holocentromeres are predominantly associated with two satellite DNA repeats (Lusy1 and Lusy2), while CENH3 also binds satellite-free gene-poor regions. Comparative repeat analysis suggests that Lusy1 plays a crucial role in centromere function across most Luzula species. Furthermore, synteny analysis between L. sylvatica (n = 6) and Juncus effusus (n = 21) suggests that holocentric chromosomes in Luzula could have arisen from chromosome fusions of ancestral monocentric chromosomes, accompanied by the expansion of CENH3-associated satellite repeats.
- MeSH
- centromera * genetika MeSH
- chromozomy rostlin * genetika MeSH
- DNA rostlinná genetika MeSH
- genom rostlinný MeSH
- hybridizace in situ fluorescenční MeSH
- molekulární evoluce MeSH
- repetitivní sekvence nukleových kyselin genetika MeSH
- satelitní DNA * genetika MeSH
- syntenie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA rostlinná MeSH
- satelitní DNA * MeSH