Nejvíce citovaný článek - PubMed ID 21540575
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
- Názvy látek
- DNA rostlinná MeSH
- satelitní DNA * MeSH
The centromere is the chromosome region where microtubules attach during cell division. In contrast to monocentric chromosomes with one centromere, holocentric species usually distribute hundreds of centromere units along the entire chromatid. We assembled the chromosome-scale reference genome and analyzed the holocentromere and (epi)genome organization of the lilioid Chionographis japonica. Remarkably, each of its holocentric chromatids consists of only 7 to 11 evenly spaced megabase-sized centromere-specific histone H3-positive units. These units contain satellite arrays of 23 and 28 bp-long monomers capable of forming palindromic structures. Like monocentric species, C. japonica forms clustered centromeres in chromocenters at interphase. In addition, the large-scale eu- and heterochromatin arrangement differs between C. japonica and other known holocentric species. Finally, using polymer simulations, we model the formation of prometaphase line-like holocentromeres from interphase centromere clusters. Our findings broaden the knowledge about centromere diversity, showing that holocentricity is not restricted to species with numerous and small centromere units.
Centromeres are essential for proper chromosome segregation to the daughter cells during mitosis and meiosis. Chromosomes of most eukaryotes studied so far have regional centromeres that form primary constrictions on metaphase chromosomes. These monocentric chromosomes vary from point centromeres to so-called "meta-polycentromeres", with multiple centromere domains in an extended primary constriction, as identified in Pisum and Lathyrus species. However, in various animal and plant lineages centromeres are distributed along almost the entire chromosome length. Therefore, they are called holocentromeres. In holocentric plants, centromere-specific proteins, at which spindle fibers usually attach, are arranged contiguously (line-like), in clusters along the chromosomes or in bands. Here, we summarize findings of ultrastructural investigations using immunolabeling with centromere-specific antibodies and super-resolution microscopy to demonstrate the structural diversity of plant centromeres. A classification of the different centromere types has been suggested based on the distribution of spindle attachment sites. Based on these findings we discuss the possible evolution and advantages of holocentricity, and potential strategies to segregate holocentric chromosomes correctly.
- Klíčová slova
- CENH3, CENP-A, Cuscuta, Lathyrus, Luzula, Pisum, Rhynchospora, clustered centromere, holocentromere, microtubule, monocentromere, structured illumination microscopy,
- MeSH
- buněčný cyklus MeSH
- centromera metabolismus MeSH
- chromozomy rostlin metabolismus MeSH
- mikroskopie * MeSH
- molekulární evoluce MeSH
- rostliny metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
The centromere is the region on a chromosome where the kinetochore assembles and spindle microtubules attach during mitosis and meiosis. In the vast majority of eukaryotes, the centromere position is determined epigenetically by the presence of the centromere-specific histone H3 variant CENH3. In species with monocentric chromosomes, CENH3 is confined to a single chromosomal region corresponding to the primary constriction on metaphase chromosomes. By contrast, in holocentrics, CENH3 (and thus centromere activity) is distributed along the entire chromosome length. Here, we report a unique pattern of CENH3 distribution in the holocentric plant Cuscuta europaea. This species expressed two major variants of CENH3, both of which were deposited into one to three discrete regions per chromosome, whereas the rest of the chromatin appeared to be devoid of CENH3. The two CENH3 variants fully co-localized, and their immunodetection signals overlapped with the positions of DAPI-positive heterochromatic bands containing the highly amplified satellite repeat CUS-TR24. This CENH3 distribution pattern contrasted with the distribution of the mitotic spindle microtubules, which attached at uniform density along the entire chromosome length. This distribution of spindle attachment sites proves the holocentric nature of C. europaea chromosomes and also suggests that, in this species, CENH3 either lost its function or acts in parallel to an additional CENH3-free mechanism of kinetochore positioning.
- Klíčová slova
- CENH3, Cuscuta, centromere, holocentric chromosomes, kinetochore, repetitive DNA analysis, satellite DNA,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: The dispersed occurrence of holocentric chromosomes across eukaryotes implies they are adaptive, but the conditions under which they confer an advantage over monocentric chromosomes remain unclear. Due to their extended kinetochore and the attachment of spindle microtubules along their entire length, holocentric chromosomes tolerate fragmentation; hence, they may be advantageous in times of exposure to factors that cause chromosomal fragmentation (clastogens). SCOPE: It is shown that holocentric organisms may, indeed, thrive better than monocentric organisms under clastogenic conditions and that such conditions of various duration and intensity have occurred many times throughout the history of Earth's biota. One of the most important clastogenic events in eukaryotic history, in which holocentric chromosomes may have played the key role, was the colonization of land by plants and animals half a billion years ago. In addition to arguments supporting the anticlastogenic hypothesis of holocentric chromosomes and a discussion of its evolutionary consequences, experiments and analyses are proposed to explore this hypothesis in more depth. CONCLUSIONS: It is argued that the tolerance to clastogens explains the origin of holocentric lineages and may also have far-reaching consequences for eukaryotic evolution in general as exemplified by the potential role of holocentric chromosomes in terrestrialization.
- Klíčová slova
- Clastogens, Zygnematophyceae, chromosomal fragmentation, cosmic radiation, desiccation, gamma radiation, herbivory, holokinetic chromosomes, land plants, monocentric chromosomes, terrestrialization, ultraviolet radiation,
- MeSH
- biologická evoluce * MeSH
- centromera fyziologie MeSH
- chromozomy rostlin MeSH
- chromozomy * fyziologie MeSH
- Eukaryota genetika MeSH
- mutace MeSH
- selekce (genetika) genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Species with holocentric chromosomes are often characterized by a rapid karyotype evolution. In contrast to species with monocentric chromosomes where acentric fragments are lost during cell division, breakage of holocentric chromosomes creates fragments with normal centromere activity. To decipher the mechanism that allows holocentric species an accelerated karyotype evolution via chromosome breakage, we analyzed the chromosome complements of irradiated Luzula elegans plants. The resulting chromosomal fragments and rearranged chromosomes revealed holocentromere-typical CENH3 and histone H2AThr120ph signals as well as the same mitotic mobility like unfragmented chromosomes. Newly synthesized telomeres at break points become detectable 3 weeks after irradiation. The presence of active telomerase suggests a telomerase-based mechanism of chromosome healing. A successful transmission of holocentric chromosome fragments across different generations was found for most offspring of irradiated plants. Hence, a combination of holokinetic centromere activity and the fast formation of new telomeres at break points enables holocentric species a rapid karyotype evolution involving chromosome fissions and rearrangements.
- Klíčová slova
- Chromosome fusion and fission, De novo telomere synthesis, Holocentric chromosome, Holocentric genome evolution, Luzula elegans,
- MeSH
- autoantigeny MeSH
- centromera * MeSH
- chromozomální proteiny, nehistonové MeSH
- chromozomy rostlin genetika MeSH
- histony MeSH
- karyotyp * MeSH
- Magnoliopsida genetika metabolismus MeSH
- molekulární evoluce * MeSH
- protein CENP-A MeSH
- rostlinné proteiny MeSH
- telomery * MeSH
- zlomy chromozomů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- autoantigeny MeSH
- chromozomální proteiny, nehistonové MeSH
- histony MeSH
- protein CENP-A MeSH
- rostlinné proteiny MeSH
Holocentric chromosomes lack a primary constriction, in contrast to monocentrics. They form kinetochores distributed along almost the entire poleward surface of the chromatids, to which spindle fibers attach. No centromere-specific DNA sequence has been found for any holocentric organism studied so far. It was proposed that centromeric repeats, typical for many monocentric species, could not occur in holocentrics, most likely because of differences in the centromere organization. Here we show that the holokinetic centromeres of the Cyperaceae Rhynchospora pubera are highly enriched by a centromeric histone H3 variant-interacting centromere-specific satellite family designated "Tyba" and by centromeric retrotransposons (i.e., CRRh) occurring as genome-wide interspersed arrays. Centromeric arrays vary in length from 3 to 16 kb and are intermingled with gene-coding sequences and transposable elements. We show that holocentromeres of metaphase chromosomes are composed of multiple centromeric units rather than possessing a diffuse organization, thus favoring the polycentric model. A cell-cycle-dependent shuffling of multiple centromeric units results in the formation of functional (poly)centromeres during mitosis. The genome-wide distribution of centromeric repeat arrays interspersing the euchromatin provides a previously unidentified type of centromeric chromatin organization among eukaryotes. Thus, different types of holocentromeres exist in different species, namely with and without centromeric repetitive sequences.
- Klíčová slova
- centromere, chromosome, evolution, holokinetic, satellite DNA,
- MeSH
- centromera * MeSH
- euchromatin genetika MeSH
- genom rostlinný * MeSH
- molekulární sekvence - údaje MeSH
- šáchorovité genetika MeSH
- satelitní DNA genetika MeSH
- tandemové repetitivní sekvence * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- euchromatin MeSH
- satelitní DNA MeSH
In most eukaryotes, centromere is determined by the presence of the centromere-specific histone variant CenH3. Two types of chromosome morphology are generally recognized with respect to centromere organization. Monocentric chromosomes possess a single CenH3-containing domain in primary constriction, whereas holocentric chromosomes lack the primary constriction and display dispersed distribution of CenH3. Recently, metapolycentric chromosomes have been reported in Pisum sativum, representing an intermediate type of centromere organization characterized by multiple CenH3-containing domains distributed across large parts of chromosomes that still form a single constriction. In this work, we show that this type of centromere is also found in other Pisum and closely related Lathyrus species, whereas Vicia and Lens genera, which belong to the same legume tribe Fabeae, possess only monocentric chromosomes. We observed extensive variability in the size of primary constriction and the arrangement of CenH3 domains both between and within individual Pisum and Lathyrus species, with no obvious correlation to genome or chromosome size. Search for CenH3 gene sequences revealed two paralogous variants, CenH3-1 and CenH3-2, which originated from a duplication event in the common ancestor of Fabeae species. The CenH3-1 gene was subsequently lost or silenced in the lineage leading to Vicia and Lens, whereas both genes are retained in Pisum and Lathyrus. Both of these genes appear to have evolved under purifying selection and produce functional CenH3 proteins which are fully colocalized. The findings described here provide the first evidence for a highly dynamic centromere structure within a group of closely related species, challenging previous concepts of centromere evolution.
- Klíčová slova
- CenH3, adaptive evolution, centromere, centromere drive, chromosome, gene duplication,
- MeSH
- centromera genetika MeSH
- chromatin metabolismus MeSH
- chromozomy rostlin genetika MeSH
- duplikace genu * MeSH
- Fabaceae cytologie genetika MeSH
- fylogeneze MeSH
- genetická variace MeSH
- metafáze genetika MeSH
- molekulární evoluce MeSH
- molekulární sekvence - údaje MeSH
- rostlinné geny * MeSH
- rostlinné proteiny chemie MeSH
- sekvence aminokyselin MeSH
- sekvence nukleotidů MeSH
- selekce (genetika) MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chromatin MeSH
- rostlinné proteiny MeSH
The centromere is a functional chromosome domain that is essential for faithful chromosome segregation during cell division and that can be reliably identified by the presence of the centromere-specific histone H3 variant CenH3. In monocentric chromosomes, the centromere is characterized by a single CenH3-containing region within a morphologically distinct primary constriction. This region usually spans up to a few Mbp composed mainly of centromere-specific satellite DNA common to all chromosomes of a given species. In holocentric chromosomes, there is no primary constriction; the centromere is composed of many CenH3 loci distributed along the entire length of a chromosome. Using correlative fluorescence light microscopy and high-resolution electron microscopy, we show that pea (Pisum sativum) chromosomes exhibit remarkably long primary constrictions that contain 3-5 explicit CenH3-containing regions, a novelty in centromere organization. In addition, we estimate that the size of the chromosome segment delimited by two outermost domains varies between 69 Mbp and 107 Mbp, several factors larger than any known centromere length. These domains are almost entirely composed of repetitive DNA sequences belonging to 13 distinct families of satellite DNA and one family of centromeric retrotransposons, all of which are unevenly distributed among pea chromosomes. We present the centromeres of Pisum as novel "meta-polycentric" functional domains. Our results demonstrate that the organization and DNA composition of functional centromere domains can be far more complex than previously thought, do not require single repetitive elements, and do not require single centromere domains in order to segregate properly. Based on these findings, we propose Pisum as a useful model for investigation of centromere architecture and the still poorly understood role of repetitive DNA in centromere evolution, determination, and function.
- MeSH
- centromera genetika MeSH
- chromozomy genetika MeSH
- histony genetika MeSH
- hrách setý * cytologie genetika MeSH
- molekulární sekvence - údaje MeSH
- repetitivní sekvence nukleových kyselin MeSH
- retroelementy genetika MeSH
- satelitní DNA * genetika MeSH
- segregace chromozomů genetika MeSH
- sekvence aminokyselin MeSH
- tubulin genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- histony MeSH
- retroelementy MeSH
- satelitní DNA * MeSH
- tubulin MeSH
