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Centromere drive model describes an evolutionary process initiated by centromeric repeats expansion, which leads to the recruitment of excess kinetochore proteins and consequent preferential segregation of an expanded centromere to the egg during female asymmetric meiosis. In response to these selfish centromeres, the histone protein CenH3, which recruits kinetochore components, adaptively evolves to restore chromosomal parity and counter the detrimental effects of centromere drive. Holocentric chromosomes, whose kinetochores are assembled along entire chromosomes, have been hypothesized to prevent expanded centromeres from acquiring a selective advantage and initiating centromere drive. In such a case, CenH3 would be subjected to less frequent or no adaptive evolution. Using codon substitution models, we analyzed 36 CenH3 sequences from 35 species of the holocentric family Cyperaceae. We found 10 positively selected codons in the CenH3 gene [six codons in the N-terminus and four in the histone fold domain (HFD)] and six branches of its phylogeny along which the positive selection occurred. One of the positively selected codons was found in the centromere targeting domain (CATD) that directly interacts with DNA and its mutations may be important in centromere drive suppression. The frequency of these positive selection events was comparable to the frequency of positive selection in monocentric clades with asymmetric female meiosis. Taken together, these results suggest that preventing centromere drive is not the primary adaptive role of holocentric chromosomes, and their ability to suppress it likely depends on their kinetochore structure in meiosis.
- Klíčová slova
- CenH3, asymmetric meiosis, centromere drive, holocentric chromosomes, meiotic drive, monocentric chromosomes, symmetric meiosis,
- 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
It has been hypothesized that species with holocentric chromosomes have a selective evolutionary advantage for developmental and reproductive success because holocentric chromosomes are less susceptible to chromosome breakage than monocentric chromosomes. We analyzed data on sterilizing doses of ionizing radiation for more than 250 species of arthropods to test whether the minimal dose for reproductive sterilization is higher for species with holocentric chromosomes than for species with monocentric chromosomes. Using linear mixed models that account for phylogeny, we show that holocentric arthropods are more tolerant of sterilizing radiation than monocentrics. Moreover, higher dose rates correlate with lower sterilizing doses in monocentrics, but not in holocentrics, which is a novel finding that may be of importance for radiosanitation practice. Under the dose rate of 1 Gy/min, holocentric arthropods are sterilized on average with a 2.9 times higher minimal dose than monocentrics. Life stage and sex have significant but considerably weaker effects on sterilizing dose than chromosome type. Adults and males require 1.2 and 1.4 times higher sterilizing doses than juveniles and females, respectively. These results support the hypothesis that holocentric lineages may originate and thrive better in times of increased exposure to chromosome-breaking factors.
In monocentric organisms with asymmetric meiosis, the kinetochore proteins, such as CENH3 and CENP-C, evolve adaptively to counterbalance the deleterious effects of centromere drive, which is caused by the expansion of centromeric satellite repeats. The selection regimes that act on CENH3 and CENP-C genes have not been analyzed in organisms with holocentric chromosomes, although holocentrism is speculated to have evolved to suppress centromere drive. We tested both CENH3 and CENP-C for positive selection in several species of the holocentric genus Caenorhabditis using the maximum likelihood approach and sliding-window analysis. Although CENP-C did not show any signs of positive selection, positive selection has been detected in the case of CENH3. These results support the hypothesis that centromere drive occurs in Nematoda, at least in the telokinetic meiosis of Caenorhabditis.
- MeSH
- Caenorhabditis elegans genetika metabolismus MeSH
- centromera metabolismus fyziologie MeSH
- chromozomální proteiny, nehistonové genetika metabolismus fyziologie MeSH
- chromozomy metabolismus MeSH
- geneticky modifikované organismy MeSH
- histony genetika fyziologie MeSH
- meióza genetika fyziologie MeSH
- pohyb fyziologie MeSH
- segregace chromozomů genetika fyziologie MeSH
- selekce (genetika) MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- centromere protein C MeSH Prohlížeč
- chromozomální proteiny, nehistonové MeSH
- histony 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
Two chromosomal structures, known as monocentric and holocentric chromosomes, have evolved in eukaryotes. Acentric fragments of monocentric chromosomes are unequally distributed to daughter cells and/or lost, while holocentric fragments are inherited normally. In monocentric species, unequal distribution should generate chimeras of cells with different nuclear DNA content. We investigated whether such differences in monocentric species are detectable by flow cytometry (FCM) as (i) a decreased nuclear DNA content and (ii) an increased coefficient of variance (CV) of the G1 peak after gamma radiation-induced fragmentation. We compared 13 monocentric and 9 holocentric plant species. Unexpectedly, monocentrics and holocentrics did not differ with respect to parameters (i) and (ii) in their response to gamma irradiation. However, we found that the proportion of G2 nuclei was highly elevated in monocentrics after irradiation, while holocentrics were negligibly affected. Therefore, we hypothesize that DNA-damaging agents induce cell cycle arrest leading to endopolyploidy only in monocentric and not (or to much lesser extent) in holocentric plants. While current microscope-dependent methods for holocentrism detection are unreliable for small and numerous chromosomes, which are common in holocentrics, FCM can use somatic nuclei. Thus, FCM may be a rapid and reliable method of high-throughput screening for holocentric candidates across plant phylogeny.
The segregation of chromosomes depends on the centromere. Most species are monocentric, with the centromere restricted to a single region per chromosome. In some organisms, the monocentric organization changed to holocentric, in which the centromere activity is distributed over the entire chromosome length. However, the causes and consequences of this transition are poorly understood. Here, we show that the transition in the genus Cuscuta was associated with dramatic changes in the kinetochore, a protein complex that mediates the attachment of chromosomes to microtubules. We found that in holocentric Cuscuta species, the KNL2 genes were lost; the CENP-C, KNL1, and ZWINT1 genes were truncated; the centromeric localization of CENH3, CENP-C, KNL1, MIS12, and NDC80 proteins was disrupted; and the spindle assembly checkpoint (SAC) degenerated. Our results demonstrate that holocentric Cuscuta species lost the ability to form a standard kinetochore and do not employ SAC to control the attachment of microtubules to chromosomes.
- Klíčová slova
- Cuscuta, centromere, holocentric, kinetochore, monocentric,
- MeSH
- centromera genetika MeSH
- Cuscuta * MeSH
- kinetochory * MeSH
- mikrotubuly metabolismus MeSH
- segregace chromozomů MeSH
- struktury chromozomu MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Satellite DNA repeats (or satDNA) are fast-evolving sequences usually associated with condensed heterochromatin. To test whether the chromosomal organisation of centromeric and non-centromeric satDNA differs in species with holocentric chromosomes, we identified and characterised the major satDNA families in the holocentric Cyperaceae species Rhynchospora ciliata (2n = 10), R. globosa (2n = 50) and R. tenuis (2n = 2x = 4 and 2n = 4x = 8). While conserved centromeric repeats (present in R. ciliata and R. tenuis) revealed linear signals at both chromatids, non-centromeric, species-specific satDNAs formed distinct clusters along the chromosomes. Colocalisation of both repeat types resulted in a ladder-like hybridisation pattern at mitotic chromosomes. In interphase, the centromeric satDNA was dispersed while non-centromeric satDNA clustered and partly colocalised to chromocentres. Despite the banding-like hybridisation patterns of the clustered satDNA, the identification of chromosome pairs was impaired due to the irregular hybridisation patterns of the homologues in R. tenuis and R. ciliata. These differences are probably caused by restricted or impaired meiotic recombination as reported for R. tenuis, or alternatively by complex chromosome rearrangements or unequal condensation of homologous metaphase chromosomes. Thus, holocentricity influences the chromosomal organisation leading to differences in the distribution patterns and condensation dynamics of centromeric and non-centromeric satDNA.
- Klíčová slova
- Chromocentre, Cyperaceae, Heterochromatin, Holocentric chromosome, Rhynchospora, Satellite repeats,
- MeSH
- centromera genetika MeSH
- chromozomy rostlin MeSH
- heterochromatin genetika MeSH
- hybridizace in situ fluorescenční MeSH
- Magnoliopsida genetika MeSH
- satelitní DNA * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- heterochromatin MeSH
- satelitní DNA * MeSH
BACKGROUND AND AIMS: It is unclear how widespread polyploidy is throughout the largest holocentric plant family - the Cyperaceae. Because of the prevalence of chromosomal fusions and fissions, which affect chromosome number but not genome size, it can be impossible to distinguish if individual plants are polyploids in holocentric lineages based on chromosome count data alone. Furthermore, it is unclear how differences in genome size and ploidy levels relate to environmental correlates within holocentric lineages, such as the Cyperaceae. METHODS: We focus our analyses on tribe Schoeneae, and more specifically the southern African clade of Schoenus. We examine broad-scale patterns of genome size evolution in tribe Schoeneae and focus more intensely on determining the prevalence of polyploidy across the southern African Schoenus by inferring ploidy level with the program ChromEvol, as well as interpreting chromosome number and genome size data. We further investigate whether there are relationships between genome size/ploidy level and environmental variables across the nutrient-poor and summer-arid Cape biodiversity hotspot. KEY RESULTS: Our results show a large increase in genome size, but not chromosome number, within Schoenus compared to other species in tribe Schoeneae. Across Schoenus, there is a positive relationship between chromosome number and genome size, and our results suggest that polyploidy is a relatively common process throughout the southern African Schoenus. At the regional scale of the Cape, we show that polyploids are more often associated with drier locations that have more variation in precipitation between dry and wet months, but these results are sensitive to the classification of ploidy level. CONCLUSIONS: Polyploidy is relatively common in the southern African Schoenus, where a positive relationship is observed between chromosome number and genome size. Thus, there may be a high incidence of polyploidy in holocentric plants, whose cell division properties differ from monocentrics.
- Klíčová slova
- Schoenus, Aneuploidy, Cape Floristic Region, Cyperaceae, Schoeneae, chromosome fission, chromosome fusion, climate, genome size, holocentric chromosomes, polyploidy, soil chemistry,
- MeSH
- biodiverzita MeSH
- chromozomy rostlin MeSH
- fylogeneze MeSH
- genom rostlinný MeSH
- ploidie MeSH
- polyploidie MeSH
- šáchorovité * genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Klíčová slova
- Cyperaceae, Paleozoic terrestrialisation, Poaceae, clastogens, holocentric chromosomes, ultraviolet radiation, vegetation plots,
- MeSH
- chromozomy rostlin * MeSH
- rostliny * genetika MeSH
- ultrafialové záření MeSH
- Publikační typ
- dopisy MeSH
- práce podpořená grantem MeSH
