Nejvíce citovaný článek - PubMed ID 24758327
Holokinetic drive: centromere drive in chromosomes without centromeres
BACKGROUND: Genome size is influenced by natural selection and genetic drift acting on variations from polyploidy and repetitive DNA sequences. We hypothesized that centromere drive, where centromeres compete for inclusion in the functional gamete during meiosis, may also affect genome and chromosome size. This competition occurs in asymmetric meiosis, where only one of the four meiotic products becomes a gamete. If centromere drive influences chromosome size evolution, it may also impact post-polyploid diploidization, where a polyploid genome is restructured to function more like a diploid through chromosomal rearrangements, including fusions. We tested if plant lineages with asymmetric meiosis exhibit faster chromosome size evolution compared to those with only symmetric meiosis, which lack centromere drive as all four meiotic products become gametes. We also examined if positive selection on centromeric histone H3 (CENH3), a protein that can suppress centromere drive, is more frequent in these asymmetric lineages. METHODS: We analysed plant groups with different meiotic modes: asymmetric in gymnosperms and angiosperms, and symmetric in bryophytes, lycophytes and ferns. We selected species based on available CENH3 gene sequences and chromosome size data. Using Ornstein-Uhlenbeck evolutionary models and phylogenetic regressions, we assessed the rates of chromosome size evolution and the frequency of positive selection on CENH3 in these clades. RESULTS: Our analyses showed that clades with asymmetric meiosis have a higher frequency of positive selection on CENH3 and increased rates of chromosome size evolution compared to symmetric clades. CONCLUSIONS: Our findings support the hypothesis that centromere drive accelerates chromosome and genome size evolution, potentially also influencing the process of post-polyploid diploidization. We propose a model which in a single framework helps explain the stability of chromosome size in symmetric lineages (bryophytes, lycophytes and ferns) and its variability in asymmetric lineages (gymnosperms and angiosperms), providing a foundation for future research in plant genome evolution.
- Klíčová slova
- Angiosperms, CENH3, asymmetric and symmetric meiosis, bryophytes, centromere drive, chromosome size, ferns, genome size, gymnosperms, lycophytes, post-polyploid diploidization,
- MeSH
- biologická evoluce MeSH
- centromera * genetika MeSH
- chromozomy rostlin * genetika MeSH
- cykasy genetika MeSH
- délka genomu * MeSH
- fylogeneze MeSH
- genom rostlinný * genetika MeSH
- histony genetika metabolismus MeSH
- kapradiny genetika fyziologie MeSH
- Magnoliopsida genetika MeSH
- meióza * genetika MeSH
- molekulární evoluce * MeSH
- polyploidie MeSH
- rostliny genetika MeSH
- selekce (genetika) MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- histony 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
BACKGROUND AND AIMS: While variation in genome size and chromosome numbers and their consequences are often investigated in plants, the biological relevance of variation in chromosome size remains poorly known. Here, we examine genome and mean chromosome size in the cyperid clade (families Cyperaceae, Juncaceae and Thurniaceae), which is the largest vascular plant lineage with predominantly holocentric chromosomes. METHODS: We measured genome size in 436 species of cyperids using flow cytometry, and augment these data with previously published datasets. We then separately compared genome and mean chromosome sizes (2C/2n) amongst the major lineages of cyperids and analysed how these two genomic traits are associated with various environmental factors using phylogenetically informed methods. KEY RESULTS: We show that cyperids have the smallest mean chromosome sizes recorded in seed plants, with a large divergence between the smallest and largest values. We found that cyperid species with smaller chromosomes have larger geographical distributions and that there is a strong inverse association between mean chromosome size and number across this lineage. CONCLUSIONS: The distinct patterns in genome size and mean chromosome size across the cyperids might be explained by holokinetic drive. The numerous small chromosomes might function to increase genetic diversity in this lineage where crossovers are limited during meiosis.
- Klíčová slova
- Chromosome number, Cyperaceae, Juncaceae, Thurniaceae, chromosome size, distribution range size, genome size, holocentric chromosomes, holokinetic drive,
- MeSH
- chromozomy rostlin * genetika MeSH
- délka genomu MeSH
- fylogeneze MeSH
- genom rostlinný genetika MeSH
- molekulární evoluce * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Previous studies on grass species suggested that the total centromere size (sum of all centromere sizes in a cell) may be determined by the genome size, possibly because stable scaling is important for proper cell division. However, it is unclear whether this relationship is universal. Here we analyze the total centromere size using the CenH3-immunofluorescence area as a proxy in 130 taxa including plants, animals, fungi, and protists. We verified the reliability of our methodological approach by comparing our measurements with available ChIP-seq-based measurements of the size of CenH3-binding domains. Data based on these two independent methods showed the same positive relationship between the total centromere size and genome size. Our results demonstrate that the genome size is a strong predictor (R-squared = 0.964) of the total centromere size universally across Eukaryotes. We also show that this relationship is independent of phylogenetic relatedness and centromere type (monocentric, metapolycentric, and holocentric), implying a common mechanism maintaining stable total centromere size in Eukaryotes.
- MeSH
- centromera fyziologie MeSH
- délka genomu MeSH
- houby genetika MeSH
- molekulární evoluce MeSH
- rostliny genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
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
Counting chromosomes is the first step towards a better understanding of the karyotype evolution and the role of chromosome evolution in species diversification within Carex; however, the chromosome count is not known yet for numerous sedges. In this paper chromosome counts were performed for 23 Carex taxa from Armenia, Austria, the Czech Republic, and Poland. Chromosome numbers were determined for the first time in three species (Carex cilicica, 2n = 54; C. phyllostachys, 2n = 56; C. randalpina, 2n = 78), two subspecies (C. muricata subsp. ashokae, 2n = 58; C. nigra subsp. transcaucasica, 2n = 84) and two hybrids (C. ×decolorans, 2n = 74; C. ×walasii, 2n = 108). Among the taxa whose number of chromosomes had been known before, the largest difference was found in C. hartmaniorum (here 2n = 52) and C. aterrima subsp. medwedewii (here 2n = 52). A difference in the chromosome count was demonstrated for C. cilicica (2n = 54) versus the species of the section Aulocystis (2n = 30 to 40) and for C. tomentosa (2n = 48) versus the species of the section Acrocystis (2n = 18 to 38). The results of this study indicate that the position of C. cilicica in Aulocystis section may raise doubts. Attention was paid to the relationship between C. phyllostachys and taxa of the subgenus Carex section Gynobasidae.
- MeSH
- Carex (rostlina) klasifikace genetika MeSH
- chromozomy rostlin genetika MeSH
- fylogeneze * MeSH
- genetická variace * MeSH
- molekulární evoluce * MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Arménie MeSH
- Česká republika MeSH
- Polsko MeSH
- Rakousko MeSH
Spiders are an ancient and extremely diverse animal order. They show a considerable diversity of genome sizes, karyotypes and sex chromosomes, which makes them promising models to analyse the evolution of these traits. Our study is focused on the evolution of the genome and chromosomes in haplogyne spiders with holokinetic chromosomes. Although holokinetic chromosomes in spiders were discovered a long time ago, information on their distribution and evolution in these arthropods is very limited. Here we show that holokinetic chromosomes are an autapomorphy of the superfamily Dysderoidea. According to our hypothesis, the karyotype of ancestral Dysderoidea comprised three autosome pairs and a single X chromosome. The subsequent evolution has frequently included inverted meiosis of the sex chromosome and an increase of 2n. We demonstrate that caponiids, a sister clade to Dysderoidea, have enormous genomes and high diploid and sex chromosome numbers. This pattern suggests a polyploid event in the ancestors of caponiids. Holokinetic chromosomes could have arisen by subsequent multiple chromosome fusions and a considerable reduction of the genome size. We propose that spider sex chromosomes probably do not pose a major barrier to polyploidy due to specific mechanisms that promote the integration of sex chromosome copies into the genome.
- MeSH
- genom * MeSH
- karyotyp * MeSH
- meióza MeSH
- molekulární evoluce * MeSH
- pavouci genetika MeSH
- polyploidie * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND AND AIMS: Studies in the carnivorous family Lentibulariaceae in the last years resulted in the discovery of the smallest plant genomes and an unusual pattern of genomic GC content evolution. However, scarcity of genomic data in other carnivorous clades still prevents a generalization of the observed patterns. Here the aim was to fill this gap by mapping genome evolution in the second largest carnivorous family, Droseraceae, where this evolution may be affected by chromosomal holokinetism in Drosera METHODS: The genome size and genomic GC content of 71 Droseraceae species were measured by flow cytometry. A dated phylogeny was constructed, and the evolution of both genomic parameters and their relationship to species climatic niches were tested using phylogeny-based statistics. KEY RESULTS: The 2C genome size of Droseraceae varied between 488 and 10 927 Mbp, and the GC content ranged between 37·1 and 44·7 %. The genome sizes and genomic GC content of carnivorous and holocentric species did not differ from those of their non-carnivorous and monocentric relatives. The genomic GC content positively correlated with genome size and annual temperature fluctuations. The genome size and chromosome numbers were inversely correlated in the Australian clade of Drosera CONCLUSIONS: Our results indicate that neither carnivory (nutrient scarcity) nor the holokinetism have a prominent effect on size and DNA base composition of Droseraceae genomes. However, the holokinetic drive seems to affect karyotype evolution in one of the major clades of Drosera Our survey confirmed that the evolution of GC content is tightly connected with the evolution of genome size and also with environmental conditions.
- Klíčová slova
- DNA base composition, DNA content, Droseraceae, GC content, carnivorous plants, flow cytometry, genome size evolution, holocentric chromosomes, holokinetic chromosomes,
- MeSH
- biologická evoluce * MeSH
- chromozomy rostlin genetika MeSH
- Droseraceae genetika MeSH
- fylogeneze MeSH
- genetická variace genetika MeSH
- genom rostlinný genetika MeSH
- masožravci MeSH
- zastoupení bazí genetika MeSH
- Publikační typ
- časopisecké články MeSH
BACKGROUND AND AIMS: The centromere drive theory explains diversity of eukaryotic centromeres as a consequence of the recurrent conflict between centromeric repeats and centromeric histone H3 (CenH3), in which selfish centromeres exploit meiotic asymmetry and CenH3 evolves adaptively to counterbalance deleterious consequences of driving centromeres. Accordingly, adaptively evolving CenH3 has so far been observed only in eukaryotes with asymmetric meiosis. However, if such evolution is a consequence of centromere drive, it should depend not only on meiotic asymmetry but also on monocentric or holokinetic chromosomal structure. Selective pressures acting on CenH3 have never been investigated in organisms with holokinetic meiosis despite the fact that holokinetic chromosomes have been hypothesized to suppress centromere drive. Therefore, the present study evaluates selective pressures acting on the CenH3 gene in holokinetic organisms for the first time, specifically in the representatives of the plant genus Luzula (Juncaceae), in which the kinetochore formation is not co-localized with any type of centromeric repeat. METHODS: PCR, cloning and sequencing, and database searches were used to obtain coding CenH3 sequences from Luzula species. Codon substitution models were employed to infer selective regimes acting on CenH3 in Luzula KEY RESULTS: In addition to the two previously published CenH3 sequences from L. nivea, 16 new CenH3 sequences have been isolated from 12 Luzula species. Two CenH3 isoforms in Luzula that originated by a duplication event prior to the divergence of analysed species were found. No signs of positive selection acting on CenH3 in Luzula were detected. Instead, evidence was found that selection on CenH3 of Luzula might have been relaxed. CONCLUSIONS: The results indicate that holokinetism itself may suppress centromere drive and, therefore, holokinetic chromosomes might have evolved as a defence against centromere drive.
- Klíčová slova
- CenH3, Luzula, centromere drive, holokinetic chromosomes, positive selection,
- MeSH
- centromera genetika MeSH
- chromozomy rostlin genetika MeSH
- fylogeneze MeSH
- genom rostlinný genetika MeSH
- histony genetika MeSH
- Magnoliopsida genetika MeSH
- meióza genetika MeSH
- sekvenční analýza DNA MeSH
- sekvenční seřazení MeSH
- selekce (genetika) genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- histony MeSH
The centromere drive model explaining rapid evolution of eukaryotic centromeres predicts higher frequency of positive selection acting on centromeric histone H3 (CenH3) in clades with asymmetric meiosis compared to the clades with only symmetric meiosis. However, despite the impression one might get from the literature, this key prediction of the centromere drive model has not only never been confirmed, but it has never been tested, because all the previous studies dealt only with the presence or absence instead of the frequency of positive selection. To provide evidence for or against different frequencies of positively selected CenH3 in asymmetrics and symmetrics, we have inferred the selective pressures acting on CenH3 in seventeen eukaryotic clades, including plants, animals, fungi, ciliates and apicomplexa, using codon-substitution models, and compared the inferred frequencies between asymmetrics and symmetrics in a quantitative manner. We have found that CenH3 has been evolving adaptively much more frequently in clades with asymmetric meiosis compared with clades displaying only symmetric meiosis which confirms the prediction of centromere drive model. Our findings indicate that the evolution of asymmetric meiosis required CenH3 to evolve adaptively more often to counterbalance the negative consequences of centromere drive.
- MeSH
- centromera genetika MeSH
- histony genetika MeSH
- houby genetika MeSH
- kodon genetika MeSH
- lidé MeSH
- meióza genetika MeSH
- molekulární evoluce * MeSH
- protein CENP-A genetika MeSH
- rostlinné proteiny genetika MeSH
- sekvenční seřazení MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- CENPA protein, human MeSH Prohlížeč
- histony MeSH
- kodon MeSH
- protein CENP-A MeSH
- rostlinné proteiny MeSH