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Chromosomes in Droseraceae and closely related families. Current knowledge of chromosome types in Droseraceae and closely related families is shown next to the dated phylogenetic tree. H - holocentric chromosomes, M - monocentric chromosomes, ? - unknown chromosomes. Timescale indicates millions of years before present day. Species from shaded clades were analyzed in the present study. The phylogenetic tree was adopted and simplified from Veleba et al. (2017). Numbers of species were taken from Angiosperm Phylogeny Website (Stevens 2017).
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Holocentric chromosomes have evolved in various plant and animal taxa, which
suggests they may confer a selective advantage in certain conditions, yet their
adaptive potential has scarcely been studied. One of the reasons may reside in our
insufficient knowledge of the phylogenetic distribution of holocentric chromosomes
across eukaryotic phylogeny...
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Citations
... Holocentric chromosomes have been reported in only a few plant lineages, such as the families Cyperaceae, Juncaceae and Droseraceae, as well as the genera Chionographis (Melanthiaceae), Myristica (Myristicaceae) and Cuscuta subgen. Cuscuta (Convolvulaceae) Kolodin et al., 2018). Because acentric chromosome fragments often remain viable and are inherited by daughter cells in holocentric organisms, chromosome fission and fusion affect chromosome number evolution more frequently in holocentrics than in monocentrics (Hipp, 2007;Bureš et al., 2013;Bureš and Zedek, 2014). ...
Background and aims:
It is unclear how widespread polyploidy is throughout the largest holocentric plant lineage-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 analyzes 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 relations 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 relation 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 relation is observed between chromosome number and genome size. Thus, there can be a high incidence of polyploidy in holocentric plants, whose cell division properties differ from monocentrics.
... Although holocentric chromosomes are rarer in eukaryotes than monocentric chromosomes (Escudero et al., 2016), they are often apomorphic or almost apomorphic for entire clades, such as the insect orders of butterflies, true bugs, and dragonflies, the spider superfamily Dysderoidea, centipedes, and millipedes, and roundworms (Melters et al., 2012;Bureš et al., 2013;Král et al., 2019;Mandrioli & Manicardi, 2020). In plants, holocentric chromosomes have been found in the families Cyperaceae, Juncaceae, Droseraceae (Melters et al., 2012;Kolodin et al., 2018;Krátká et al., 2021), the subfamily Chionographidae (Melanthiaceae; Tanaka, 1977;, the genera Cuscuta (Convolvulaceae; Oliveira et al., 2020) and Myristica (Myristicaceae; Flach, 1966), and also in streptophyte algae of the class Zygnematophyceae (King, 1960;Godward, 1966). cytogenetic models as well as important crops, their chromosomal monocentrism is supported by a large body of cytogenetic literature. ...
Plants continuously face stress from ultraviolet-B radiation that can cause chromosomes to fragment. The impact of fragmentation may depend on chromosome type: holocentric chromosomes tolerate fragmentation but monocentric chromosomes do not. Our field experiments on holocentric cyperids and monocentric grasses suggested that holocentric plants might indeed be less stressed with higher UV-B doses. However, whether holocentric chromosomes may also convey a competitive advantage under higher UV-B doses remains an open question.
Here we test whether holocentric plants are more competitive under higher UV-B by comparing the vegetation percent cover of cyperids (holocentric) and grasses (monocentric) in 291,883 vegetation plots across a fine-grid UV-B gradient spanning all of Europe, while accounting for habitat-specific conditions (soil moisture, nutrients, soil reaction, and temperature).
We found that although habitat-specific conditions strongly affect cyperid/grass competition, the cyperid/grass cover ratio nevertheless increases with UV-B dose.
Our results suggest that in addition to mitigating stress, holocentric chromosomes can confer a competitive advantage under high UV-B influx, which may have helped early cyperids to colonize open UV-B exposed habitats and spread around the world. Our findings may also have implications for the hypothesized role of holocentric chromosomes in the colonization of land in the Paleozoic.
... However, this is not the case in organisms with holocentric chromosomes, in which CenH3 nucleosomes assemble (and microtubules thus bind) along the entire chromosome (Bureš et al., 2013). Holocentric chromosomes have originated independently at least 15 times in plants and animals (Melters et al., 2012;Drinnenberg et al., 2014;Escudero et al., 2016), but it is still unclear what evolutionary advantage allows the holocentric structure to arise and persist (Kolodin et al., 2018). ...
... Contrary to the previous report (Zedek et al., 2016), monocentric chromosomes were recently proven by CenH3 and microtubule immunolabeling in mitosis of Prionium serratum from a small related cyperid family Thurniaceae (Baez et al., 2020). Monocentric chromosomes were also suggested in four species of the genus Juncus from the sister family Juncaceae (Guerra et al., 2019), although the authors base their conclusions on DAPI and CMA staining and histone phosphorylation patterns (Guerra et al., 2019), none of which are reliable markers for holo-or monocentricity (Kolodin et al., 2018;Neumann et al., 2020). On the other hand, although we cannot be entirely sure that all Cyperaceae are holocentric, so far, there is no evidence to the contrary. ...
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.
... Beyond endopolyploidy, we recently hypothesized that species with holocentric chromosomes may be less sensitive to radiation-induced DNA damage (Zedek and Bureš, 2018). Although holocentric chromosomes are rarer than monocentric chromosomes in eukaryotes, they are often apomorphic or almost apomorphic for entire clades, such as the plant families Cyperaceae, Juncaceae and Droseraceae (Melters et al., 2012;Kolodin et al., 2018), subfamily Chionographidae (Melanthiaceae; Tanaka, 2020), and genera Cuscuta (Convolvulaceae; Oliveira et al., 2020) and Myristica (Myristicaceae); among animals, they can be found in nematodes and various arthropod orders such as butterflies, true bugs and some spiders (Melters et al., 2012;Bureš et al., 2013;Král et al., 2019). Whereas monocentric chromosomes form the kinetochore (the structure to which spindle microtubules are attached during cell division) only in the centromere area, holocentric chromosomes form their kinetochore almost along their entire length (Cuacos et al., 2015;. ...
... In the resulting fluorescence histograms, 2C peaks were gated automatically using FloMax software (Partec). To standardize across samples, peaks for higher ploidy levels were gated manually in such a way that the lower and upper boundaries of the 2C peak from automatic gating were multiplied by 2 to obtain the boundaries of the 4C peak, by 4 to obtain the boundaries of the 8C peak and so on Kolodin et al., 2018). The numbers of cells with different ploidy levels were then used to calculate the endopolyploidy level, expressed as the endopolyploidy index (EI; Barow and Meister, 2003): ...
Background and Aims: UV-B radiation damages the DNA, cells, and photosynthetic apparatus of plants. Plants commonly prevent this damage by synthetizing UV-B protective compounds. Recent laboratory experiments in Arabidopsis and cucumber indicate that plants can also respond to UV-B stress with endopolyploidy. Here we test the generality of this response in natural plant populations, considering their monocentric or holocentric chromosomal structure.
Methods: We measured the endopolyploidy index (flow cytometry) and the concentration of UV-B protective compounds in leaves of 12 herbaceous species (1007 individuals) from forest interiors and neighboring clearings where they were exposed to increased UV-B radiation (103 forest+clearing populations). Then we analyzed the data using phylogenetic mixed models.
Key Results: Concentration of UV-B protectives increased with UV-B doses estimated from hemispheric photographs of the sky above sample collection sites, but the increase was more rapid in species with monocentric chromosomes. Endopolyploidy index increased with UV-B doses and with concentrations of UV-B absorbing compounds only in species with monocentric chromosomes, while holocentric species responded negligibly.
Conclusions: Endopolyploidy seems to be a common response to increased UV-B in monocentric plants. Low sensitivity to UV-B in holocentric species might relate to their success in high-UV stressed habitats and corroborates the hypothesized role of holocentric chromosomes in plant terrestrialization.
... In plants, holocentric chromosomes have been found in zygnematophycean algae [39], in the genera Myristica (Myristicaceae), Chionographis (Melanthiaceae), Cuscuta (Convolvulaceae) and Droseraceae [40][41][42], in the species Trithuria submersa (Hydatellaceae), Prionium serratum (Thurniaceae) [43,44] and, among higher-plants, in many genera belonging to families Cyperaceae and Juncaceae, including the snowy woodrush Luzula nivea (Juncaceae), the most well-studied holocentric plant [45,46]. In Luzula spp, the centromeric activity is localized simultaneously at several evenly spaced sites along each chromosome and chromosomes can be fragmented naturally or by irradiation into smaller (but viable) chromosomes [47,48]. ...
Holocentric chromosomes possess multiple kinetochores along their length rather than the single centromere typical of other chromosomes [1]. They have been described for the first time in cytogenetic experiments dating from 1935 and, since this first observation, the term holocentric chromosome has referred to chromosomes that: i. lack the primary constriction corresponding to centromere observed in monocentric chromosomes [2]; ii. possess multiple kinetochores dispersed along the chromosomal axis so that microtubules bind to chromosomes along their entire length and move broadside to the pole from the metaphase plate [3]. These chromosomes are also termed holokinetic, because, during cell division, chromatids move apart in parallel and do not form the classical V-shaped figures typical of monocentric chromosomes [4–6]. Holocentric chromosomes evolved several times during both animal and plant evolution and are currently reported in about eight hundred diverse species, including plants, insects, arachnids and nematodes [7,8]. As a consequence of their diffuse kinetochores, holocentric chromosomes may stabilize chromosomal fragments favouring karyotype rearrangements [9,10]. However, holocentric chromosome may also present limitations to crossing over causing a restriction of the number of chiasma in bivalents [11] and may cause a restructuring of meiotic divisions resulting in an inverted meiosis [12].
... Could it be that the development of holocentricity is advantageous to move large chromosomes during cell divisions? Obviously, this is not a reason because, similar to the large chromosomes of Luzula [41] and Rhynchospora [47,51], the much smaller chromosomes of Cuscuta [46], Drosera [92][93][94][95] and Chionographis [96,97] are holocentric, and the holokinetic chromosomes of the spider superfamily Could it be that the development of holocentricity is advantageous to move large chromosomes during cell divisions? Obviously, this is not a reason because, similar to the large chromosomes of Luzula [41] and Rhynchospora [47,51], the much smaller chromosomes of Cuscuta [46], Drosera [92][93][94][95] and Chionographis [96,97] are holocentric, and the holokinetic chromosomes of the spider superfamily Dysderoidea are of different size [80]. ...
... Obviously, this is not a reason because, similar to the large chromosomes of Luzula [41] and Rhynchospora [47,51], the much smaller chromosomes of Cuscuta [46], Drosera [92][93][94][95] and Chionographis [96,97] are holocentric, and the holokinetic chromosomes of the spider superfamily Could it be that the development of holocentricity is advantageous to move large chromosomes during cell divisions? Obviously, this is not a reason because, similar to the large chromosomes of Luzula [41] and Rhynchospora [47,51], the much smaller chromosomes of Cuscuta [46], Drosera [92][93][94][95] and Chionographis [96,97] are holocentric, and the holokinetic chromosomes of the spider superfamily Dysderoidea are of different size [80]. On the other hand, the very large chromosomes of lilies, of Triticeae, of some legumes, and of conifers, for instance, are monocentric. ...
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.
... The chromosome number variability in different species within a genus with monokinetic chromosomes is usually a result of polyploidy or aneuploidy [6,10,11]. In those species with holokinetic chromosomes, the frequent aneuploidy is complemented by two additional mechanisms which may lead to differences in the chromosome count: agmatoploidy (fission of chromosomes) and symploidy (fusion of chromosomes) [10,[12][13][14][15]. It seems that evolution of karyotypes in sedges, important for species diversification, is driven by fusion and fission of chromosomes [16]. ...
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. phyl-lostachys and taxa of the subgenus Carex section Gynobasidae.
... Holocentric taxa have a broad phylogenetic distribution, including various groups of nematodes, arthropods, and plants (Melters et al., 2012). In flowering plants, they represent a minor fraction, including, for example, families Juncaceae (Bozek et al., 2012), Cyperaceae (Luceño et al., 1998;Roalson et al., 2007;Håkansson, 2010), Droseraceae (Kolodin et al., 2018); genus Chionographis [Liliaceae; (Tanaka and Tanaka, 1979)]; and some species from the genus Cuscuta (Pazy and Plitmann, 1994;Pazy and Plitmann, 1995;Pazy and Plitmann, 2002). Because holocentric taxa are often embedded within broader phylogenetic lineages possessing monocentric chromosomes, it is thought that holocentric chromosome organization originated from the monocentric format and that this transition occurred independently in multiple phylogenetic lineages (Melters et al., 2012). ...
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.
... These included genes involved in kinetochore formation [17,18] (Suppl. Results Fig. 6), which have previously been shown to be associated with the occurrence of holocentric chromosomes [19][20][21]. Further losses affected the ubiquitin (UBQ) gene family often involved in stress responses (Suppl. ...
... Recently, holocentry has been proposed for two additional lineages: the early divergent Trithuria submersa (Nymphaeales, Kynast et al., 2014) and a species from the sister family of the Cyperaceae plus Juncaceae clade, Prionium serratum (Thurniaceae, Zedek et al., 2016). However, there are uncertainties about the distribution of holocentry in Cuscuta, Drosera, Melanthiaceae and Myristicaceae (Kolodin et al., 2018;Márquez-Corro et al., 2018). Besides angiosperms, holocentric chromosomes have not been detected in any other Archaeoplastida lineage, with the exception of the green algae family Zygnematophyceae (Brook, 1981;King, 1960). ...
Holocentric chromosomes are characterised by the presence of kinetochoric activity along the chromosome length. This atypical chromosomal architecture has evolved independently in a wide array of lineages across the tree of life. Different mechanisms have been developed to overcome meiotic problems posed by holocentry, such as inverted meiosis and restricted kinetochore activity. Although holocentric karyotypes present potential advantages through the fission and fusion events that characterise chromosome evolution in several holocentric lineages, there is no consistent evidence of increased diversification rates in holocentric lineages relative to monocentric lineages. The extended kinetochore in holocentric chromosomes has been hypothesised to enable a unique type of meiotic drive, ‘holocentric drive’, analogous to the meiotic drive of monocentric chromosomes. However, much research remains to understand holocentrism, especially elucidating the mechanism and evolutionary implications of meiosis in unrelated holocentric lineages. Monocentric chromosomes are distinct from holocentric chromosomes during mitotic segregation, in which chromosomes generally adopt a V shape in the former and segregate parallel to the equatorial plate in the latter. Holocentric chromosomes are present in distantly related plant and animal lineages, suggesting several independent origins of holocentry. Monocentry appears to be ancestral in eukaryotes, and evolutionary transitions appear to have occurred from monocentric to holocentric, and vice versa. Reversions from holocentric to monocentric chromosomes appear to have occurred more frequently than transitions from monocentry to holocentry. Although holocentric chromosomes would seem like an adaptive advantage, there is no clear pattern when compared to monocentric lineages, as both types could present different evolutionary advantages.
