Abstract
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.
Highlights
Centromeres are chromosomal regions that facilitate faithful chromosome segregation during cell division
Because our strategy for investigating holocentric chromosomes of C. europaea required the visualization of CENH3 protein, which is a universal marker of the centromeric chromatin in plants, we first identified CENH3-coding genes in this species
We found a single CENH3 sequence in C. japonica (CENH3CJAPO) and two sequence variants in C. campestris (CENH3CCAMP-a and CENH3CCAMP-b), which corresponded to their diploid and tetraploid chromosome numbers, respectively
Summary
Centromeres are chromosomal regions that facilitate faithful chromosome segregation during cell division. 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). The factors that induced this transition and its mechanisms are currently unknown
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