Chromosome numbers of eight Carex taxa in Korea (Cyperaceae)

In the flora of Korea, Carex L. is one of the most species-rich genera. Among nearly 157 Carex taxa, less than 30 have had their chromosome numbers reported. We report the meiotic chromosome numbers of eight Carex taxa from Korean populations, which include the first count for C. accrescens Ohwi (n = 37II) and the first chromosome investigations of Korean populations for three taxa: C. bostrychostigma Maxim. (n = 22II), C. lanceolata Boott (n = 36II), and C. paxii Kük. (n = 38II). In most species, chromosome counts observed in the study are included within the variation ranges of previous chromosome numbers. However, C. bostrychostigma Maxim. (n = 22II) and C. planiculmis Kom. (n = 29II) are assigned new chromosome numbers. Carex is known to have holocentric chromosomes, lacking visible primary constrictions and exhibiting great variance in its chromosome number. Further investigations of the diversity of Carex chromosomes will provide basic information with which to understand the high species diversity of the genus.

Meiosis Progression and Recombination in Holocentric Plants: What Is Known?

Differently from the common monocentric organization of eukaryotic chromosomes, the so-called holocentric chromosomes present many centromeric regions along their length. This chromosomal organization can be found in animal and plant lineages, whose distribution suggests that it has evolved independently several times. Holocentric chromosomes present an advantage: even broken chromosome parts can be correctly segregated upon cell division. However, the evolution of holocentricity brought about consequences to nuclear processes and several adaptations are necessary to cope with this new organization. Centromeres of monocentric chromosomes are involved in a two-step cohesion release during meiosis. To deal with that holocentric lineages developed different adaptations, like the chromosome remodeling strategy in Caenorhabditis elegans or the inverted meiosis in plants. Furthermore, the frequency of recombination at or around centromeres is normally very low and the presence of centromeric regions throughout the entire length of the chromosomes could potentially pose a problem for recombination in holocentric organisms. However, meiotic recombination happens, with exceptions, in those lineages in spite of their holocentric organization suggesting that the role of centromere as recombination suppressor might be altered in these lineages. Most of the available information about adaptations to meiosis in holocentric organisms is derived from the animal model C. elegans. As holocentricity evolved independently in different lineages, adaptations observed in C. elegans probably do not apply to other lineages and very limited research is available for holocentric plants. Currently, we still lack a holocentric model for plants, but good candidates may be found among Cyperaceae, a large angiosperm family. Besides holocentricity, chiasmatic and achiasmatic inverted meiosis are found in the family. Here, we introduce the main concepts of meiotic constraints and adaptations with special focus in meiosis progression and recombination in holocentric plants. Finally, we present the main challenges and perspectives for future research in the field of chromosome biology and meiosis in holocentric plants.

A simple model explains the cell cycle-dependent assembly of centromeric nucleosomes in holocentric species

ABSTRACTCentromeres are essential for chromosome movement. In independent taxa, species with holocentric chromosomes exist. In contrast to monocentric species, where no obvious dispersion of centromeres occurs during interphase, the organization of holocentromeres differs between condensed and decondensed chromosomes. During interphase, centromeres are dispersed into a large number of CENH3-positive nucleosome clusters in a number of holocentric species. With the onset of chromosome condensation, the centromeric nucleosomes join and form line-like holocentromeres. Using polymer simulations, we propose a mechanism, relying on the interaction between centromeric nucleosomes and Structural Maintenance of Chromosomes (SMC) proteins. All simulations represented a ~20 Mbp-long chromosome, corresponding to ~100,000 nucleosomes. Different sets of molecular dynamic simulations were evaluated by testing four parameters: 1) the concentration of Loop Extruders (LEs) corresponding to SMCs; 2) the distribution and number of centromeric nucleosomes; 3) the effect of centromeric nucleosomes on interacting LEs; and 4) the assembly of kinetochores bound to centromeric nucleosomes. We observed the formation of a line-like holocentromere, due to the aggregation of the centromeric nucleosomes when the chromosome was compacted into loops. A groove-like holocentromere structure formed after a kinetochore complex was simulated along the centromeric line. Similar mechanisms may also organize a monocentric chromosome constriction, and its regulation may cause different centromere types during evolution.

Holocentric Chromosomes Probably Do Not Prevent Centromere Drive in Cyperaceae

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.

A telomere-to-telomere assembly of Oscheius tipulae and the evolution of rhabditid nematode chromosomes

Eukaryotic chromosomes have phylogenetic persistence. In many taxa, each chromosome has a single functional centromere with essential roles in spindle attachment and segregation. Fusion and fission can generate chromosomes with no or multiple centromeres, leading to genome instability. Groups with holocentric chromosomes (where centromeric function is distributed along each chromosome) might be expected to show karyotypic instability. This is generally not the case, and in Caenorhabditis elegans, it has been proposed that the role of maintenance of a stable karyotype has been transferred to the meiotic pairing centers, which are found at one end of each chromosome. Here, we explore the phylogenetic stability of nematode chromosomes using a new telomere-to-telomere assembly of the rhabditine nematode Oscheius tipulae generated from nanopore long reads. The 60-Mb O. tipulae genome is resolved into six chromosomal molecules. We find the evidence of specific chromatin diminution at all telomeres. Comparing this chromosomal O. tipulae assembly with chromosomal assemblies of diverse rhabditid nematodes, we identify seven ancestral chromosomal elements (Nigon elements) and present a model for the evolution of nematode chromosomes through rearrangement and fusion of these elements. We identify frequent fusion events involving NigonX, the element associated with the rhabditid X chromosome, and thus sex chromosome-associated gene sets differ markedly between species. Despite the karyotypic stability, gene order within chromosomes defined by Nigon elements is not conserved. Our model for nematode chromosome evolution provides a platform for investigation of the tensions between local genome rearrangement and karyotypic evolution in generating extant genome architectures.

New cytogenetic data for three species of Pentatomidae (Heteroptera): Dichelops melacanthus (Dallas, 1851), Loxa viridis (Palisot de Beauvois, 1805), and Edessa collaris (Dallas, 1851)

In this paper, we present new cytogenetic data for three species of the family Pentatomidae: Dichelops melacanthus (Dallas, 1851), Loxa viridis (Palisot de Beauvois, 1805), and Edessa collaris (Dallas, 1851). All studied species presented holocentric chromosomes and inverted meiosis for the sex chromosomes. D. melacanthus has 2n = 12 (10A + XY); L. viridis showed 2n = 14 (12A + XY); and E. collaris showed 2n = 14 (12A + XY). C-banding was performed for the first time in these species and revealed terminal and interstitial heterochromatic regions on the autosomes; DAPI/CMA3 staining showed different fluorescent patterns. In all species, fluorescence in situ hybridization (FISH) with 18S rDNA probe identified signals on one autosomal bivalent, this being the first report of FISH application in the species D. melacanthus and L. viridis. The results obtained add to those already existing in the literature, enabling a better understanding of the meiotic behavior of these insects.

New cytogenetic data for three species of Pentatomidae (Heteroptera): Dichelops melacanthus (Dallas, 1851), Loxa viridis (Palisot de Beauvois, 1805), and Edessa collaris (Dallas, 1851)

In this paper, we present new cytogenetic data for three species of the family Pentatomidae: Dichelops melacanthus (Dallas, 1851), Loxa viridis (Palisot de Beauvois, 1805), and Edessa collaris (Dallas, 1851). All studied species presented holocentric chromosomes and inverted meiosis for the sex chromosomes. D. melacanthus has 2n = 12 (10A + XY); L. viridis showed 2n = 14 (12A + XY); and E. collaris showed 2n = 14 (12A + XY). C-banding was performed for the first time in these species and revealed terminal and interstitial heterochromatic regions on the autosomes; DAPI/CMA3 staining showed different fluorescent patterns. In all species, fluorescence in situ hybridization (FISH) with 18S rDNA probe identified signals on one autosomal bivalent, this being the first report of FISH application in the species D. melacanthus and L. viridis. The results obtained add to those already existing in the literature, enabling a better understanding of the meiotic behavior of these insects.

Spatial and temporal control of targeting Polo-like kinase during meiotic prophase

Polo-like kinases (PLKs) play widely conserved roles in orchestrating meiotic chromosome dynamics. However, how PLKs are targeted to distinct subcellular localizations during meiotic progression remains poorly understood. Here, we demonstrate that the cyclin-dependent kinase CDK-1 primes the recruitment of PLK-2 to the synaptonemal complex (SC) through phosphorylation of SYP-1 in C. elegans. SYP-1 phosphorylation by CDK-1 occurs just before meiotic onset. However, PLK-2 docking to the SC is prevented by the nucleoplasmic HAL-2/3 complex until crossover designation, which constrains PLK-2 to special chromosomal regions known as pairing centers to ensure proper homologue pairing and synapsis. PLK-2 is targeted to crossover sites primed by CDK-1 and spreads along the SC by reinforcing SYP-1 phosphorylation on one side of each crossover only when threshold levels of crossovers are generated. Thus, the integration of chromosome-autonomous signaling and a nucleus-wide crossover-counting mechanism partitions holocentric chromosomes relative to the crossover site, which ultimately defines the pattern of chromosome segregation during meiosis I.