Centromeres are essential for kinetochore assembly and spindle attachment. While chromosomes of most species are monocentric with a single centromere, a minority exhibit holocentricity, with a centromere along the chromatid length. Sporadic emergence of holocentricity suggests multiple independent transitions. To explore this, we compare the centromere and (epi)genome organization of two sister genera with contrasting centromere types: Chamaelirium luteum with large macro-monocentromeres and Chionographis japonica with holocentromeres. Both exhibit chromosome-wide histone phosphorylation patterns distinct from typical monocentric species. Kinetochore analysis reveals similar chimeric Borealin in both species, with additional KNL2 loss and NSL1 chimerism in Cha. luteum. The broad-scale synteny between both genomes supports de novo holocentromere formation in Chi. japonica. Despite sharing features with both centromere types, macro-monocentromeres do not represent a direct link between mono- and holocentromeres. We propose a model for the divergent evolution involving kinetochore gene mutations, altered histone phosphorylation patterns, and centromeric satellite DNA amplification.

Biology Centre Czech Academy of Sciences Institute of Plant Molecular Biology Branišovská 31 České Budějovice Czech Republic

Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben Corrensstrasse 3 Seeland Germany

Molecular Cell Biology Joseph Gottlieb Kölreuter Institute for Plant Sciences Karlsruhe Institute of Technology Fritz Haber Weg 4 Karlsruhe Germany

Multidisciplinary Institute of Plant Biology National Council for Scientific and Technical Research National University of Córdoba Córdoba Argentina

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Flemming W. Zellsubstanz, Kern und Zelltheilung.

Schubert, V. et al. Super-resolution microscopy reveals diversity of plant centromere architecture. PubMed DOI PMC

Kuo, Y. T., Schubert, V., Marques, A., Schubert, I. & Houben, A. Centromere diversity: how different repeat-based holocentromeres may have evolved. PubMed DOI

Macas, J. et al. Assembly of the 81.6 Mb centromere of pea chromosome 6 elucidates the structure and evolution of metapolycentric chromosomes. PubMed DOI PMC

Neumann, P. et al. Stretching the rules: monocentric chromosomes with multiple centromere domains. PubMed DOI PMC

Grzan, T., Despot-Slade, E., Mestrovic, N., Plohl, M. & Mravinac, B. CenH3 distribution reveals extended centromeres in the model beetle PubMed DOI PMC

McKinley, K. L. & Cheeseman, I. M. The molecular basis for centromere identity and function. PubMed DOI PMC

Ochs, F. et al. Sister chromatid cohesion is mediated by individual cohesin complexes. PubMed DOI

Schmitz, M. L., Higgins, J. M. G. & Seibert, M. Priming chromatin for segregation: functional roles of mitotic histone modifications. PubMed DOI PMC

Houben, A. et al. The cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes. PubMed DOI

Gernand, D., Demidov, D. & Houben, A. The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes. PubMed DOI

Caperta, A. D. et al. Distribution patterns of phosphorylated Thr 3 and Thr 32 of histone H3 in plant mitosis and meiosis. PubMed DOI

Agueci, F., Karimi, R. & Houben, A. Characterisation of Nima- and Haspin-like kinases in

Dong, Q. & Han, F. Phosphorylation of histone H2A is associated with centromere function and maintenance in meiosis. PubMed DOI

Demidov, D. et al. Anti-phosphorylated histone H2AThr120: a universal microscopic marker for centromeric chromatin of mono- and holocentric plant species. PubMed DOI

Marques, A. & Drinnenberg, I. A. Same but different: Centromere regulations in holocentric insects and plants. PubMed DOI

Senaratne, A. P., Cortes-Silva, N. & Drinnenberg I. A. Evolution of holocentric chromosomes: drivers, diversity, and deterrents. PubMed

Drinnenberg, I. A., Henikoff, S. & Malik, H. S. Evolutionary turnover of kinetochore proteins: a ship of theseus? PubMed DOI PMC

Neumann, P. et al. Disruption of the standard kinetochore in holocentric PubMed DOI PMC

Drinnenberg, I. A., deYoung, D., Henikoff, S. & Malik, H. S. Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. PubMed DOI PMC

Senaratne, A. P. et al. Formation of the CenH3-deficient holocentromere in PubMed DOI

Cortes-Silva, N. et al. CenH3-independent kinetochore assembly in PubMed DOI

Tanaka, N. & Tanaka, N. Chromosome studies in DOI

Tanaka, N. & Tanaka, N. Chromosome studies in DOI

Tanaka, N. Chromosomal variation in populations of DOI

Tanaka, N. High Stability in Chromosomal Traits of DOI

Pellicer, J., Kelly, L. J., Leitch, I. J., Zomlefer, W. B. & Fay, M. F. A universe of dwarfs and giants: genome size and chromosome evolution in the monocot family Melanthiaceae. PubMed DOI

Tanaka, N. Chromosomal traits of

Kim, C., Kim, S.-C. & Kim, J.-H. Historical Biogeography of melanthiaceae: a case of Out-of-North America through the bering land bridge. PubMed PMC

Tanaka, N. A synopsis of the genus

Kuo, Y.-T. et al. Holocentromeres can consist of merely a few megabase-sized satellite arrays. PubMed DOI PMC

Hofstatter, P. G. et al. Repeat-based holocentromeres influence genome architecture and karyotype evolution. PubMed DOI

Talbert, P. B. & Henikoff, S. What makes a centromere? PubMed DOI

Fransz, P., de Jong, J. H., Lysak, M., Castiglione, M. R. & Schubert, I. Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. PubMed DOI PMC

Kuo, Y.-T. et al. The evolutionary dynamics of repetitive DNA and its impact on the genome diversification in the Genus PubMed PMC

Muller, H., Gil, J. & Drinnenberg, I. A. The impact of centromeres on spatial genome architecture. PubMed DOI

van Hooff, J. J., Tromer, E., van Wijk, L. M., Snel, B. & Kops, G. J. Evolutionary dynamics of the kinetochore network in eukaryotes as revealed by comparative genomics. PubMed PMC

Ishii, M. & Akiyoshi, B. Plasticity in centromere organization and kinetochore composition: lessons from diversity. PubMed DOI PMC

Petrovic, A. et al. The MIS12 complex is a protein interaction hub for outer kinetochore assembly. PubMed DOI PMC

Petrovic, A. et al. Structure of the MIS12 complex and molecular basis of its interaction with CENP-C at human kinetochores. PubMed DOI PMC

Oliveira, L. et al. KNL1 and NDC80 represent new universal markers for the detection of functional centromeres in plants. PubMed DOI

Houben, A. et al. Phosphorylation of histone H3 in plants-a dynamic affair. PubMed DOI

Hindriksen, S., Lens, S. M. A. & Hadders, M. A. The ins and outs of Aurora B inner centromere localization. PubMed DOI PMC

Mata-Sucre, Y. et al. Repeat-based holocentromeres of the woodrush PubMed DOI PMC

Abad, M. A. et al. Borealin-nucleosome interaction secures chromosome association of the chromosomal passenger complex. PubMed DOI PMC

DeBose-Scarlett, E. M. & Sullivan, B. A. Genomic and epigenetic foundations of neocentromere formation. PubMed DOI

Mirkin, E. & Mirkin, S. Replication fork stalling at natural impediments. PubMed DOI PMC

Sproul, J. S. et al. Dynamic evolution of euchromatic satellites on the X chromosome in PubMed DOI PMC

Kasinathan, S. & Henikoff, S. Non-B-form DNA is enriched at centromeres. PubMed DOI PMC

Shi, J. et al. Widespread gene conversion in centromere cores. PubMed DOI PMC

Dong, X. et al. The mutational dynamics of the Arabidopsis centromeres.

Lermontova, I. et al. Arabidopsis kinetochore null2 is an upstream component for centromeric histone H3 variant cenH3 deposition at centromeres. PubMed DOI PMC

Zuo, S. et al. Recurrent plant-specific duplications of KNL2 and its conserved function as a kinetochore assembly factor. PubMed DOI PMC

Hori, T. et al. Association of M18BP1/KNL2 with CENP-A nucleosome is essential for centromere formation in non-mammalian vertebrates. PubMed DOI

French, B. T., Westhorpe, F. G., Limouse, C. & Straight, A. F. Xenopus laevis M18BP1 directly binds existing CENP-A nucleosomes to promote centromeric chromatin assembly. PubMed DOI PMC

Maddox, P. S., Hyndman, F., Monen, J., Oegema, K. & Desai, A. Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. PubMed DOI PMC

Steiner, F. A. & Henikoff, S. Holocentromeres are dispersed point centromeres localized at transcription factor hotspots. PubMed DOI PMC

Oliveira, L. et al. Mitotic spindle attachment to the holocentric chromosomes of PubMed DOI PMC

Le Goff, S. et al. The H3 histone chaperone NASP(SIM3) escorts CenH3 in Arabidopsis. PubMed DOI

Takeuchi, H., Nagahara, S., Higashiyama, T. & Berger, F. The chaperone NASP contributes to de novo deposition of the centromeric histone variant CENH3 in Arabidopsis early embryogenesis. PubMed DOI PMC

Maksimov, V. et al. The H3 chaperone function of NASP is conserved in Arabidopsis. PubMed DOI

Patthy, L. Modular assembly of genes and the evolution of new functions. PubMed DOI

Tromer, E. C., van Hooff, J. J. E., Kops, G. & Snel, B. Mosaic origin of the eukaryotic kinetochore. PubMed DOI PMC

Carmena, M., Wheelock, M., Funabiki, H. & Earnshaw, W. C. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. PubMed DOI PMC

Wang, F. et al. A positive feedback loop involving haspin and Aurora B promotes CPC accumulation at centromeres in mitosis. PubMed DOI PMC

Venkei, Z., Przewloka, M. R. & Glover, D. M. Drosophila Mis12 complex acts as a single functional unit essential for anaphase chromosome movement and a robust spindle assembly checkpoint. PubMed DOI PMC

Ge, X. et al. The structure and assembly of the hetero-octameric BLOC-one-related complex. PubMed DOI

More, K. J., Kaufman, J. G. G., Dacks, J. B. & Manna, P. T. Evolutionary origins of the lysosome-related organelle sorting machinery reveal ancient homology in post-endosome trafficking pathways. PubMed DOI PMC

Nielsen, M., Albrethsen, J., Larsen, F. H. & Skriver, K. The Arabidopsis ADP-ribosylation factor (ARF) and ARF-like (ARL) system and its regulation by BIG2, a large ARF–GEF. DOI

Richardson, D. N., Simmons, M. P. & Reddy, A. S. N. Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. PubMed PMC

Bunning, A. R. & Gupta, M. L. Jr. The importance of microtubule-dependent tension in accurate chromosome segregation. PubMed DOI PMC

Dolezel, J., Bartos, J., Voglmayr, H. & Greilhuber, J. Nuclear DNA content and genome size of trout and human. PubMed

Padmarasu S., Himmelbach A., Mascher M. & Stein N. PubMed

Cheng, H., Concepcion, G. T., Feng, X., Zhang, H. & Li, H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. PubMed DOI PMC

Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. PubMed DOI PMC

Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. PubMed DOI

Guan, D. et al. Identifying and removing haplotypic duplication in primary genome assemblies. PubMed DOI PMC

Zhou, C., McCarthy, S. A. & Durbin, R. YaHS: yet another Hi-C scaffolding tool. PubMed DOI PMC

Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. PubMed DOI PMC

Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. PubMed DOI PMC

Pertea, G., Pertea, M. GFF utilities: GffRead and GffCompare. PubMed PMC

Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. PubMed DOI PMC

Gabriel, L. et al. BRAKER3: Fully automated genome annotation using RNA-seq and protein evidence with GeneMark-ETP, AUGUSTUS, and TSEBRA. PubMed DOI PMC

He, W. et al. NGenomeSyn: an easy-to-use and flexible tool for publication-ready visualization of syntenic relationships across multiple genomes. PubMed DOI PMC

Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. PubMed DOI PMC

Komaki, S. & Schnittger, A. The spindle assembly checkpoint in Arabidopsis is rapidly shut off during severe stress. PubMed DOI

Su, H. et al. Knl1 participates in spindle assembly checkpoint signaling in maize. PubMed PMC

Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. PubMed DOI

Birney, E., Clamp, M. & Durbin, R. GeneWise and Genomewise. PubMed DOI PMC

Thompson, J. D., Higgins, D. G. & Gibson, T. J. Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. PubMed DOI PMC

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. PubMed DOI PMC

Trifinopoulos, J., Nguyen, L. T., von Haeseler, A. & Minh, B. Q. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. PubMed DOI PMC

Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. PubMed DOI

Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. PubMed DOI PMC

Dolezel, J., Binarova, P. & Lucretti, S. Analysis of nuclear DNA content in plant cells by flow cytometry. DOI

Pellicer, J., Fernandez, P., Fay, M. F., Michalkova, E. & Leitch, I. J. Genome size doubling arises from the differential repetitive DNA dynamics in the genus PubMed DOI PMC

Andrews, S. FastQC: a quality control tool for high throughput sequence data (2010). Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (accessed on 24 November 2010).

Novak, P., Neumann, P. & Macas, J. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. PubMed DOI PMC

Novak, P., Neumann, P., Pech, J., Steinhaisl, J. & Macas, J. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. PubMed DOI

Novák, P., Neumann, P. & Macas, J. Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. PubMed DOI

Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. PubMed DOI PMC

Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. PubMed DOI PMC

Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). PubMed DOI PMC

Ramirez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. PubMed DOI PMC

Lopez-Delisle, L. et al. pyGenomeTracks: reproducible plots for multivariate genomic data sets. PubMed PMC

Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. PubMed DOI PMC

Vasimuddin, M., Misra, S., Li, H. & Aluru, S. Efficient architecture-aware acceleration of BWA-MEM for multicore systems. In

Li, H. et al. The sequence alignment/map format and SAMtools. PubMed DOI PMC

Novak, P. et al. TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. PubMed DOI PMC

Richards, E. J. & Ausubel, F. M. Isolation of a higher eukaryotic telomere from PubMed DOI

Zhang, T., Liu, G., Zhao, H., Braz, G. T. & Jiang, J. Chorus2: design of genome-scale oligonucleotide-based probes for fluorescence in situ hybridization. PubMed DOI PMC

Baez, M. et al. Analysis of the small chromosomal PubMed DOI PMC

Weisshart, K., Fuchs, J. & Schubert, V. Structured illumination microscopy (SIM) and photoactivated localization microscopy (PALM) to analyze the abundance and distribution of RNA polymerase II molecules on flow-sorted Arabidopsis nuclei. DOI