In most studied eukaryotes, chromosomes are monocentric, with centromere activity confined to a single region. However, the rush family (Juncaceae) includes species with both monocentric (Juncus) and holocentric (Luzula) chromosomes, where centromere activity is distributed along the entire chromosome length. Here, we combine chromosome-scale genome assembly, epigenetic analysis, immuno-FISH and super-resolution microscopy to study the transition to holocentricity in Luzula sylvatica. We report repeat-based holocentromeres with an irregular distribution of features along the chromosomes. Luzula sylvatica holocentromeres are predominantly associated with two satellite DNA repeats (Lusy1 and Lusy2), while CENH3 also binds satellite-free gene-poor regions. Comparative repeat analysis suggests that Lusy1 plays a crucial role in centromere function across most Luzula species. Furthermore, synteny analysis between L. sylvatica (n = 6) and Juncus effusus (n = 21) suggests that holocentric chromosomes in Luzula could have arisen from chromosome fusions of ancestral monocentric chromosomes, accompanied by the expansion of CENH3-associated satellite repeats.

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

Cluster of Excellence on Plant Sciences Heinrich Heine University Düsseldorf Germany

Department of Chromosome Biology Max Planck Institute for Plant Breeding Research Cologne Germany

Department of Plant Developmental Genetics Institute of Biophysics of the Czech Academy of Sciences Kralovopolska 135 61200 Brno Czech Republic

Laboratório de Citogenética e Evolução Vegetal Departamento de Botânica Centro de Biociências Universidade Federal de Pernambuco Recife PE 50670 901 Brazil

Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben 06466 Seeland Germany

Max Planck Genome Centre Max Planck Institute for Plant Breeding Research Cologne Germany

National Centre for Biomolecular Research Faculty of Science Masaryk University Kamenice 5 625 00 Brno Czech Republic

Zobrazit více v PubMed

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

Schubert, V. et al. Super-Resolution Microscopy Reveals Diversity of Plant Centromere Architecture. PubMed DOI PMC

Heckmann, S. et al. The holocentric species PubMed DOI

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

Escudero, M., Marques, A., Lucek, K. & Hipp, A. L. Genomic hotspots of chromosome rearrangements explain conserved synteny despite high rates of chromosome evolution in a holocentric lineage. PubMed PMC

Mata-Sucre, Y. et al. Oligo-barcode illuminates holocentric karyotype evolution in Rhynchospora (Cyperaceae). PubMed DOI PMC

Escudero, M., Márquez-Corro, J. I. & Hipp, A. L. The Phylogenetic Origins and Evolutionary History of Holocentric Chromosomes. DOI

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

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

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

Plohl, M., Meštrović, N. & Mravinac, B. Centromere identity from the DNA point of view. PubMed DOI PMC

Šatović-Vukšić, E. & Plohl, M. Satellite DNAs—From Localized to Highly Dispersed Genome Components. PubMed DOI PMC

Hobza, R. et al. An accumulation of tandem DNA repeats on the Y chromosome in Silene latifolia during early stages of sex chromosome evolution. PubMed DOI

Kasinathan, S. & Henikoff, S. Non-B-Form DNA Is Enriched at Centromeres. PubMed DOI PMC

Marques, A. et al. Holocentromeres in PubMed DOI PMC

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

Ma, B. et al. The gap-free genome of mulberry elucidates the architecture and evolution of polycentric chromosomes. PubMed DOI PMC

Despot-Slade, E. et al. The Centromere Histone Is Conserved and Associated with Tandem Repeats Sharing a Conserved 19-bp Box in the Holocentromere of PubMed DOI PMC

POWO. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Published on the Internet; http://www.plantsoftheworldonline.org/ (2024).

Guerra, M., Ribeiro, T. & Felix, L. P. Monocentric chromosomes in Juncus ( Juncaceae) and implications for the chromosome evolution of the family. DOI

Mata-Sucre, Y. et al. Repeat-based phylogenomics shed light on unclear relationships in the monocentric genus Juncus L. ( Juncaceae). PubMed DOI

Dias, Y. et al. How diverse a monocentric chromosome can be? Repeatome and centromeric organization of PubMed

Nagaki, K., Kashihara, K. & Murata, M. Visualization of Diffuse Centromeres with Centromere-Specific Histone H3 in the Holocentric Plant PubMed DOI PMC

Heckmann, S. et al. Holocentric Chromosomes of PubMed DOI

Bozek, M., Leitch, A. R., Leitch, I. J., Záveská Drábková, L. & Kuta, E. Chromosome and genome size variation in DOI

Haizel, T., Lim, Y. K., Leitch, A. R. & Moore, G. Molecular analysis of holocentric centromeres of PubMed DOI

Goodwin, Z. A. et al. The genome sequence of great wood-rush, Luzula sylvatica (Huds) Gaudin. PubMed DOI PMC

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

Wang, J. et al. A high-quality chromosome-scale assembly of the centipedegrass [Eremochloa ophiuroides (Munro) Hack.] genome provides insights into chromosomal structural evolution and prostrate growth habit. PubMed DOI PMC

Drábková, L. Z. A Survey of Karyological Phenomena in the Juncaceae with Emphasis on Chromosome Number Variation and Evolution. DOI

Lucek, K., Augustijnen, H. & Escudero, M. A holocentric twist to chromosomal speciation? PubMed DOI

Cortes-Silva, N. et al. CenH3-Independent Kinetochore Assembly in Lepidoptera Requires CCAN, Including CENP-T. PubMed DOI

Jankowska, M. et al. Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution. PubMed DOI

Castellani, M. et al. Meiotic recombination dynamics in plants with repeat-based holocentromeres shed light on the primary drivers of crossover patterning. PubMed DOI PMC

Souza, T. B. D. et al. Distinct patterns of satDNA distribution in holocentric chromosomes of spike-sedges (Eleocharis, Cyperaceae). PubMed

Liu, H. et al. The genome of PubMed PMC

Ribeiro, T. et al. Centromeric and non-centromeric satellite DNA organisation differs in holocentric Rhynchospora species. PubMed DOI

Costa, L., Marques, A., Buddenhagen, C. E., Pedrosa-Harand, A. & Souza, G. Investigating the diversification of holocentromeric satellite DNA PubMed DOI PMC

Wlodzimierz, P. et al. Cycles of satellite and transposon evolution in Arabidopsis centromeres. PubMed DOI

Hiatt, E. N., Kentner, E. K. & Dawe, R. K. Independently Regulated Neocentromere Activity of Two Classes of Tandem Repeat Arrays. PubMed DOI PMC

Piras, F. M. et al. Uncoupling of Satellite DNA and Centromeric Function in the Genus Equus. PubMed DOI PMC

Cappelletti, E. et al. Robertsonian Fusion and Centromere Repositioning Contributed to the Formation of Satellite-free Centromeres During the Evolution of Zebras. PubMed DOI PMC

Ning, Y. et al. The chromosome-scale genome of PubMed DOI PMC

Wright, C. J., Stevens, L., Mackintosh, A., Lawniczak, M. & Blaxter, M. Comparative genomics reveals the dynamics of chromosome evolution in Lepidoptera. PubMed PMC

Augustijnen, H. et al. A macroevolutionary role for chromosomal fusion and fission in PubMed DOI PMC

Elliott, T. L. & Davies, T. J. Phylogenetic attributes, conservation status and geographical origin of species gained and lost over 50 years in a UNESCO Biosphere Reserve. DOI

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

Seppey, M., Manni, M. & Zdobnov, E. M. BUSCO: Assessing Genome Assembly and Annotation Completeness. in PubMed

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

Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. PubMed DOI PMC

Ghurye, J. et al. Integrating Hi-C links with assembly graphs for chromosome-scale assembly. PubMed DOI PMC

Durand, N. C. et al. Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom. PubMed DOI PMC

Dudchenko, O. et al. De novo assembly of the PubMed DOI PMC

Sun, H., Ding, J., Piednoël, M. & Schneeberger, K. PubMed DOI

Marçais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of PubMed DOI PMC

Ma, W. et al. The distribution of α-kleisin during meiosis in the holocentromeric plant Luzula elegans. PubMed DOI

Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. DOI

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

Ramírez, 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 datasets. PubMed DOI PMC

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

Stovner, E. B. & Sætrom, P. epic2 efficiently finds diffuse domains in ChIP-seq data. PubMed DOI

Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. PubMed DOI PMC

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

Novák, P., Hoštáková, N., Neumann, P. & Macas, J. DANTE and DANTE_LTR: lineage-centric annotation pipelines for long terminal repeat retrotransposons in plant genomes. PubMed DOI PMC

Neumann, P. et al. Plant centromeric retrotransposons: a structural and cytogenetic perspective. PubMed DOI PMC

Neumann, P., Novák, P., Hoštáková, N. & Macas, J. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. PubMed DOI PMC

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

Sonnhammer, E. L. L. & Durbin, R. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. PubMed DOI

Kearse, M. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. PubMed DOI PMC

Yu, Y., Ouyang, Y. & Yao, W. shinyCircos: an R/Shiny application for interactive creation of Circos plot. PubMed DOI

Sweeten, A. P., Schatz, M. C. & Phillippy, A. M. ModDotPlot—rapid and interactive visualization of tandem repeats. PubMed DOI PMC

Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. PubMed DOI PMC

Hunter, J. D. Matplotlib: A 2D Graphics Environment. DOI

McKinney, W. pandas: a foundational Python library for data analysis and statistics.

Dale, R. K., Pedersen, B. S. & Quinlan, A. R. Pybedtools: a flexible Python library for manipulating genomic datasets and annotations. PubMed DOI PMC

Harris, C. R. et al. Array programming with NumPy. PubMed DOI PMC

Waskom, M. seaborn: statistical data visualization. DOI

Lyons, E., Pedersen, B., Kane, J. & Freeling, M. The Value of Nonmodel Genomes and an Example Using SynMap Within CoGe to Dissect the Hexaploidy that Predates the Rosids. DOI

Soderlund, C., Bomhoff, M. & Nelson, W. M. SyMAP v3.4: a turnkey synteny system with application to plant genomes. PubMed DOI PMC

Lovell, J. T. et al. GENESPACE tracks regions of interest and gene copy number variation across multiple genomes. PubMed DOI PMC

Hao, Z. et al. PubMed DOI PMC

Kanduri, C., Bock, C., Gundersen, S., Hovig, E. & Sandve, G. K. Colocalization analyses of genomic elements: approaches, recommendations and challenges. 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.

Krátká, M. Repeat-based-holocentromeres-of-Luzula-sylvatica. PubMed PMC

Kinetochore mutations and histone phosphorylation pattern changes accompany holo- and macro-monocentromere evolution

Repeat-based holocentromeres of the woodrush Luzula sylvatica reveal insights into the evolutionary transition to holocentricity

Zobrazit více v PubMed

BioProject
PRJNA1135980