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

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.

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Publication Details

Journal
Nature Communications
Published
2024-11-05
DOI
https://doi.org/10.1038/s41467-024-53944-5
Citations
13
Primary Topic
Chromosomal and Genetic Variations
Type
article
Field-Weighted Citation Impact
7.79

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article

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

André Marques, Ludmila Oliveira, Veit Schubert, Pavel Neumann et al.
13 citations
Nature Communications
Chromosomal and Genetic Variations
7.79
article

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

André Marques, Ludmila Oliveira, Veit Schubert, Pavel Neumann, Gustavo Souza, Andreas Houben, Eduard Kejnovský, Yennifer Mata‐Sucre, Jir̆ı́ Macas, Bruno Hüettel, Andrea Pedrosa‐Harand, Marie Krátká
article en
13 citations

Abstract

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.

Nature CommunicationsVol. 15(1)
Czech Academy of Sciences (CZ), Masaryk University (CZ), Universidade Federal de Pernambuco (BR), Czech Academy of Sciences, Institute of Biophysics (CZ), Institute of Plant Molecular Biology (CZ), Cluster of Excellence on Plant Sciences (DE), Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK) (DE), Max Planck Institute for Plant Breeding Research (DE), Czech Academy of Sciences, Biology Centre (CZ), Heinrich Heine University Düsseldorf (DE)
European Commission, Deutscher Akademischer Austauschdienst, Deutsche Forschungsgemeinschaft, Grantová Agentura České Republiky, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Conselho Nacional de Desenvolvimento Científico e Tecnológico, Max-Planck-Gesellschaft
Life in Land
Openalex Percentile: Top 3%
Chromosomal and Genetic Variations
7.79
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