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

Yennifer Mata-Sucre, Marie Krátká, Ludmila Oliveira, Pavel Neumann, Jiří Macas, Veit Schubert, Bruno Huettel, Eduard Kejnovský, Andreas Houben, Andrea Pedrosa-Harand, Gustavo Souza and André Marques ()
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Yennifer Mata-Sucre: Max Planck Institute for Plant Breeding Research
Marie Krátká: Max Planck Institute for Plant Breeding Research
Ludmila Oliveira: Institute of Plant Molecular Biology
Pavel Neumann: Institute of Plant Molecular Biology
Jiří Macas: Institute of Plant Molecular Biology
Veit Schubert: Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben
Bruno Huettel: Max Planck Institute for Plant Breeding Research
Eduard Kejnovský: Institute of Biophysics of the Czech Academy of Sciences
Andreas Houben: Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben
Andrea Pedrosa-Harand: Universidade Federal de Pernambuco
Gustavo Souza: Universidade Federal de Pernambuco
André Marques: Max Planck Institute for Plant Breeding Research

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-53944-5

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