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Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin

Current biology, 2020-02, Vol.30 (4), p.573-588.e7 [Peer Reviewed Journal]

2019 ;Crown Copyright © 2019. Published by Elsevier Inc. All rights reserved. ;Distributed under a Creative Commons Attribution 4.0 International License ;ISSN: 0960-9822 ;EISSN: 1879-0445 ;DOI: 10.1016/j.cub.2019.12.015 ;PMID: 32004456

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Title:
Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin
Author: Montgomery, Sean A. ; Tanizawa, Yasuhiro ; Galik, Bence ; Wang, Nan ; Ito, Tasuku ; Mochizuki, Takako ; Akimcheva, Svetlana ; Bowman, John L. ; Cognat, Valérie ; Maréchal-Drouard, Laurence ; Ekker, Heinz ; Hong, Syuan-Fei ; Kohchi, Takayuki ; Lin, Shih-Shun ; Liu, Li-Yu Daisy ; Nakamura, Yasukazu ; Valeeva, Lia R. ; Shakirov, Eugene V. ; Shippen, Dorothy E. ; Wei, Wei-Lun ; Yagura, Masaru ; Yamaoka, Shohei ; Yamato, Katsuyuki T. ; Liu, Chang ; Berger, Frédéric
Subjects: Botanics ; bryophytes ; chromatin ; Chromatin - physiology ; DNA Transposable Elements - physiology ; Embryophyta - physiology ; evolution ; Evolution, Molecular ; Genetics ; genome ; H3K27me3 ; Heterochromatin - physiology ; Life Sciences ; Marchantia ; Plants genetics ; sex chromosome ; transposon ; Vegetal Biology
Is Part Of: Current biology, 2020-02, Vol.30 (4), p.573-588.e7
Description: Genome packaging by nucleosomes is a hallmark of eukaryotes. Histones and the pathways that deposit, remove, and read histone modifications are deeply conserved. Yet, we lack information regarding chromatin landscapes in extant representatives of ancestors of the main groups of eukaryotes, and our knowledge of the evolution of chromatin-related processes is limited. We used the bryophyte Marchantia polymorpha, which diverged from vascular plants circa 400 mya, to obtain a whole chromosome genome assembly and explore the chromatin landscape and three-dimensional genome organization in an early diverging land plant lineage. Based on genomic profiles of ten chromatin marks, we conclude that the relationship between active marks and gene expression is conserved across land plants. In contrast, we observed distinctive features of transposons and other repetitive sequences in Marchantia compared with flowering plants. Silenced transposons and repeats did not accumulate around centromeres. Although a large fraction of constitutive heterochromatin was marked by H3K9 methylation as in flowering plants, a significant proportion of transposons were marked by H3K27me3, which is otherwise dedicated to the transcriptional repression of protein-coding genes in flowering plants. Chromatin compartmentalization analyses of Hi-C data revealed that repressed B compartments were densely decorated with H3K27me3 but not H3K9 or DNA methylation as reported in flowering plants. We conclude that, in early plants, H3K27me3 played an essential role in heterochromatin function, suggesting an ancestral role of this mark in transposon silencing. •A database combining genomic information and chromatin profiles for Marchantia•Correlations between chromatin marks and transcription are conserved in land plants•A significant portion of constitutive heterochromatin is marked by H3K27me3•Insights into the evolution of TAD organization in plants Montgomery et al. provide a chromosome-scale genome assembly of the early diverging land plant Marchantia polymorpha. Profiling of chromatin marks shows conserved roles of active marks and suggests an ancestral association between H3K27me3 and transposons that is partly retained in Marchantia and replaced by H3K9 methylation in flowering plants.
Publisher: England: Elsevier Inc
Language: English
Identifier: ISSN: 0960-9822
EISSN: 1879-0445
DOI: 10.1016/j.cub.2019.12.015
PMID: 32004456
Source: Hyper Article en Ligne (HAL) (Open Access)
MEDLINE
Open Access: Cell Press Free Archives

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Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin

2019 ;Crown Copyright © 2019. Published by Elsevier Inc. All rights reserved. ;Distributed under a Creative Commons Attribution 4.0 International License ;ISSN: 0960-9822 ;EISSN: 1879-0445 ;DOI: 10.1016/j.cub.2019.12.015 ;PMID: 32004456

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