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Curr Biol. 2020 Jan 24. pii: S0960-9822(19)31610-0. doi: 10.1016/j.cub.2019.12.015. [Epub ahead of print]

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

Author information

1
Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Dr. Bohr Gasse 3, 1030 Vienna, Austria.
2
Department of Informatics, National Institute of Genetics, Research Organization of Information and Systems, 1111 Yata, Mishima, Japan.
3
Center for Plant Molecular Biology (ZMBP), University of Tübingen, Auf der Morgenstelle 32, 72076 Tübingen, Germany.
4
John Innes Centre, Colney lane, Norwich NR4 7UH, UK.
5
School of Biological Sciences, Monash University, Melbourne, 3800 VIC, Australia.
6
Institut de biologie moléculaire des plantes-CNRS, Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg, France.
7
Vienna BioCenter Core Facilities (VBCF), Next Generation Sequencing facility, Dr. Bohr Gasse 3, 1030 Vienna, Austria.
8
Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan.
9
Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan.
10
Department of Agronomy, National Taiwan University, Taipei 106, Taiwan.
11
Institute of Fundamental Medicine and Biology, Kazan (Volga Region) Federal University, Kazan, Republic of Tatarstan 420008, Russia.
12
Institute of Fundamental Medicine and Biology, Kazan (Volga Region) Federal University, Kazan, Republic of Tatarstan 420008, Russia; Department of Biological Sciences, Marshall University, Huntington, WV 25701, USA.
13
Department of Biochemistry and Biophysics, Texas A&M University, 2128 TAMU, College Station, TX 77843-2128, USA.
14
Faculty of Biology-Oriented Science and Technology, Kindai University, Kinokawa, Wakayama 649-6493, Japan.
15
Center for Plant Molecular Biology (ZMBP), University of Tübingen, Auf der Morgenstelle 32, 72076 Tübingen, Germany. Electronic address: chang.liu@zmbp.uni-tuebingen.de.
16
Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Dr. Bohr Gasse 3, 1030 Vienna, Austria. Electronic address: frederic.berger@gmi.oeaw.ac.at.

Abstract

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.

KEYWORDS:

H3K27me3; Marchantia; bryophytes; chromatin; evolution; genome; sex chromosome; transposon

PMID:
32004456
DOI:
10.1016/j.cub.2019.12.015
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Conflict of interest statement

Declaration of Interests The authors declare no competing interests.

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