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

First author: Sean A. Montgomery; Affiliations: Gregor Mendel Institute (孟德尔研究所): Vienna, Austria

Corresponding author: Frédéric Berger

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.

核小体包装的基因组是真核生物的标志。组蛋白以及负责沉积、移除和读取组蛋白修饰的通路在真核生物中十分保守。然而，我们对于现存真核生物主要类群的古老代表种的染色质全景仍缺乏了解，另外对于染色质相关进程演化方面的知识也有所欠缺。本文中，作者利用了与维管植物分化了约400个百万年的苔藓植物地钱（Marchantia polymorpha），获得了一个染色体级别的参考基因组，并探索了一个早期分化形成的陆地植物支系的染色质全景与3D基因组组织。基于十个染色质标记的全基因组图谱，作者发现活性标记与基因表达之间的关系在陆地植物中比较保守。相反，作者发现地钱中转座子及其它重复序列与开花植物具有不同的特性。在地钱基因组中，沉默的转座子和重复序列并不积累在着丝粒附近。尽管在开花植物中，有很大一部分结构异染色质具有H3K9甲基化的修饰，但大部分的转座子由H3K27me3修饰所标记，如果去除这些H3K27me3甲基化修饰，这些转座子则会广泛作用于蛋白编码基因的转录抑制。通过Hi-C数据进行的染色质区室化分析显示，地钱基因组上B compartment显著沉积密集的H3K27me3修饰，而在开花植物中则是由H3K9或DNA甲基化所标记。作者总结道在早期分化的陆地植物中，H3K27me3在异染色质功能方面发挥重要的作用，说明该标记在转座子沉默反面的古老功能。

p.s. Hi-C数据获得交互矩阵后进行归一化，而后计算相关系数矩阵，然后对相关系数矩阵进行PCA降维，在第一主成分PC1上，人为将染色质区域划分为两个compartments，其中正值为A compartment，负值为B compartment。A/B compartments在基因组中一般呈间隔分布，A compartment呈松散染色质状态，基因密度高，属于转录活跃区域；而B compartment则呈压缩染色质状态，基因密度低，属于转录抑制区域。（参见https://doi.org/10.1126/science.1181369）

通讯：Frédéric Berger (https://www.oeaw.ac.at/gmi/research/research-groups/frederic-berger/profile/)

个人简介：里昂高等师范学院，学士；1994年，里昂高等师范学院，博士；1995-1996年，约翰·英内斯中心，博士后。

研究方向：核心组蛋白变体对于基因组表达、组织及遗传的影响；组蛋白变体与染色质修饰之间的关系。

doi: https://doi.org/10.1016/j.cub.2019.12.015

Journal: Current Biology

Published date: January 30, 2020