Plant lamin-like proteins mediate chromatin tethering at the nuclear periphery

Bo Hu,Anna-Lena Weber,Ezgi Süheyla Karaaslan,Nan Wang,Chang Liu,Wangsheng Zhu,Xiuli Bi,Kenneth Wayne Berendzen

doi:10.1186/s13059-019-1694-3

Abstract

BackgroundThe nuclear envelope not only serves as a physical barrier separating nuclear content from the cytoplasm but also plays critical roles in modulating the three-dimensional organization of genomic DNA. For both plants and animals, the nuclear periphery is a functional compartment enriched with heterochromatin. To date, how plants manage to selectively tether chromatin at the nuclear periphery is unclear.ResultsBy conducting dual-color fluorescence in situ hybridization experiments on 2C nuclei, we show that in Arabidopsis thaliana, specific chromatin positioning at the nuclear periphery requires plant lamin-like proteins CROWDED NUCLEI 1 (CRWN1), CRWN4, and DNA methylation in CHG and CHH contexts. With chromosome painting and Hi-C analyses, we show global attenuation of spatial chromatin compartmentalization and chromatin positioning patterns at the nuclear periphery in both the crwn1 and crwn4 mutants. Furthermore, ChIP-seq analysis indicates that CRWN1 directly interacts with chromatin domains localized at the nuclear periphery, which mainly contains non-accessible chromatin.ConclusionsIn summary, we conclude that CRWN1 is a key component of the lamina-chromatin network in plants. It is functionally equivalent to animal lamins, playing critical roles in modulating patterns of chromatin positioning at the nuclear periphery.

Highlights

The nuclear envelope serves as a physical barrier separating nuclear content from the cytoplasm and plays critical roles in modulating the three-dimensional organization of genomic DNA
The closer a locus is to the pericentromeric regions (PRs) the stronger it tends to be localized to the nuclear periphery (NP) (Fig. 1a, b)
We showed that the localization of Arabidopsis transposable elements (TEs) in the nucleus is correlated with the type of CHH (H stands for A, C, or T) DNA methylation pathway [27]

Summary

Introduction

The nuclear envelope serves as a physical barrier separating nuclear content from the cytoplasm and plays critical roles in modulating the three-dimensional organization of genomic DNA. For both plants and animals, the nuclear periphery is a functional compartment enriched with heterochromatin. Genomic DNA in interphase nuclei shows non-random distribution patterns with respect to sub-nuclear space including the nuclear periphery (NP). Three types of plant-specific proteins, localized preferentially or exclusively at the inner nuclear membrane (INM), have been listed as candidate lamin analogs.

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Conclusion