Subnuclear gene positioning through lamina association affects copper tolerance

Yuki Sakamoto,Kiminori Toyooka,Yoshikatsu Sato,Hiroshi Kimura,Kentaro Tamura,Yasuyuki Ohkawa,Sachihiro Matsunaga,Chieko Goto,Ikuko Hara-Nishimura,Mayuko Sato,Shingo Takagi,Akihito Harada,Takamasa Suzuki

doi:10.1038/s41467-020-19621-z

Abstract

The nuclear lamina plays an important role in the regulation of chromatin organization and gene positioning in animals. CROWDED NUCLEI (CRWN) is a strong candidate for the plant nuclear lamina protein in Arabidopsis thaliana but its biological function was largely unknown. Here, we show that CRWNs localize at the nuclear lamina and build the meshwork structure. Fluorescence in situ hybridization and RNA-seq analyses revealed that CRWNs regulate chromatin distribution and gene expression. More than 2000 differentially expressed genes were identified in the crwn1crwn4 double mutant. Copper-associated (CA) genes that form a gene cluster on chromosome 5 were among the downregulated genes in the double mutant exhibiting low tolerance to excess copper. Our analyses showed this low tolerance to copper was associated with the suppression of CA gene expression and that CRWN1 interacts with the CA gene locus, enabling the locus to localize at the nuclear lamina under excess copper conditions.

Highlights

The nuclear lamina plays an important role in the regulation of chromatin organization and gene positioning in animals
CRWN1–3 exhibited similar continuous structures (Fig. 1g). These results suggested that CRWN1–3 proteins built the meshwork structure at the plant nuclear lamina area
We show that CROWDED NUCLEI (CRWN) localize at the nuclear lamina and form interactions that build the meshwork structure

Summary

Introduction

The nuclear lamina plays an important role in the regulation of chromatin organization and gene positioning in animals. CROWDED NUCLEI (CRWN) is a strong candidate for the plant nuclear lamina protein in Arabidopsis thaliana but its biological function was largely unknown. Copper-associated (CA) genes that form a gene cluster on chromosome 5 were among the downregulated genes in the double mutant exhibiting low tolerance to excess copper Our analyses showed this low tolerance to copper was associated with the suppression of CA gene expression and that CRWN1 interacts with the CA gene locus, enabling the locus to localize at the nuclear lamina under excess copper conditions. The nuclear lamina, a meshwork structure beneath the inner nuclear membrane, has been observed in animal and plant cells[9,10]. The gene locus interacts with CRWN1 and is anchored to the nuclear periphery, which activates gene expression, only under excess copper conditions

Methods

Results

Conclusion