How genes change spatial positioning for gene expression in response to environmental changes clarified
A group of researchers from Osaka University and The University of Tokyo verified that in Arabidopsis thaliana (Mouse-ear Cress), crowded nuclei (CRWN) proteins localize at the nuclear lamina* and form a meshwork structure that mechanically supports the nuclear membrane.
*The nuclear lamina, filaments located in the inner nuclear membrane, contains lamins and other proteins involved in chromatin architecture.
The group also clarified that the CRWNs change the spatial positioning of copper (Cu)-associated genes (CA genes) in response to changes in Cu availability and that the expression of the genes is turned on.
DNAs are packaged into a 3-dimensional (3D) structure in the nucleus. Within the cell nucleus, DNA is wrapped around histones, forming a densely packed structure known as chromatin. Genes are sections of DNA that code for specific proteins, and gene expression is controlled by unfolding certain segments of DNA or changing spatial positioning of a gene within the nucleus, but its mechanisms were unknown.
In this study, the researchers demonstrated that CRWNs localized at the nuclear lamina and built a meshwork structure (beneath the inner nuclear membrane) that mechanically supports the nuclear membrane.
In animals, lamin is known as a protein that supports the nuclear membrane. However, since CRWN shares no amino acid similarity to lamin and plants lack lamin genes, which protein supports the plant cell nucleus was unknown. In addition, although Cu is an essential plant micronutrient, excessive Cu can adversely affect plant growth. Thus, plants have evolved copper tolerance mechanisms aimed at maintaining the balance of essential mineral elements.
In this study, the researchers examined CRWN-deficient mutants (crwn mutants) and found that Cu-associated protein suppressed CA gene expression. The 11 CA genes (CA1–11) formed a gene cluster and 5 of them exhibited low transcript levels. In crwn1crwn4 mutants, copper tolerance was significantly low.
Using a chromatin integration labeling (ChIL) assay, the researchers investigated the interaction between CRWNs and CA genes to evaluate the chromatin status on the CA gene locus and found that the CA gene locus interacted with CRWNs.
The group also checked the position of the CA gene locus by Fluorescence in situ hybridization (FISH) and found that the gene locus interacted with CRWN1 and moved from the nucleoplasm to the nuclear periphery under excess copper conditions, but this was not observed in CRWN mutants. When CA gene positioning was anchored to the nuclear periphery, the CA gene locus bound to CRWN, which activated transcription activity and showed copper tolerance. From these findings, the group assumes that CRWNs change the spatial arrangement of the CA genes in the nucleus through interacting with them, which affects their transcriptional activity.
This group’s research marks a breakthrough for research on molecular mechanisms for gene expression by changing the spatial positioning of genes. This is an epoch-making discovery that special layout concept is introduced to gene expression control.
Since CRWNs share some functional similarities with their animal lamin counterparts, this research is expected to lead to the development of gene expression control methods in both plants and animals. By introducing the concept to control gene positioning, it will become possible to develop new molecular breeding to produce farm products that can adapt to environmental changes.
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The article, “Subnuclear gene positioning through lamina association affects copper tolerance,” was published in Nature Communications at DOI: https://www.nature.com/articles/s41467-020-19621-z.
