A methylated‐DNA‐binding complex required for plant development mediates transcriptional activation of promoter methylated genes

Abstract

Although the mechanism of DNA methylation‐mediated gene silencing is extensively studied, relatively little is known about how promoter methylated genes are protected from transcriptional silencing. SUVH1, an Arabidopsis Su(var)3‐9 homolog, was previously shown to be required for the expression of a few promoter methylated genes. By chromatin immunoprecipitation combined with sequencing, we demonstrate that SUVH1 binds to methylated genomic loci targeted by RNA‐directed DNA methylation. SUVH1 and its homolog SUVH3 function partially redundantly and interact with three DNAJ domain‐containing homologs, SDJ1, SDJ2, and SDJ3, thus forming a complex which we named SUVH‐SDJ. The SUVH‐SDJ complex components are co‐localized in a large number of methylated promoters and are required for the expression of a subset of promoter methylated genes. We demonstrate that the SUVH‐SDJ complex components have transcriptional activation activity. SUVH1 and SUVH3 function synergistically with SDJ1, SDJ2, and SDJ3 and are required for plant viability. This study reveals how the SUVH‐SDJ complex protects promoter methylated genes from transcriptional silencing and suggests that the transcriptional activation of promoter methylated genes mediated by the SUVH‐SDJ complex may play a critical role in plant growth and development.

Critical function of DNA methyltransferase 1 in tomato development and regulation of the DNA methylome and transcriptome

“…DNA methylation at the fifth position of cytosine is an epigenetic mark present in animals and plants. Through regulation of nuclear transcriptional activities, DNA methylation is critical for a wide range of cellular functions such as genome stability and defense, imprinting, X chromosome inactivation, paramutation, tissue‐specific gene regulation, carcinogenesis, and aging (Bird ; Bender ; Zhu ; Zhao et al ). In plants, DNA methylation exists in all cytosine contexts, i.e., CG, CHG (H is A, T, or C), and CHH (Law and Jacobsen ).…”

A group of SUVH methyl‐DNA binding proteins regulate expression of the DNA demethylase ROS1 in Arabidopsis

“…During the preparation of this manuscript, Harris and colleagues also identified SUVH1, SUVH3 and DnaJ proteins as components of a DNA methylation reader complex that activates gene expression (Harris et al ). It is interesting to note that in this issue of the Journal , Zhao and colleagues show SUVH1 and SUVH3 function synergistically with these DnaJ proteins to prevent promoter methylated genes from silencing (Zhao et al ).…”

A SUVH‐DNAJ/SDJ protein complex activates the expression of promoter‐methylated genes in Arabidopsis

“…However, Xiao et al found 1674 hyper‐methylated regions (HMRs) in suvh1/3/7/8 quadruple mutant compared to Col‐0. Interestingly, in all of the three studies, they observed reduced ROS1 expression in suvh1/3 , sdj1/2 , and sdj 1/2/3 mutants (Harris et al ; Xiao et al ; Zhao et al ). Reduced ROS1 expression is usually associated with increase of DNA methylation at ROS1 target loci.…”

“…These studies suggest that SUVHs promote gene expression without altering DNA methylation at binding loci, and SUVHs function down‐stream of DNA methylation (Li et al ; Harris et al ; Xiao et al ; Zhao et al ). Zhao et al () found that DNA methylation level was not disturbed in suvh1/3 and sdj1/2/3 mutants. Li et al identified some activated genes in suvh1 mutant without changing promoter DNA methylation (Li et al ).…”

“…Given that more than 1,000 (67%) of suvh1/3/7/8 HMRs were also hypermethylated in the ros1‐4 mutant (Xiao et al ), SUVHs may facilitate DNA demethylation indirectly through the regulation of ROS1 expression and thereby promote gene expression. Moreover, it is worth noting that Zhao et al showed that both SUVH and SDJ proteins have transcriptional activation abilities as determined by a LUC reporter assay in Arabidopsis mesophyll protoplasts (Zhao et al ). The transcriptional activation ability of DNAJ1 (i.e., SDJ1) was also reported by Harris et al ().…”