Redox Components: Key Regulators of Epigenetic Modifications in Plants

Abstract

Epigenetic modifications including DNA methylation, histone modifications, and chromatin remodeling are crucial regulators of chromatin architecture and gene expression in plants. Their dynamics are significantly influenced by oxidants, such as reactive oxygen species (ROS) and nitric oxide (NO), and antioxidants, like pyridine nucleotides and glutathione in plants. These redox intermediates regulate the activities and expression of many enzymes involved in DNA methylation, histone methylation and acetylation, and chromatin remodeling, consequently controlling plant growth and development, and responses to diverse environmental stresses. In recent years, much progress has been made in understanding the functional mechanisms of epigenetic modifications and the roles of redox mediators in controlling gene expression in plants. However, the integrated view of the mechanisms for redox regulation of the epigenetic marks is limited. In this review, we summarize recent advances on the roles and mechanisms of redox components in regulating multiple epigenetic modifications, with a focus of the functions of ROS, NO, and multiple antioxidants in plants.

Keywords: DNA methylation; antioxidants; chromatin remodeling; epigenetic modifications; histone modification; nitric oxide; reactive oxygen species; redox regulation.

Figure 1

Redox components modulate SAM synthesis through folate cycle in plants. Folate cycle begins with the conversion of DHF to THF through DHFR by utilizing the reducing equivalents from NADPH. Methyls derived from THFs (5,10-CH2-THF, 5,10-CH=THF) are synthesized by SHMT and MTHFD, respectively. 5,10-CH=THF is reduced to 5-CH3-THF by MTHFR. The methyl group from 5-CH3-THF is transferred to Hcy to synthesize Met through MS. The produced Met generates SAM through SAMS. SAM donates methyl groups to DNA or proteins through DNA methyltransferase (DNMT)/HKMT/PRMT, and gets converted to SAH. SAH is further processed to Hcy through SAHH/HOG1. The key enzymes influenced by the cellular redox components are: SAMS/MAT, DNMT/HKMT/PRMT, SAHH/HOG1, MS and MSR. K: lysine; R: arginine; Me: methyl. Dashed lines mean uncharacterized regulation.

Figure 2

Redox components regulate DCL4 and RTL1 activities. (a) Processing of siRNA precursors by DCL4 requires dsRNA-binding protein (DRB), especially DRB4. GSH and TRXs are able to restore DCL4 activity from the inactive state. Activated DCL4 promotes 21 nt siRNA production. (b) GSSG/GRXs influence RTL1 activity. RTL1 has RNase III domain and dsRNA binding domains (dsRBD), and acts dimers to perform functions. GSSG treatment results in RTL1 glutathionylation at Cys230 position and inhibits its activity. RTL1 activity is restored by glutaredoxin proteins (GRXs). RTL1 negatively regulates siRNA production prior to DCL–mediated cleavage of the siRNA precursors. The dashed line indicates uncharacterized regulation.

Figure 3

Redox components influence histone acetylations. In the cytoplasm, glucose is broken down to pyruvate, which enters into mitochondria, and is converted to acetyl CoA through mitochondrial pyruvate dehydrogenase (mPDH) by reducing NAD⁺. Acetyl CoA combines with oxaloacetate (OAA) produced in the TCA cycle to form citrate, which enters cytoplasm. In cytoplasm, citrate is converted back to OAA and acetyl CoA through ATP-citrate lyase (ACL). Acetyl CoA synthesized in the cytoplasm enters into the nucleus as the source supplier of acetyl group for the histone acetylation process. HAT utilizes the acetyl group from acetyl CoA to introduce acetylation marks (Ac) over the lysine residues of the histone tail, thus weakening the contact between DNA and histone and facilitating gene expression. HDAC removes histone acetyl group, leading to chromatin compaction. Different HAT and HDAC enzymes are affected by ROS, NO, and NAD⁺.