Redox-Epigenetic Crosstalk in Plant Stress Responses: The Roles of Reactive Oxygen and Nitrogen Species in Modulating Chromatin Dynamics

Abstract

Plants are constantly exposed to environmental stressors such as drought, salinity, and extreme temperatures, which threaten their growth and productivity. To counter these challenges, they employ complex molecular defense systems, including epigenetic modifications that regulate gene expression without altering the underlying DNA sequence. This review comprehensively examines the emerging roles of reactive oxygen species (ROS) and reactive nitrogen species (RNS) as central signaling molecules orchestrating epigenetic changes in response to abiotic stress. In addition, biotic factors such as pathogen infection and microbial interactions are considered for their ability to trigger ROS/RNS generation and epigenetic remodeling. It explores how ROS and RNS influence DNA methylation, histone modifications, and small RNA pathways, thereby modulating chromatin structure and stress-responsive gene expression. Mechanistic insights into redox-mediated regulation of DNA methyltransferases, histone acetyltransferases, and microRNA expression are discussed in the context of plant stress resilience. The review also highlights cutting-edge epigenomic technologies such as whole-genome bisulfite sequencing (WGBS), chromatin immunoprecipitation sequencing (ChIP-seq), and small RNA sequencing, which are enabling precise mapping of stress-induced epigenetic landscapes. By integrating redox biology with epigenetics, this work provides a novel framework for engineering climate-resilient crops through the targeted manipulation of stress-responsive epigenomic signatures.

Keywords: chromatin dynamics; crop improvement; epigenomic analysis; gene regulation; molecular signaling; stress adaptation.

Figure 1

Crosstalk between reactive oxygen species and reactive nitrogen species in plant stress signaling and adaptation. This schematic illustrates the dynamic redox signaling network formed by ROS and RNS under stress conditions. In the ROS pathway, NADPH oxidase-generated superoxide (O₂•⁻) is converted to hydrogen peroxide (H₂O₂) by superoxide dismutase (SOD), which acts as a signaling molecule inducing oxidative stress responses, including gene expression regulation through catalase (CAT) activity. In parallel, nitric oxide (NO) in the RNS pathway contributes to redox balance by scavenging ROS and modulating protein activity through S-nitrosylation. The interaction between O₂•⁻ and NO produces peroxynitrite (ONOO⁻), a reactive species causing oxidative/nitrosative stress and macromolecular damage. Importantly, both ROS and RNS affect epigenetic regulation by modulating DNA methylation, histone modifications, and chromatin remodeling. H₂O₂ can oxidize histone residues, while NO can S-nitrosylate epigenetic enzymes, altering gene expression.

Figure 2

Proposed model of ROS- and RNS-induced DNA methylation modifications in plants under abiotic stress. This schematic illustrates the impact of environmental stressors, such as drought, salinity (NaCl), heat, cold, and excess light, on the generation of reactive oxygen species (ROS) and reactive nitrogen species (RNS) in plant cells. These reactive molecules, including superoxide radicals (O₂•⁻), hydrogen peroxide (H₂O₂), hydroxyl radicals (•OH), nitric oxide (NO), and peroxynitrite (ONOO⁻), influence DNA methylation through two primary mechanisms: direct DNA damage and epigenetic regulation. ROS and RNS interact with DNA methyltransferases (DNMTs), promoting the formation of 5-methylcytosine (5mC) via methyl group (CH₃) addition to cytosine residues. These modifications modulate gene expression by either activating stress-responsive genes (hypomethylation) or repressing specific gene sets (hypermethylation), ultimately enhancing plant tolerance to abiotic stress conditions.

Figure 3

Crosstalk between reactive oxygen species (ROS) and reactive nitrogen species (RNS) in regulating histone modifications and stress memory in plants. This diagram illustrates how environmental stress induces ROS and RNS production in plants, leading to epigenetic modifications of histones. RNS, through S-nitrosylation (SNO) of HDACs, influences histone acetylation, while ROS contributes to changes in chromatin structure and gene expression. These modifications regulate stress-responsive gene activity and contribute to the formation of stress memory. The resulting epigenetic reprogramming enables enhanced plant tolerance during subsequent stress events, supporting long-term adaptation.

Figure 4

Proposed model of ROS-mediated miRNA regulation and gene expression in plant stress tolerance. This model illustrates how abiotic stresses, including drought, salinity, and osmotic stress, as well as biotic stresses such as pathogen infection induce the generation of reactive oxygen species (ROS) such as hydrogen peroxide (H₂O₂), superoxide (O₂⁻), and hydroxyl radicals (•OH). These ROS function as signaling molecules that modulate the expression of specific microRNAs (miRNAs). The miRNAs, in turn, regulate gene expression involved in redox balance, antioxidant enzyme activity, pathogen defense, and growth under stress. This post-transcriptional regulation supports ROS homeostasis, enhances antioxidant defenses, improves disease resistance, and promotes adaptation to oxidative and osmotic stress.

Figure 5

Proposed model of NO-mediated miRNA regulation in plant stress responses and development. Abiotic (drought, low temperature, methane) and biotic (pathogen infection) stresses activate NO biosynthesis through nitrate reductase (NR) and NO-associated protein 1 (NOA1). The resulting NO modulates microRNA (miRNA) expression, which in turn targets specific mRNAs. These mRNAs encode key regulators of stress adaptation, contributing to enhanced root development, defense mechanisms, cold stress tolerance, and hormonal crosstalk (including abscisic acid [ABA] and salicylic acid [SA] pathways).

Figure 6

Technological platforms linking redox signaling to epigenetic regulation under abiotic stress. Abiotic stresses such as drought, salinity, and extreme temperatures trigger the production of ROS and RNS, which in turn modulate key epigenetic mechanisms. This figure illustrates how epigenomic platforms, including whole-genome bisulfite sequencing (WGBS), chromatin immunoprecipitation sequencing (ChIP-seq), and small RNA sequencing (sRNA-seq), enable high-resolution mapping of stress-induced modifications in DNA methylation, histone marks, and small RNA pathways. These technologies provide a foundational framework to decode the redox-sensitive epigenetic landscape that shapes plant stress responses and chromatin dynamics.

Figure 7

Integrative framework linking redox signaling and epigenetic modulation to stress-resilient crop engineering. Reactive oxygen species (e.g., H₂O₂) and reactive nitrogen species (e.g., NO, ONOO⁻) act as redox signals that trigger epigenetic reprogramming through mechanisms such as DNA methylation, histone modifications (e.g., acetylation, methylation), chromatin remodeling, and chromatin regulation. These modifications collectively activate stress-response genes, contributing to stable epigenetic memory and heritable stress tolerance. Through targeted engineering strategies, such as genome/epigenome editing, epigenetic priming, and modulation of transcriptional regulators, these memory traits can be enhanced to improve root plasticity, nutrient acquisition, and osmotic regulation. Together, these processes support the development of climate-resilient crop varieties.