Redox Balance-DDR-miRNA Triangle: Relevance in Genome Stability and Stress Responses in Plants

Abstract

Plants are continuously faced with complex environmental conditions which can affect the oxidative metabolism and photosynthetic efficiency, thus leading to the over-production of reactive oxygen species (ROS). Over a certain threshold, ROS can damage DNA. DNA damage, unless repaired, can affect genome stability, thus interfering with cell survival and severely reducing crop productivity. A complex network of pathways involved in DNA damage response (DDR) needs to be activated in order to maintain genome integrity. The expression of specific genes belonging to these pathways can be used as indicators of oxidative DNA damage and effective DNA repair in plants subjected to stress conditions. Managing ROS levels by modulating their production and scavenging systems shifts the role of these compounds from toxic molecules to key messengers involved in plant tolerance acquisition. Oxidative and anti-oxidative signals normally move among the different cell compartments, including the nucleus, cytosol, and organelles. Nuclei are dynamically equipped with different redox systems, such as glutathione (GSH), thiol reductases, and redox regulated transcription factors (TFs). The nuclear redox network participates in the regulation of the DNA metabolism, in terms of transcriptional events, replication, and repair mechanisms. This mainly occurs through redox-dependent regulatory mechanisms comprising redox buffering and post-translational modifications, such as the thiol-disulphide switch, glutathionylation, and S-nitrosylation. The regulatory role of microRNAs (miRNAs) is also emerging for the maintenance of genome stability and the modulation of antioxidative machinery under adverse environmental conditions. In fact, redox systems and DDR pathways can be controlled at a post-transcriptional level by miRNAs. This review reports on the interconnections between the DDR pathways and redox balancing systems. It presents a new dynamic picture by taking into account the shared regulatory mechanism mediated by miRNAs in plant defense responses to stress.

Exploring microRNA Signatures of DNA Damage Response Using an Innovative System of Genotoxic Stress in Medicago truncatula Seedlings

“…Predictive studies were employed as well; Liang et al (2017) reported that MUTL-homolog 1 (MLH1) and MRE11 were putatively targeted by miR5176 and miR5261 in Citrus sinensis whereas the Brachypodium distachyon novel_mir_69 was identified to putatively target the RAD50 mRNA ( Lv et al, 2016 ). Based on recent reviews of literature, an interrelation between DDR, redox systems, and miRNAs, has been proposed ( Cimini et al, 2019 ). Nonetheless, specific hurdles have been pinpointed to explain the poorly represented examples in plants.…”

Human Genes AreIn SilicoPotential Targets For Rice miRNA

“…Such pl-miRs usually participate in maintaining the basic physiological functions of plants (productivity, resistance to biotic and abiotic stresses, growth and development). For example, developed rice lines overexpressing MIR529a have been shown to have increased resistance to oxidative stress (Chen & Li, 2018; Cimini et al, 2019). The participation of osa-miR159f, osa-miR1871, osa-miR398b, osa-miR408-3p, osa-miR2878-5p, osa-miR528-5p and osa-miR397a in the regulation of a number of physiological processes of rice has been established (Balyan et al, 2017).…”

Interplay Among Hydrogen Sulfide, Nitric Oxide, Reactive Oxygen Species, and Mitochondrial DNA Oxidative Damage

“…Oxidative damage of nuclear DNA and mtDNA can be induced by the excessive accumulation of ROS in plant cells, which could also cause epigenetic variations in plants, such as DNA methylation/demethylation (Katsuya-Gaviria et al, 2020;Nagaraja et al, 2021) and histone modifications (Zheng et al, 2021) influencing plant development and growth. DNA damage caused by ROS could trigger the nuclear redox network and affect DNA metabolism through redox-dependent regulatory mechanisms comprising redox buffering and posttranslational modifications, such as the thiol-disulfide switch, glutathionylation, and S-nitrosation (Cimini et al, 2019). Recently, it has been found that ROS can function as catalysts of DNA methylation (Wu and Ni, 2015;Teng et al, 2018).…”

“…Exogenous SNP and S-nitrosoglutathione (GSNO), as NO donors, cause the S-nitrosation of Cys49 and Cys53, promoting a conformational change in the secondary structure in proteins of the AtMYB30 transcription factor and inhibiting the DNA binding ability of R2R3-MYB2 from Arabidopsis (Serpa et al, 2007;Tavares et al, 2014). Histone deamination could be repaired through the BER pathway, which is responsible for the repair of damaged single bases resulting from deamination, alkylation, and oxidized bases (Cimini et al, 2019). H 2 S can modify the thiol group of cysteine (-SH) in proteins into a persulfide group (-SSH) through the process of S-sulfhydration, which is considered as the protective mechanism for proteins against oxidative damage (Aroca et al, 2018).…”