Melatonin-induced DNA demethylation of metal transporters and antioxidant genes alleviates lead stress in radish plants

Abstract

Melatonin (MT) is a tryptophan-derived natural product that plays a vital role in plant response to abiotic stresses, including heavy metals (HMs). However, it remains elusive how exogenous MT mediates lead (Pb) accumulation and detoxification at the methylation and transcriptional levels in radish. In this study, decreased Pb accumulation and increased antioxidant enzyme activity were detected under MT treatment in radish. Single-base resolution maps of DNA methylation under Pb stress (Pb200) and Pb plus MT treatment (Pb_50MT) were first generated. The genome-wide methylation level was increased under Pb stress, while an overall loss of DNA methylation was observed under MT treatment. The differentially methylated region (DMR)-associated genes between Pb_50MT and Pb200 were uniquely enriched in ion binding terms, including cation binding, iron ion binding, and transition metal ion binding. Hyper-DMRs between Pb200 and Control exhibited a decreasing trend of methylation under Pb_50MT treatment. A few critical upregulated antioxidant genes (e.g., RsAPX2, RsPOD52 and RsGST) exhibited decreased methylation levels under MT treatment, which enabled the radish plants to scavenge lead-induced reactive oxygen species (ROS) and decrease oxidative stress. Notably, several MT-induced HM transporter genes with low methylation (e.g., RsABCF5, RsYSL7 and RsHMT) and transcription factors (e.g., RsWRKY41 and RsMYB2) were involved in reducing Pb accumulation in radish roots. These findings could facilitate comprehensive elucidation of the molecular mechanism underlying MT-mediated Pb accumulation and detoxification in radish and other root vegetable crops.

DNA Methylation in Plant Responses and Adaption to Abiotic Stresses

“…Nipponbare), and more hypermethylated genes were found than hypomethylated ones [85]. The level of total methylation in radish and soybean (Glycine max) increased after Cd exposure with a significant dose-dependent relationship [86,87]. Methylation levels in the roots of heavy metal tolerant plants is significantly higher than that of sensitive plants, comparing clover (Trifolium repens L., sensitive species) with hemp (Cannabis sativa L., partial tolerant) [88], as well as Ni-tolerant Noccaea caerulescens with Ni-susceptible A. thaliana [89].…”

“…Transposable elements are one of the most heavily methylated DNA regions and were shown to play a role in Al stress responses in tolerant accessions of barley [94]. Furthermore, it was also found that a high density of TEs were strongly methylated in radish under Pb treatment [86]. Gene expression controlled by DNA methylation is another epigenetic response to heavy metal stress.…”

The Role of Membrane Transporters in Plant Growth and Development, and Abiotic Stress Tolerance

“…Overexpression of TaZnF in A. thaliana significantly increased tolerance to heat and cold stress as well as promoted early flowering [ 16 ]. Similarly, there are numerous studies in many plant species that evidenced the pivotal role of MTs in uptake, sequestration, translocation and detoxification of toxic HMs including cadmium (Cd) [ 17 ], chromium (Cr) [ 18 ], lead (Pb) [ 19 ], As [ 20 ], cobalt (Co) and zinc (Zn) [ 21 ] (for more details, see Section 3 ).…”

Melatonin-Mediated Abiotic Stress Tolerance in Plants

“…Notably, melatonin treatment balances endogenous GA and ABA levels and improves thiol-mediated detoxification in two indica rice. Furthermore, melatonin reduces Pb damage in radish plants via DNA demethylation of metal transporters and antioxidant genes ( Tang et al, 2021 ).…”