DNA methylation is enhanced during Cd hyperaccumulation in Noccaea caerulescens ecotype Ganges

Abstract

In this study, we assess the DNA damage occurring in response to cadmium (Cd) in the Cd hyperaccumulator Noccaea caerulescens Ganges (GA) vs the non-accumulator and close-relative species Arabidopsis thaliana. At this purpose, the alkaline comet assay was utilized to evaluate the Cd-induced variations in nucleoids and the methy-sens comet assay, and semiquantitative real-time (qRT)-PCR were also performed to associate nucleus variations to possible DNA modifications. Cadmium induced high DNA damages in nuclei of A. thaliana while only a small increase in DNA migration was observed in N. caerulescens GA. In addition, in N. caerulescens GA, CpG DNA methylation increase upon Cd when compared to control condition, along with an increase in the expression of MET1 gene, coding for the DNA-methyltransferase. N. caerulescens GA does not show any oxidative stress under Cd treatment, while A. thaliana Cd-treated plants showed an upregulation of transcripts of the respiratory burst oxidase, accumulation of reactive oxygen species, and enhanced superoxide dismutase activity. These data suggest that epigenetic modifications occur in the N. caerulescens GA exposed to Cd to preserve genome integrity, contributing to Cd tolerance.

Epigenetic Control of Plant Response to Heavy Metals

“…However, the phenomenon is complex and strongly depends on the plant genotype, the metal considered, and the experimental conditions; indeed, contrasting profiles have been observed in different species and metals. For example, Trifolium repens (metal sensitive) and Cannabis sativa (metal tolerant) both showed changes in DNA methylation tending toward hypomethylation when grown in soils artificially polluted with Cd, Cr, and Ni [ 65 ]; similarly, Cd produced demethylation in Brassica napus [ 66 ] and A. thaliana [ 67 ]. On the contrary, Cd treatment resulted in increased methylation in Posidonia oceanica [ 68 ], Datura stramonium [ 69 ], Noccaea caerulescens [ 67 ], and Hibiscus cannabinus [ 70 ]; hypermethylation was also produced by Cr in B. napus [ 71 ] and Zea mays [ 72 ], by Pb in Raphanus sativus [ 73 ], and by Cu in Hydrilla verticillata , the latter in a ROS-dependent manner [ 74 ].…”

“…In fact, differences are very evident when directly comparing non-tolerant vs. tolerant species. For example, non-tolerant A. thaliana had a higher basal methylation level than hyperaccumulator N. caerulescens and reacted to Cd treatment with DNA demethylation, whereas N. caerulescens showed an increased global methylation level [ 67 ]. Even at the level of population or cultivar, epigenetic-mediated adaption to metal-polluted soils was demonstrated.…”

The role of epigenetic and epitranscriptomic modifications in plants exposed to non-essential metals

“…LRR-RLK and NAC71 were down-regulated, while NPF2.7, DHX51, TTP-D and NADP-ME were up-regulated ( Luo et al., 2023 ). Another study compared the response of metal hyperaccumulator Noccaea caerulescens L. and non-hyperaccumulator, Arabidopsis thaliana ( Galati et al., 2023 ). Although N. caerulescens accumulated over threefold more Cd than A. thaliana , the latter one showed significantly higher degree of DNA damage and higher level of the DNA oxidation marker, 7,8-dihydro8-oxo-2-deoxyguanosine (8-oxo-dG), in reaction to Cd.…”

SpSIZ1 from hyperaccumulator Sedum plumbizincicola orchestrates SpABI5 to fine-tune cadmium tolerance

“…On the other hand, Cd inhibits various physiological processes in plants, including photosynthesis, respiration, and water movement, leading to damage in plant metabolism ( Rizwan et al., 2016 ). Moreover, Cd stress can induce DNA damage, ultimately resulting in plant mortality ( Galati et al., 2023 ). Therefore, it is crucial to reduce and mitigate Cd-induced pollution for the sake of environmental protection and human well-being.…”