Lead, Cadmium and Zinc Phytotoxicity Alter DNA Methylation Levels to Confer Heavy Metal Tolerance in Wheat

Abstract

Being a staple food, wheat (Triticum aestivum) nutritionally fulfills all requirements of human health and also serves as a significant link in the food chain for the ingestion of pollutants by humans and animals. Therefore, the presence of the heavy metals such as lead (Pb) and cadmium (Cd) in soil is not only responsible for the reduction of wheat crop yield but also the potential threat for human and animal health. However, the link between DNA methylation and heavy metal stress tolerance in wheat has not been investigated yet. In this study, eight high yielding wheat varieties were screened based on their phenotype in response to Pb stress. Out of these, Pirsabak 2004 and Fakhar-e-sarhad were identified as Pb resistant and sensitive varieties, respectively. In addition, Pirsabak 2004 and Fakhar-e-sarhad varieties were also found resistant and sensitive to Cd and Zinc (Zn) stress, respectively. Antioxidant activity was decreased in Fakhar-e-sarhad compared with control in response to Pb/Cd/Zn stresses, but Fakhar-e-sarhad and Pirsabak 2004 accumulated similar levels of Pb, Cd and Zn in their roots. The expression of Heavy Metal ATPase 2 (TaHMA2) and ATP-Binding Cassette (TaABCC2/3/4) metal detoxification transporters are significantly upregulated in Pirsabak 2004 compared with Fakhar-e-sarhad and non-treated controls in response to Pb, Cd and Zn metal stresses. Consistent with upregulation of metal detoxification transporters, CG DNA hypomethylation was also found at the promoter region of these transporters in Pirsabak 2004 compared with Fakhar-e-sarhad and non-treated control, which indicates that DNA methylation regulates the expression of metal detoxification transporters to confer resistance against metal toxicity in wheat. This study recommends the farmers to cultivate Pirsabak 2004 variety in metal contaminated soils and also highlights that DNA methylation is associated with metal stress tolerance in wheat.

Insight into the Role of Epigenetic Processes in Abiotic and Biotic Stress Response in Wheat and Barley

“…Notably, the methylation level at the promoter of a stress-responsive gene TaFLS1 (encoding a flavonol synthase) was lower in the salinity tolerant wheat cultivar SR3 than in salinity susceptible wheat cultivar JN177, which is opposite to the higher gene expression in SR3 than in JN177, suggesting that DNA methylation might get involved in regulation of wheat salinity tolerance [25]. Besides, the modulation of metal-stress response by DNA methylation is reported in wheat and barley [37,38]. In heavy metal detoxifications, the multidrug resistance-associated protein (MRP) type ATP-binding cassette (ABC) transporters play important roles, which also involve in other plant biological processes such as pathogen response and development [39][40][41][42].…”

“…As an important epigenetic process, DNA methylation generally regulates plant responses to environmental stresses such as salinity and heavy metal stress in wheat and barley [36,37]. For instance, a recent report showed that DNA methylation could regulate the expression of a salinity-responsive gene in bread wheat [25].…”

“…Eighteen MRP-type ABC transporter genes were identified from the wheat genome [41]. Shafiq et al found that the expression of TaABCCs and HEAVY METAL ATPASE 2 (TaHMA2) was higher in the heavy metal-resistant wheat varieties than in heavy metal-sensitive varieties upon exposure to the heavy metal stresses [37]. Furthermore, DNA methylation levels at the promoter of TaABCCs and TaHMA2 were lower in heavy metal-resistant varieties than in heavy metal-sensitive varieties under heavy metal stresses, suggesting that DNA methylation is associated with metal stress tolerance in wheat [37].…”

“…Shafiq et al found that the expression of TaABCCs and HEAVY METAL ATPASE 2 (TaHMA2) was higher in the heavy metal-resistant wheat varieties than in heavy metal-sensitive varieties upon exposure to the heavy metal stresses [37]. Furthermore, DNA methylation levels at the promoter of TaABCCs and TaHMA2 were lower in heavy metal-resistant varieties than in heavy metal-sensitive varieties under heavy metal stresses, suggesting that DNA methylation is associated with metal stress tolerance in wheat [37]. In barley, Al-activated citrate transporter1 (HvAACT1) is a major gene in charge of citrate efflux from roots for external Al detoxification in the rhizosphere [45,46].…”

Cadmium Uptake by Wheat (Triticum aestivum L.): An Overview

“…The main roles of heavy metals in plant metabolism are the basis of their involvement in reduction/oxidation procedures [4]. Cadmium toxicity is also associated with diminished plant growth, enzyme activity, and metabolism [5].…”