Transcriptomic, osmoregulatory and translocation changes modulates Ni toxicity in Theobroma cacao

• Published in: Plant physiology and biochemistry Vol. 196; pp. 624 - 633
• Main Authors: Silva, José Victor dos Santos, Baligar, Virupax C., Ahrnet, Dário, de Almeida, Alex-Alan Furtado
• Format: Journal Article
• Language: English
• Published: France Elsevier Masson SAS 01.03.2023
• Subjects: Antioxidants - metabolism; Cacao; Humans; Metabolic disorders; Metal toxicity; Oxidative stress; Plants - genetics; ROS; Soil; Soil Pollutants - metabolism; Tolerance strategy; Transcriptome; Tolerance strategy; Oxidative stress; Cacao; Metabolic disorders; ROS; Metal toxicity
• ISSN: 0981-9428; 1873-2690
• DOI: 10.1016/j.plaphy.2023.01.053

Nickel is one of the most released trace elements in the environment and in the case of bioaccumulation in foods and beverages derived from cocoa beans can cause risk to human health. It is very important to understand how plants respond to toxic metals and which are the defense strategies they adopt to mitigate their effects. In the present study we used young plants of T. cacao, submitted to increasing Ni doses (0, 100, 200, 300, 400 and 500 mg Ni kg−1 soil) and evaluated them for a period of 30 days. Doses of Ni, from 300 mg of Ni kg−1 onwards in the soil, promoted changes in photosynthetic, antioxidant, osmoregulatory, transcriptomic and translocation levels, evidenced by the increase in the activity of antioxidant enzymes, proline, glycine betaine, upregulation of the metallothionein 2B gene (Mt2b), and lipid peroxidation of the cell membranes. Foliar gas exchange was severely affected at higher doses of Ni. In addition, reduced levels of stomatal conductivity and transpiration rate were observed from 300 mg Ni kg−1 dose onwards in the soil, which consequently affected CO2 assimilation. Phytostabilization and exclusion mechanisms control the translocation of Ni from the root to the shoot and reduce harmful effects on plant metabolism. Our results highlighted the toxicity of Ni, a trace element often underestimated in T. cacao. In particular, it was noted that doses of 100 and 200 Ni kg−1 soil, although high, do not induce toxicity in T. cacao plants. But Ni toxicity is observed from 300 mg Ni kg−1 soil onwards. This study contributed to the understanding of the harmful effects of higher doses of Ni in cacao plants and the biochemical processes the plant uses to mitigate the effects of this metal. [Display omitted] •APX and GPX enzymes were more effective in eliminating excess ROS, when compared with SOD and CAT.•Ni2+ toxicity induces the activation of a complex signaling network, in a sequential manner, modulated by enzymatic and no enzymatic antioxidatives systems.•There is a threshold of 300 mg/kg Ni2+ in soil that induces a series of metabolic responses in Theobroma cacao•Theobroma cacao plants demonstrate potential phytostabilization/exclusion mechanism in the Ni2+ translocation from root to the aerial part.•Ni2+ accumulation in the roots alleviates the Ni2+ toxicity in the shoot.•The MTs gene expression was increased in response to the different Ni2+ concentrations, indicating their crucial roles in the detoxification, inactivation, and compartmentalization of Ni in Theobroma cacao plants.