Physiological, ultrastructural, biochemical and molecular responses of young cocoa plants to the toxicity of cr (iii) in soil

Authors: NASCIMENTO, J - UNIVERSITY OF SANTA CRUZ - BRAZIL; ALMEIDA, A-A - UNIVERSITY OF SANTA CRUZ - BRAZIL; BARROSO, J - UNIVERSITY OF SANTA CRUZ - BRAZIL; MANGABEIRA, P.A - UNIVERSITY OF SANTA CRUZ - BRAZIL; AHNERT, D - UNIVERSITY OF SANTA CRUZ - BRAZIL; SOUZA, A - UNIVERSITY OF SANTA CRUZ - BRAZIL; SILVA, J - UNIVERSITY OF SANTA CRUZ - BRAZIL; BALIGAR, VIRUPAX

Submitted to: Ecotoxicology and Environmental Safety
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/26/2018
Publication Date: 5/21/2018
Citation: Nascimento, J.L., Almeida, A.F., Barroso, J.P., Mangabeira, P.O., Ahnert, D., Souza, A.G., Silva, J.V., Baligar, V.C. 2018. Physiological, ultrastructural, biochemical and molecular responses of young cocoa plants to the toxicity of cr (iii) in soil. Ecotoxicology and Environmental Safety. 159:272-283.

Interpretive Summary: Cacao is a tropical crop of high importance, mainly due to the commercial value of its beans. Cacao in South America is grown on soils that have high levels of heavy metals such as chromium (Cr). Chromium from soil is transported to aerial parts of the plant and into cocoa beans. Cr at low concentrations may promote beneficial effects in some plant species, but at toxic level it interferes in the physiological and biochemical processes. In this paper, we report that toxic levels of Cr in the growth medium caused inhibition and abnormalities of plant growth, and induced ultrastructural damage to chloroplasts there by affecting photosynthesis. This information will be useful to farmers and scientists to avoid land areas that are high in Cr levels to grow sustainable cacao and to produce cocoa beans with low Cr content in order to protect its market value.

Technical Abstract: Theobroma cacao L. is a tropical crop of high importance due to the commercial value of its beans, which are used in the manufacture of chocolate. The presence of chromium (Cr) in beans and cocoa by-products has been reported. Cr at low concentrations may promote beneficial effects in some plant species, but at high doses it is a highly toxic metal. The objective of this study was to evaluate Cr toxicity in young plants of the CCN 51 cocoa genotype at different concentrations of Cr3+ in the soil (0, 100, 200, 400 and 600 mg kg-1) through physiological, ultrastructural, antioxidant and molecular changes. Doses of 400 and 600 mg Cr3+ kg-1 soil severely affected foliar gas exchange, promoted by ultrastructural damages in chloroplasts and photosynthetic machinery evidenced by the decrease in CO2 fixation. Decreased expression of psbA and psbO genes, changes in enzymatic activity and lipid peroxidation also affected leaf gas exchange. A hormesis effect was observed at 100 mg Cr3+ kg-1 soil for the photosynthetic activity. As a metal exclusion response, the roots of the cocoa plants immobilized, on average, 75% of the total Cr absorbed. Ultrastructural changes in leaf mesophyll and roots, with destruction of mitochondria, plasmolysis and formation of vesicles, were related to the oxidative stress promoted by excess ROS. The activity of the antioxidant enzymes SOD, APX, GPX and CAT and the amino acid proline coincided with the greater expression of the sod cyt gene demonstrating synchronicity in the elimination of ROS. It was concluded, therefore, that the tolerance of the cocoa plants to the toxicity of Cr3+ depends on the concentration and time of exposure to the metal. Higher doses of Cr3+ in the soil promoted irreversible damage to the photosynthetic machinery and the cellular ultrastructure, interfering in the enzymatic and non-enzymatic systems related to oxidative stress and gene expression. However, the low mobility of the metal to the shoot is presented as a strategy of tolerance to Cr3+.