Unveiling how cadmium and manganeseinteract spatio-temporally during sunflower plants development

Abstract

Due to the increase in industrial activities, environmental pollution has grown exponentially in recent decades. This fact is directly associated with the exposure of ecosystems to high concentrations of trace elements. Tolerant plants used in the phytoremediation of contaminated environments have become an excellent economic option for the remediation of these areas. Sunflower (Helianthus annuus L.) is a plant with high hyperaccumulator potential due to its ability to resist different soil and climate conditions, accumulate high concentrations of trace elements and high biomass production. Although phytoremediation plants are known for their mechanisms of tolerance to high concentrations of trace elements, the increase of these elements in different plant tissues can promote morphophysiological and biochemical changes, thus modifying the growth and development of these species. Thus, this work aims to understand how sunflower plants deal with the joint disposition of the non-essential element cadmium (Cd) and the essential element manganese (Mn) in high concentrations in the soil, as well as the response mechanisms related to this interaction and how they affect the synthesis of metabolites and photoassimilates. For this, the plants were cultivated under six conditions: control (T1); 1.3 mg. Kg-1 of Cd (T2); 5 mg. Kg-1 of Cd (T3); 400 mg.Kg-1 of Mn (T4); 1.3 mg.Kg-1 of Cd and 400 mg.Kg-1 of Mn (T5); 5 mg.Kg-1 of Cd and 400 mg.Kg-1 of Mn (T6). Biochemical and photosynthetic parameters and chlorophyll a fluorescence were evaluated in the vegetative and reproductive phases (stages V4, V8, R4 and R7, according to the BBCH phenological scale). At the end, the biomass, oil content of achenes and concentrations of Cd, Mn and P in soil, roots, leaves and achenes were quantified. The bioaccumulation potential, translocation rate and element tolerance were also calculated. It is possible to infer that sunflower is tolerant to the evaluated concentrations of Cd, which accumulate mostly in the roots as a mechanism of tolerance and stress relief. When placed together in the soil, the plant was able to tolerate Cd and Mn in both concentrations evaluated. In these situations, the responses to the stressful condition are related to metabolic adjustments, without significant damage to the photosynthetic apparatus. In addition, Mn enhances Cd extraction and Cd negatively affects Mn uptake. Contrary to what occurs in other species, Cd did not interfere with the absorption of the essential element phosphorus (P). Changes in photosynthetic metabolism were observed at high Mn concentration with reduction in CO2 assimilation rate, stomatal conductance and Ci/Ca ratio. Interestingly, Cd concentrations did not cause photosynthetic changes, but, when available together with Mn, photosynthetic rates, stomatal conductance and Ci/Ca increased as an adjustment mechanism. These events directly affected the total dry matter and root/shoot ratio, with treatment containing 400 Mn presenting the lowest values, followed by the treatments containing Cd and Mn. There was also a delay in development in plants grown in 400Mn and with the joint disposition of Cd and Mn, mainly in the reproductive period, although all plants have completed the biocycle.