Unraveling the mechanisms controlling Cd accumulation and Cd‐tolerance in Brachiaria decumbens and Panicum maximum under summer and winter weather conditions

Abstract

We evaluated the mechanisms that control Cd accumulation and distribution, and the mechanisms that protect the photosynthetic apparatus of Brachiaria decumbens Stapf. cv. Basilisk and Panicum maximum Jacq. cv. Massai from Cd‐induced oxidative stress, as well as the effects of simulated summer or winter conditions on these mechanisms. Both grasses were grown in unpolluted and Cd‐polluted Oxisol (0.63 and 3.6 mg Cd kg−1 soil, respectively) at summer and winter conditions. Grasses grown in the Cd‐polluted Oxisol presented higher Cd concentration in their tissues in the winter conditions, but the shoot biomass production of both grasses was not affected by the experimental conditions. Cadmium was more accumulated in the root apoplast than the root symplast, contributing to increase the diameter and cell layers of the cambial region of both grasses. Roots of B. decumbens were more susceptible to disturbed nutrients uptake and nitrogen metabolism than roots of P. maximum. Both grasses translocated high amounts of Cd to their shoots resulting in oxidative stress. Oxidative stress in the leaves of both grasses was higher in summer than winter, but only in P. maximum superoxide dismutase (SOD) and ascorbate peroxidase (APX) activities were increased. However, CO2 assimilation was not affected due to the protection provided by reduced glutathione (GSH) and phytochelatins (PCs) that were more synthesized in shoots than roots. In summary, the root apoplast was not sufficiently effective to prevent Cd translocation from roots to shoot, but GSH and PCs provided good protection for the photosynthetic apparatus of both grasses.

Are Grasses Really Useful for the Phytoremediation of Potentially Toxic Trace Elements? A Review

“…In the roots of Brachiaria decumbens (also known as Urochloa decumbens ) and P. maximum grown for 64 days in an Oxisol with 3.6 mg Cd kg –1 ( Rabêlo et al, 2021 ), the PC concentrations were only slightly higher than in the unpolluted control soil. Cadmium binding by cell walls (apoplast) was probably the process that most contributed to Cd accumulation in the roots of grasses under prolonged Cd exposure ( Rabêlo et al, 2021 ). As speculated by Clemens (2006) , Cd exposure time influences the binding partners for Cd accumulation.…”

“…Cell walls tend to bind divalent and trivalent trace element cations during their uptake by cells and at the final stage of their sequestration from the cytosol to decrease the toxicity due to free trace element into the cells ( Hall, 2002 ; Krzesłowska, 2011 ). Almost 60% of Cd retained in the roots of P. maximum and B. decumbens was situated in the root apoplast, probably adsorbed to the cell walls ( Rabêlo et al, 2021 ). Similarly, in P. australis , most Zn accumulated within the root apoplast and Zn concentrations followed the gradient: intercellular spaces > cell walls > vacuoles > cytosol ( Jiang and Wang, 2008 ).…”

“…The processes involved in the transport of trace element-PCs complexes from the cytosol to the vacuole were reviewed in detail ( Sharma et al, 2016 ). Although PCs are important players in trace element detoxification, they are not always induced under trace element exposure due to the combined action of other detoxification processes ( Rabêlo et al, 2019 ), as observed in D. cespitosa exposed to Ni ( Hayward et al, 2013 ) and B. decumbens and P. maximum exposed to Cd ( Rabêlo et al, 2021 ). Besides the PCs, MTs are supposed to function as trace element-binding ligands in plant cells ( Cobbett and Goldsbrough, 2002 ), although their role in plants remains to be confirmed.…”

“…Moreover, GSH is used as a substrate for PCs synthesis and can also act as a ligand for trace elements, besides transmitting specific information tuning cellular signaling pathways under trace element stress conditions (for a comprehensive review see Seth et al, 2012 ). The beneficial effects of GSH on trace element tolerance were described in L. perenne grown in soil polluted with As, Cu, Hg, Pb, and Zn ( Anjum et al, 2013 ), Poa pratensis exposed to Cu ( Liu et al, 2016 ), and both P. maximum and B. decumbens exposed to Cd ( Rabêlo et al, 2021 ). Under high Cd accumulation, symptoms of oxidative stress, such as lipid peroxidation, can occur as a consequence of GSH depletion due to the binding of Cd 2+ to GSH and the formation of GSH-derived PCs ( Clemens, 2006 ).…”

Changes in Tillering, Nutritional Status, and Biomass Yield of Panicum Maximum Used for Cadmium Phytoextraction

“…4G). Maybe such result is associated to the fact that P. maximum preferentially accumulates Cd bound to cell wall in the root apoplast (Rabêlo et al 2021b). In this case, the deleterious effects of Cd are more noticeable on root length and root surface than root weight (Rabêlo et al 2020b), since the thickening of the roots due to ligni cation and suberization (Lux et al 2011) can compensate the root weight.…”