METAL TOXICITY; SIMILARITIES IN MECHANISMS AND RESPONSES
In general, metal toxicity has two main effects; firstly, it interferes
with nutrient homeostasis and secondly it causes secondary stress
particularly in the form of oxidative damage. Some metal(loid)s are
nutrients in their own right but may be present at toxic levels. Other
metal(loid)s share chemico-physical properties with essential nutrients,
and thus affect nutrient homeostasis by disrupting their uptake and
distribution. Furthermore, metal(loid)s can affect enzyme activity by
competing with physiological metal cofactors. This is particularly the
case with elements that have identical charge and similar ionic radius,
for example Cd2+ and Ca2+(calcium).
The propensity to alter the cellular redox potential, through binding
with thiol groups and/or through production of reactive oxygen species,
means metal(loid)s are prone to cause oxidative stress. Thus, faced with
toxic levels of harmful metals and metalloids plants show great
similarities in their responses which are summarised in Figure 1 and
further discussed below.
The role of root exudates: Roots extrude H+(protons) and carbon compounds such as organic acids, phenols and
phytosiderophores to promote solubility of essential nutrients (Bali et
al., 2020). H+ lower the rhizosphere pH which
increases soil mineral solubility and hence the release of essential
nutrients such as Fe, P (phosphorus), Ca, Mg and S (sulfur), but also
the release of toxic metals. Organic exudates have negatively charged
reactive groups such as sulfhydryls, carboxyls and hydroxyls with a high
affinity for metals. For example, root exuded citrate and malate are
known to chelate various metals such as Al (aluminium), Cd and Pb.
Exudation levels typically increase in response to metal presence but
the details are species related. Thus in sorghum exposure to Cd
augmented malate extrusion whereas the same heavy metal induced citrate
release in maize roots (Pinto et al., 2008). Phenolics are a further
compound that is often released by plant roots in response to heavy
metal stress. The hydroxyl group of these aromatic molecules can bind
metals (Guo et al., 2016). In general, phenolic and organic acid-metal
complexes are not taken up by the plant and hence lower soil toxicity by
reducing metal(loid) bioavailability.
Metal(loid) chelation: Two major cellular ligands that prevent
the occurrence of metals in ionic (reactive) form are glutathione and
phytochelatin (Figure 2). Both contain sulfhydryl groups with high
affinity for metal binding (Singh et al., 2016). Phytochelatin is a
glutathione oligomer with a structure that consists of multiple
γ-glutamate-cysteine moieties, followed by a terminal glycine. The
formation of phytochelatins is influenced by the presence of heavy
metal(loid)s and under control of the phytochelatin synthase enzyme.
Metallothionein is another glutathione-based, cysteine-rich protein that
binds metal. Its expression is raised in response to heavy metal stress.
Lastly, amino acids like histidine can bind metals and appear
particularly important for xylem mediated translocation of metals like
Ni and Zn (Kozhevnikova et al., 2014a, Kozhevnikova et al., 2014b).
Vacuolar sequestration: The relative lack of biochemical
machinery in the vacuole means it is the preferred cellular storage
compartment for toxic metal(loid)s. The transport of metal(loid)s
complexed to glutathione or phytochelatins across the tonoplast is
carried out by tonoplast ATP-Binding-Cassette (ABC) transporters that
are members of the ABCC family (Song et al., 2014). Tonoplast ABC
transporters for liganded metal(loid)s are expressed in many tissues. In
rice this includes roots, leaves, nodes, peduncles and rachis and ABC
proteins are instrumental in the vacuolar sequestration of Cd, As and a
range of other metals (Clemens and Ma, 2016). Vacuolar deposition of
metals in ionic form also occurs and can be mediated by members of the
Cation Diffusion Facilitator family known in plants as MTP (Metal
Tolerance Protein) family (Clemens and Ma, 2016). Metal(loid) storage in
root vacuoles is also an important factor to prevent large scale
translocation of metal(loid)s to above ground tissues.
Alteration of root architecture: Root architecture is sensitive
to metal toxicity. This includes biosynthesis of suberin and lignin to
strengthen the exo- and endodermic barriers that limit apoplastic
transfer (Figure 2). Callose deposition also reduces root metal(loid)
permeability. Furthermore, root architecture alteration in the presence
of heavy metals often involves the root ‘avoidance response’, i.e. the
propensity to either stop growth or grow away from polluted substrates.
Root avoidance has been observed in many species for multiple metals
including Zn, Ni and Cd (Tognacchini et al., 2020). The opposite
response can be found in hyperaccumulators where roots actively forage
for metals by increased rooting in soil patches with high metal content
(Whiting et al., 2000).
Oxidative stress: Increased levels of heavy metal(loid)s lead to
oxidative stress by generating reactive oxygen species (ROS) that can
cause lipid oxidation and DNA damage (Noctor et al., 2016). This is
countered by increased levels of enzymatic antioxidants like superoxide
dismutase, catalase and ascorbate peroxidase, and non-enzymatic
antioxidants like tocopherol, glutathione, phenolic compounds and amino
acids such as proline. Many studies have shown improved metal(loid)
tolerance when the genes and pathways that encode these factors are
upregulated (e.g. (Bhaduri and Fulekar, 2012). For example, proline
accumulation was observed in rice plants exposed after exposure to Hg
stress (Hayat et al., 2012).