Cadmium
Cadmium has atomic number 48, an atomic weight of 112, a density of 8.65
g/cm3 and appears as a silvery bluish-grey metal.
Cadmium levels in uncontaminated soils are very low (< 1 ppm)
whereas polluted soils can contain over 50 ppm. Contamination is largely
due to human activities such as discharge and emission from industry,
mining, use of sewage sludge and Pi fertilisers and application of Cd
containing pesticide. Cd polluted agricultural soils are ubiquitous and
found on all continents and Cd exposure suppresses germination, inhibits
plant growth and reduces agricultural yields. Cadmium is highly toxic to
most plants with toxicity symptoms occurring when tissue levels are a
few ppm.
Processes in the rhizosphere related to Cd toxicity Dissolved,
bioavailable Cd is typically found in its ionic form
(Cd2+). Whether the concentration of Cd in the soil
solution becomes toxic will depend greatly on multiple processes that
take place in the rhizosphere. Cd chelation is an important aspect of
detoxification. Chelation occurs via several ways; plant released
organic acids and phytosiderophores can remove some of the soluble Cd
fraction from the soil solution though siderophore production may only
be significant during Fe stress (Bali et al., 2020). Organic acids and
phenolic compounds also bind considerable amounts of Cd (Pinto et al.,
2008, Guo et al., 2016).
Binding of Cd in the apoplast is another mechanism that may contribute
to imobilising Cd. Especially cell wall components like pectins contain
large numbers of carboxyl and hydroxyl groups. Apposing carboxyl and
carbonyl groups are typically bridged by divalent Ca2+via electrostatic interactions, but Cd2+ can
substitute Ca2+ in this process. Binding to the root
cell wall could provide an explanation for the often-observed linear
component of Cd uptake kinetics (Lux et al., 2011).
Strategies to imobilise free Cd can also include the use of
plant-growth-promoting rhizobacteria (PGPR). Many Cd-tolerant soil
bacteria have been identified within the genera of Pseudomonas,
Bacillus, Arthrobacter and Ralstonia . These microbes can have a
profound effect on the Cd bioavailability and thus plant toxicity. Like
their plant counterparts, microbes can alter the rhizosphere pH and
therefore Cd solubility. As mentioned above for the root apoplast,
adsorption and binding at the bacterial cell surface can take place at
negative groups such as NH2−,
COOH−, OH−,
PO43−, and
SO42− and thereby lower the metal
content in the rhizosphere.
Mycorrhizal fungi also can improve plant tolerance to heavy metals. Some
of the mechanisms discussed above such as adsorption to the cell surface
may play a role as will hyphal uptake of metals which reduces their
soluble fraction. However, it appears that mycorrhizal fungi can also
impact on metal compartmentation of the plant host; in Lotus
japonicus Cd immobilisation in plant roots was observed which led to a
significant reduction in shoot Cd (Chen et al., 2018). This shows that
mycorrhizal fungi may be important for the phytostabilisation of
Cd-contaminated soil, possibly via altering transport pathways of Cd in
the host.
Cadmium uptake/distribution Cd2+ uptake
typically has a Km value in the nanomolar range and its sensitivity to
the presence of other cations such as Ca, Fe, Zn and Mn points to
substrate competition (but this may occur at multiple transport sites)
(Cataldo et al., 1983). Proteins that mediate Cd2+influx are members of the ZIP (Zinc regulated transporter/Iron-regulated
transporter-like Protein) family (Clemens and Ma, 2016). Some authors
also mention non-selective cation channels and low affinity cation
transporters (LCT1) as possible pathways for Cd entry (e.g. (Greger et
al., 2016) but the latter seems unlikely given that the ambient Cd
concentration is typically micromolar while competing cations like Na, K
and Ca are present at much higher concentrations. Complexed forms of Cd
require different uptake mechanisms; in the form of chelates such as
Fe-Cd-siderophores or Cd-nicotianamine, influx takes place via YSL
(Yellow-Stripe 1-Like) proteins (Feng et al., 2017).
The majority of Cd that enters the plant becomes sequestered in the
root. This can occur through apoplastic adsorption or through vacuolar
deposition (Figure 3). The transport mechanism for vacuolar storage also
depends on the chemical form of Cd. The divalent ion likely competes
with Ca2+ and/or Zn2+ at binding
sites of transporters that are normally involved in the transport of
these nutrients. Thus vacuolar uptake of Cd2+ can be
catalysed by tonoplast cation:proton antiporters from the CAX family and
Zn transporters of the MTP family. More selective heavy metal ATPases of
the HMA (Heavy Metal ATPase) family that transport
Cd2+ form another pathway for vacuolar storage.
Complexed forms of cytoplasmic Cd consist of Cd bound to glutathione and
phytochelatin and these Cd-species rely on the activity of ABC
transporters from the C subfamily for vacuolar storage (Zhang et al.,
2018). Vacuolar Cd release is likely via NRAMP (Natural-Resistance
Associated Macrophage Proteins) type transporters (Song et al., 2017).
Release of Cd into the xylem for translocation to the shoot depends on
HMA ATPases (e.g. (Fontanili et al., 2016). For example, HMA3 is
primarily expressed in the root and a major determinant of leaf Cd
accumulation in Arabidopsis and rice (Chao et al., 2012).
Cellular detoxification of Cd Reducing the amount of Cd that
enters the plant symplast and partitioning into less sensitive organs
and organelles form a potent mechanism to reduce cellular toxicity. This
critically depends on the activity of multiple membrane transporters
(Figure 3). Gene expression and genomic association studies do show
different transporter alleles and expression levels between plants that
vary in Cd tolerance (Zhang et al., 2018). For example, expression of
AtABCC3 is induced in response to Cd treatment, augmenting the vacuolar
sequestration of phytochelatin bound Cd (Zhang et al., 2018). A rice QTL
study showed that weak and non-functional alleles of HMA3, which
mediates vacuolar Cd sequestration, caused increased Cd translocation to
the shoot and a ‘high accumulator’ phenotype (Ueno et al., 2010).
Overexpression of proteins involved in the production of chelating
agents improves Cd tolerance (Zanella et al., 2016). Similarly,
regulatory proteins such as transcription factors have been identified
(Shim et al., 2009) such as HsfA4a in wheat and rice, that increase
biosynthesis of metallothioneins.