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.