Table of Contents:
Mechanism of hyperaccumulation
The degree of hyperaccumulation of heavy metals can vary significantly in different species or even in populations or different ecotypes (Сарра et al. 2014). However, all hyperaccumulators show a few characteristic traits which distinguish them from the non-accumulators. These common traits are:
Studies have shown that genes responsible for accomplishing the key steps of hyperaccumulation are common to both hyperaccumulators and non hyperaccumulators, but are differently expressed and regulated in the two types of plants (Verbruggen et al. 2009). The ability of hyperaccumulators, however, depends upon the uptake capacity and intracellular transportation of plants. Figure 1 gives an account of the processes involved in hyperaccumulation.
Figure 1. Different processes involved in the bioactivation of heavy metals in the rhizosphere.
Heavy metal uptake
One of the most significant features of hyperaccumulating plants is their extraordinary capacity to absorb metals from the soil (Ma et al. 2001, Yang et al. 2006). The bioavailability and uptake of heavy metals in the soil are significantly affected by the metal content, pH, organic substance and other elements present in the rhizosphere. Most of the heavy metals have low mobility in soils and are not easily absorbed by plant roots (Knight et al. 1994).
Bioactivation of rhizosphere
Many of the hyperaccumulating plants show a tendency to increase the heavy metal uptake from the soil via the bioactivation of rhizosphere (Figure 1). Hyperaccumulating plants bring about changes at the soil root interphase by releasing organic and inorganic compounds (Fonia et al. 2017). The root exudates may include organic acids, phytochelatins, amino acids, protons, enzymes, etc. and may not only improve the metal bioavailability in the rhizosphere but also affect the number and activity of microorganisms by reducing soil pH or by producing chelators and siderophores (Abou-Slianab et al. 2003, Wenzel et al. 2003). Secretion of protons by the roots of hyperaccumulators may reduce the pH, thereby increasing the metal dissolution (Bernal et al. 1994). Studies have demonstrated that Cu accumulating plant species, Elsholtzia splendens, showed a lower pH in the rhizosphere than in the bulk soil (Peng et al. 2005). Secretion of organic acids fr om the roots of hyperaccumulator plants can enhance the absoiption from the soil by mobilizing the heavy metals present in the rhizosphere (Krishnamurti et al. 1997). Cieslinski et al. (1998) observed many low molecular organic acids such as acetic acid and succinate in the rhizosphere of Cd accumulating genotype (Areola). Root exudates of Zn/Cd hyperaccumulating plant species Section cdfredi Hance could extract more Zn and Pb from the contaminated soil (Li et al. 2012). The secretion of amino acid histidine in the root extracts of Allysum enhanced the transport and hyperaccumulation of Ni (Kramer et al. 1996).
Rhizosphere is populated by large concentration of microorganisms which play a significant role in increasing the bioavailability of various heavy metal ions for uptake (Figure 1). Xanthomonas maltophyta catalyzes the transformation of several toxic metal ions including Cri+, Pb2+, Hg2+,
Au3+, Te4+, Ag+ and oxyanions such as Se04~ (Weber et al. 2004, Zhao et al. 2002). Another bacterium, Shewanella alga, is known to increase the mobility of As, thus enhancing its uptake by hyperaccumulators (Lombi et al. 2001). Certain organisms are known to enhance Zn accumulation in the shoots of Thlaspi caerulescens by facilitating an increase in solubility of non-labile Zn in the soil, thus enhancing its bioavailability (Liu 2008). Soil microorganisms are also known to create cexlain organic exudates which significantly increase the bioavailability of certain metals like Mn2~ and Cd2+ (Hall 2002).
Uptake ofheavy metals by root cells is mediated by specific metal transpoxt proteins (Verbruggen et al. 2009, Rascio and Navari-Izzo 2011). Metal transporters generally have broad substrate specificities and are encoded by genes of different fanxilies like ZIP (Zinc aixd Iron Regulated Transporter Proteins). HMA (Heavy Metal transporting ATPase), MATE (Multidrug And Toxin Efflux), YSL (Yellow Stxipe 1 Like), MTP (Metal Tolerance Protein), etc. (Figxxre 2). Studies have shown that increased Zn xxptake by Thlaspi caerulescens, and Arabidopsis halleri roots, as compared to their related non hyperaccumulator species, can be attributed to the coixstinxtive overexpressiou of some genes belonging to the ZIP family, and coding for Zn transporters located in the plasma membrane (Kotrba et al. 2009). The expression of ZIP genes in non hyperaccunmlating species is regulated, i.e., they express only under Zn deficient conditions (Assuncao et al. 2001). In hyperaccumulating species, ZIP genes are expressed at high Zn concentrations as well, persisting at high Zn availability (Assuncao et al. 2001, Weber et al. 2004). Rascio and Navar-Izzo (2011) reported a decline in Cd uptake in presence of Zn in Cd/Zn hyperaccunxxxlator Arabidopsis halleri and most ecotypes of Thlaspi caerulescens. This observation clearly suggests that Cd uptake is largely mediated by Zn transporters with a strong preference for Zn over Cd (Zhao et al. 2002). However, in another Zn accumulator ecotype of T. caerulescens, Cd uptake remains unaffected by Zn concexxtration indicating the presence of an efficient and independent Cd transport system (Lombi et al. 2001).
Figure 2. Mechanism of heavy metal uptake, transport and accumulation in plants.
Similarly, the preference of Zn over Ni in some Zn/Ni hyperaccumulators supplied with the same concentrations of both the heavy metals strongly suggests that Zn transporters are involved in Ni uptake by the roots (Assuncao et al. 2000, Kotrba et al. 2009, Assuncao et al. 2010, Rascio and Navari-Izzo 2011).
Transport of As in form of arsenate is mediated by phosphate/arsenate transporters associated with the plasma membranes in the root cells of As hyperaccumulator Pteris vittata (Meharg and Whittaker 2002). Again, the density of these transporters is more in hyperaccumulating species as compared to non hyperaccumulators probably due to constitutive gene overexpression (Calle et al.
2005). He et al. (2016) reported an aquaporin gene PvTEP4 to mediate As uptake in Pteris vittata. However, in addition to the role of phosphate/arsenate transporters, arsenic uptake also depends upon the plants’ ability to increase the As bioavailability in rhizosphere by reducing pH via root exudation of organic carbon (Gonzaga et al. 2009).
Similarly, transport of Selenium (Se), in the form of selenate, is facilitated by sulphate transport owing to their chemical analogy and high affinity of the sulphate transporters towards Se (Shibagaki et al. 2002, Hirai et al. 2003). It has been observed that in hyperaccumulator species such as Astragalus bisulcatus (Fabaceae) and Stanleya pinnata (Brassicaceae), the Se/S ratio in shoots is much higher than their non hyperaccumulator counterparts (Galeas et al. 2007).