Emerging mechanisms for heavy metal transport in plants

Abstract

Heavy metal ions such as Cu(2+), Zn(2+), Mn(2+), Fe(2+), Ni(2+) and Co(2+) are essential micronutrients for plant metabolism but when present in excess, these, and non-essential metals such as Cd(2+), Hg(2+) and Pb(2+), can become extremely toxic. Thus mechanisms must exist to satisfy the requirements of cellular metabolism but also to protect cells from toxic effects. The mechanisms deployed in the acquisition of essential heavy metal micronutrients have not been clearly defined although a number of genes have now been identified which encode potential transporters. This review concentrates on three classes of membrane transporters that have been implicated in the transport of heavy metals in a variety of organisms and could serve such a role in plants: the heavy metal (CPx-type) ATPases, the natural resistance-associated macrophage protein (Nramp) family and members of the cation diffusion facilitator (CDF) family. We aim to give an overview of the main features of these transporters in plants in terms of structure, function and regulation drawing on information from studies in a wide variety of organisms.

Identification of Thlaspi caerulescens Genes That May Be Involved in Heavy Metal Hyperaccumulation and Tolerance. Characterization of a Novel Heavy Metal Transporting ATPase

“…It has previously been suggested that the Cys dipeptides and His-rich domains in heavy metal ATPases may be involved in heavy metal-binding (Solioz and Vulpe, 1996;Williams et al, 2000), and the findings presented here confirm these speculations for the TcHMA4 protein. Based on the association constants for the binding of heavy metals to di-Cys and di-His residues (Motekaitis et al, 1997), the His and Cys repeats, particularly in the longer peptide, should provide a large number of high-affinity binding sites for a range of heavy metals and micronutrients, including Cd, Pb, mercury, Zn, Co, Ni, and Cu.…”

Identification of mouse SLC39A8 as the transporter responsible for cadmium-induced toxicity in the testis

“…Cd uptake and efflux, and the inhibition of metal transport by Cd, are well characterized in plants, yeast, and mollusk (6,8,(50)(51)(52)(53)(54)(55)(56)(57)(58)(59). In mammalian-cultured cells, many studies of Cd transport and inhibition of divalent cation transport by Cd have shown Cd uptake and toxicity (11,42,43,(60)(61), but there were no studies correlating Cd uptake with toxicity in any organ or specific cell type of any intact vertebrate.…”

“…The subcellular events by which Cd is taken up by cells or removed from cells remain obscure, although such knowledge could provide potential therapeutic targets for protection or intervention against Cd toxicity. Several proteins transport Cd into bacteria, yeast, plants, and mammalian cells in culture (6)(7)(8)(9)(10)(11), but their specific roles in causing toxicity are unclear; these studies underscore the difficulties in extrapolating from observations in cell culture to the intact animal.…”

Characterization of a Thermophilic P-type Ag+/Cu+-ATPase from the ExtremophileArchaeoglobus fulgidus

“…In the last decade, the identification of numerous CPx-ATPases and in particular the two human isoforms has brought much attention to these heavy metal transport ATPases (11)(12)(13). These enzymes present interesting structural features such as the N-MBDs repeats in their cytoplasmic amino terminus or the distinct location of the large cytoplasmic loop in relation to their eight TMs.…”

“…Among these, ATPases in the PIB subfamily transport transition metals (Cu ϩ , Ag ϩ , Zn 2ϩ , Cd 2ϩ , Pb 2ϩ , and Co 2ϩ ). In light of their substrates, these enzymes appear as central elements in the processes of metal biotolerance and bioaccumulation (11)(12)(13). For instance, the two PIB-type ATPases present in humans are Cu ϩ transporters, and mutations in these proteins are responsible for Menkes' and Wilson's disease (13)(14)(15)(16).…”