Arsenite transport in plants

Abstract

Arsenic is a metalloid which is toxic to living organisms. Natural occurrence of arsenic and human activities have led to widespread contamination in many areas of the world, exposing a large section of the human population to potential arsenic poisoning. Arsenic intake can occur through consumption of contaminated crops and it is therefore important to understand the mechanisms of transport, metabolism and tolerance that plants display in response to arsenic. Plants are mainly exposed to the inorganic forms of arsenic, arsenate and arsenite. Recently, significant progress has been made in the identification and characterisation of proteins responsible for movement of arsenite into and within plants. Aquaporins of the NIP (nodulin26-like intrinsic protein) subfamily were shown to transport arsenite in planta and in heterologous systems. In this review, we will evaluate the implications of these new findings and assess how this may help in developing safer and more tolerant crops.

Fig. 1

Arsenic metabolism in prokaryotes and eukaryotes. a The main uptake of arsenate (As^V) into bacterial cells occurs via PhoS, PstC, and PstB phosphate (P_i) transporters. Arsenite (As^III) enters the bacterial cells via the GlpF aquaglyceroporin (AQGP). As^V is reduced to As^III by the bacterial ArsC arsenate reductase using glutathione (GSH) as reductant. ArsB, an As^III:H⁺-antiporter, or ArsAB, an As^III ATPase, extrude As^III into the external environment. In addition, As^III can be released into the environment in volatile form after subsequent methylation steps carried out by As^III-S-adenosylmethionine methyltransferase. MMA monomethylarsonic acid, DMA dimethylarsinic acid, TMAO trimethylarsine oxide, TMA trimethylarsine. b In yeast, uptake of arsenate is facilitated by Pho87 type phosphate transporters, and arsenite is taken up mainly via the AQGP Fps1p but may also enter cells through hexose permeases (HXTs). The reduction of arsenate to arsenite in yeast cells is provided by the Acr2p arsenate reductase via glutathione oxidation (GSH to GS). Removal of cellular As^III can occur through conjugation to glutathione (As(GS)₃) which is sequestered into vacuoles by the ABC transporter Ycf1p, or through extrusion of As^III via the plasma membrane carrier Acr3. c As in yeast, uptake of As^III in mammalian cells can occur via aquaporins such as AQP7 and AQP9 and via HXTs. Specific proteins responsible for arsenate uptake and arsenate reduction in mammals have yet to be identified. The main efflux mechanisms for As^III in mammals appear to be ABC transporters from the MRP and MDR subfamilies. Methylation of As^III by arsenic methyltransferases such as AS3MT increases mobility of arsenicals in the body and facilitates removal through skin and urine

Fig. 2

Mechanisms of arsenic uptake in plants a Plants take up As^V through phosphate transporters (Pi) such as those belonging to the PHT1 family. As^III influx occurs through aquaglyceroporins of the NIP (nodulin like intrinsic protein) subfamily. As^V is reduced to As^III by arsenate reductase (AR) using glutathione (GSH) as a reductant and As^III can form complexes with thiol groups from glutathione and phytochelatins (PCs) to lower its cytotoxicity. The complexed As^III and inorganic As^III are believed to be mostly sequestered into the central vacuole via as yet unknown transporters. Inorganic As^V and As^III are the major arsenicals found in the xylem sap of plants. b Most plant species act as ‘excluders’ i.e. a very small proportion of arsenic is translocated to shoot tissue where similar reduction and sequestration mechanisms are present. c Via the phloem, some of the total arsenic content ends up in the vacuoles and other tissues of edible parts such as seeds

Fig. 3

The involvement of NIPs in plant arsenite transport. a Generalised secondary structure of an aquaporin monomer with six transmembrane domains (S1–S6) and two canonical NPA motifs between S2 and S3 and S5 and S6. The arrows 1–4 point to the approximate positions of residues that make up the Ar/R (aromatic/arginine) region that is essential for channel selectivity. b Each monomer forms a pore (arrow) with the Ar/R residues (in yellow) forming the narrowest part of the channel pore. c Four monomers form a functional aquaporin. Views in (b) and (c) are perpendicular to the membrane from the outside. d Phylogenetic tree of plant NIPs. At Arabidopsis thaliana, Os Oryza sativa, Zm Zea mays, Mt Medicago truncatula, Cp Cucubrita pepo, Nal Nicotiana alata, Lj Lotus japonicus, Pt Pinus taeda, Atrn Atriplex nummularia, Car Cicer arietinum, Gm Glycine max, Ps Pisum sativum, Ec Escherichia coli, Ss Saccharomyces cerevisiae. For comparison, AtPIP1;1, a non-NIP plasma membrane intrinsic protein, and As^III conducting aquaglyceroporins from mammals (AQP7 and AQP9), yeast (Fps1) and bacteria (GlpF) are included. The color fields represent different subgroups of the NIP proteins and isoforms that have been shown to be able to conduct As^III are shown in bold. The alignment of amino acid sequences was performed using ClustalX 2.0.9