Three Genes Define a Bacterial-Like Arsenic Tolerance Mechanism in the Arsenic Hyperaccumulating Fern Pteris vittata

Abstract

Arsenic is a carcinogenic contaminant of water and food and a growing threat to human health in many regions of the world. This study focuses on the fern Pteris vittata (Pteridaceae), which is extraordinary in its ability to tolerate and hyperaccumulate very high levels of arsenic that would kill any other plant or animal outside the Pteridaceae. Here, we use RNA-seq to identify three genes (GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE (PvGAPC1), ORGANIC CATION TRANSPORTER 4 (PvOCT4), and GLUTATHIONE S-TRANSFERASE (PvGSTF1) that are highly upregulated by arsenic and are necessary for arsenic tolerance, as demonstrated by RNAi. The proteins encoded by these genes have unexpected properties: PvGAPC1 has an unusual active site and a much greater affinity for arsenate than phosphate; PvGSTF1 has arsenate reductase activity; and PvOCT4 localizes as puncta in the cytoplasm. Surprisingly, PvGAPC1, PvGSTF1, and arsenate localize in a similar pattern. These results are consistent with a model that describes the fate of arsenate once it enters the cell. It involves the conversion of arsenate into 1-arseno-3-phosphoglycerate by PvGAPC1. This ''chemically trapped'' arsenate is pumped into specific arsenic metabolizing vesicles by the PvOCT4 protein. Once inside these vesicles, 1-arseno-3phosphoglycerate hydrolyses to release arsenate, which is then reduced by PvGSTF1 to arsenite, the form of arsenic stored in the vacuoles of this fern. This mechanism is strikingly similar to one recently described Pseudomonas aeruginosa, whose tolerance to arsenic also involves the biosynthesis and transport of 1-arseno-3-phosphoglycerate, indicating that P. vittata has evolved a simple, bacteriallike mechanism for arsenic tolerance.

Exploration of the role of a lithophytic fern, Pteris vittata L. in wound tissue regeneration and remodelling of genes in hyperglycaemic rat model

“…During the literature search on PV it was found that using RNAi-based gene silencing, other authors demonstrated critical roles for three genes in establishing arsenate tolerance in PV which were PV GAPC1 (Glyceraldehyde 3-Phosphate Dehydrogenase), PV OCT 4 (Organic Cation Transporter 4) and PvGSTF1 Glutathione S-Transferase) [40].…”

Plant Nanobionic Sensors for Arsenic Detection

“…[ 59 ] Similarly, the GAPC1, GSTF1 , and OCT4 proteins are required for the import and reduction of arsenate inside the cells. [ 65 ] However, the uptake pathway of arsenite in Pteridaceae ferns has not been fully elucidated, partly due to the difficulty in generating transgenic ferns. [ 66 ] In rice, the uptake of arsenite into rice roots is primarily facilitated by OsNIP2;1 ( Ls1 ), a member of the nodulin‐26 like intrinsic proteins (NIPs) that is also responsible for the uptake of silicon (Si).…”

How Plants Handle Trivalent (+3) Elements

“…The expression of PvACR3;1 from P. vittata in A. thaliana and tobacco ( Nicotiana tabacum ) was shown to increase As retention in the roots, thereby decreasing As accumulation in the shoots [205]. Recent gene expression studies revealed a close cooperation of different uptake and storage mechanisms responsible for As hyperaccumulation and hypertolerance in the gametophytes of P. vittata [206]. Based on a similar mechanism previously established for As tolerance in Pseudomonas aeruginosa [207], Cai et al, [206] proposed the following model for As hyperaccumulation and tolerance in P. vittata : As(III) crosses the plasma membrane by the aquaporin AsTIP4 and is transported through the tonoplast for vacuolar storage by PvACR3.…”