Arsenic Induced Phytate Exudation, and Promoted FeAsO₄ Dissolution and Plant Growth in As-Hyperaccumulator Pteris vittata

Abstract

Arsenic hyperaccumulator Pteris vittata (PV) is efficient in taking up As and nutrients from As-contaminated soils. We evaluated the mechanisms used by PV to mobilize As and Fe by examining the impacts of As and root exudates on FeAsO4 solubilization, and As and Fe uptake in four plants: As-hyperaccumulators PV and Pteris multifida (PM), nonhyperaccumulator Pteris ensiformis (PE), and angiosperm plant tomato (Solanum lycopersicum). Phytate and oxalate were dominant in fern plants (>93%), which were 50-83, 15-42, and 0-32 mg kg(-1) phytate and 10-15, 7-26, and 4-12 mg kg(-1) oxalate for PV, PM, and PE respectively, with higher As inducing greater phytate exudation and no phytate being detected in tomato exudates. PV treated with phytate+FeAsO4 had higher As and Fe contents and larger biomass than phytate or FeAsO4 treatment, which were 340 vs 20 and 130 mg kg(-1) As in the fronds and 7900 vs 1600 and 4100 mg kg(-1) Fe in the roots. We hypothesized that As-induced phytate exudation helped PV to take up Fe and As from insoluble FeAsO4 and promoted PV growth. Our study suggests that phytate exudation may be special to fern plants, which may play an important role in enhancing As and nutrient uptake by plants, thereby increasing their efficiency in phytoremediation of As-contaminated soils.

Phytate induced arsenic uptake and plant growth in arsenic-hyperaccumulator Pteris vittata

“…Monoferric phytate is water soluble, but tetraferric phytate is not, indicating the solubility of Fe-phytate decreases with increasing Fe in the complex. Liu et al (2016) found that 96% and 87% of Fe is sequestered as insoluble Fephytate at phytate:Fe ratios of 3:1 and 8:1. The 0.5-strength MS medium contains 50 mM Fe.…”

“…Iron is an essential nutrient for plant growth and health. Liu et al (2015Liu et al ( , 2016 observed that PV biomass was closely correlated with plant Fe content (R 2 ¼~0.80), illustrating the important role of Fe in PV growth.…”

“…Besides, phytate is also the predominant form of P storage in plant seeds and grains (Park et al, 2006). Furthermore, its production as low molecular weight organic acid (LMWOA) has been detected in PV root exudates, which contributes to its efficient Fe and As acquisition from insoluble Fe-As minerals (Liu et al, 2016;Tu et al, 2004). Unlike typical plant LMWOAs (e.g., citrate and oxalate), as an organic P and the dominant LMWOA in PV rhizosphere microniche, phytate may affect As uptake by PV thus its phytoremediation efficiency of As-contaminated soils.…”

Pteris vittata Arsenic Accumulation Only Partially Explains Soil Arsenic Depletion during Field-Scale Phytoextraction

“…The mixed redox status of rhizosphere solid-phase arsenic we observed could be coupled to dissolved organic carbon (DOC) mobilization and/or oxidation in the P. vittata rhizosphere. Root exudates have been suggested to play an important role in arsenic release from soil solid surfaces for uptake into P. vittata [42,93]. Arsenic and DOC cycles in P. vittata rhizosphere soil could intersect through a combination of processes including: (1) release of arsenic(V) from iron oxide surfaces due to ion exchange or ligand-enhanced dissolution with DOC [44,47], leading to fern uptake and/or leaching of soluble arsenic(V) [47,92,94,95] and/or DOC [96,97]; (2) enhanced weathering of sulfide residues in pyrite cinders [98], decreasing pH locally [75] and solubilizing arsenic(III) and/or arsenic(V); (3) reduction of arsenic(V) within roots [99]; (4) microbially-mediated arsenic reduction in the rhizosphere coupled to DOC oxidation [47,48]; (5) fern uptake of soluble arsenic(III) [100]; and/or (6) replenishment of soil arsenic through leaching from foliage [101] or excretion of soluble arsenic(III) from roots to soil [102,103] and subsequent sorption to soil.…”

Phosphorus- and Iron-Deficiency Stresses Affect Arsenic Accumulation and Root Exudates in Pteris vittata

“…After 7 days of treatments, the plants were treated by washing the roots with Milli-Q water to remove surface adsorbed As. Root exudates were collected according Liu et al [13]. Briefly, in order to restrain microbial growth of rhizosphere, plant roots were soaked in 30 mg L −1 antibiotic solution, chloramphenicol (Sigma-Aldrich, St. Louis, USA) for 2 h. And afterward, plants were transferred into the shading plastic flask contained 20 mL Milli-Q water, subsequently used to collect root exudates for 12 h. The collected solution was instantly filtrated by 0.45 μm filters and stored at 4°C.…”