Transfer Mechanism, Uptake Kinetic Process, and Bioavailability of P

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Transfer Mechanism, Uptake Kinetic Process and Bioavailability of P, Cu, Cd, Pb and Zn in Macrophyte Rhizosphere Using DGT Shengrui Wang, Zhihao Wu, and Jun Luo Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b01578 • Publication Date (Web): 14 Dec 2017 Downloaded from http://pubs.acs.org on December 15, 2017

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Environmental Science & Technology

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Transfer Mechanism, Uptake Kinetic Process and

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Bioavailability of P, Cu, Cd, Pb and Zn in Macrophyte

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Rhizosphere Using DGT

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Shengrui Wang, †.‡.§ *

Zhihao Wu, ‡.§

Jun Luo ς

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†. College of Water Sciences, Beijing Normal University, Beijing 100875, China.

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‡. National Engineering Laboratory for lake water pollution control and ecological restoration

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technology ， Research Center of Lake Eco-environment, Chinese Research Academy of

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Environmental Sciences, Beijing, 100012 China.

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§. State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research

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Academy of Environmental Sciences, Beijing, 100012 China.

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ς. State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment,

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Nanjing University, Nanjing, Jiangsu 210023, PR China.

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*Corresponding author. Tel: +86-10-84915277 Fax: +86-10-84915277; E-mail: [email protected]

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ABSTRACT: The transfer-uptake-bioavailability of phosphorus (P), Cu, Cd, Zn and Pb in

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rhizosphere of Zizania latifolia (ZL) and Myriophyllum verticiilaturn (MV) cultivated in

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rhizoboxes in Lake Erhai (China) is evaluated by DGT (diffusive gradients in thin films)

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technique. DGT induced fluxes in sediments (DIFS) model reveals that resupply ability (r), liable

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pool size in sediment solid (kd), kinetic parameter (k-1) or response time (Tc) control the

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diffusion-resupply characters of P and Cu (standing for four metals) in rhizosphere interface. The

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linear fitting curves of element content in ZL or MV roots (Croot) against DGT (CDGT), porewater

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(C0) or sediment concentration demonstrate that Croot for five elements can be predicted by CDGT

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more effectively than the other methods. (I) DOC (dissolved organic carbon) in porewater

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controlled by OM (organic matter) in solid plus pH for Cu and Cd or (II) DOP/DTP ratio in

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porewater (between dissolved organic P and dissolved total P) for P controlled by Fe-bound P and

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OM in solid, can affect phytoavailability in rhizosphere. They lead to (I) the larger slope (s) and

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the linear regression coefficient (R2) in the first part than those for the complete fitting curve (ZL

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or MV root against CDGT (Cu) or C0(Cu); and MV root against CDGT (Cd)) or (II) the outliers

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above or below the fitting curve (ZL root (P) against C0 (P) or CDGT(P)) and the larger R2 without

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outliers. DGT-rhizobox-DIFS should be a reliable tool to research phytoremediation mechanism

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of macrophytes.

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■ INTRODUCTION

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The emerged macrophyte with root and rhizome in bottom sediment and stem

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and leaf above water, and the submerged macrophyte with root/stem/leaf below water

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surface are widely distributed in lakes worldwide. 1, 2 The aquatic macrophyte root has

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important effects on the cycles of nutrient and metals at sediment/water interface

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through both abiotic and biotic processes.

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of wetland (lake) due to their phytoextraction ability.

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applies the element-accumulating plant to remove nutrients or metals from

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contaminated soil (sediment) by harvesting aboveground part of plant.

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important to reveal the uptake-accumulation of phosphorus (P) or trace metals by

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macrophytes and mobility-bioavailability at two interfaces (root/porewater and

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porewater/sediment solid phase) (Fig. S1).

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Macrophytes can improve water quality 5,6

Phytoextraction method

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So, it’s

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Roots of aquatic macrophytes absorb nutrients and trace metals from the

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sediment porewater in rhizosphere and accumulate the high element concentration,

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which are transferred to above-ground part. 8 It’s important to understand root uptake

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mechanism, transfer process and bioavailability of elements in complex rhizosphere

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environment 9-12 responsible for phytoextraction ability. The biogeochemistry and the

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transfer mechanism in macrophyte rhizosphere

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effect

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impact of trace metals on physiological and biochemical characteristics such as the

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and phytoextraction function.15,

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8, 13

are related to ecotoxicological

Ecotoxicological effect refers to the

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damage of cell membrane structure and the inhibition of cellular respiration,

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photosynthesis

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detoxification and tolerance functions can accumulate trace metals to restore

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contaminated sediments. These functions include the anti-oxidant ability,18 the effect

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of cytoderm

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agents (phytochelatin, amino acid and organic acid) for detoxification.21

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and

growing

and root exudate

development.17

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Some

macrophytes

with

the

on inhibiting absorption, and metal complexing

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Macrophytes can change Eh, pH and organic matter (OM) in rhizosphere

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sediment.22-24 Fe-plaque existing on macrophyte root surface due to O2 released from

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root can serve as a sink for trace metals and P.25-27 P sorption capacity in sediments is

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related to ferric oxyhydroxides or hydroxide, aluminum hydroxide and calcium

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carbonate.25, 28 Hypolimnetic P release occurs under anoxic condition that leads to the

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reductive dissolution of ferric hydroxide. 29-31 It also causes the release of trace metals

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into porewater.29 P bioavailability in macrophyte rhizosphere is dependent on P forms

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(inorganic P and organic P) in sediment solution, chemical and physical factors such

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as pH, Eh, temperature, water dynamic conditions, P fractions in solid and P release

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from solid into solution. 32, 33

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Pb, Cu, Zn or Cd can deteriorate lake ecology because of their persistent, toxic,

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nondestructible characters in sediment-water and the bioaccumulation in macrophytes

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or aquatilias. 34-37 Some contaminated macrophytes can be a source of food and lead

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to bioaccumulation and toxicity of trace metals in food chain.38 In macrophyte

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rhizosphere, dissolved organic matter (DOM) binding to trace metals, 39 solubility and 5



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speciation of metals,

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accumulation of trace metals, 41, 42 Eh and pH

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The metal’s bioavailability to macrophytes relies on sediment concentration, plant

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growth form, adsorption mechanism, exposure time, metal affinity for adsorption sites

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and metal species. 8,13

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root exudate (organic acid) with chelating agents for the 43

can influence metals’ bioavailability.

However, to date, little is known on the “in-situ” dynamic processes of P and 44

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metals in rhizosphere

at two interfaces (root/porewater and porewater/sediment

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solid phase) and the prediction of uptake-accumulation in plant tissues. The

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conventional methods for the element’s bioavailability and mobility in root-soil 45, 46

(sediment) system include porewater extraction,

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total element analysis for soil (sediment).

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solution can’t reflect the capability of soil (sediment) to resupply porewater following

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the depletion due to plant uptake; 49 chemical extractions can’t avoid the redistribution

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and readsorption in sediment during extraction.

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(sediment) embraces the fractions unavailable to plants. Moreover, those methods

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isolate the transfer in rhizosphere and can’t reflect the “real” kinetic exchange

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between porewater/solid interface.

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chemical extraction

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and

However, P or metals in sediment

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The total element content in soil

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Diffusive gradients in thin films (DGT), an “in-situ” technique has been

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developed for the element’s availability and the dynamic process in rhizosphere, and

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the prediction of metal concentration in plant tissue. 44 DGT measurement is involved

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in the kinetics and the capacity of solid phase, and DGT induced flux in soil (sediment)

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related to diffusion and resupply processes. DGT induced fluxes in soil (sediment)

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(DIFS) model

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model (DPUM)

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resupply of As from soil solid to porewater in rhizosphere zone of Pteris vittata L.

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cultivated in rhizobox

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hypothetical porewater concentration that should be needed to accumulate the

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measured amount of element on DGT resin if there was solely diﬀusional supply.

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The effect of DOC (dissolved organic carbon) on the bioavailability of Cd in

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rhizosphere sediment has been investigated using DGT and WHAM (Windermere

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Humic Aqueous Model).

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DGT concentration or CE.

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transfer-phytoavailability of P and trace metals in macrophyte rhizosphere.

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for DGT-soil (sediment) is consistent with the dynamic plant uptake 52

for root. DIFS (1D or 2D) has been used to (i) reveal the kinetic

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or (ii) derive the effective concentration (CE), i.e. the

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The metal content in plant tissue has been predicted by 49, 54

Until now, there is no DGT research on the

Zizania latifolia (Zizania Gronov. ex L, Gramineae), 1 one perennial emerged 47

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macrophyte, and one submerged macrophyte (Myriophyllum verticiilaturn),

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both widely distributed in Lake Erhai in Yunnan province (China) (Fig. S2-1). Based

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on the method proposed by Aviani et al. (2006),

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with multi-layers in vertical direction, a sediment-root compartment (R-zone) and a

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bulk sediment compartment (B-zone), has been designed for the cultivation of Zizania

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latifolia (ZL) and Myriophyllum verticiilaturn (MV) in lake, the separation of

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rhizosphere and non-rhizosphere zones, DGT tests and the collection of sediment and

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root samples. DGT technique and RB are designed to reveal the kinetic exchange

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are

in this research, a rhizobox (RB)

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between porewater/solid interface, the mobility and bioavailability of P, Cu, Cd, Pb

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and Zn in macrophyte rhizosphere and the bioaccumulation.

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Specially, three questions are proposed, (i) What is the transfer process

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(diffusion and resupply) at the DGT(root)/porewater/solid phase interfaces? (ii) Does

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DGT-RB technique provide a reliable method to evaluate the uptake kinetics and

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bioaccumulation? (iii) How do pH, dissolved organic carbon (DOC) and dissolved

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organic P (DOP) in rhizosphere sediment solution influence bioavailability?

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■ MATERIALS AND METHODS

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Study Sites and Sediment Pretreatment. The floating flat (Fig. S2-2) for the

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growth of ZL and MV was situated at site 1 in Lake Erhai. Sediments (SE-I and -II)

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and sands (SA-I and -II) for the cultivation in RBs were collected at sites (2-5) (Fig.

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S2-1). After dried, grinded, and sieved using screens (100 or 200 µm for sediment or

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sand, respectively), the SE-I+SA-I or SE-II+SA-II were mixed according to the ratios

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(w/w, dw) in Table S1-1 for the plant growth. The mixed SE+SA samples for ZL or

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MV RBs (n=15) were amended with nitrate stock solutions for Pb, Zn, Cu and Cd

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with the final contents in Table S1-2. Total P contents (TP) in the mixed SE+SA are

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378.4-1486 (ZL) and 102.5-1095 (MV) (mg kg-1 (dw)) (Table S1-2). SE+SA mixtures

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were kept in a dark place to reach equilibrium for one year while maintaining

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approximately 30% water holding capacity before usage. The sub-mixture (SE+SA)

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was kept for analysis. 8


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Rhizobox and Plant Cultivation. The graphics for (i) the cross view of RB and

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the ancillary equipment and (ii) the front view of RB are indicated in Fig. 1 and Fig.

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S3, respectively. RB mainly consisted of a sediment-root compartment (R-zone), a

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bulk sediment compartment (B-zone) and the porous membranes (A-D). The inner

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wall for RB with the diameter of 30 cm was made of PVC material. The membranes

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(B, C and D) prohibited root from penetrating into B-zone. 57 R- or B-zone standed for

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the rhizosphere or bulk sediment, respectively. RB was divided into three layers

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vertically, marked with M, L and K. The L and M layers were filled with the amended

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SE+SA sediments as mentioned in Sect. “Study Sites and Sediment Pretreatment”.

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The holes (P and N) in mesh C were used for the growth of stem and leaf in layer K

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on the top of R-zone or F (the monitor sonde) to measure Eh/pH/temperature in R- or

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B-zone. The other two holes with two plugs (G) in the middle of mesh D and the side

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wall (E) in L layer were used for DGT measurement and sediment sampling in R- and

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B-zones. The detailed inform about RB is indicated in SI A.

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ZL seedling and top shoot of MV were selected from the greenhouse after 14-d 1

and the cuttage method for MV

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germination. Vegetative shoots with roots (ZL)

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were used for each RB. The ZL seedlings (n=15) or top shoots of MV (n=30) with

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little difference in weight and length (RSD0.60

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between DIFS parameters (R-zone) was used to evaluate the effects of the labile pool

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size in solid (kd), resupply ratio (r), kinetic constants such as desorption-sorption

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constant (k-1 or k1), response time (Tc) and sediment properties (Pc and porsed) on the

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diffusion-resupply characters.

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The detailed information about the dependence of the diffusion-resupply on

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DIFS parameters is present in SI C. CDGT and C0 for P and Cu (ZL and MV) were

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controlled by solid properties (porsed and Pc) and the labile pool in solid

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(LS-P1+BD-P2 for P or EXC1 for Cu) (Table S7). The r range (0.25-0.78) in all

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R-zones (ZL and MV) (Table S6) belonged to “partially sustained” case

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(0.10

Transfer Mechanism, Uptake Kinetic Process, and Bioavailability of P

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