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Cadmium localization and quantification

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Cadmium localization and quantification

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Cadmium localization and quantification in the plant

Arabidopsis thaliana using micro-PIXE

F.J Ager a,*, M.D Ynsa a, J.R Domıınguez-Solııs b, C Gotor b,

a

Centro Nacional de Aceleradores, Av Thomas A Edison s/n, E-41092 Sevilla, Spain

b

Instituto de Bioquıımica Vegetal y Fotosııntesis, Av Am eerico Vespucio s/n, E-41092 Sevilla, Spain

Abstract

Remediation of metal-contaminated soils and waters poses a challenging problem due to its implications in the environment and the human health The use of metal-accumulating plants to remove toxic metals, including Cd, from soil and aqueous streams has been proposed as a possible solution to this problem The process of using plants for environmental restoration is termed phytoremediation Cd is a particularly favourable target metal for this technology because it is readily transported and accumulated in the shoots of several plant species This paper investigates the sites

of metal localization within Arabidopsis thaliana leaves, when plants are grown in a cadmium-rich environment, by making use of nuclear microscopy techniques Micro-PIXE, RBS and SEM analyses were performed on the scanning proton microprobe at the CNA in Seville (Spain), showing that cadmium is sequestered within the trichomes on the leaf surface Additionally, regular PIXE analyses were performed on samples prepared by an acid digestion method in order

to assess the metal accumulation of such plants Ó 2002 Published by Elsevier Science B.V

PACS: 89.60; 78.70.E; 82.80.Yc

Keywords: Arabidopsis; Cadmium accumulator; Phytoremediation; Nuclear microprobe; PIXE

1 Introduction

The ability of certain terrestrial plants to absorb

and accumulate metals such as cadmium, nickel,

zinc, manganese, copper or cobalt makes them very

attractive when the decontamination of soils is

sought These plants are called metal

hyperaccu-mulators [1] if they accumulate for instance more

than 0.01% of Cd, 0.1% of Ni or 1% of Zn per dry

weight in their shoots in a natural environment However, the mechanisms for metal uptake, trans-location and compartmentation are not yet well understood and in the past recent years an im-portant effort has been made in this direction From the practical point of view, the comprehen-sion of those mechanisms will probably lead to the enhancement of metal absorption by means of plant hybridation or by producing new transgenic plants for environmental remediation purposes For example, genetic engineering of Arabidopsis tha-liana plant has been demonstrated to be a useful technique to improve heavy metal tolerance by phytoremediation purposes [2]

www.elsevier.com/locate/nimb

*

Corresponding author Tel.: 954460553; fax:

+34-954460145.

E-mail address: fjager@us.es (F.J Ager).

0168-583X/02/$ - see front matter Ó 2002 Published by Elsevier Science B.V.

PII: S 0 1 6 8 - 5 8 3 X ( 0 1 ) 0 1 1 3 0 - 2

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There is evidence that trichomes on the leaf

surface may play a role in the detoxification of

heavy metals [3] In Alyssum lesbiacum [4]

micro-PIXE analysis proved that epidermal trichomes

represent a site of preferential nickel

accumula-tion In A thaliana, trichomes are specialized

uni-cellular structures with uncertain functions, but

recent works suggest their possible role as a sink

during detoxification processes [5]

The nuclear microprobe allows investigators to

obtain quantitative or semi-quantitative elemental

distribution maps of major and trace elements

with high resolution and sensitivity, and is

be-coming a useful tool for localizing the sites of

el-ement accumulation in a wide variety of studies

In the present study we used the scanning

nu-clear microprobe to determine the elemental

con-centrations and the sites of preferential Cd

accumulation within A thaliana leaves in plants

grown in Cd-enriched soils Regular PIXE analysis

was also performed to evaluate the Cd

accumula-tion in the plant leaves

2 Materials and methods

2.1 Plant material

Wild type A thaliana (ecotype Columbia)

plants were grown, in a controlled environment

room, on moist vermiculite supplemented with

Hoagland medium at 20°C in the light and 18 °C

in the dark, under a 16-h white light/8-h dark

photoperiod with a photon flux density of 130 lE/

m2s and 70% humidity

Cadmium chloride treatments were performed

by addition to the Hoagland medium of CdCl2to

250 and 2500 lMfinal concentration The plants

were daily watered with this medium during 14

days

2.2 Sample preparation for analysis

In order to minimise the possibility of ion

mo-bilisation, plant leaves were cut off from living

plants taken directly from the growth chamber,

rinsed briefly in deionised water, dried,

immedi-ately frozen at 80°C in an ultralow temperature

freezer (mod Nuaire NU-6511) and then freeze-dried for 72 h at 50 °C at a pressure of 10 3

mbar After this preparation, two different treat-ments were used depending on the subsequent analysis procedure

Leaves for macrobeam analysis were prepared

by microwave acid digestion Plant material (100 mg) was digested in a Teflon bomb in a solution of HNO3 and Y as internal standard, following standard procedures [6] For elemental analysis, a

10 ll volume of the resulting solution was pipetted

on a polycarbonate film and dried in vacuum Leaves for microbeam analysis were mounted

on carbon tape on a standard aluminium frame and just placed on the sample holder inside the microprobe target chamber (pres 10 7mbar) 2.3 Instrumentation and analytical methods The microbeam analyses were performed with 3.0 MeV protons focused to a 3 3 lm beam normal to the sample with a proton current of 100–

300 pA, using the CNA scanning nuclear microp-robe [7] PIXE, backscattering spectrometry and electron imaging were carried out simultaneously PIXE spectra were collected using a Si(Li) X-ray detector manufactured by Canberra at 45° to the beam, with a 12.5 mm2 active area, 8 lm Be re-movable window and a 50 lm Mylarâfilter to at-tenuate X-rays from light elements The distance from the detector to the sample was chosen to be 40

mm in order to keep good counting statistics with

Table 1 PIXE analysis of A thaliana leaves treated with CdCl 2 (250 lM) prepared by microwave acid digestion

Element Concentration (ppm)

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low pile-up background and dead time

Backscat-tered protons were detected using a surface barrier

detector of an active area of 300 mm2at an angle of

37° to the beam, in Cornell geometry Emitted

electrons were detected using a channeltron

detec-tor An electron gun generating 50 mA was used to

avert electrostatic charging of the insulating

bio-logical material All signals were recorded together

with the beam position using the OM_DAQ data

acquisition system [8]

Macro-PIXE analyses were performed with a

2.4 MeV proton beam from the 3 MV Van de

Graaff accelerator of the ITN (Portugal), colli-mated up to 5 mm diameter with a current of 100

nA and a total accumulated charge of 100 lC The incoming proton beam angle was 15° X-rays were detected with a Linke Si(Li) detector at an angle

of 55°, 8 lm Be window, a 350 lm Mylarâ filter and a 2.7 mm diameter collimator placed in front

of the detector specially for improvement of the line shape

Data analysis was carried out using GUPIX [9] for PIXE spectra and RUMP [10] and SIMNRA [11] for RBS spectra

Fig 1 PIXE elemental maps of a leaf edge of an Arabidopsis plant grown in CdCl 2 (250 lM), showing Ca, K, P, Si, Mn and Fe Area

of scan is 100  100 lm 2 The maps correspond to two consecutive scans so that the lower right end of the first row of elements coincides with the central area of the second row.

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3 Results and discussion

Macro-PIXE analysis of plant leaves treated

with CdCl2 (250 lM) and prepared by acid

di-gestion in microwave oven gives a Cd

concentra-tion of 0:024 0:006 wt.% as shown in Table 1

Micro-PIXE elemental maps and point analyses

of different leaves were recorded Si, P, S, Cl, K,

Ca, Fe, Mn, Zn and Cd were all detected by PIXE

For Cd-treated leaves, Cd mapping is unpractical

because of the long acquisition times needed for

this purpose However, once the leaf structure is

known by means of the other maps (electron

imaging, Ca, K, etc.), those maps can be

comple-mented with analyses at selected points or regions

of interest

Fig 1 shows elemental maps (side view,

100 100 lm2) of a leaf of an Arabidopsis plant

grown in CdCl2(250 lM) Thus, the trichome can

be divided in three different areas according to

their composition: the base, richer in Si, K and P; a

central zone, richer in metals such as Mn and Fe;

and the head, richer in Ca The main elements

detected in the leaf are K, S, Ca and Cl (not shown

in Fig 1)

A front view of a trichome emerging from the

leaf surface is presented in Fig 2 (250 250 lm2),

showing the typical impact points for analysis in trichome (T) and leaf (L)

Cd concentration can be ideally computed from the Kaline of the PIXE spectrum because it lies in

a very clean region far from other peaks and from pile-up effects from the main detected elements (Ca, K, etc.) Fig 3 depicts the Cd contents found

by PIXE microanalysis in different leaves Cad-mium is present in both trichome and leaf, but the

Fig 2 Secondary electron image and maps of elemental distribution of Ca, K, Cl, P and Mn (250  250 lm 2 ) of a leaf of Arabidopsis grown in CdCl 2 (2500 lM) The image corresponds to a front view of a trichome emerging from the leaf surface The typical impact points for analysis in trichome (T) and leaf (L) are presented.

Fig 3 Bar chart of cadmium contents obtained by PIXE mi-croanalysis in A thaliana leaves Question marks indicate points where there is no data available Error bars are also shown.

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highest amount of Cd is found in the trichomes.

For plants treated with CdCl2 (250 lM), Cd was

detectable in the trichomes but it required a high

integrated charge in order to be quantified with

low errors To circumvent this difficulty, a higher

Cd dose (2500 lMCdCl2) was used This

treat-ment would result in the increase of the metal

uptake by the plant and the enhancement in the

Cd concentration in the plant tissues In effect,

analyses show that Cd concentration in leaf

epi-dermis and trichome is increased when the plants

are treated with CdCl2 (2500 lM), although the

growth was affected by such toxic levels of Cd

(smaller plants with shorter purplish leaves) The

Cd content also depends on the point of analysis

and the orientation of the trichome, being higher

when the trichome is analysed in the head with the

ion beam coming from its growth direction

4 Conclusions

The preliminary results presented in this study

suggest that Cd is preferentially accumulated in

the epidermal trichomes of the cadmium

accumu-lator plant A thaliana However, further analyses

are being performed at present to establish the

distribution of Cd along the trichomes, because

there are evidences [2,5] that the base could

con-centrate even more Cd than the head or the stem

This work also contributes to progress in the

decontamination of metal polluted soils by means

of phytoremediation techniques Present

investi-gations by the same authors are also aimed at

comparing the wild variety of A thaliana with

ge-netically modified specimens produced to be more resistant to heavy metal contamination

Acknowledgements

We thank Dr Teresa Pinheiro for her assistance during the preparation and analysis of samples at the ITN

References

[1] R.R Brooks, B.H Robinson, in: R.R Brooks (Ed.), Plants that Hyperaccumulate Heavy Metals, CAB Inter-national, Wallingford, UK, 1998.

[2] J.R Domıınguez-Solııs, G Guti eerrez-Alcal a a, L Romero,

C Gotor, J Biol Chem 276 (2001) 9297.

[3] H K€ u upper, E Lombi, F.J Zhao, S.P McGrath, Planta

212 (2000) 75.

[4] U Kr€ a amer, G.W Grime, J.A.C Smith, C.R Hawes, A.J.M Baker, Nucl Instr and Meth B 130 (1997) 346.

[5] G Guti eerrez-Alcal a a, C Gotor, A.J Meyer, M Fricker, J.M Vega, L.C Romero, Proc Natl Acad Sci USA 97 (20) (2000) 11108.

[6] M Stoeppler, Sampling and Sample Preparation, Springer, Berlin, 1997.

[7] J Garcııa L o opez, F.J Ager, M Barbadillo Rank, M  A A Ontalba, M  A A Respaldiza, M.D Ynsa, Nucl Instr and Meth B 161–163 (2000) 1137.

[8] G.W Grime, M Dawson, Nucl Instr and Meth B 104 (1995) 107.

[9] J.A Maxwell, J.L Campbell, W.J Teesdale, Nucl Instr and Meth B 43 (1989) 218.

[10] L.R Doolitle, Nucl Instr and Meth B 9 (1985) 344 [11] M Mayer, SIMNRA User’s Guide, Technical Report IPP 9/113, Max-Planck-Institut f€ u ur Plasmaphysik, Garching, Germany, 1997.

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