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Ecological Engineering 71 (2014) 623–627

Contents lists available at ScienceDirect

Ecological Engineering

jou rn al hom ep age: www.elsev ier .com/ locate /eco leng

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omparative study of Cd tolerance and accumulation potentialetween Cakile maritima L. (halophyte) and Brassica juncea L.

anel Taamalli a,1, Rim Ghabrichea, Taoufik Amaria, Mejda Mnasria, Lello Zollab,tanley Luttsc,d, Chedly Abdelya, Tahar Ghnayaa,∗,1

Laboratoire des Plantes Extrêmophiles, Centre de Biotechnologie de Borj Cédria, BP 901, Hammam-Lif 2050, TunisiaDepartment of Ecological and Biological Sciences, University of Tuscia, Largo dell’Università, snc, 01100 Viterbo, ItalyGroupe de Recherche en Physiologie Végétale (GRPV), Université Catholique de Louvain, Louvain-la-Neuve, BelgiqueEarth and Life Institute, Université Catholique de Louvain, Louvain-la-Neuve, Belgique

r t i c l e i n f o

rticle history:eceived 8 April 2014eceived in revised form 17 July 2014ccepted 8 August 2014vailable online 3 September 2014

eywords:

a b s t r a c t

In this work we evaluated Cd-phytoextraction ability of the halophyte Cakile maritima comparatively tothe glycophyte Brassica juncea commonly recommended for phytoextraction. Seedlings were grown innutrient solution added with 0–100 �M Cd for 21 days. Cd impaired growth in B. juncea but had no sig-nificant impact on C. maritima. The halophyte C. maritima maintained also higher photosynthetic activitythan the glycophyte B. juncea. Cd decreased leaf chlorophyll (Chl) and carotenoids concentrations as wellas PSII efficiency (Fv/Fm, Fv/F0 and ˚PSII) in B. juncea while it increased intercellular CO2 concentration in

−1

. maritima. junceadhytoextractionolerancehotosynthesis

this species. Shoot Cd content was higher in the halophyte C. maritima reaching 1365 �g g dw at 100 �Mwhile it was 548 �g g−1dw in B. juncea at the same dose. The translocation factor (TF) was higher for C.maritima than for B. juncea at all external Cd doses. It is concluded that the halophyte C. maritima couldbe considered as a promising plant material for Cd-phytoextraction.

© 2014 Elsevier B.V. All rights reserved.

maaStmYcaioa2

utrition.

. Introduction

Cd is placed as seventh hazardous substances list as providedy the American Agency for Toxic Substance and Disease Reg-

stry (Kamnev and van der Lelie, 2000). This metal cannot beiodegraded and must be extracted from contaminated soils. Phy-oextracion is less expensive and more environmental friendly thanonventional remediation techniques (Zhang et al., 2013). How-ver, identification of suitable plants for this process is the mostmportant and difficult task.

Plants for this purpose need to combine high Cd tolerancend high Cd accumulation in shoots. Noccaea cerulescens a Cd-yperaccumulator gathers both requisites (Lombi et al., 2000)

ut slow growth and low biomass limit its application in phy-oextraction. The fast growing Brassica juncea, although not ayperaccumualtor, has been found to tolerate considerable shoot

∗ Corresponding author. Tel.: +216 79 325 848; fax: +216 79 325 848.E-mail addresses: Tahar.ghnaya@gmail.com, ghnayatahar@gmail.com,

hnayatahar@gmail.com (T. Ghnaya).1 Both authors Tahar Ghnaya and Manel Taamalli contributed equally to this work.

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ttp://dx.doi.org/10.1016/j.ecoleng.2014.08.013925-8574/© 2014 Elsevier B.V. All rights reserved.

etal concentrations (Sanità di Toppi et al., 2001; Zaier et al., 2010)nd this species is considered as a reference species for Cd toler-nce and accumulation (Mohamed et al., 2012; Sharma et al., 2010;ingh et al., 2007). More recently, it has been suggested that salt-olerant plant species would be more efficient to cope with heavy

etals (Ghnaya et al., 2005; Jordan et al., 2002; López-Chuken andoung, 2005; Zaier et al., 2010), than salt-sensitive (glycophytic)rop plants commonly chosen for phytoextraction. Halophytes areble to sequester Cl− and Na+ in tissues without expressing toxic-ty. Several studies demonstrated that some tolerance mechanismsperating at the whole-plant level are not always specific to sodiumnd could be applied to metals (Lutts et al., 2004; Sousa et al.,008). C. maritma is fast growing halophyte tolerates NaCl up to00 mM (Debez et al., 2004). This species colonizes also heavyetals contaminated saline soils suggesting its tolerance to these

lements.In this work, we conducted to a comparative physiological

tudy to evaluate the potential of Cd tolerance and accumulation

n the halophyte Cakile maritima (Brassicaceae) compared withhat of Brassica juncea. It reports the impact of increasing Cd con-entrations (0–100 �M) on growth, nutrition, photosynthesis andd accumulation in both species. The applied objective of this

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3.4. Cadmium effect on chlorophyll and carotenoid contents

24 M. Taamalli et al. / Ecologica

tudy will be the use of this halophyte to rehabilitate saline Cd-ontaminated soils.

. Materials and methods

.1. Plant material and culture conditions

Seeds of Cakile maritima were harvested from the beach ofaoued (suburb of Tunis). Seeds of Indian mustard (Brassica juncea,ccession no. 426308) were kindly provided by the North Cen-ral Regional Plant Introduction Station of the US Department ofgriculture. The experiments were carried out under glass houseonditions (16 h photoperiod, day/night temperatures of 25/20 ◦Cnd 55/75% relative humidity). After seed germination, seedlingsere transferred to plastic pots filled with 5 L Hoagland’s nutri-

nt solution (pH = 5.8). Two weeks later, plants were randomlyssigned to four different Cd treatments: 0–100 �M CdCl2 during1 days. At harvest, plants were divided into shoots and roots. Rootsere immediately dipped in a cold solution of HCl (0.01 M) during

min to eliminate elements adsorbed at the root surface and thenently blotted with filter-paper (Ghnaya et al., 2007). Fresh weightf organs was immediately measured and the dry one after the des-ccation of shoots and roots at 60 ◦C. The relative growth rate (RGR)

as calculated according to Hunt (1990).

.2. Pigment content

Pigments were extracted by placing 50 mg of fresh leaf in 2 mL of00% acetone. The samples were incubated in darkness until com-lete chlorophyll extraction. Chlorophyll and carotenoids contents

n supernatants were analyzed spectrophotometrically at 644.8,61.6 and 470 nm.

.3. Photosynthetic parameter measurements

.3.1. Leaf gas exchangesThe net photosynthetic rate (Pn), stomatal conductance (gs),

ntercellular CO2 concentration (Ci), transpiration rate (E) andater use efficiency (WUE; defined as the ratio Pn/E) were mea-

ured in the third fully expanded leaf from the top shoot at thend of the treatment. All measurements have been made between1:00 a.m. and 13:00 p.m., at light saturation intensity. Six plantser treatment were assessed using a portable photosynthesis sys-em (LCpro32471, ADC BioScientific).

.3.2. Chlorophyll fluorescenceParameters were recorded in parallel to gas exchange mea-

urements on the same leaf, using a direct portable fluorometer.eaves were acclimated to dark for 20 min before measurementsere taken. After measuring the initial fluorescence (F0), maxi-al fluoroscence (Fm) was determined at the beginning of eacheasurement using a saturating pulse of 9000 � mol m−2 s−1 for

.7 s. The variable fluorescence (Fv) was calculated as Fv = Fm − F0.he maximum PSII quantum yield (Fv/Fm = (Fm − F0)/Fm) and theffective quantum efficiency of PSII (˚PSII = (F′

m − Fs)/F′m) and the

on-photochemical quenching of chlorophyll fluorescence, NPQ =Fm − F′

m)/F′m.

.4. Determination of Cd and mineral elements

Ca, Mg, Fe, Zn and Cd concentrations were measured, after com-

lete mineralization of tissues in 4/1 (v/v) HNO3/HClO4 mixturet 100 ◦C (Ghnaya et al., 2007), by atomic absorption spectro-hotometry (Spectra AA 220 FS, Varian). K concentrations wereetermined in the same homogenate by flame spectrometry and

tm

neering 71 (2014) 623–627

he total nitrogen content in shoots was determined according tojeldahl method.

.5. Statistical analysis

Analyses of variance (ANOVA) with orthogonal contrasts andean comparison procedures were used to detect differences

etween treatments. Mean separation procedures were conductedsing the multiple range tests with Fisher’s least significant differ-nce (LSD) (P < 0.05).

. Results

.1. Effect of Cd on plant morphology and growth

During the first week of treatment, cadmium up to 100 �M didot cause any visible toxicity symptoms in C. maritima while it

nduced chlorosis in B. juncea. After two weeks exposure to 100 �Md, severe chlorosis and leaf abscission was observed in B. juncea.

n C. maritima, leaves howed chlorosis but no abscission occurredven at 100 �M Cd2+.

For all treatments, B. juncea produced more dry matter than C.artima. Cd significantly reduced biomass in B. juncea (Fig. 1A).ontrastingly, Cd had no significant impact on biomass produc-ion in the halophyte (Fig. 1A). The variation of growth activityRGR) in response to shoot Cd accumulation, (Fig. 1B), we demon-trated that in B. juncea Cd sequestered in the shoots reduced RGRrom high 0.14 to low 0.11 irrespective to variation of external Cdoncentration. Nevertheless, despite the higher Cd-shoot concen-ration, growth activity was slightly and insignificantly decreasedn C. maritima (Fig. 1B).

.2. Cadmium accumulation and translocation

Shoot Cd concentrations in both species increased with increas-ng external Cd (Table 1). For all Cd doses, the halophyte C. martimaccumulated much more Cd in the shoots than B. juncea. At00 �M, shoot Cd concentration in C. maritima was three timesigher than in B. juncea (Table 1). The translocation factor (TF),ere higher in C. maritima than in B. juncea at all Cd doses,

Table 1).

.3. Cd effect on nutriment concentrations

Cd induced a drastic decrease in Ca shoot accumulation in B.uncea which accentuated with increasing Cd supply (Table 1). Cahoot concentrations in C. maritima were less affected by Cd andhowed significant decrease only at 100 �M. Mg accumulation wasess affected than Ca and showed a reduction in B. juncea leaves

hen Cd supply exceeded 50 �M. K concentration decreased in thehoots of B. juncea subjected to Cd but no significant effect wasecorded in the halophyte C. maritima. Total nitrogen concentra-ions in the shoots of plant were not affected by Cd in any of thepecies.

Even at the lowest concentration supplied, Cd caused a signif-cant decrease in shoot Fe and Zn concentrations in both speciesTable 1).

Cadmium supply had a strong negative effect on the concen-rations of chlorophylls and carotenoids in B. juncea but not in C.aritima. (Fig. 1C).

M. Taamalli et al. / Ecological Engineering 71 (2014) 623–627 625

Fig. 1. (A) Changes in whole plant dry matter (g plant−1) in by B. juncea and C. maritima treated during 21 days by various CdCl2 concentrations. (B) Relationship betweenthe variations of the RGR values (d−1) and Cd2+ shoot concentrations (�g g−1 DW) in Brassica juncea and Cakile maritima. (C) Variation in Chl a (�g g−1 FW), Chl b (�g g−1 FW)a ssica jo at th

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nd Chl a + b (�g g−1 FW) and carotenoids (�g g−1 FW) contents in the leaves of Braf eight replicates. Different indices indicate that the data are significantly different

.5. Cadmium effect on gas exchange and chlorophylluorescence

Cadmium produced a steep decline in net photosynthetic ratePn) of B. juncea, but not in C. maritime (Table 2). All applied Cdoses decreased stomatal conductance (gs), transpiration rate (E)nd water use efficiency (WUE) in B. juncea leaves (Table 2) whereashese parameters were hardly affected in C. maritima leaves. Inter-ellular CO2 concentration (Ci) was increased by more than 30% in. juncea and remained constant in C. maritima under Cd treatmenthen compared to the control values.

In response to Cd application F0 and Fm decreased to a similarxtent in the leaves of B. juncea as compared to controls (Table 3).owever, in C. maritima F0 and Fm were not affected by Cd. The

v/Fm, ratio significantly declined (P < 0.05) in B. juncea. The Fv/F0atio was more sensitive to Cd than Fv/Fm suggesting that the

hotosynthetic capacity of PSII in B. juncea was strongly reducedy Cd. In C. maritima no effects of Cd on either Fv/Fm or wasbserved Fv/F0 (Table 3). Cd inhibited ˚PSII of B. juncea, but not in. maritima. Unexpectedly, Cd caused significant reduction in the

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able 1d2+, Ca2+, Mg2+, K+, N, Fe2+, Zn2+ concentrations in the shoots and the total amounts of Cdo 0–100 �M Cd in nutrient solution. Values in parenthesis represent translocation factoright replicates ± S.E. Different indices indicate that the data are significantly different at

CdCl2 (�M) Pn E

Brassica0 17.4 ± 0.01a 5.4 ± 0.49a

25 7.7 ± 1.2b 4.8 ± 0.4a

50 5.6 ± 1.3bc 3.4 ± 0.2b

100 6.1 ± 1.2bc 3.6 ± 0.2b

Cakile0 4.7 ± 0.7c 2.5 ± 0.3c

25 4.4 ± 0.5c 2.9 ± 0.3bc

50 4.5 ± 1.2c 2.6 ± 0.2c

100 4.1 ± 0.7c 2.2 ± 0.03c

uncea and Cakile maritime with Cd supply. For all parameters, values are the meane level of P ≤ 0.05.

on-photochemical quenching of fluorescence (NPQ) in B. junceaTable 3) but no significant differences were observed betweenhese values at the three Cd doses in C. maritima leaves.

. Discussion

One major issue in phytoextraction is to select suitable heavyetals accumulator and fast growing species able to remove high

mounts of pollutant from a contaminated substrate.To the best of our knowledge, no report is available regarding

d uptake and tolerance in C. maritima while numerous reportsstimate that B. juncea is an efficient species for Cd extractionBauddh and Singh, 2012; Chigbo and Batty, 2013). The presentork demonstrates that the tested halophyte specie C. maritima

s much more Cd tolerant and accumulates higher shoot Cd con-entrations than B. juncea. This affirmation is based on the analysis

f several well-established physiological markers for Cd toxicitydopted in many previous work as: RGR, chlorophyll concentra-ion (Molnárová and Fargasová, 2012; López-Millán et al., 2009),nhibition of photosynthesis (Baryla et al., 2001), water relations

extracted in the shoots of Brassica juncea and Cakile maritima exposed for 21 days (TF = shoot metal concentration/root metal concentration). Values are the mean of

the level of P ≤ 0.05. n.d.: not detected.

gs WUE Ci

0.32 ± 0.04a 3.2 ± 0.3a 237.6 ± 5.5d0.26 ± 0.02b 1.69 ± 0.2bc 309.2 ± 11.5a0.14 ± 0.01 cd 1.72 ± 0.5bc 316.6 ± 7.2a0.15 ± 0.01c 1.85 ± 0.24bc 308.6 ± 3.9ab

0.14 ± 0.01 cd 2.53 ± 0.07ab 269.8 ± 11.8c0.11 ± 0.01 cd 1.64 ± 0.1bc 291.7 ± 6.1abc0.10 ± 0.01de 1.55 ± 0.5c 281.2 ± 6.7bc0.08 ± 0.01e 1.86 ± 0.3bc 267.4 ± 17.3c

626 M. Taamalli et al. / Ecological Engineering 71 (2014) 623–627

Table 2Effect of Cd on gas exchange parameters: net photosynthetic rate (Pn, �mol CO2 m-2 s-1), transpiration rate (E, mmol H2O m-2 s-1), stomatal conductance (gs, mmol H2O m-2

s-1), water use efficiency (WUE, �mol CO2 mmol H2O) and intercellular CO2 concentration (Ci, �mol CO2 mol air-1) measured on the third fully expanded leaves in plants ofBrassica juncea and Cakile maritima exposed for 21 days to 0–100 �M. Values are the mean of five replicates ± S.E. Different indices indicate that the data are significantlydifferent at the level of P ≤ 0.05.

CdCl2 (�M) Fo Fm Fv/Fm Fv/Fo QPSII NPQ

Brassica0 443 ± 11a 2285 ± 93a 0.8 ± 0.0a 4.04 ± 0.2a 0.69 ± 0.02a 2.78 ± 0.6a25 350 ± 33b 1328 ± 137b 0.75 ± 0.02ab 3.01 ± 0.2bc 0.64 ± 0.01ab 1.29 ± 0.4b50 366 ± 14ab 1276 ± 40b 0.62 ± 0.08c 1.97 ± 0.5de 0.61 ± 0.03b 1.36 ± 1.1b100 386 ± 92ab 1366 ± 79b 0.65 ± 0.08bc 1.47 ± 0.3e 0.62 ± 0.05b 1.30 ± 0.4bCakile0 324 ± 14b 1463 ± 28b 0.77 ± 0.03a 3.43 ± 0.4ab 0.68 ± 0.01a 0.72 ± 0,08b25 359 ± 12b 1329 ± 89b 0.73 ± 0.02ab 2.7 ± 0.2bcd 0.66 ± 0.01ab 0.61 ± 0,09b50 385 ± 43ab 1358 ± 180b 0.72 ± 0.01abc 2.52 ± 0.2 cd 0.63 ± 0.01ab 0.73 ± 0,19b100 362 ± 26b 1413 ± 88b 0.74 ± 0.03ab 2.84 ± 0.4bc 0.65 ± 0.02ab 0.45 ± 0,07b

Table 3Cd effect on chlorophyll fluorescence parameters: initial fluorescence (F0), maximal fluoroscence (Fm), maximum efficiency of PSII (Fv/Fm), variable chlorophyll fluorescenceratio (Fv/F0), the effective quantum efficiency of PSII (˚PSII), and non-photochemical quenching (NPQ) measured at the end of the experiment on the third fully expandedleaves in plants of Brassica juncea and Cakile maritima exposed for 21 days to 0–100 �M Cd. Values are the mean of five replicates ± S.E. Different indices indicate that thedata are significantly different at the level of P ≤ 0.05.

CdCl2(�M) 0 25 50 100

Cd concentration �g/g DWBrassica n.d. 389.1 ± 36d (0.13b) 425.3 ± 24 cd (0.08bc) 547.6 ± 47c (0.06c)Cakile n.d. 472.9 ± 53 cd (0.3a) 905.5 ± 78 (0.28a) 1365.2 ± 206a (0.29a)Cd content (�g/plant)Brassica n.d. 130 ± 11b 130 ± 11b 150 ± 14bCakile n.d. 133 ± 33b 187.± 32b 262 ± 62a

Ca2+ mg/g DWBrassica 23 ± 3.8c 19 ± 4.1d 18 ± 1.9d 11 ± 2.6eCakile 45 ± 4.2a 36 ± 6.0ab 32 ± 3.5ab 27 ± 2.6cMg2+ (mg/g DW)Brassica 47 ± 5.9a 49 ± 6a 35 ± 6.1b 32 ± 4.5bCakile 30 ± 3.7bc 35 ± 5.6abc 32 ± 4.8bc 34 ± 3.6bc

K+ mg/g DWBrassica 56 ± 4.9a 45 ± 3b 38 ± 3.9bc 40 ± 1.9bcCakile 55 ± 1.5a 54 ± 2.3a 54 ± 2.4a 54 ± 1.9aN (mg/g DW)Brassica 41 ± 1.9c 40 ± 2.7c 39 ± 0.9bc 37 ± 3.4bcCakile 48 ± 2.7ab 51 ± 3.2a 50 ± 0.8ab 46 ± 1.2abFe2+ (mg/g DW)Brassica 0.56 ± 0.07a 0.38 ± 0.08c 0.24 ± 0.02d 0.3 ± 0.09dcCakile 0.60 ± 0.01a 0.47 ± 0.03ab 0.49 ± 0.04ab 0.45 ± 0.02abc

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Zn (mg/g DW)Brassica 0.16 ± 0.02a 0.08 ± 0.01b

Cakile 0.14 ± 0.03a 0.09 ± 0.01b

Poschenrieder et al., 1989) and nutrient deficiency (Ghnaya et al.,007; Mohamed et al., 2012). All these processes were considerablyffected by Cd in B. juncea while C. maritima was hardly affected.his considerably higher Cd tolerance in C. maritima clearly was notelated to better Cd exclusion. On the contrary, the halophyte accu-ulated higher shoot Cd concentrations than B. juncea suggesting

hat the tested halophyte plant is equipped with an efficient systemf free Cd2+ detoxification allowing the preservation of photosyn-hesis and nutrients acquisition.

The comparison of the metal extraction potential based on themounts of metal accumulated in the shoots, which is the productf metal concentration by the produced biomass, showed that dueo its high potential to accumulate Cd and to maintain biomass,. maritima is more efficient than B. juncea for Cd-phytoextractionTable 1). The superiority of halophytes to tolerate and accumulatearious heavy metals comparatively to glycophyte was shown ineveral works (Jordan et al., 2002; Shevyakova et al., 2003; Zaiert al., 2010). In fact, since Thomas et al. (1998) demonstrated that

he halophyte Mesembryanthemum crystallinum was more efficiento tolerate and absorb Cu than Arabidopsis thaliana, the num-er works devoted to phytoremediation of metal contaminatedoils using halophyte increased (Ben Rejeb et al., 2013; Ghnaya

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0.07 ± 0.00bc 0.08 ± 0.02b0.07 ± 0.00bc 0.09 ± 0.02b

t al., 2005; Zaier et al., 2010). It has been postulated that halo-hytes species recruit non-selective salt-resistance mechanismso sequester toxic ions in the vacuole and/or salt glands or tri-homes (Lutts et al., 2004). Metal deposit in the cell walls as aesult of binding to pectic compounds could be also considered asn important mechanism for metal detoxification in halophytes,s demonstrated in Halimione portulacoïdes (Sousa et al., 2008).hus, evaluation of ion distribution within tissues and even cellsf C. maritima should enable us to get a better understanding of thed-tolerance mechanisms in this species.

Hence, we concluded that the halophyte C. maritima is more tol-rant to Cd than B. juncea. C. maritima was able to maintain growthnd photosynthesis despite high levels of Cd accumulation in thehoots. Regarding Cd accumulation, C. maritima can be considereds a Cd accumulator and can be used in Cd-phytoextraction. Fur-her research is needed to obtain information about the metabolicasis for Cd tolerance and accumulation of this species.

cknowledgements

This work was supported by the Tunisian Ministry ofigher Education and Scientific Research (LR10CBBC02). Seeds of

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rassica juncea acc. 426308 were kindly provided by the North Cen-ral Regional Plant Introduction Station (NCRPIS), of USA.

The authors thank Professor Charlotte POSCHENRIEDER fromhe Departamento de Fisiologia Vegetal, Facultad de Ciencias, Uni-ersidad Autonoma de Barcelona, E-08193 Bellaterra, Spain foraluable advice, critical reading of the manuscript and Englishmprovement.

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