phytoremediation capacity of populus and salix

8/10/2019 Phytoremediation capacity of Populus and Salix

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IN RODUC ION

As environmental restoration of metal-pollutedsoils by traditional physical and chemical meth-ods demands large investments of economic andtechnological resources, efforts are underway toinvolvein situ methods in environmental protection.Phytoremediation is an emerging technology whichutilizes plants and rhizosphere microorganisms toremove and transform toxic chemicals in soils,sediments, ground water, surface water, and theatmosphere (Kumar et al., 1995; Susarla et al., 2002;Ghosh and Singh, 2005; Pajevi et al., 2008). Heavymetal accumulation by plants is useful as a phyto-extraction technique in phytoremediation, whichrefers to the use of plants that can extract and movecontaminants to their harvestable parts (Marchiol etal., 2004). he efficiency of phytoextraction dependson the metal bioavailability, as well as on severalcharacteristics of the plant-remediator: fast growth,a deep and extended root system, the capability of

(hyper)accumulating essential and unessential met-

als, and the ability to translocate metals to the aerialparts (Zacchini et al., 2008).

Over the last few years, metal-accumulatingwoody species have been considered for phytoex-traction of metal-contaminated sites (Greger andLandberg, 1999; Rosselli et al., 2003; Dickinson andPulford, 2005).

Apart from cleaning the environment, anotheradvantage of using forest plants in this technol-ogy is their high production of biomass, which caneventually be used in producing energy (Laureysenset al., 2004). Fast growing, high biomass-producingwoody plants that tend to accumulate metals in aer-ial tissues could be a source for the development offeasible phytoextraction technology (Unterbrunneret al., 2007).

Much attention has been paid to the study ofwater use efficiency (WUE) in order to dene the

interdependence of water balance and biomass pro-

PHYTOREMEDIATION CAPACITY OF POPLAR POPULUS SPP.AND WILLOW SALIX SPP. CLONES IN RELATION TO PHOTOSYNTHESIS

SLOBODANKA PAJEVI1, M. BORIEV1, NA AA NIKOLI1, B. KRS I1,A. PILIPOVI2, and S. ORLOVI2

1Department of Biology and Ecology, Faculty of Science, University of Novi Sad,21000 Novi Sad, Serbia2Institute of Lowland Forestry and Environment,21000 Novi Sad, Serbia

Abstract Good photosynthetic features and a favorable water regimes of woody plants improve their survival and reme-diation potential under unfavorable ecological conditions. Accordingly, we here present results of testing plant toleranceof Pb, Cd, Ni, and diesel fuel based on gas exchange parameters and WUE of four poplar and two willow clones grown ina greenhouse on soil culture. Photosynthesis and transpiration of plants grown on soils with individually applied heavymetals decreased significantly, but this was less obvious in the case of Cd treatment. A heavy metal mixture in the soilinduced significant reduction in photosynthesis (by more than 50%). Diesel fuel as the only pollutant in soil caused verystrong and significant inhibition of photosynthesis and transpiration of willow clones. he results indicate genotypicspecificity of all investigated physiological parameters and mark poplar clones as very useful in phytoextraction technol-ogy for the bio-cleaning of chemically polluted soils.

Key words : Poplar, willow, photosynthesis, transpiration, WUE, phytoremediation, heavy metals

UDC 581.132:58

239

Arch. Biol. Sci., Belgrade, 61 (2), 239-247, 2009 DOI:10.2298/ABS0901239P


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S. PAJEVIE AL.240

duction and detect genotypes which consume lesswater during efficient and productive photosynthe-sis (Orlovi et al., 2002; Martin and Stephens, 2006).Genotype adaptive values should be expressed inhigh photosynthetic potential, relatively high andstabile WUE, and high biomass production with highaccumulation of pollutants (heavy metals in particu-lar) in tissue. In this sense, the aim of breeding pro-grams is to produce cultivars (clones) characterizedby superior growth and resistance to high levels ofpollutants, which have to be extracted from the soiland translocated to aboveground plant parts.

he aim of this investigation was to quantify thephotosynthetic capacity of four poplar clones andtwo willow clones growing on soil contaminated byheavy metals and diesel fuel during the early grow-ing period. A relatively high photosynthesis/transpi-ration ratio on contaminated soil would distinguishgenotypes with high adaptive potential in a contami-nated environment, high biomass production, andhigh phytoextraction capacity.

MA ERIAL AND ME HODS

he experimental material consisted of four poplarand two willow genotypes ( able 1).

Genotypes were obtained from the Institute of were obtained from the Institute ofLowland Forestry and Environmental Protection,Novi Sad, Serbia. he genotypes chosen for screen-ing are the result of a long period selection of genesthat cause high biomass production.

he experiment was set in May of 2008. Plantswere grown in a semi-controlled environment

(greenhouse) by the soil culture method. emperaturewas kept under 30C. Illumination was natural and

dependent on the outside light conditions. Sixwoody cuttings, 20 cm long with one shoot percutting, were grown in each of several Mitscherlichpots. Each treatment consisted of 24 poplar and 36willow cuttings. Pot distribution was randomized.he soil was watered constantly to maintain optimalsoil humidity. Every four weeks, 0.2 l of full-strength-strengthHoagland solution was added to the pots. heheexperiment included a control group of plants andsix treatments of pollution: Pb, Cd, Ni, Pb+Cd+Ni,diesel fuel, and diesel fuel+Pb+Cd+Ni. he con-centrations of metals in the soil in individual metaltreatments were: Pb - 360.35 mg/kg, Ni - 205.37 mg/kg, and Cd - 8.14 mg/kg. In combined metal treat-ments, the concentrations were: Pb - 382.29 mg/kg,Ni - 185.25 mg/kg, and Cd - 1.34 mg/kg. otal soilhydrocarbon content in diesel treatment was 9.825g/kg of dry soil. Concentration of metals in the soilof dry soil. Concentration of metals in the soilwas achieved using aqueous metal solutions. hehemetals used were Cd (10-4 M and 10-5 M, suppliedas CdCl2H2O), Ni (10-4 M and 10-5 M, supplied asNiSO46 H2O), and Pb (10-4 M and 10-5 M, suppliedas Pb-EDA). Photosynthesis and transpirationPhotosynthesis and transpiration

were measured in June of 2008, after 42 days oftreatment.

Photosynthesis and transpiration were measuredusing the LCpro+ portable photosynthesis system,manufactured by ADC BioScientific Ltd. Light con-ditions were set using the LCpro+ light unit, whichemitted photosynthetically active radiation (PAR) at1000 mol m-2 s-1. he air supply unit provided aflow of ambient air to the leaf chamber at a constantrate of 100 mol s-1. emperature, CO2 concentra-tion, and humidity were at ambient levels.

Parameters of chlorophyll fluorescence induc-

Table 1. Poplars and willows used in the experiment.

No. Species Working name1 Populus x euramericana Panonia2 Populus deltoides PD 33 Populus deltoides B 814 Populus deltoides B 2295 Salix alba V 16 Salix alba V 2


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PHY OREMEDIA ION IN POPLAR AND WILLOW CLONES IN RELA ION O PHO OSYN HESIS 241

tion kinetics were measured using a PSM fluorim-eter (BioMonitor) from middle-leaf parts adapted todarkness (quist and Wass, 1988). After illumina-tion by saturated red light, the values of minimalfluorescence (Fo), maximal fluorescence (Fm), andpotential quantum yield: (Fm-Fo)/Fm (also definedas Fv/Fm), were determined.

Parameter WUE (water use efficiency) was cal-culated as the ratio of photosynthesis to transpirationand expressed in moles of CO2 m-2 s-1/mmolesof H2O m-2 s-1.

Stomatal conducance of water vapor was mea-sured automaticallyin vitro and expressed in molesof H2O m-2 s-1.

Statistical analyses were conducted usingDuncans multiple range test at a significance level ofp


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S. PAJEVIE AL.242

for plants grown on Ni and diesel fuel+Pb+Cd+Ni.his genotype ofPopulus x euramericana (Panonia)can be singled out on the basis of photosynthet-ic capacity as suitable for phytoextraction of Cdand diesel fuel in single contamination treatmentsbecause in these conditions it had stable and rela-tively high photosynthesis ( ables 2 and 3). he B229 Populus deltoides genotype showed the lowestphotosynthesis and had the lowest remediationpotential because all applied treatments induced adecrease of photosynthesis for more than 60%.

he registered photosynthetic activities of wil-low clones were lower than those of poplar clones,average values for the control plants being 6.88moles of CO2 m-2 s-1(Salix alba - V 1) and 5.92moles of CO2 m-2 s-1 (Salix alba - V 2). As inpoplar clones, the most obvious inhibitory effect

on photosynthesis in willow clones was detectedfor diesel fuel+Cd+Ni+Pb and heavy metal mix-ture treatments. Willow genotypes were definedas unsuitable for phytoextraction of diesel becausetheir photosynthetic rates were very low, belowthe level of registration. o judge from the resultsobtained on photosynthetic activity, willow cloneV 1 could be used for remediation of Ni from soilpolluted with this heavy metal. Excessive concentra-tions of Cd in the soil had the lowest effect on pho-tosynthesis of almost all of the investigated poplar

and willow clones ( able 2).he relatively stable values of chlorophyll fluo-

rescence parameter Fv/Fm in polluted conditionsindicated stability of thylakoid structure and elec-tron flow through the photosystems ( able 3).

Table 3. Chlorophyll uorescence parameter Fv/Fm in poplar and willow leaves.

Poplar genotypes Willow genotypes Species/ clones

reatment

Populusx euramericana -

Panonia

Populus deltoides - PD 3

Populus deltoides - B 81

Populus deltoides - B 229 Salix alba- V 2

Salix alba- V 1

Pb 0.753 a 0.707 a 0.681 b 0.694 ab 0.732 a 0.742 aCd 0.708 a 0.714 a 0.711 ab 0.747 a 0.745 a 0.741 aNi 0.753 a 0.765 a 0.747 ab 0.731 ab 0.726 a 0.739 aPb+Cd+Ni 0.732 a 0.742 a 0.735 ab 0.739 ab 0.692 a 0.691 abDiesel fuel 0.754 a 0.736 a 0.764 a 0.724 ab 0.660 ab 0.632 bD.f.+Metals 0.754 a 0.719 a 0.551 c 0.695 ab 0.587 b 0.628 bControl 0.711 a 0.752 a 0.717 ab 0.677 b 0.736 a 0.743 aLSD0.05 0.063 0.063 0.063 0.063 0.089 0.063

Table 4. Rate of transpiration in poplar and willow leaves (mmoles of H 2O m-2 s-1).


reatment


PanoniaPopulus deltoides

- PD 3Populus deltoides

- B 81Populus deltoides

- B 229Salix alba- V 2

Salix alba - V 1

Pb 1.02 bc 0.74 b 0.73 bc 0.97 b 0.72 c 0.75 bCd 1.53 ab 1.62 a 1.62 a 1.15 b 0.83 bc 0.61 bcNi 0.84 c 1.56 a 1.39 abab 0.96 b 1.11 ab 0.50 cPb+Cd+Ni 0.85 c 0.77 b 1.69 a 0.74 b 0.69 c 0.63 bcDiesel fuel 1.91 a 1.63 a 1.75 a 0.00 c 0.00 d 0.00 dD.f.+Metals 1.07 bc 0.00 c 0.25 c 0.00 c 0.00 d 0.00 dControl 1.78 a 2.21 a 1.95 a1.95 a 8.87 a 1.41 a 1.11 aLSD

0.05 0.64 0.62 0.68 0.65 0.32 0.18


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Photosynthetic light reactions and electrontransport through PSII were disturbed the most inboth willow clones and poplar clone B 81 in soiltreated with diesel fuel and all metals ( able 3).

ranspiration rates measured on the youngestleaves were similar in poplar clones and rangedfrom 2.37 mmoles of H2O m-2 s-1 (clone B 229)to 1.78 mmoles of H2O m-2 s-1 (clone Panonia).Statistical analysis showed a very similar pollutioneffect on transpiration of different clones ( able 4).As in the case of the photosynthetic rate, clone B

229 exhibited the lowest transpiration rate in pol-luted conditions, especially pollution with dieselfuel+metals, which distinguished it as the genotypewith the lowest remediation potential.

he investigated willow genotypes showed sig-nificant metabolic disturbance in conditions of pol-lution: their photosynthetic and transpiration rateswere very low (below the registration level) in soilpolluted with diesel fuel and heavy metals ( able 4).

Stomatal conductance of water vapor in leaves

of poplar and willow clones was in correlation withtranspiration rates. Inhibition of stomatal conduc-tance in plants grown under conditions of soil con-tamination indicated that depression of photosyn-thesis and transpiration occurred to a great extent atthe stomatal level.

Water use efficiency (WUE) is a good economicindicator of bioproduction per unit of water volume

consumed, and we expressed it as the photosynthe-sis/transpiration ratio ( able 5).

he results obtained on WUE of poplar clonesindicated that diesel fuel and diesel fuel+metals inthe soil significantly disturbed water consumptionby the plants and consequently their photosyntheticorganic production ( able 5). he Panonia and B 81genotypes showed very stable WUE during growthin polluted soil, and only treatment of soil with dieselfuel and a metal mixture together provoked severedepression of WUE in genotype B 81. Stable WUE

values in unfavorable environmental conditionsis sign of high organic production and indicates agood remediation potential of those genotypes inwhich they are recorded.

Willow clone V 2 grown in contaminated soilsshowed signicantly lower WUE in contaminatedsoil compared to V 1 and other poplar genotypes,which distinguishes it as the least suitable for phyto-extraction and remediation.

DISCUSSION

here are many forest localities that are pollutedby heavy metals originating from atmospheric depo-sition of industrial and traffic emissions. Soil pollu-tion with heavy metals has been found to decreaseforest biomass productivity. A very useful ecologicalsolution for cleaning contaminated forest areas andobtaining high biomass (wood) production is grow-ing plant species that have a good heavy metal accu-

Table 5. Rate of transpiration in poplar and willow leaves (mmoles of H 2O m-2 s-1).


reatment


PanoniaPopulus deltoides

- PD 3Populus deltoides

- B 81Populus deltoides

- B 229Salix alba

- V 2Salix alba

- V 1

Pb 5.09 ab 6.16 a 5.36 a 5.32 a 4.69 a 3.59 bCd 5.16 ab 5.50 ab 5.25 a 4.42 ab 4.04 a 3.88 bNi 4.60 ab 4.97 ab 4.25 a 3.91 b 4.47 a 2.92 bPb+Cd+Ni 4.28 ab 3.85 b 4.44 a 1.24 c 1.53 b 1.71 cDiesel fuel 3.88 b 4.08 b 3.84 a 0.00 c 0.00 c 0.00 dD.f.+Metals 4.08 ab 0.00 c 0.45 b 0.00 c 0.00 c 0.00 dControl 6.15 a 4.17 b 4.31 a 3.78 b 4.90 a 5.48 aLSD0.05 1.96 1.68 1.52 1.30 1.19 1.06


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mulation capacity on contaminated soils. he heavymetal-accumulating plantsPopulus sp. andSalix sp.have been suggested for phytoremediation by manyauthors (Robinson et al., 2000). Poplar trees repre-sent one vegetation option for phytostabilizationof heavy metal-contaminated sites and can be usedfor the in situ decontamination of polluted soils.Rosselli et al. (2003) found thatSalix and Betulatransferred zinc and cadmium to leaves and twigs,but Alnus, Fraxinus, and Sorbusexcluded them fromtheir aboveground tissues.

As good heavy metal-remediators are needed inorder to obtain high biomass production and inten-sive plant growth, it is of great interest to establishwhether their photosynthetic features improve theirsurvival and growing potential under unfavorable(polluted) ecological conditions. Defining CO2 pho-tosynthetic assimilation of different woody speciesis important in order to choose genotypes suitablefor phytoremediation breeding programs. Heavymetal uptake and translocation from the root zoneto stems and leaves of plants are driven by transpira-tion, and the water status of plant tissues and soilmoisture are therefore of crucial importance forphotosynthesis and organic assimilation (Marchiolet al., 2004). According to Klang-Westin and Perttu(2002), water availability is a critical factor forgrowth ofSalix , and water availability will probablybe the most limiting factor for growth during someperiods of the growing season.

Our results suggest that morphological andecological characteristics of clones and species wereaffected by heavy metal and diesel fuel treatment indifferent ways. he high toxicity of bivalent heavymetal ions for overall plant metabolism is mostobvious in inhibition of photosynthesis. Multipleinhibitory effects were manifested as leaf chlorosis,decrease of leaf area, and reduced biomass produc-tion. he most depressive effect on the rate of photo-synthetic CO2 assimilation in all of the investigatedpoplar and willow genotypes was evident in plantsgrown on diesel fuel and a metal mixture in thesoil. Also, diesel fuel alone caused very strong andsignificant inhibition of photosynthesis and transpi-ration of willow clones, but the same treatment didnot provoke drastic decrease of the photosynthetic

rate in poplar clones, except in the case of clone B229. Relatively stable values of fluorescence param-eter Fv/Fm in polluted conditions indicated stabilityof thylakoid structure and electron flow throughthe photosystems, but disturbance of photosyn-thesis occurred on the level of carboxylation. hisobservation is contrary to the findings of Kpper etal. (2007), who reported that during excessive Cd-induced stress, a few mesophyll cells became moreinhibited and accumulated more Cd than the major-ity, while this heterogeneity disappeared duringacclimation in good remediator-plants. Chlorophyllfluorescence parameters related to photochemis-try were more strongly affected by Cd stress thannonphotochemical parameters, indicating that Cdinhibits photosynthetic light reactions more thanthe Calvin-Benson cycle.

reatment with combined excessive Pb, Cd, andNi was herein found to be a very strong stress factorfor photosynthetic productivity, especially that ofwillow clones and poplar clone B 229. he nega-tive effects of a mix of contaminating metals on thephysiology (assimilation and growth) of some otherplant species (Brassica napus and Raphanus sativus)in the presence of metals was previously verified byMarchiol et al. (2004). Substitution of heavy metalsin chlorophyll leads to a breakdown in photosyn-thesis. he concomitant presence of metals exertedstrong influence on growth of the plants and alsoon their phytoextraction efficiency, probably due toadditive effects of the metals on plant metabolism.Also, vacuolar compartmentalization appears to bean important source of hypertolerance of naturalhyperaccumulator plants (Chaney et al., 1997). he

presence of heavy metals in plant tissue can reducephotosynthetic CO2 fixation through partial closureof stomata in developed leaves, which is in agreewith our results.

Our results indicated that a combination of met-als (Pb+Cd+Ni) in the soil had a stronger inhibitoryeffect on photosynthesis in comparison with theeffect of single metals.

Among the poplar genotypes, clone B 229 exhib-ited the lowest photosynthetic potential in a con-taminated environment, which distinguishes it as


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the least suitable for good biomass production inpolluted soils. Also, comparison of the results refer-ring to photosynthetic potential indicates thatSalix species are characterized by significantly lower bio-mass production and remediation ability in a chemi-cally loaded environment. Comparing remediationpotentials of the two species rape (Brassica napus L.)and willow (Salix spp.), Mth-Gspr and Anton(2005) found that uptake and translocation of metalswere generally higher in willow than in rape. heirresults indicated that increased uptake and translo-cation of Cd and Zn from root to shoot make pos-sible phytoextraction technology, while high Cu andPb concentrations in roots with a low rate of translo-cation suggested the phytostabilization method.

In well-adapted species, higher adaptability tostress is accomplished through a high rate of photo-synthesis per unit of water loss, i.e., high WUE. Inour study, WUE of poplar clones did not decreasein pollution treatments as photosynthesis did. hisis because the transpiration rate was also affectedby heavy metal stress, and plants that are betteradapted to a polluted environment expend less waterfor nutrient absorption. Plant populations whichsuffer strong selection pressure from contaminatedconditions have lower WUE and higher N content,suggesting that the plants may be wasting water toincrease N delivery for photosynthetic apparatuses via the transpiration stream (Donovan et al., 2007).

A good potential for adaptation exists in plantsthat retain high WUE and good distribution ofnitrogen in photosynthesis during heavy metalinduced-stress, in other words ones characterizedby good resource investment in bioproduction. Ourresults confirmed that all of the genotypes are par-tially tolerant to heavy metals and indicated poplarclones Panonia, PD 3, and B 81 and willow clone V1 as genotypes with high bioproduction potentials incontaminated environmental conditions.

Becerril et al. (1989) found that different met-als may have different effects on transpiration andgrowth in the same plant, Pb caused a drastic reduc-tion of water use efficiency, while Cd inhibited tran-spiration and carbon assimilation to a similar degreeand thus did not change WUE. Te study of Menon

et al. (2007) showed that young trees of different spe-cies can respond to heavy metal soil contaminationdifferently, and that these responses may depend onsubsoil properties and their variation from year toyear.

Our results indicated genotypic specificity ofall the investigated physiological parameters andmarked poplar clones as very useful in phytoextrac-tion technology for bio-cleaning of chemically pol-luted soils.

More extensive characterization of genotypesunder a variety of conditions, including heavy metalsoil pollution, is likely to reveal more about the suit-ability of each hybrid for site-specific remediation. Acknowledgment his study was supported by the Ministryof Science and echnological Development of the Republic ofSerbia as a part of Project R20001.

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and A. Massacci(2008). Metal tolerance, accumulation,Metal tolerance, accumulation,and translocation in poplar and willow clones treated withcadmium in hydroponics.Water Air Soil Pollut., http://www.springerlink.com/content/l373560054931563/full-text.pdf.


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: Pb, Ni, Cd, - Pb+Cd+Ni, +Pb+Cd+Ni.

CO2 (mol m-2 s-1) - 10.77 8.22 mol CO2 m-2 s-1. (- 6.5 mol CO2 m-2 s-1). ,

Cd. 50 %.

(mmol H2O m-2 s-1) -

. - . - . -, WUE, - . -

, "-" .

phytoremediation capacity of populus and salix

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