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Hyperaccumulation of thallium is population-specific and uncorrelated with caesium accumulation in the thallium hyperaccumulator, Biscutella laevigata


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Aims Thallium hyperaccumulation has previously been observed in the field but there are no laboratory confirmations for Biscutella laevigata. Tolerance and accumulation of thallium and its chemical analogue caesium were compared in one non-metallicolous and three metallicolous (calamine) populations of the candidate Tl hyperaccumulator species, B. laevigata. Methods Tolerance and accumulation were evaluated in hydroponics. Moreover, Tl and Cs accumulation were measured at different K concentrations in the nutrient solution. Seedlings were also grown in Tl contaminated calamine soil. Results Estimated from their root growth response, all the calamine populations showed hypertolerance to Tl, although to very different degrees. Foliar Tl hyperaccumulation from hydroponics and soil was apparent in two populations. In one of them, it was a high-affinity phenomenon, but it was only apparent at high Tl exposure levels, and not associated with enhanced root-to-shoot translocation in the other one. There was no considerable inter-population variation in Cs tolerance and accumulation, except that one population showed a relatively low Cs retention in its roots under low exposure. Conclusions Tl hyperaccumulation and hypertolerance are population-specific traits in B. laevigata. Cs accumulation and tolerance are less variable and largely uncorrelated with Tl accumulation and tolerance.
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Hyperaccumulation of thallium is population-specific
and uncorrelated with caesium accumulation in the thallium
hyperaccumulator, Biscutella laevigata
Filip Pošćić & Luca Marchiol & Henk Schat
Received: 7 May 2012 / Accepted: 13 July 2012 / Published online: 24 July 2012
Springer Science+Business Media B.V. 2012
Aims Thallium hyperaccumulation has previously
been observed in the field but there are no laboratory
confirmations for Biscutella laevigata. Tolerance and
accumulation of thallium and its chemical analogue
caesium were compared in one non-metallicolous and
three metallicolous (calamine) populations of the can-
didate Tl hyperaccumulator species, B. laevigata.
Methods Tolerance and accumulation were evaluated
in hydroponics. Moreover, Tl and Cs accumulation
were measured at different K concentrations in the
nutrient solution. Seedlings were also grown in Tl
contaminated calamine soil.
Results Estimated from their root growth response, all
the calamine populations showed hypertolerance to Tl,
although to very different degrees. Foliar Tl hyper-
accumulation from hydroponics and soil was apparent
in two population s. In one of them, it was a high-
affinity phenomenon, but it was only apparent at high
Tl exposure levels, and not associated with enhanced
root-to-shoot translocation in the other one. There was
no considerable inter-population variation in Cs toler-
ance and accumulation, exc ept that one population
showed a relatively low Cs retention in its roots under
low exposure.
Conclusions Tl hyperaccumulation and hypertoler-
ance are population-specific traits in B. laevigata.Cs
accumulation and tolerance are less variable and large-
ly uncorrelated with Tl accum ulation and tolerance.
Keywords Thallium
Biscutella laevigata
Thallium is a toxic heavy metal, which locally occurs as
an environmental contaminant, as a result of natural
processes and from man-made sources (Saha 2005).
Natural thallium concentrations in soils are within the
range of 0.022.8mgkg
(Kabata-Pendias 2001).
However, many geochemically anomalous areas with
higher Tl levels are present worldwide (Xiao et al.
2004a, b;Pavlíčková et al. 2006; Escarré et al. 2011).
Tl is more toxic to mammals (Zitko 1975), or plants
(Allus et al. 1988) than Cd, Cu, Hg, Pb, or Zn. Therefore
Tl is listed by USEPA as one of the 13 priority pollutants
(Keith and Telliard 1979). Tl toxicity is believed to
result from its high affinity towards S and P containing
Plant Soil (2013) 365:8191
DOI 10.1007/s11104-012-1384-3
Responsible Editor: Juan Barcelo.
F. Pošćić (*)
L. Marchiol
Dipartimento di Scienze Agrarie e Ambientali,
Università degli Studi di Udine,
Via delle Scienze 208,
33100 Udine, Italy
F. Pošćić
H. Schat
Department of Genetics, Faculty of Earth and Life Sciences,
Vrije Universiteit Amsterdam,
De Boelelaan 1085,
1081 HV Amsterdam, The Netherlands
ligands, leading to substitution of K at specific
binding sit es. Thi s interf eres wi th K-met abolism
and, in many cases, wit h the formation of ATP in
respiration (Sager 1994). Early studies of Siegel and
Siegel (1975, 1976a, b) have s hown that K is an
inhibitor of T l toxicity, w hile Cataldo and Wildung
(1978 ) r eported that absorption of Tl by plants is
under metabolic control, and that K acts as a non-
competitive inhibitor of Tl uptake. Günther and
Umland (1989) have shown that the major part of
Tl exists as free Tl(I) ions in Brassica napus.This
was also found for Sinapsis alba and Entondon
schreberi (Krasnodębska-Ostręga et al. 2008). Tl
can be readily taken up by plants because it is
generally present in soil a s t hermodynamically sta-
ble Tl(I), which is chemically similar to K(I) (Nolan
et al. 2004; Galván-Arzate and Santamaría 1998).
Cs is much less toxic than Tl (Bystrzejewska-
Piotrowska and Urban 2003; Hampton et al. 2004). It
is mined mostly as pollucite, and its concentrations in
normal soils are low and non-toxic (W hite and
Broadley 2000). Bystrzejewska-Piotrowska and
Urban (2003) showed that Cs accumulation in
leaves of Lepidium sativum negatively affects the
water balance, tissue hydration, gas exchan ge
parameters, and biomass productivity. As a late
effect, a decrease of photosystem II yield was also
observed. Hampton et al. (2004)haveshownthat
Cs phytotoxicity in Arabidopsis thaliana results
from competition between K and Cs for K-
binding sites on essential proteins. Only in areas
containing Cs-rich pollucite ores, su ch as those
found in southern-eastern Manitoba (Teertstra et
al. 1992), might Cs cause environmental toxicity
(White and Broadley 2000).
However, radioisotopes of Cs are produced as fis-
sion products in nuclear reactors. Owing to incidents
involving nuclear power plants, these isotopes can be
released into the environment. Especially
deserves attention because of its high fission yields,
long half-life (t
0 30.2 years), and influence on hu-
man health (Dushenkov 2003). Because of the pro-
nounced radiotoxicity and the diffuse nature of
pollution, it has been considered desirable to develop
phytoremediator crops that could effectively phytoex-
tract it from the soil within a short period (Dushenkov
Similar to Tl, also Cs is a chemical analogue of K,
and is therefore relatively easily taken up by plants
(White and Broadley 2000). Kanter et al. (2010) re-
cently identified an amino acid substitution close to
the K-pore, the cyclic nucleotide gated channel 1
(CNGC1) in the Sorbo accession of Arabidopsis thali-
ana. This substitution might be responsible for the
relatively hi gh Cs
accumulation capacity in Sorbo
accession (Kanter et al. 2010).
Up to the present, no natural hyperaccumulators of
Cs have been reported. However, since both Tl and Cs
are chemical analogues of K, it seems not unlikely that
Cs hyperacumulators might be found among the spe-
cies that have been reported to hyperaccumulate Tl.
These species are: Galium sp., with 1.7 % (w/w)Tlin
flowers (Zyka 1972), Iberis intermedia, with 1.3 % Tl
in mature leaves (Scheckel et al. 2004), Silene latifo-
lia, with 0.15 % Tl in shoots (Escarré et al. 2011), and
Biscutella laevigata, with 1.5 % Tl in whole-plant dry
matter (Anderson et al. 1999). Exceptional Tl accu-
mulation has also been reported for Brassica oleracea
var. acephala (Pavlíčková et al. 2006 ), Lolium per-
enne (Al-Attar et al. 1988) and Plantago lanceolata
(Wierzbicka et al. 20 04 ), whereas Brassica napus,
Dianthus carthusianorum, Silene vulgaris, Triticum
aestivum and Zea mays exhibit variable, but relatively
low or negligible levels of Tl accumulation (Tremel et
al. 1997; Al-Najar et al. 2005; Wierzbicka et al. 2004;
Escarré et al. 2011).
Regarding Tl hyperaccumulation, B. laevigata
seems to be a very interesting species, because there
is evidence of considerable intra-specific variation.
Biscutella laevigata L. (Brassicaceae) is a European,
yellow-flowering hemicryptophyte with a sporo-
phytic self-incompatibility system (Olowokudejo
and Heywood 1984). It is a facultative metallo-
phyte, with both non-metallicolous and metallico-
lous populations, the latter showing population-
specific hypertolerances to the metals that are pres-
ent at toxic concentration in the soil at their popu-
lation sites, e.g., Zn/Pb mine waste deposits
(Wierzbicka and Pielichowska 2004). The reports
on Tl hyperaccumulation in B. laevigata are contra-
dictory. The populations from the Zn/Pb mines
Les Avinières, near the village of Ganges, South
France (Anderson et al. 1999
), and Cave del Predil,
Tarvisio, North Italy (Pošćić, unpublished), are
doubtlessly able to hyperaccumulate Tl, with foliar
Tl concentrations above the threshold limits of
1,000 mg kg
(Krämer 2010)andfarinexcessof
those in the soil, which precludes the possibility of
82 Plant Soil (2013) 365:8191
significant contributions of airborne contamination.
On the other hand, the population from the Zn/Pb
mine waste deposit at Boles łav, Olkusz, Poland, is
definitely not hyperaccumulating Tl, in spite of the
relatively high soil Tl concentration at this site
(Wierzbicka et al. 2004). These field observations
clearly suggest that Tl hyperaccumulation capacity
is a population-specific rather than a species-wide
trait in B. laevigata, but experimental confirmation
is lacking to date. In addition, it is not clear whether
the colonization of m etalliferous, calamine soils has
led to Tl hypertolerance in this (or any other) metal-
lophyte, and if so, whether s uch Tl hypertolerance is
confined to Tl hyperaccumulating populations.
Therefore, the first aim of this study was to c om-
pare the tolerance and accumulation of Tl among
different non-metallicolous and metallico lous B.
laevigata populations under controlled experimen-
tal conditions. In addition, we addressed the ques-
tion of whether Cs tolerance and accumulation is
predictable from T l tolerance and accumulation
Materials and methods
Plant materials and experimental conditions
Seeds of Biscutella laevigata were collected from plants
growing at the tailing ponds of the Zn/Pb mines of Cave
del Predil (northern Italy) (Cap) and Les Avinièr es
(southern France) (Lea), both of having been in use
from Roman times until the end of the twentieth century
(Zucchini 1998; Escar et al. 2011). Seeds were also
collected at the 100-year-old (Wierzbicka et al. 2004)
Zn/Pb smelter waste deposits from Bolesław (southern
Poland) (Bol) and from non-metalliferous soil in the
Tatra Mountains (southern Poland) (Tat). Plants were
confirmed to be accessions of the same subspecies lae-
vigata, according to Tremetsberger et al. (2002) and
confirmed by botanists of Udine University and the
Władysław Szafer Institute of Botany (personal com-
munication). A brief description of the collection sites is
given in Table 1.
Seeds were sown in a garden peat soil (Jongkind,
nr. 7, Aalsmeer, Netherlands) and left for 3 weeks in a
growth chamber. Seedlings were then transferred to
aerated hydroponic culture, in 1-L polyethylene pots
(one plant per pot) containing a modified half-strength
Hoaglands solution composed of 3 mM KNO
20 μM Fe(Na)-EDTA,1 μMKCl,25μMH
2 μMMnSO
0.1 μM (NH
in demineralised water buff-
ered with 2 m M 2-N-morpholino-ethanesulphonic
acid (MES), pH 5.5, adjusted with KOH. Nutrient
solutions were renewed weekly and plants were grown
in a growth chamber (20/15 °C day/night; light
intensity 220 μEm
, 14 hday
; relative humidity
75 %).
Testing Tl and Cs tolerance
After 10 days of pre-culture, plants were exposed to a
series of Tl or Cs (0, 4, 1 6, 32, 64, 128, 256 μM
or CsCl) concentrations (one plant per pot,
ten plants per population per concentration, in a rand-
omised design), in a background solution of the same
composition as the pre-culture solution. Thallium(I)
nitrate and CsCl were chosen because of their high
solubility in water. Prior to exposure, roots were
stained with active coal powd er to facilitate the mea-
surement of root growth (Schat and ten Bookum
1992). After 5 days of exposure, the length of the
longest unstained root segment was meas ured (Schat
and ten Bookum 1992).
Growth in contaminated soil
Seeds were sown direc tly in 1-L pots with a perforated
bottom (five seeds per pot, five pots per population),
filled with contaminated soil from the former Zn/Pb
mine tailing ponds of Cave del Predil (northern Italy,
Table 1) and from a Zn/Pb smelter sinter deposit near
Plombières (eastern Belgium) containing 157±29;
17,000±3,201; 27,000±1,830 mg kg
dry soil Cd,
negligible amounts of T l (Pošćić, unpublished).
Water was added weekly via the dishes under the
pots, thus a voiding leaching. Af ter the de velop-
ment of the t hir d le af, t he p lan ts wer e ha rv es ted ,
the cotyledons were removed, and the roots were
carefully washed twice in demineralised wa ter,
rinsed with ice-cold lead nitrate (5 mM) for
30 min to desorb metals from the root free space
and then blotted with paper tissue. Subsequently
until analysis.
Plant Soil (2013) 365:8191 83
Testing the effect of K supply on Tl and Cs
After 10 days of pre-culture, plants were exposed to 2
and 8 μM TlNO
or CsCl in a background solution of
the same composition as the pre-culture solution, ex-
cept for the K concentrations, which were set at 1, 3,
or 6 mM KNO
. Ten plants (one per pot) per popula-
tion per concentration were exposed for 5 days and
then analysed.
Determination of Tl and Cs concentrations
Tl and Cs concentrati ons were determined in roots and
shoots (ten plants per population per concentration).
Root material was carefully rinsed with ice-cold lead
nitrate (5 mM) for 30 min to desorb metals from the
root free space and then blotted with paper tissue. Tl
and Cs were determined by digesting 20100 mg of
oven-dried plant material in 2 ml of a 1 to 4 (v/v)
mixture of 37 % (v/v) HCl and 65 % (v/v) HNO
Teflon cylinders for 7 h at 140 °C, after which the
water. Tl and Cs were determined using atomic ab-
sorption and flame emis sion spectrophotometry, re-
spectively (Perkin Elmer 2100; Perkin Elmer
Nederland, Nieuwerkerk a/d Yssel, The Netherlands).
The detection limits were 0.04 and 0.02 mg l
for Tl
and Cs respectively.
Statistical analysis was carried out with one-, two- and
three-way ANOVA. A posteriori comparison of indi-
vidual means was performed using Tukeys test. Data
from hydroponics were subjected to logarithmic trans-
formation prior to analysis, which effectively homog-
enized the vari ances and pr oduced app roxim ately
normal distributions. Consequently, we chose to pres-
ent the median values instead of the arithmetic means.
Effects of Tl and Cs on root growth
As estimated from the root growth response, there was
a remarkable inter-population variation in Tl tolerance
(Fig. 1). The Cap population was the most tolerant,
Table 1 Description of the sites of collection of Biscutella laevigata seeds.
Site Code Habitat description Altitude (m) Latitude (N) Longitude (E) Cd (mg kg
) Pb (mg kg
) Tl (mg kg
) Zn (mg kg
) References
Bolesław (Bukowno, Olkusz,
S Poland)
Bol Zn/Pb calamine waste
313 50° 17 35 19° 29 08 170
1,650 43±12
4,000 Wierzbicka et al. 2004;
Wierzbicka and
Pielichowska 2004
Cave del Predil (Tarvisio,
N Italy)
Cap Former Zn/Pb mine
tailing ponds
901 46° 26 26 13° 34 16 17.8±5.1
7,740±2,349 521± 88.7 23,722±3,494 Pošćić, unpublished
Les Avinières (Saint-Laurent-
le-Minier, Ganges, S France)
Lea Former Zn/Pb mine
tailing ponds
175 43° 55 59 39 59 35.2745
4,13584,130 6.4115.1 9,929131,365 Escarré et al. 2011
Tatra Mountains (S Poland) Tat Natural mountain site 1,8002,850 49° 15 12 19° 55 54 7
65 Wierzbicka and
Pielichowska 2004
An estimate of meandispersion data are not available
Mean ± SD
Mean ± SE
Range of means from different soil Horizons
Not known
84 Plant Soil (2013) 365:8191
showing significant root growth reduction exclusively at
the highest (256 μM) Tl treatment, followed by the Lea
population. The latter showed significant growth reduc-
tion already at the next highest (128 μM) Tl treatment
and complete growth inhibition at the highest. The third
metallicolous population, Bol, was much more sensitive
than Lea and Cap, showing significant growth reduction
already at 16 μM Tl, but significantly more tolerant than
the non-metallicolous population, which was already
significantly inhibited at 4 μMTl.
In comparison with Tl tolerance, Cs tolerance var-
ied much less among the populations (Fig. 2). At the
highest concentration (256 μM Cs), all the populations
maintained considerable root growth rates, which were
significantly lower than in the controls only in Bol and
Tat (p<0.05), but not so in Lea and Cap. When com-
pared at the same concentration, significant differen-
ces were only found at the 128-μM Cs treatment,
where Lea and Cap performed slightly, but significant-
ly better than Bol and Tat (p<0.05), and at the 64-μM
treatment, where Bol showed less root growth than
any of the other populations (p<0.05).
Tl and Cs accumulation in hydroponics
For Tl accumulation in roots and shoots, we performed
the statistical analyses (one-way ANOVA, followed by
Tukeys test) first with the data from the lowest Tl
treatment (4 μM), since this was the only treatment that
allowed at least some root growth in all of the popula-
tions. The root Tl concentrations decreased in the order
Cap > Lea > Bol > Tat, each of the populations being
significantly different from all of the others (p<0.05).At
16 μM Tl the same order was found, with Cap and Lea
showing significantly higher root Tl concentrations than
Bol (Tat was not included, because its root systems were
dead, or close to dead). At exposure levels higher than
16 μM the root Tl concentration levelled off in Lea
continued to increase sharply in Cap, up to the highest
exposure level (Fig. 3).
The Tl concentrations in the shoot showed a pattern
very different from that in roots. At the 4-μM expo-
sure level the highest shoot Tl concentration was
found in Lea, i.e. about four-fold higher than in Cap,
and about seven-fold higher than in Bol and Tat. The
Fig. 1 Tl-imposed root
growth inhibition (mm) of
four populations of Biscu-
tella laevigata (triangles,
Bol; circles, Cap; squares,
Lea; stars, Tat) (median±
SE, n0 10) after exposure to
increasing Tl concentrations
(μM) for 5 days
Fig. 2 Cs-imposed root
growth inhibition (mm) of
four populations of Biscu-
tella laevigata (triangles,
Bol; circles, Cap; squares,
Lea; stars, Tat) (median±
SE, n0 10) after exposure to
increasing Cs concentrations
(μM) for 5 days
Plant Soil (2013) 365:8191 85
same pattern was found at the 16 μM Tl exposure
level. At 32 μM Tl the shoot concentration levelled
off in Lea, but continued to increase with exposure
level in Cap, resulting in almost equal shoot concen-
trations at the 128 μM-exposure level (Fig. 4).
The shoot to roo t Tl concentration ratios v aried
strongly and significantly between populations, de-
creasing in the order Lea > Tat/Bol > Cap, where /
indicates a non-significan t difference. The ratio was
consistently higher than unity in Lea, increasing with
the Tl exposure level from 2.5 at 4 μMto3.5at
128 μM. In the other populations the ratios were close
to unity (Tat/Bol), or significantly lower than unity in
Cap, increasing from 0.4 at 4 μM to 0.8 at 256 μM Tl.
The root Cs concentrations were significantly lower
in Cap, at all the exposure levels, than in the other
populations, which were not significantly different
among each other (Fig. 5). The shoot Cs concentra-
tions did not significantly vary among the populations
(Fig. 6).
As expected, the Cs shoot to root concentration
ratio was significantly higher in Cap, decreasing with
exposure level from 11.1 at 4 μM to 1.7 at 256 μM, in
comparison with the other populations, in which the
ratio decreased from 2.0 at 4 μM to 1.4 at 256 μM Cs.
Tl accumulation from mine soil
The populations performed very distinctly in soil from
the Cave del Predil mine tailing. The Tat plants were
stunted and heavily chlorotic, and died before the end
of the experiment. Also the Bol plants were stunted,
but they survived. Only the Cap and Lea plants devel-
oped normally, without displaying toxicity symptoms.
The plants from the Cap and Lea populations showed
significantly lower (p<0.01) Tl concentrations in their
roots than did the Bol
plants (Fig. 7). The shoot Tl
concentrations were significantly different among all
the populations (p<0.001), decreasing in the order
Lea > Cap > Bol. The root to shoot Tl concentration
ratios decreased in the order Lea > Cap > Bol (Fig. 7).
In soil from the Plombières smelter sinter deposit
all the plants were stunted and heavily chlorotic, and
died before the end of the experiment.
Fig. 3 Root Tl concentra-
tions (μmol g
d.w.) of
four populations of Biscu-
tella laevigata (triangles,
Bol; circles, Cap; squares,
Lea; stars, Tat) (median±
SE, n0 10) after exposure to
increasing Tl concentrations
(μM) for 5 days. There is an
enlargement of the figure at
4 μM Tl concentration val-
ues in the upper-left corner
Fig. 4 Shoot Tl concentra-
tions (μmol g
d.w.) of four
populations of Biscutella
laevigata (triangles, Bol;
circles, Cap; squares, Lea;
stars, Tat) (median ±SE, n0
10) after exposure to in-
creasing Tl concentrations
(μM) for 5 days. There is an
enlargement of the figure at
4 μM Tl concentration val-
ues in the upper-left corner
86 Plant Soil (2013) 365:8191
Testing the effect of K on Cs and Tl accumulation
In a preliminary experiment we found that there were no
significant effects on biomass productivity and root
length growth, when KNO
was supplied at 1 or
6 mM, instead of the standard 3-mM supply (data not
shown). The root and shoot Tl concentrations were
significantly affected by the K concentration in the
nutrient solution (three-way ANOVA, p<0.001). How-
ever, the population × K interaction was significant too
(p<0.001), both for shoots and roots, showing that there
was inter-population variation in the nature or degree of
the K effect (Table 2). In particular, the shoot Tl con-
centrations in the highest K treatment (6 mM) were
more strongly decreased (about 50 %), in comparison
with those in the lowest K treatment (1 mM), in Bol and
Lea (at 8 μM Tl) than they were in Cap and Tat.The
root Tl concentrations were strongly decreased by high
KinBol and Cap, but not at all or insignificantly in Lea
and Tat. The effect of high K on the shoot to root Tl
concentration ratios was also significantly population-
specific (p<0.001), i.e. increasing in Cap (only at
6 mM K), decreasing in Lea, and insignificant in Bol
and Tat, suggesting that K affected both Tl uptake and Tl
root to shoot translocation in a population-specific way.
The root and shoot concentrations of Cs were also
significantly affected by high K supply, albeit much
less than the Tl concentrations (Table 2). The popula-
tion × K interaction was insignificant for the shoot Cs
concentrations, but highl y significant (p<0.001) for
the root ones, due to the relatively strong effects in
Cap at 3 and 6 mM K, and in Lea at 6 mM K (Table 2),
with parallel effects on the shoot to root concentration
Our results unambiguously confirm the postulated Tl
hyperaccumulator status of the calamine Biscutella lae-
vigata population from Les Avinières (Lea)(Anderson
et al. 1999). It showed all the characteristics of a true
hyperaccumulator, these are, 1) an extremely high level
of Tl accumulation in its foliage, even at relatively low
Fig. 5 Root Cs concentra-
tions (μmol g
d.w.) of
four populations of Biscu-
tella laevigata (triangles,
Bol; circles, Cap; squares,
Lea; stars, Tat) (median±
SE, n0 10) after exposure to
increasing Cs concentrations
(μM) for 5 days. There is an
enlargement of the figure
showing low Cs concentra-
tion values in the upper-left
Fig. 6 Shoot Cs concentra-
tions (μmol g
d.w.) of four
populations of Biscutella
laevigata (triangles, Bol;
circles, Cap; squares, Lea;
stars, Tat) (median ±SE, n0
10) after exposure to in-
creasing Cs concentrations
(μM) for 5 days
Plant Soil (2013) 365:8191 87
levels of Tl exposure, 2) a shoot to root Tl concentration
ratio higher than unity, 3) an extraordinary level of Tl
tolerance. Furthermore, it has been shown to hyperac-
cumulate both in its natural environment but also, as
shown in the present study, in greenhouse or climate
room experiments that use either hydroponics or soil,
the latter clearly demonstrating that the apparent foliar
hyperaccumulation of Tl of this population in the
field (Escarré et al. 2011) is not owing to air-borne
Tl hyperaccumulation is obviously not a species-
wide property in B. laevigata. The non-metallicolous
population from the Tatra Mountains (Tat) did not show
any of the typical hyperaccumulator traits (see above).
In agreement with field observations (Wierzbicka et al.
2004), also the metallicolous population from Bolesłav
(Bol) appeared to lack any propensity for Tl hyperaccu-
mulation. The calamine population from Cave del Predil
(Cap) presents a special case. In their own natural envi-
ronment, the Cave del Predil mine tailing, these plants
often exceed the threshold criterion for foliar hyperac-
cumulation of Tl (Pošćić, unpublished), which has been
dry weight (Krämer 2010). In fact,
according to this criterion, Cap plants hyperaccumulated
also in our experiments, both in their native soil and in
hydroponics, although they never displayed a
hyperaccumulator-like Tl root-to-shoot translocation.
However , as suggested by our hydroponics experiments,
foliar Tl hyperaccumulation in the Cap population seems
to occur exclusively at extremely high, normally lethal
exposure levels. Therefore, it seems that the foliar Tl
hyperaccumulation of the plants in their natural environ-
ment can be explained by their extreme Tl tolerance, in
combination with the extraordinarily high soil Tl concen-
tration at the Cave del Predil mine tailing. In other words,
in the particular case of Cap, foliar Tl hyperaccumulation
may not be associated with specific physiological attrib-
utes other than (extreme) hypertolerance. To test this
hypothesis, it should be checked in future experiments
whether Cap plants are able to hyperaccumulate Tl also
from les s Tl-enriched soils, su ch as those from the
Bolesłav and Les Avinières mine tailings.
To date there is not much information on Tl toler-
ance in metallophytes. In the present study we consis-
tently found significantly enhanced Tl tolerance
(hypertolerance) in three metallicolous B. laevigata pop-
ulations, in comparison with a non-metallicolous one.
This suggests that Tl is often present at potentially
phytotoxic concentrations in calamine soils. However,
there was a huge variation in the degree of Tl hyper-
tolerance among the metallicolous populations. It is not
yet clear whether this variation is correlated with the
degrees of soil Tl toxicity, but at least the most tolerant
population (Cap) originates from the most Tl-enriched
soil. On the other hand, Lea is much more Tl-tolerant
than Bol, in spite of the more or less similar degrees of
Tl-enrichment at their sites of origin. Therefore, it may
be speculated that the high level of tolerance in Lea may
have something to do with the fact that the Lea popula-
tion is the only unambiguous Tl hyperaccumulator.
Our experiment with soil from Cave del Predil did
not give any clue regarding the nature of the growth-
Fig. 7 Roots (black columns) and shoots (white columns)Tl
concentrations (μmol g
d.w.) of three Biscutella laevi gata
populations (Bol, Cap, Lea) (mean ± SE, n0 5) after growing
in contaminated soil from the former Zn/Pb mine tailing ponds
of Cave del Predil (southern Italy). The Tat plants were not
capable to survive. Different letters indicate significant differ-
ences between treatments (p<0.01, Tukeys test). Capital letters
refer to roots while lowercase letters to shoots
88 Plant Soil (2013) 365:8191
Table 2 Median ± SE (μmol g
d.w.) for (a) Tl or (b) Cs accumulation in shoots or roots at different K and Tl or Cs concentrations in hydroponics in four populations
(a) Plant fraction K (mM) 2 μM Tl in solution 8 μM Tl in solution Tukeys between populations
Bol Cap Lea Tat Bol Cap Lea Tat 2 μM Tl in solution 8 μM Tl in solution
Shoot 1 0.67±0.04 1.40±0.13 12.13±0.49 0.69 ±0.04 2.56±0.16 5.43±0.47 36.73±5.19 2.10±0.10 Lea > Cap > Bol/Tat Lea > Cap > Bol/Tat
3 0.53±0.03 0.97±0.08 10.80±0.60 0.46 ±0.04* 1.80±0.25 3.49±0.25* 17.58±2.28* 2.12±0.12 Lea > Cap > Bol/Tat Lea > Cap > Bol/Tat
6 0.38±0.04* 0.87±0.03* 9.76±0.72 0.44 ±0.04* 1.17±0.11* 3.14±0.13* 14.29±1.46* 1.53 ±0.09 Lea > Cap > Bol/Tat Lea > Cap > Bol/Tat
Root 1 1.06±0.10 2.84±0.49 1.21 ± 0.18 0.40±0.05 3.06±0.36 12.11±1.76 7.06±0.79 2.52 ± 0.23 Cap > Lea/Bol > Tat Cap > Lea > Bol/Tat
3 1.29±0.13 1.94±0.19 1.36 ± 0.16 0.67±0.05 2.10±0.22 8.06±1.39 5.15±1.29 2.14±0.14 Cap > Lea/Bol > Tat Cap/Lea > Bol/Tat
6 0.57±0.08* 0.73±0.13* 1.52±0.16 0.52 ±0.04 1.60±0.20 4.13±0.52* 6.02±2.33 1.95±0.15 Lea > Cap/Bol/Tat Lea > Cap/Bol/Tat
(b) Plant fraction K (mM) 2 μM Cs in solution 8 μM Cs in solution Tukeys between populations
Bol Cap Lea Tat Bol Cap Lea Tat 2 μM Cs in solution 8
μM Cs in solution
Shoot 1 0.45±0.03 0.46±0.02 0.61 ± 0.03 0.48±0.02 1.70±0.06 1.46±0.08 2.11±0.08 1.55±0.12 Lea/Tat/Cap/Bol Lea/Bol/Tat/Cap
3 0.45±0.02 0.48±0.01 0.52 ± 0.04 0.44±0.02 1.73±0.03 1.64±0.08 2.00±0.13 1.68±0.07 Lea/Cap/Bol/Tat Lea/Bol/Tat/Cap
6 0.37±0.03* 0.34±0.01* 0.40±0.01* 0.38±0.04 1.41±0.09 1.12± 0.09* 1.80±0.10 1.61±0.09 Lea/Ta t/Bol/Cap Lea/Tat/Bol/Cap
Root 1 0.31±0.01 0.14±0.002 0.32±0.01 0.17 ±0.01 1.12±0.11 0.33±0.05 0.58±0.09 0.87 ±0.06 Lea/Bol > Tat /Cap Bol/Tat > Lea > Cap
3 0.26±0.02 0.04±0.01* 0.39±0.07 0.16 ±0.01 1.14±0.06 0.28±0.01 0.63±0.08 0.98 ±0.06 Lea > Bol/Tat > Cap Bol/Tat > Lea > Cap
6 0.24±0.01 0.05±0.01* 0.14±0.003* 0.13±0.02 0.72±0.05* 0.32 ±0.04 0.75±0.49 0.91±0.05 Bol > Lea/Tat > Cap Tat/Bol > Lea > Cap
The populations are ordered from the highest to the lowest accumulation and interconnected by / in the case they are ns, or by > in the case of p<0.05
p<0.05 for K levels for each population
Plant Soil (2013) 365:8191 89
limiting toxic metal. Most likely, all the met als, or at
least Zn, Cd, and Tl are present at levels expected to
be toxic for Tat, but this is not necessarily true for the
Bol population, which has been shown to be highly
tolerant to Zn, Cd and Pb, in comparison with Tat
(Wierzbicka and Pielichowska 2004). Since none of
the populations survived in the Tl-poor calamine soil
from Plombières, we have no indication that Tl was
indeed limiting for Bol in the Cave del Predil soil.
Regarding Cs accumulation and tolerance, our
study clearly shows that there is little or no correspon-
dence with the patterns observed for Tl. Cs tolerance
was just slightly higher in Lea and Cap than in Bol and
Tat, in sharp contrast with the huge difference in Tl
tolerance. Moreov er, there was no significant inter-
population variation in Cs accumulation in root and
shoot, except for Cap, which retained less Cs in its
roots than any of the other populations. Even the Tl
hyperaccumulating population (Lea) did not show any
incre ased foliar accumulation of Cs, in comparison
with the other populations. In addition, the patterns
of K-imposed inhibition o f Cs accumulation were
generally less pronounced and very different from
those found for Tl accumulation. Therefore, it can be
concluded safely that C s and Tl accumulation use
different pathways, although both are K analogues.
Broadley et al. (1999) reported that shoot Cs accu-
mulation is influenced by taxonomy. Caesium concen-
trations in the rhizosphere exceeding 200 μMare
inhibiting growth in many plant species (Cline and
Hungate 1960;Kordan1987; Sheahan et al. 1993;
Hasegawa 1996; White and Broadley 2000). There-
fore, it seems that B. laevigata is highly tolerant in
comparison with other species. From the phytoreme-
diation viewpoint it may be interesting that there was a
very low degree of Cs retention in roots in the Cap
population, but this was, unfortunately, not associated
with a higher accumulation in the shoot. However, we
only screened four populations, and the possibility
remains that variation in shoot Cs accumulat ion does
exist. In any case, Cs accumulation capacity is not
predictable from Tl accumulation.
This study showed that 1) all the calamine B. laevigata
populations are Tl-hypertolerant, albeit to very different
degrees, indicating that Tl is usually a highly toxic
component of calamine ores, 2) Tl hyperaccumulation
is a population-specific trait, and 3) not associated with
any tendency to accumulate Cs, 4) Cs accumulation and
tolerance were almost non-variable among the popula-
tions, therefore we did not find any indication that
phytoremediation of (radioactive)-Cs would be possible
with natural Tl hyperaccumulators, 5) the patterns of
interference with K varied between Tl and Cs, showing
that these metals use different K transporters.
Acknowledgements We thank Alicja A. Kostecka (Władysław
Szafer Institute of Botany, Polish Academy of Sciences, Poland)
for providing Polish Biscutella laevigata seeds. Technical assis-
tance by Ahmad Mohtadi (University of Isfahan, Iran) and Mazhar
Iqbal (Vrije Universiteit Amsterdam, The Netherlands) are grate-
fully acknowledged.
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A simulated wetland experiment was used to investigate the effect of thallium (Tl) accumulation on the growth of Arundo donax L., its photosynthetic characteristics and its antioxidant enzyme activities. Tl accumulated in the order of stems<leaves<roots and increased gradually with increasing Tl concentrations (from 0 to 2.5µgL–1). Moderate Tl applications (from 0.2 to 2.5µgL–1) increased the rate of both photosynthesises (Pn) and transpiration (Tr), as well as catalase and peroxidase activity. Tl significantly affected stomatal conductivity, but had no effect on the relative chlorophyll content (SPAD values) or the potential and effective photochemical efficiency of photosystem II. However, intercellular CO2 concentrations and superoxide dismutase decreased in response to increasing Tl concentrations. Although 50µgL–1 Tl significantly decreased the SPAD values, as well as the potential and effective photochemical efficiency of photosystem II, it had no effect on Pn or Tr. These results suggest that root restriction and oxidative stress are involved in the mechanism of Tl toxicity, but the photosynthetic system of A. donax was not harmed by certain concentrations of Tl, indicating the strong tolerance of this species to increased Tl pollution.
... B. laevigata is classified as a hyperaccumulator of such metals as thallium and lead [38,44,49]. In the research on several plant species from the zinc-lead heaps (enriched in nickel, thallium and gold) occurring near Montpellier (France), the thallium deposition in the B. laevigata plants was observed -above 1.5% [44]. ...
Biscutella laevigata is the strongest known thallium (Tl) hyperaccumulator. Little is known about physiological processes leading to root uptake and translocation of Tl in this species, and the interactions between Tl and its chemical analogue potassium (K). Biscutella laevigata was subjected to hydroponics exposed to Tl and K, and to a rhizobox experiment. Laboratory micro-X-ray fluorescence spectroscopy (μXRF) was used to reveal Tl distribution in roots and leaves, while synchrotron-based μXRF was utilised to reveal elemental distribution in seeds. Thallium was mainly stored in the endosperm and cotyledons. In adult plants, Tl was highest in intermediate leaves (16,100 μg g⁻¹), while it was one order of magnitude lower in the stem and roots. Potassium did not inhibit or enhance Tl uptake in Biscutella laevigata. Thallium was localised in the blade and margins of leaves. Roots foraged for Tl and cycled Tl across roots growing in control soils. Biscutella laevigata has evolved specialised mechanisms to tolerate high Tl concentrations in shoots. The lack of interaction and competition between Tl and K suggests that it is unlikely that Tl is taken up via K channels. High affinity Tl transporters remain to be identified in this species. Thallium is not only highly toxic but also a valuable metal and Tl phytoextraction using B. laevigata should be explored.
Biscutella auriculata L. is a plant that belongs to the Brassicaceae family and it has been found growing in a metal-contaminated area of the San Quíntín mine (Ciudad Real, Spain). The purpose of this work was to evaluate the mechanisms that allow this plant to tolerate high concentrations of copper. Seedlings were grown in a semihydroponic system for 15 days under 125 μM of Cu (NO3)2. Exposure to copper resulted in growth inhibition and reduction in the photosynthetic parameters. Copper was mainly accumulated in vascular tissue and vacuoles of the roots and only a minor proportion was transferred to the shoot. Biothiol analysis showed a greater enhancement of reduced glutathione in leaves and increases of phytochelatins (PC2 and PC3) in both leaves and roots. Copper treatment induced oxidative stress, which triggered a response of the enzymatic and non-enzymatic antioxidant mechanisms. The results show that B. auriculata is able to tolerate high metal levels through the activation of specific mechanisms to neutralize the oxidative stress produced and also by metal sequestration through phytochelatins. The preferential accumulation of copper in roots provides clues for further studies on the use of this plant for phytostabilization and environmental recovery purposes in Cu-contaminated areas.
Among heavy metal plants (the metallophytes), facultative species can live both in soils contaminated by an excess of heavy metals and in non-affected sites. In contrast, obligate metallophytes are restricted to polluted areas. Metallophytes offer a fascinating biology, due to the fact that species have developed different strategies to cope with the adverse conditions of heavy metal soils. The literature distinguishes between hyperaccumulating, accumulating, tolerant and excluding metallophytes, but the borderline between these categories is blurred. Due to the fact that heavy metal soils are dry, nutrient limited and are not uniform but have a patchy distribution in many instances, drought-tolerant or low nutrient demanding species are often regarded as metallophytes in the literature. In only a few cases, the concentrations of heavy metals in soils are so toxic that only a few specifically adapted plants, the genuine metallophytes, can cope with these adverse soil conditions. Current molecular biological studies focus on the genetically amenable and hyperaccumulating Arabidopsis halleri and Noccaea (Thlaspi) caerulescens of the Brassicaceae. Armeria maritima ssp. halleri utilizes glands for the excretion of heavy metals and is, therefore, a heavy metal excluder. The two endemic zinc violets of Western Europe, Viola lutea ssp. calaminaria of the Aachen-Liège area and Viola lutea ssp. westfalica of the Pb-Cu-ditch of Blankenrode, Eastern Westphalia, as well as Viola tricolor ecotypes of Eastern Europe, keep their cells free of excess heavy metals by arbuscular mycorrhizal fungi which bind heavy metals. The Caryophyllaceae, Silene vulgaris f. humilis and Minuartia verna, apparently discard leaves when overloaded with heavy metals. All Central European metallophytes have close relatives that grow in areas outside of heavy metal soils, mainly in the Alps, and have, therefore, been considered as relicts of the glacial epoch in the past. However, the current literature favours the idea that hyperaccumulation of heavy metals serves plants as deterrent against attack by feeding animals (termed elemental defense hypothesis). The capability to hyperaccumulate heavy metals in A. halleri and N. caerulescens is achieved by duplications and alterations of the cis-regulatory properties of genes coding for heavy metal transporting/excreting proteins. Several metallophytes have developed ecotypes with a varying content of such heavy metal transporters as an adaption to the specific toxicity of a heavy metal site.
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First published as an Advance Article on the web 17th May 2004 Speciation of thallium was investigated in a Tl hyperaccumulator plant, Iberis intermedia, by ion chromatography (IC) and size-exclusion chromatography (SEC) coupled with on-line ICP-MS detection. The leaves, stems and roots of the plant were extracted with a buffer solution (pH 6.2) containing DTPA and ammonium acetate. DTPA was used to complex unstable Tl(III) to form the stable Tl(III)–DTPA anionic complex. The two species, Tl(I) and Tl(III)–DTPA, were separated by using two separation mechanisms, anion exchange chromatography and SEC, with 100 mmol L 21 ammonium acetate (pH 6.2) as eluant. The anion exchange chromatograms indicated that the chemical form of Tl present in extracts of both fresh and freeze-dried samples of the roots, stems and leaves is predominantly Tl(I), and this was confirmed by size-exclusion chromatography and electrospray mass spectromety.
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Chromosome counts were determined for 46 populations ofBiscutella representing 28 taxa. The genus was found to contain diploid taxa with 2n = 12, 16 and 18, tetraploid taxa with 2n = 36 and hexaploid taxa having 2n = 54.B. laevigata L. s. l. consists of diploid and tetraploid populations which are poorly differentiated morphologically. TetraploidB. laevigata s. l. and hexaploidB. variegata Boiss. & Reuter (s. l.) are characterized by chromosomal instability. The variation in chromosome numbers and the occurrence of polyploidy is discussed in relation to the taxonomy of the genus. An investigation of the breeding system showed that most of the annual species were self-compatible and partly inbreeding and most of the perennial species self-incompatible and, therefore, outbreeding, while one annual species,B. cichoriifolia Loisel., showed both systems.
The chemical properties of Tl can be used as key parameters to explain its ecological behaviour and occurrence as well as its action on living biota. This review presents recent knowledge from the molecular level to symptoms of illness. Tl mainly occurs in Sulfides and acid silicates. After weathering or thermal volatilization, it is quite mobile in soils, sediments and subsurface clays as a monovalent cation. Monovalent Tl is similar to K with respect to fit into the silicate lattice, complex formation, solubility and Sorption properties. Inside the living cell, however, stronger affinities towards S‐ and P‐ containing ligands lead to substitution of K at specific adsorption sites. This interferes with K‐metabolism and, in many cases, with the formation of ATP by respiration. Pathological changes have been documented in mitochondria and ribosomes, as well in peripherous nerve cells, liver cells and renal tissues. Muscle cells are activated by Tl similar to K. Contrary to many other metal cations, actions of Tl are mainly reversible. Some microorganisms get accustomed to higher Tl‐levels by using Tl like K. Main toxic effects on animals and man are observed in the nervous and digestion/excretion systems. The blood‐liquor barrier protects man and animals, leaving the plankton in aquatic ecosystems more sensitive to Tl pollution than fish. In green plants, protein binding is limited and uptake and effects are highly variable. Rape strongly accumulates thallium, bound to a low molecular species, without showing symptoms. As a therapy against intoxication, enforced excretion and supply of K have been successfully used.
241I. INTRODUCTION: CAESIUM IN THE ENVIRONMENT 242II. UPTAKE OF CAESIUM BY PLANT ROOTS 2431. Evidence for multiple mechanisms of Cs+uptake by plant roots 2432. Caesium uptake is affected by the presence of other cations 2443. Caesium inhibits the uptake of other cations 244III. MOLECULAR MECHANISMS CATALYSING CAESIUM UPTAKE 2451. ‘High-affinity’transport mechanisms 2452. Inward-rectifying potassium (KIR) channels 2453. Outward-rectifying potassium (KOR) channels 2484. Voltage-insensitive cation (VIC) channels 2495. Ca2+-permeable channels 249IV. MODELLING CAESIUM INFLUX TO ROOT CELLS 2491. Predicted Cs+influx through high-affinity mechanisms 2502. Predicted Cs+influx through cation channels 2503. Predicted dependence of Cs+influx on[Cs+]ext 252V. PERSPECTIVE 253Acknowledgements 254References 254Caesium (Cs) is a Group I alkali metal with chemical properties similar to potassium (K). It is present in solution as the monovalent cation Cs+. Concentrations of the stable caesium isotope 133Cs in soils occur up to 25 μg g−1 dry soil. This corresponds to low micromolar Cs+ concentrations in soil solutions. There is no known role for Cs in plant nutrition, but excessive Cs can be toxic to plants. Studies of the mechanism of Cs+ uptake are important for understanding the implications arising from releases of radioisotopes of Cs, which are produced in nuclear reactors and thermonuclear explosions. Two radioisotopes of Cs (134Cs and 137Cs) are of environmental concern owing to their relatively long half-lives, emissions of β and γ radiation during decay and rapid incorporation into biological systems. The soil concentrations of these radioisotopes are six orders of magnitude lower than those of 133Cs. Early physiological studies demonstrated that K+ and Cs+ competed for influx to excised roots, suggesting that the influx of these cations to root cells is mediated by the same molecular mechanism(s). The molecular identity and/or electrophysiological signature of many K+ transporters expressed in the plasma membrane of root cells have been described. The inward-rectifying K+ (KIR), outward-rectifying K+ (KOR) and voltage-insensitive cation (VIC) channels are all permeable to Cs+ and, by analogy with their bacterial counterparts, it is likely that ‘high-affinity’ K+/H+ symporters (tentatively ascribed here to KUP genes) also transport Cs+. By modelling cation fluxes through these transporters into a stereotypical root cell, it can be predicted that VIC channels mediate most (30–90%) of the Cs+ influx under physiological conditions and that the KUP transporters mediate the bulk of the remainder. Cation influx through KIR channels is likely to be blocked by extracellular Cs+ under typical ionic conditions in the soil. Further simulations suggest that the combined Cs+ influxes through VIC channels and KUP transporters can produce the characteristic ‘dual isotherm’ relationship between Cs+ influx to excised roots and external Cs+ concentrations below 200 μM. Thus, molecular targets for modulating Cs+ influx to root cells have been identified. This information can be used to direct future genetic modification of plants, allowing them to accumulate more, or less, Cs and thereby to remediate contaminated sites.
The study examines the transfer factor (TF) for cesium in a soil-plant system and cesium accumulation in cress Lepidium sativum L. plants grown in hydroponic culture and subjected to root and foliar application of 0.3 mM CsCl. The experiments showed a high TF for radiocesium: 2.97 (kBq/kg plant DW)/(kBq/kg soil DW). High accumulation of cesium was observed in leaves after both root and foliar treatments. A higher concentration of cesium (3 mM) caused significant disturbance in water uptake, tissue hydration (FW/DW) and production of biomass (DW). Accumulation of cesium in leaves affected gas exchange parameters. Stomatal conductance (C) and transpiration rate (E) were strongly inhibited but photosynthetic CC-2 assimilation (P) was disturbed to a lesser extent. As a result, photosynthetic water utilization efficiency (P/E) was unaffected by 3 mM cesium at photosynthetically active radiation (PAR) of 220 μmol x m -2 x s -1. Increasing PAR from 220 to 450 μmol x m -2 x s -1 stimulated the photosynthetic rate after 3 days, but no stimulation was observed after 5 days of cesium treatment, in comparison with potassium-grown plants. Changes in chlorophyll fluorescence, indicating maximal quantum yield of photosystem II (PSII) photochemistry, were observed only as a late stress effect. Decreased stomatal opening was an early effect of cesium stress in Lepidium sativum, which resulted in limitation of transpiration and water uptake. It is suggested that the decrease in tissue hydration is what limits photosynthetic CO 2 assimilation, synthesis of organic matter and light reactions of photosynthesis.
Potassium-deficient cucumber seedlings are more sensitive to thallium than are those receiving exogenous potassium. Limiting potassium, short of an overt expression of deficiency, increased the sensitivity of the plants to thallium and further demonstrates a mitigation of thallium toxicity. Relatively high levels of T1-ion (10 mM) precipitate K+-deficiency symptoms. The epicotyl is more sensitive to T1-ion than are preformed hypocotyls, suggesting that developmental processes dependent on cell multiplication may be more sensitive to thallium than those entailing cell enlargement and differentiation.
By the addition of potassium to the nutrient substrate, Cs/sup 137/ and Rb/sup 68/ uptake by bean plants was reduced less than expected from an assumed physiological equivalence of those ions. Plants discriminated against cesium at low potasium nutrient concentrations; but with increasing substrate potassium. this discrimination diminished. Discrimination of Rb/sup 68/ from potassium approximated that observed for Cs/sup 137/. Potential errors from the use of ratios in predicting uptake of Cs/sup 137/ were discussed. Some toxicity was noted when significant quantities of nonradioactive cesium were in the nutrient solution. (auth)