This article was downloaded by: [Irina Shtangeeva]

On: 10 July 2011, At: 11:37

Publisher: Taylor & Francis
Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered
office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Journal of Plant Nutrition

Publication details, including instructions for authors and
subscription information:
http://www.tandfonline.com/loi/lpla20

SILVER-INDUCED CHANGES IN THE

NUTRIENT AND TRACE ELEMENT UPTAKE
BY WHEAT AND AMOUNT OF THE
RHIZOSPHERE PROTEINS
a

Irina Shtangeeva , Salla Venlinen , Helin Hartikainen ,

a

Marina Surgik & Sergey Timofeev

Chemical Department, St. Petersburg University, St. Petersburg,

Russian Federation
b

Department of Applied Chemistry and Microbiology, University of

Helsinki, Helsinki, Finland
Available online: 04 Jul 2011

To cite this article: Irina Shtangeeva, Salla Venlinen, Helin Hartikainen, Marina Surgik & Sergey
Timofeev (2011): SILVER-INDUCED CHANGES IN THE NUTRIENT AND TRACE ELEMENT UPTAKE BY WHEAT
AND AMOUNT OF THE RHIZOSPHERE PROTEINS, Journal of Plant Nutrition, 34:10, 1497-1506
To link to this article: http://dx.doi.org/10.1080/01904167.2011.585206

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions
This article may be used for research, teaching and private study purposes. Any
substantial or systematic reproduction, re-distribution, re-selling, loan, sub-licensing,
systematic supply or distribution in any form to anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation
that the contents will be complete or accurate or up to date. The accuracy of any
instructions, formulae and drug doses should be independently verified with primary
sources. The publisher shall not be liable for any loss, actions, claims, proceedings,
demand or costs or damages whatsoever or howsoever caused arising directly or indirectly
in connection with or arising out of the use of this material.

Journal of Plant Nutrition, 34:14971506, 2011

C Taylor & Francis Group, LLC
Copyright

ISSN: 0190-4167 print / 1532-4087 online
DOI: 10.1080/01904167.2011.585206

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

SILVER-INDUCED CHANGES IN THE NUTRIENT

AND TRACE ELEMENT UPTAKE BY WHEAT AND AMOUNT
OF THE RHIZOSPHERE PROTEINS

2
ainen,

Irina Shtangeeva,1 Salla Venal

Helina Hartikainen,2 Marina Surgik,1
1
and Sergey Timofeev
1
Chemical Department, St. Petersburg University, St. Petersburg, Russian Federation
2
Department of Applied Chemistry and Microbiology, University of Helsinki, Helsinki,
Finland

The information on biogeochemistry of silver (Ag) is scarce and mechanisms of Ag uptake by

plants are still unclear. We studied the impact of silver sulfate (Ag2 SO4 ) and silver nitrate (AgNO3 )
on biomass of wheat seedlings, the rhizosphere proteins and uptake of nutrients and trace elements.
Most part of Ag was accumulated in roots. Concentrations of Ag in leaves remained the same as
in control plants. Both treatments (Ag2 SO4 and AgNO3 ) affected biomass of the seedlings. Plant
biomass was decreased more after treatment with AgNO3 . Both Ag2 SO4 and AgNO3 reduced leaf
concentrations of sodium and barium and root concentrations of calcium. Over time (three days),
protein concentration in the rhizosphere of control plants and plants treated with AgNO3 increased,
whereas treatment with Ag2 SO4 reduced concentration of the rhizosphere proteins. In soil treated
with Ag2 SO4 only low-molecular-weight proteins were found. In the control soil and in soil treated
with AgNO3 we also observed polydisperse fraction.
Keywords:

silver, wheat seedlings, nutrients, trace elements, soil proteins

INTRODUCTION
Generally the list of commonly accepted so-called heavy metals includes few trace elements, both metals and metalloids such as arsenic (As),
cadmium (Cd), chromium (Cr), copper (Cu), mercury (Hg), nickel (Ni),
lead (Pb), selenium (Se), and zinc (Zn). Until now, there is not much information on biogeochemistry of many other trace and ultratrace elements.
Among them, silver (Ag) is one of the most interesting trace metals, although
the literature about Ag environmental chemistry is scarce.
Received 22 May 2009; accepted 29 September 2009.
Address correspondence to Irina Shtangeeva, Chemical Department, St. Petersburg University,
Universitetskaya nab., 719, St. Petersburg 199304, Russia. E-mail: shtangeeva@gmail.com

1497

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

1498

I. Shtangeeva et al.

Ag is relatively rare in the Earths crust. The average Ag concentration

in soils is 100 g kg1, ranging from 10 to 5000 g kg1 (Kabata-Pendias,
2000). Silver is a normal trace constituent of many organisms. In terrestrial
plants, Ag concentration is usually less than 0.1 mg kg1 dry weight (Smith
and Carson, 1977). Even if the soil is amended with Ag-containing sewage
sludge or the plants are grown on tailings from Ag mines, the accumulation of Ag by terrestrial plants from soils is low and takes place mainly in
the root system (Ratte, 1999). On the other hand, water-grown plants can
accumulate rather large amounts of Ag. The ability to accumulate dissolved
Ag varies widely between species. Some reported bioconcentration factors
for marine organisms (calculated as milligrams of Ag per kilogram fresh
weight organism divided by milligrams of Ag per liter of medium) are from
210 in diatoms to 18,700 in oysters. Bioconcentration factors for freshwater
organisms have been reported to range from negligible in bluegills (Lepomis
macrochirus) to 60 in daphnids. It should be noted that these values represent uptake of bioavailable Ag in laboratory experiments (Howe and Dobson,
2002).
The mechanisms of Ag uptake by plants are still unclear. One might
anticipate that Ag+ could enter the plant cells via transport system involving another monovalent cation, for example, potassium (K +). However, an
increase of K + of 25 times did not inhibit Ag uptake (Fortin and Campbell, 2000). On the other hand, an exposure to sub-lethal Cu concentrations
(500 nM at pH 5) inhibited Ag uptake by 60% compared to the Cu-free
control (Macfie et al., 1994). Cu+ and Ag+ have similar chemical properties (ionic charge, affinity for thiol ligands and chloride), which suggest the
possibility of competition between these two ions. Ionic silver (Ag+) is also a
physicochemical analogue of ion sodium (Na+) and consequently appears to
enter the ion transporting cells via sodium channels (Bury and Wood, 1999).
Inside the cell, Ag can disrupt carbonic anhydrase and Na+, K +-ATPase, the
ionoregulatory enzymes that drive Na transport (Morgan et al., 1997, 2004).
Despite Ag+ is an analogue of alkali metals, there are many essential differences between these cations. Silver has a smaller ionic radius and, thus, in
contrast to other alkali metals, it can easier form complexes with polar ions
and molecules of varying biological activity. The biological effects of these
chemical compounds may be rather different. In particular, it was reported
that toxicity of silver sulfate (Ag2 SO4 ), even at high total concentrations, is
low. On the other hand, silver nitrate (AgNO3 ) is known as one of the most
toxic Ag compounds (Ratte, 1999).
The aims of this work were (1) to compare Ag uptake and Ag translocation within wheat Triticum aestivum L. seedlings cultivated in soil contaminated with two Ag compounds (AgNO3 and Ag2 SO4 ), (2) to examine the
Ag-induced changes in the uptake and translocation of nutrients and trace
elements, and (3) to monitor the variations in the amount of the rhizosphere
proteins resulting from increased soil Ag concentration.

Silver-Induced Changes

1499

Since young seedling stage is the most metal-sensitive stage for plant
(Bajji et al., 2002), it would be interesting to assess possible effects of Ag
exposure on the plants between very beginning (after seed germination)
and first stages of the plant growth.

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

MATERIALS AND METHODS

In a greenhouse experiment wheat Triticum aestivum L. (sort Umanka)
seeds were germinated on a moist filter paper. Uniformed four-day-old germinated seedlings were transferred to pots (20 seedlings in a pot) filled with
soil (7 kg of soil in each pot). The soil was classified as Ferric Podzol (FAOUNESCO, 1988) with a sandy loam texture. Before planting, the soil was
carefully mixed and watered as follows: one part of the pots (control) was
watered with 500 mL of deionized water, the second part with a solution of
AgNO3 , and the third part with a solution of Ag2 SO4 . Concentration of Ag
in the solutions was 30 mg L1. Just after this step, first (initial) soil samples
were taken from all the pots for analysis. Then the pots were watered every
day throughout the experiment. The temperature in a naturally illuminated
greenhouse was typically 25 C during the day and 22 C at night. The experiment was performed in triplicate. Plants and soil (the rhizosphere soil,
from surface of the plant roots) were collected within one and three days
after transfer of the seedlings to soil (at 10 a.m. and 7 p.m., each date of
sampling). The roots were separated from the leaves and their biomasses
were weighed. To estimate possible leaching of Ag to deeper soil layers we
also collected soil at the end of the experiment from the bottom of the pots
(from the part of a pot where roots could not penetrate). Just after sampling, the plants were carefully washed with ultrapure water to remove dust
and small particles of soil from the surface of the plant leaves and especially
from the plant roots. The soil and plant samples were air-dried at room temperature to a constant weight. Then they were digested for 16 minutes in
microwave oven (Ethos 1600 Advanced Microwave Lab, Milestone, Shelton,
CT, USA) using 10 mL of 65% nitric acid (HNO3 ) and 1 mL of hydrogen
peroxide (H2 O2 ), cooled for 3060 min and filtered through a filter paper
(Schleicher and Shull, Dassel, Germany). Concentrations of Ag, aluminium
(Al), barium (Ba), calcium (Ca), Cr, Cu, K, lithium (Li), magnesium (Mg),
manganese (Mn), sodium (Na), lead (Pb), and zinc (Zn) in the filtrates were
determined by inductively coupled plasma mass spectroscopy ICP-MS (Sciex
Elan6000, Perkin Elmer, Waltham, MA, USA). Additionally, we determined
the total amount of proteins in the soil samples. Each sample was thoroughly
mixed and air-dried. Proteins were extracted from the soil samples for 60
minutes using Tris buffer (66 mM), pH 8.0, triton X-100 (0.033%), ethylenediaminetetraacetic acid (EDTA) (1.5 mM) and guanidine thiocionate (4.4
M). After extraction, the samples were centrifuged at 10000 rpm for 10 min.

1500

I. Shtangeeva et al.

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

The method of Bradford (Bradford, 1981) was used to determine the total
amount of proteins using bovine serum albumin as standard. To identify
the molecular weights of the extracted proteins we used electrophoresis.
Data analysis was performed using STATISTICA for Windows 6.0 Software
package (StatSoft, Tulsa, OK, USA). The statistical treatment included a
calculation of mean concentrations of elements and analysis of variances to
estimate statistically significant differences between groups of the samples.
Additionally, cluster analysis was applied to experimental data to give a better insight into uptake of elements by plants and to assess the contribution
of specific factors that may have an effect on soil/plant interactions.

RESULTS AND DISCUSSION

The initial mean concentration of Ag in the control soil was 0.2 mg kg1.
This concentration was also found in the soil samples taken from the bottom
layer of all pots at the end of the experiment. Only in the treatment with
AgNO3 we observed some leaching of Ag to the deeper soil layers where
concentration of Ag increased to 0.6 mg kg1. Concentration of Ag in the
initial soil (just after adding Ag to the soil) was 17 and 15 mg kg1 for soils
treated with AgNO3 and of Ag2 SO4 , respectively. Growth of wheat seedlings
in the soil for three days did not result in any change in Ag concentration in
the bulk soil. However, content of Ag in the rhizosphere soil decreased up to
11.5 mg kg1 (both treatments), and Ag concentration in roots of the plants
grown in the soil increased significantly (Figure 1). Concentration of Ag in
leaves of all plants was rather low (below the detection limit, 0.05 mg kg1).
This finding agrees with reported data that in soil-grown plants Ag usually
does not translocate to the leaves in measurable amounts (Pettersson, 1976).
In this respect there is a big difference between soil-grown plants and plants
grown in Ag-enriched liquid media where concentration of Ag can increase
significantly not only in roots but also in leaves (Hirsch, 1998).
These contrasting responses of the plants grown in soil and in liquid
media provide evidence that soil constituents can efficiently retain Ag, thus
reducing its bioavailability. In particular, it was shown that humic and fulvic acids are important components affecting Ag cycling because they can
strongly bind Ag+ in soils (Jones and Peterson, 1986). Jacobson et al. (2005)
confirmed this finding in their systematic experiments with trace-level Ag
additions and provided evidence that the sorption is unaffected by the presence of monovalent cations such as K + and ammonium (NH4 +). Li et al.
(2004) reported that the sorption Ag+ on the humic acids and Fe oxides
becomes more irreversible with longer contact time between Ag+ and the
adsorbent.
Considering high concentration of Ag in roots of the wheat seedlings
grown in soil amended with AgNO3 and Ag2 SO4 we might assume that Ag

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

Silver-Induced Changes

1501

FIGURE 1 Dynamics of Ag in soil and in roots of wheat seedlings (after addition to soil Ag2 SO4 ). 1:
before plants were transferred to pots; 2: soil and plants were collected after one-day growth of the
seedlings in the soil; 3: soil and plants were collected after three-day growth of the seedlings in the soil.

could just be adsorbed onto the surface of the plant roots. However, previous
experiments (Teller and Klein, 1974) showed that careful washing of roots
of the plants exposed to Ag (in liquid media) removed only limited amounts
of Ag. This indicates that Ag was already bound to and/or complexed with
membrane constituents and possibly active sites on some enzymes and thus,
it could in turn affect the membrane permeability.
Both treatments (Ag2 SO4 and AgNO3 ) affected biomass of the seedlings
(Table 1). Effect of treatment with AgNO3 was more significant (dry biomass
of roots and leaves was statistically significantly lower compared to biomass
of control plants) than effect of treatment with Ag2 SO4 . As was reported,
AgNO3 could greatly decrease photosynthesis process (Akermoun et al.,
2002) On the other hand, Hirsch (1998) stated that the presence of Ag
sulfide in sludge-amended soils at concentrations as high as 106 mg Ag per
kg of soil did not affect growth and yields of corn, oat and turnip plants,
thus concluding that Ag sulfide can hardly influence adversely the crop
growth. Niemietz and Tyerman (2002) tested inhibition of water flux in
the cell membrane of soybean. The authors showed that among numerous
other transition elements investigated, only gold also inhibited water flux
in the membranes as much as silver did. It was concluded that silver is
the most potent inhibitor of aquaporins so far described. Falandysz et al.
(1994) reported that Ag+ ion added to the substrate in concentrations up to
10.3 mg kg1 did not exhibit toxic effects against mycelium and growth of
Agaricus Bisporus. Drew et al. (1981) found that small amounts of Ag might

1502

I. Shtangeeva et al.

TABLE 1 Dry biomass of wheat seedlings (mg) and concentrations of elements (mg kg1) in roots and
leaves of the plants

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

Control

Biomass1
Biomass2
Ag
Al
Ba
Ca
Cr
Cu
K,%
Mg
Mn
Na
Pb
Zn

AgNO3

Ag2 SO4

Roots

Leaves

Roots

Leaves

Roots

Leaves

128 13
531 9
<0.05
314 117
30.4 12.2
5590 2440
12.3 1.9
8.49 1.84
1.44 0.24
2660 623
63.0 16.2
7710 1690
7.39 4.89
234 66

215 44
992 47
<0.05
29.2 3.9
16.0 2.0
2590 854
6.66 1.13
6.70 1.34
2.57 1.22
1520 282
44.1 7.8
1600 330
2.08 0.45
62.2 12.0

456 28
13.2 3.6
224 89
22.7 8.1
1490 1870
14.0 4.6
7.60 0.45
1.20 0.13
2560 289
67.8 13.9
5990 1120
4.67 1.52
281 47

862 22
<0.05
23.9 5.1
12.7 2.2
2260 807
7.02 0.73
6.88 1.27
2.15 0.78
1630 380
46.8 11.8
779 120
2.34 0.24
61.9 5.9

497 17
35.5 43.8
236 49
17.3 2.6
1970 1540
9.99 1.29
9.13 1.95
1.31 0.25
2640 509
65.2 3.0
5830 1350
0.86 1.72
259 53

908 30
<0.05
22.9 4.1
12.2 2.0
1370 940
5.69 1.95
7.63 1.27
2.32 0.89
1540 330
43.4 11.4
844 244
1.10 1.30
62.4 1.8

1dry biomass of wheat seedlings before they were transferred to soil.

2dry biomass of the seedlings grown in soil for three days.
differences between control and treatments are statistically significant (P < 0.05).

provide positive effects on the plant development; however, as a result of Ag

bioaccumulation, there were indications of toxicity to the plants.
Figure 2 illustrates results of cluster analysis of soil samples. The statistical analysis was performed using data on concentrations of all elements
determined in the soils. The soil samples are well separated into initial soils
(before the soil was placed into pots) and those taken from the bottom of

FIGURE 2 Cluster analysis (Wards method) of initial (i) and bottom (b) soil samples. 1: control, 2:
after addition to the soil AgNO3 , 3after addition to the soil Ag2 SO4 .

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

Silver-Induced Changes

1503

the pots after the end of the experiment. As expected, there was significant difference between control soil and soils amended with Ag. We may
assume that main contribution to the separation was provided by higher
Ag concentration in the soils treated with Ag2 SO4 or AgNO3 compared to
that in the control soil. It should be also noted that in soil treated with
Ag2 SO4 concentrations of Ca and Ba (chemically similar elements) were
statistically significantly higher than those in the soil treated with AgNO3 . In
AgNO3 -treated soil, concentration of Mg was lower than in the control soil
(P < 0.05). Concentrations of other elements in the soils did not change
significantly after the treatments.
Figures 3 and 4 demonstrate results of cluster analysis of plants grown
in soil amended with different compounds of Ag. Leaves are rather well
separated into two groups: plants grown in soil enriched with Ag2 SO4 and
plants grown in soil enriched with AgNO3 (Figure 3). It is known that fertilization of soils with nitrogen (N) and sulfur (S) can affect differently plant
quality, including plant concentrations of essential nutrients (Finear and
Kausto, 2000; Qian and Schoenau, 2007). Lerner et al. (2006) reported that
N- and S-fertilizer application influenced various characteristics of wheat
plants, and the effect of N was more significant than the effect of S. We may
assume that such a separation of leaves of the plants grown in soil amended
with Ag2 SO4 and AgNO3 was rather provided by the effect on the leaves of
the wheat seedlings either S or N components of the Ag compounds. On
the other hand, we did not observe such a good separation in roots (Figure 4). Instead, regardless of the soil treatment, roots were divided into two
groups according to the date of sampling of the plants. Probably, this may be

FIGURE 3 Cluster analysis (Wards method) of wheat leaves. N- treatment with AgNO3 , S: treatment
with Ag2 SO4 . 1: plants were collected in one day after sowing, at 10 a.m.; 2: plants were collected in one
day after sowing, at 7 p.m.; 3: plants were collected in three days after sowing, at 10 a.m.; 4: plants were
collected in three days after sowing, at 7 p.m.

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

1504

I. Shtangeeva et al.

FIGURE 4 Cluster analysis (Wards method) of wheat roots. N: treatment with AgNO3 , S: treatment
with Ag2 SO4 . 1: plants were collected in one day after sowing, at 10 a.m.; 2: plants were collected in one
day after sowing, at 7 p.m.; 3: plants were collected in three days after sowing, at 10 a.m.; 4: plants were
collected in three days after sowing, at 7 p.m.

explained by different concentration of Ag in roots in the two sampling dates:

it increased significantly with time (see Figure 1).
Our results showed that despite the fact that roots absorbed almost all
Ag and concentration of Ag in leaves was kept very low (below the detection limit), concentration of Na and Ba in leaves decreased significantly
(P < 0.05) after treatment of soil with both Ag2 SO4 and AgNO3 (Table 1).
Besides, concentration of Ca in roots of the plants grown in soil enriched
with Ag was statistically significantly lower than that in the control plants.
Concentrations of other elements remained unchanged. As one can see,
relative sensitivity of roots and leaves to Ag was a bit different. As was mentioned above, Ag can affect Na transport in plant cells (Bury and Wood,
1999; Morgan et al., 1997). Therefore, the variations in plant Na concentrations might be expected. As was reported (Smith, 1971), the distribution of
Ba between plant tissues contrasted with that of Ca. Thus, differences in the
behavior of these two earth alkali elements may also take place. The balance
between different elements in plants is a basic condition of their proper
growth and development. Therefore, decrease in biomass of the seedlings
grown in Ag-enriched soil might be predictable.
Total amount of proteins in the soil collected from bottom of all pots
(bulk soil) at the end of the experiment was nearly the same for all the
treatments (Figure 5). Meanwhile, in the rhizosphere soil of the plants total amount of proteins varied significantly. Over time the amount of soil
proteins in control soil and in AgNO3 -treated soil increased (the variations
in treated with AgNO3 soil were more significant compared to control).
On the other hand, total concentration of proteins in the soil treated with
Ag2 SO4 decreased with time. Interestingly, in the soil treated with Ag2 SO4
only low-molecular-weight proteins were found (molecular weight is about

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

Silver-Induced Changes

1505

FIGURE 5 Variations in the total amount of proteins in the bulk and the rhizosphere soil (mg L1). 1:
soil was taken from the bottom of the pots (bulk); 2: initial soil; 3: the rhizosphere soil was taken from
the plant roots in three days after sowing, at 10 a.m.; 4: the rhizosphere soil was taken from the plant
roots in three days after sowing, at 7 p.m.

6000 dalton). In the control soil and in the soil treated with AgNO3 we also
observed polydisperse fraction with molecular weight from 6000 to 90000
dalton. Therefore, probably, not only Ag itself but also N and S components
of the Ag compounds could provide these effects.
CONCLUSIONS
Even after rather short (three days) growth of wheat seedlings in Ag2 SO4
and AgNO3 amended soil biomass of the plants decreased compared to
biomass of control plants. A more significant decrease was observed when
the plants were grown in soil enriched with AgNO3 . Wheat accumulated
large amounts of Ag. Almost all Ag from the rhizosphere soil was transferred
to the seedling roots. However, there was no translocation of Ag from roots
to leaves. As a result of growth of the plants in Ag-amended soil concentrations of some elements in roots and leaves changed. Concentrations of
alkali (Na) and earth alkaline (Ca and Ba) metals in the plants were affected
more than concentrations of other elements. The total amount of the rhizosphere proteins was also affected by the treatments. Concentration of the
soil proteins increased after treatment of soil with AgNO3 and decreased
after treatment of soil with Ag2 SO4 .
REFERENCES
Akermoun, M., E. Testet, C. Cassagne, and J.-J. Bessoule. 2002. Inhibition of the plastidial phosphatidylcholine synthesis by silver, copper, lead and mercury induced by formation of mercaptides with the
lyso-PC acyltransferase. Biochimica et Biophysica Acta 158: 2128.

Downloaded by [Irina Shtangeeva] at 11:37 10 July 2011

1506

I. Shtangeeva et al.

Bajji, M., J.-M. Kinet, and S. Lutts. 2002. Osmotic and ionic effects of NaCl on germination early
seedling growth, and ion content of Atriplex halimus (Chenopodiaceae). Canadian Journal of Botany
80: 297304.
Bradford, M. M. 1981. Minimization of variation in the response to different proteins of the Coomassie
Blue G Dye-Binding assay for protein. Analytical Biochemistry 116: 5364.
Bury, N. R., and C. M. Wood. 1999. Mechanism of branchial apical silver uptake by rainbow trout is via
the proton-coupled Na+ channel. American Journal of Physiology 277: R1385R1391.
Drew, M. C., M. B. Jackson, S. D. Giffard, and R. Campbell. 1981. Inhibition by silver ions of gas space
(aerechyma) formation in adventitious roots of Zea mays L. Subjected to exogenous ethylene or to
oxygen deficiency. Planta 153: 217224.
Falandysz, J., H. Bona, and D. Danisiewicz. 1994. Siver uptake by Agaricus bisporus from an artificially
enriched substrate. Z. Lebensm Unters Forsch 199: 225228.
FAO-UNESCO. 1988. Soil Map of the World, Revised Legend. World Soil Resource Report 60. Rome:
FAO.
Finear L., and S. Kausto. 2000. Variation in stemwood nutrient concentrations in Scotts pine growing on
peatland. Scandinavian Journal of Forest Research 15: 424432.
Fortin, C., and P. G. C. Campbell. 2000. Silver uptake by the green alga Chlamydomonas reinhardtii in
relation to chemical speciation: Influence of chloride. Environmental Toxicology and Chemistry 19:
27692778.
Hirsch, M. P. 1998. Availability of sludge-borne silver to agricultural crops. Environmental Toxicology and
Chemistry 17: 610616.
Howe, P. D., and S. Dobson. 2002. Silver and silver compounds: Environmental aspects,inter-organization
programme for the sound management of chemicals. Geneva: World Health Organization.
Jacobson, A. R., M. B. McBride, P. Baveye, and T. S. Steenhuis. 2005. Environmental factors determining
the trace-level sorption of silver and thallium to soils. Science of the Total Environment 345: 191205.
Jones, K. C., and P. J. Peterson. 1986. The influence of humic and fulvic acids on silver uptake by perennial
ryegrass, and its relevance to the cycling of silver in soils. Plant and Soil 95: 38.
Kabata-Pendias, A. 2000. Trace Elements in Soil and Plants, 3rd ed. Boca Raton, FL: CRC Press.
Lerner, S. E., M. L. Seghezzo, E. R. Molfese, N. R. Ponzio, M. Cogliatti, and W. J. Rogers. 2006. N- and
S-fertilizer effects on grain composition, industrial quality and end-use in durum wheat. Journal of
Cereal Science 44: 211.
Li, J., A. W. Rate, and R. J. Gilkes. 2004. Silver ion desorption kinetics from iron oxides and soil organic
matter: Effect of adsorption period. Australian Journal of Soil Research 42: 5967.
Macfie, S. M., Y. Tarmohamed, and P. M. Welbourn. 1994. Effects of cadmium, cobalt, copper, and
nickel on growth of the green alga Chlamydomonas reinhardtii: The influences of the cell wall and
pH. Archives of Environmental Contamination and Toxicology 27: 454458.
Morgan, I. J., R. P. Henry, and C. M. Wood. 1997. The mechanism of acute silver nitrate toxicity in
freshwater rainbow trout (Oncorhynchus mykiss) is inhibition of gill Na+ and Cl transport. Aquatic
Toxicology 38: 14516.
Morgan, T. P., M. Grosell, K. M. Gilmour, R. C. Playle, and C. M. Wood. 2004. Time course analysis of
the mechanism by which silver inhibits active Na+ and Cl uptake in gills of rainbow trout. American
Journal of Physiology 287: R234R242.
Niemietz, C. M., and S. D. Tyerman. 2002. New potent inhibitors of aquaporins: Silver and gold compounds inhibit aquaporins of plant and human origin. FEBS Letters 531: 443447.
Pettersson, O. 1976. Heavy-metal ion uptake by plants from nutrient solutions with metal ion, plant
species and growth period variations. Plant and Soil 45: 445459.
Qian, P., and J. J. Schoenau. 2007. Using an anion exchange membrane to predict soil available N and S
supplies and the impact of N and S fertilization on canola and wheat growth. Pedosphere 17: 7783.
Ratte, H. T. 1999. Bioaccumulation and toxicity of silver compounds: A review. Environmental Toxicology
and Chemistry 18: 89108.
Smith, K. A. 1971. The comparative uptake and translocation by plants of calcium, strontium, barium
and radium. I. Bertholletia excels (Brazil nut tree). Plant and Soil 34: 369379.
Smith, I., and B. Carson. 1977. Trace Metals in the Environment. Silver, vol. 2. Ann Arbor, MI: Ann Arbor
Science Publishers.
Teller, H. L., and D. A. Klein. 1974. Disposition and environmental impact of silver iodine in the national
Hail Research Expt. Operation Report No3. Fort Collins, CO: Colorado State University.