for Henry only

i attached the article to read and the questions to answer. Thank you

Article Assignment

Due date: December 11, 2012 by 1 pm

Influence of aluminum on the uptake of various cations from a solution into carrots

Read the article and answer the following questions:

1. What causes acidification of rain and what is the main effect of the acidification on crops?

2. Provide name of all elements that were utilized for preparation of multitracer solution.

3. Above what Al concentration was the deformation of carrot roots observed? At what AlCl3 concentration was the rate of cerium uptake into intact roots the highest? What is the pattern in uptake rate for rear earth elements?

4. What is the reported influence of Al3+ on the uptake of beryllium, strontium and barium by a carrot roots? What is responsible for this uptake?

5. Compare uptake of manganese, cobalt and zinc into roots and leaves at 0.002 ppm of Al.

Answers to all questions must be typed.

NOTE
: You may need to find secondary sources to answer question 1. In such case, you must cite your sources at the end of the assignment, following the examples below. Remember that reproducing text from a source verbatim is plagiarism, and such incidences can become part of your academic record.

How to cite a web page:

National Library of Medicine. Environmental Health and Toxicology: Specialized Information Services. http://sis.nlm.nih.gov/enviro.html (accessed Aug 23, 2004).

How to cite a scientific journal article:

Evans, D. A.; Fitch, D. M.; Smith, T. E.; Cee, V. J. Application of Complex Aldol Reactions to the Total Synthesis of Phorboxazole B. J. Am. Chem. Soc.
2000,
122, 10033-10046.

Effects of Ionic Valency
of Interacting Metal Elements

in Ion Uptake by Carrot
(Daucas carota cv. U.S.

harumakigosun)
TAKUO OZAKI,*,1 SHIZUKO AMBE,2 YOSHITAKA MINAI,3
SHUICHI ENOMOTO,2 FUMIO YATAGAI,2 TOMOKO ABE,2

SHIGEO YOSHIDA,2 AND YOSHIHIRO MAKIDE4
1Japan Atomic Energy Research Institute, Tokai,

Ibaraki, 319-1195, Japan; 2The Institute of Physical and
Chemical Research (RIKEN), Wako, Saitama 351-0198, Japan;

3Faculty of Humanities, Musashi University, Toyotama-kami,
Tokyo 176-8534, Japan; and 4Radio Isotope Center,

Tokyo University, Yayoi, Tokyo 113-0032, Japan

Received April 27, 2001; Accepted June 28, 2001

ABSTRACT

Interaction of elements in the course of element uptake by carrot
(Daucas carota cv. U.S. harumakigosun) exerted by the addition of ele-
ments, such as Rb, Zn, and Al, was investigated. For the purpose of pre-
cise evaluation of uptake behavior, the simultaneous determination of
absorption of Na, Be, Sr, Mn, Co, Zn, Ce, Pm, and Gd was conducted by
the multitracer technique. For root uptakes, Al exhibited its influence on
the uptake of essential elements and on the uptake of toxic or unbenefi-
cial ones, presumably as a result of the large electric valency that caused
cell membrane disintegrity. On the other hand, Zn as a divalent cation
only affected the uptake of essential and beneficial elements. Rubidium,
which is a monovalent cation, did not exhibit any effect on the uptake of
other ions. Concerning shoot uptakes, inhibition by Zn and Al, but not
by Rb, was observed for the uptake of Sr, Mn, Co, and Zn. From the pres-
ent investigation, it is suggested that there exists an interaction between
added ions and the elements taken into plants and that the degree of

Biological Trace Element Research 197 Vol. 84, 2001

© Copyright 2001 by Humana Press Inc.
All rights of any nature, whatsoever, reserved.
0163-4984/01/197–211 $13.75

*Author to whom all correspondence and reprint requests should be addressed.

interaction increases in the increasing order of ionic valency: M+ (Rb),
M2+ (Zn), and M3+ (Al).

Index Entries: Ion uptake; ionic valency; interaction; metal; muti-
tracer; toxic effect; Daucas carota.

INTRODUCTION

Generally, there exists a significant gap between nutrient concentra-
tions in soil or nutrient solution and the nutrient requirement of plants.
Soil and, in some cases, nutrient solutions may contain very high concen-
trations of nutrient elements, exceeding the capacity for appropriate
uptake balance. Therefore, various effects can be caused when plants are
exposed to unfavorable concentrations of more than one element. Alu-
minum and Mn toxicity in plants, for example, is a serious problem, which
is caused by acidic rain. It was elucidated that Al inhibits Ca uptake by
blocking Ca2+ channels in the plasma membrane (1) and inhibits Mg
uptake by blocking binding sites of transport proteins (2). High concentra-
tions of Mn2+ also inhibit Ca and, in particular, Mg uptake (3). Leaching of
metals from mining sites can also be a serious problem. An excess amount
of Cu was demonstrated to be an inhibitor for the uptake of Zn, affecting
plasma membrane–H+ ATPase activity (4). A study on the ion-competition
effects on the uptake revealed that the uptake of elements, in general,
decreases with an increase in the concentration of nutrient solution (5).

For the uptake of ions from the soil or nutrient solutions into the cyto-
plasm, the first important step is the binding of ions at the transport sites
in the plasma membrane. In the external solution, both cations and anions
are present in different concentrations and forms. Various interactions
between ions during their uptake are therefore to be expected. Competi-
tion between ions, particularly those with similar physical and chemical
properties, is expected, assuming that the number of the sites is small com-
pared to that of competing ions. For example, arsenate and phosphate are
taken up by the same transport system in plants (6). The examples of
strong competition between K+ and Rb+ and between anions such as SO42–
and SeO42– demonstrate that the selectivity of the binding sites in plasma
membranes is not a reflection of the function of a particular nutrient ele-
ment in plant metabolism, but only a reflection of the physicochemical
similarities between ions that are plant nutrients (e.g., K+ and SO42–).
Plants are thus unable to exclude unrequired ions from uptake. Most of all,
the driving force for each element to be attracted to the sites is electrostatic
power; therefore, electric valency is considered to be an important factor
for competition, particularly in the early process of ion uptake when the
biological toxic effect need not be taken into consideration. As a general
rule, the strength of interaction toward membrane constituents, such as
phospholipids and sulfolipids, and proteins is known to increase in the fol-
lowing order:

198 Ozaki et al.

Biological Trace Element Research Vol. 84, 2001

Uncharged molecules < M+ < M2+ < M3+

Conversely, the uptake rate often decreases in this order, suggesting
some role of ionic valency of interacting elements in ion uptake by plants.

The multitracer technique was developed by Ambe et al. using the
RIKEN Ring Cyclotron, which opened a new field in radiochemistry,
namely simultaneous tracing of the behavior of various elements (7–9). By
virtue of the high performance of the RIKEN Ring Cyclotron, ion beams,
such as 12C or 14N, can be accelerated up to 135 MeV/nucleon, which is
sufficiently strong to cause fragmentation reactions in target metals.
Application of this technique allows us to observe the behavior of various
elements at the same time. This is of great advantage, especially for bio-
logical samples from the point of view that biological samples are always
accompanied with relatively large individual differences, and metal toxic-
ity is not necessary to be taken into consideration because multitracers are
in a carrier-free state. The usability of this technique has been demon-
strated in plant research (5,10–15).

This study was conducted in an attempt to evaluate the effects of
valency of added metal cations on the uptake of various elements by car-
rot. In this investigation, Al, Zn, and Rb were chosen as representatives for
trivalent, divalent, and monovalent ions, respectively.

MATERIALS AND METHODS

Preparation of Plant Samples

Carrot (Daucas carota cv. U.S. harumakigosun) was selected as a sam-
ple species, because it thrives well in a hydroponic culture and grows
quickly. Surface sterilized seeds of carrot were germinated on filter paper
and afterward the seedlings were grown on Kureha Horticulture soil,
purchased from the Kureha Chemical Industry Co., Tokyo., for 20 d in a
growth chamber under the controlled climatic conditions (day/night
16/8 h; light intensity: 150 µmol/m2/s; temperature: 25±2°C; relative
humidity: 70–80%). The plant samples of approximately 7 cm in length
were transplanted to ultrapurified water and maintained there for 3 d
with constant bubbling of air under the same photoperiod and tempera-
ture as above. For the purpose of minimizing the effect of the adherent
soil and of injury to root surfaces caused by transplantation, the ultrapu-
rified water was changed every several hours. Additional details are
described in the literature (16,17).

Preparation of a Multitracer Solution

A 300-µm-thick Au plate was irradiated with a 135-MeV/nucleon 12C or
14N ion beam accelerated by the RIKEN Ring Cyclotron. The irradiated Au
target containing various kinds of radioisotope was dissolved in aqua regia

Effect of Ionic Valency on Metal Ion Uptake 199

Biological Trace Element Research Vol. 84, 2001

and this acid solution was evaporated to near dryness. After the residue was
dissolved in 1.5 mol/dm3 HCl, a Au ion was completely extracted with ethyl
acetate, leaving the radioisotopes as a multitracer in carrier- and salt-free
states. Additional details are described in the literature (9).

Preparation of Al, Zn, and Rb Solutions

For the preparation of the cation solutions of which the effects on the
uptake of various elements were to be observed, standard Al, Zn, and Rb
solutions for the atomic absorption were purchased from Wako-Junyaku
Japan. The solution was gently evaporated to remove the acid in the orig-
inal standard solutions. By diluting the solution with ultrapurified water,
solutions with desired concentrations of Al, Zn, or Rb containing the
multitracer were obtained. The pH of solutions was adjusted to 4.5 ± 0.2
using 0.01 mol/dm3 HCl. Final concentrations were 74, 7.4, 0.74, 0.074, and
0.0074 µmol/dm3 for Al, 31, 3.1, 0.31, and 0.031 µmol/dm3 for Zn, and 120,
1.2, and 0.12 µmol/dm3 for Rb.

Uptake Experiment and Measurement

An uptake experiment was performed over 2 d with the roots of sam-
ples kept in 50 mL of Al, Zn, or Rb multitracer solution. After the uptake
period, the roots were thoroughly washed with distilled water and
0.1 mol/dm3 HCl, then blotted dry with filter paper. The plant bodies were
divided into roots and shoots and then dried at 30°C. The γ-rays released
from each radioisotope in the samples were measured with pure Ge detec-
tors. Each radioactive nuclide in the multitracer was identified on the basis
of its γ-ray energy and half-life.

RESULTS AND DISCUSSION

After 2 d of cultivation, no visible symptom of metal toxicity was
observed with respect to plant growth, so that the results obtained in this
research can be evaluated as attributable to the competition effects, and
not resulting from biological toxic effects of the elements added. The pH of
solutions measured at the end of the uptake period was the same as that
of the initial pH of the solutions (4.5 ± 0.2). The uptake ratio was evaluated
in terms of the percentage of administered dose per gram of plant shoots
and roots as

Uptake ratio (%) = 100 × (radioactivity in each part / total amount of
radioactivity added to the uptake solution) / fresh weight

of the corresponding part

In order to be able to grasp the extent of the impact of the added
cations, we adopted the relative uptake value for which the uptake ratio of
each element was normalized by that for 0 µmol/dm3 of Al, Zn, or Rb in

200 Ozaki et al.

Biological Trace Element Research Vol. 84, 2001

the uptake solution. Each datum point in the Figs. 1–6 are expressed as the
mean ± standard deviation of five to seven replications.

Root Uptake

In roots, ions from the external solution can accumulate in the free
space. The portion adsorbed exogenously on the surface of the roots is con-
sidered to be desorbed by washing with 0.1 mol/dm3 HCl, whereas the
other portion that has permeated the cytoplasm or the unexchangeable
fraction in the apoplast where carboxylic groups function as cation
exchangers cannot be washed out with the HCl solution. Previous work
demonstrated that the uptake of all elements studied into the intact roots
was much higher than that into the excised roots. These results indicate
that the uptake of elements occurred primarily as a biological process and
not just as a result of adsorption (16). Based on this, we discuss the effect
of each cation with different valencies on the uptake of other elements.

Figure 1 shows the relative uptake of Be and Sr by the roots. The
uptake of Be increased by almost threefold that without Al at an Al con-
centration of 0.074 µmol/dm3, then decreased with increasing Al concen-
trations, whereas no influence was exerted by Zn and Rb. Transporters act
as catalysts, performing vectorial reactions where ions are conveyed
specifically from one side to the other. The transporters must possess spe-
cific binding sites for ions. However, Be is regarded as a toxic element to
plants, so that no specific mechanisms are expected for Be uptake. The
observed increase would be best accommodated by influx via transporters
that should not convey Be by nature. Extensive research has been per-
formed on the competitive inhibition of ion uptakes by Al (18,19). The tox-
icity of Al is exerted in various ways, and one of them involves
interference with the physiological processes of plant cells (20). As a triva-

Effect of Ionic Valency on Metal Ion Uptake 201

Biological Trace Element Research Vol. 84, 2001

Fig. 1. Relative uptake of Be and Sr by roots with either Al (●), Zn (◆), or Rb
(■) added in the uptake solution. Values are normalized with those for 0 µmol/dm3
Al, Zn, or Rb. Error bars represent standard deviations for five to seven replications.

202 Ozaki et al.

Biological Trace Element Research Vol. 84, 2001

F
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Effect of Ionic Valency on Metal Ion Uptake 203

Biological Trace Element Research Vol. 84, 2001
F
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lent cation, Al favors a high transmembrane electropotential by reacting
with negatively charged groups, thereby influencing the physicochemical
properties and function of biomembranes. The above results indicate that
the physiological interaction on the surface of cells was exerted by Al, par-
ticularly because of its large electric valency compared with those of Zn
and Rb. It may be also true that the influence was enhanced in the absence
of Ca in the uptake solution. One of the functions of Ca in plants is to
maintain membrane stability, playing an important role in the selectivity
of ion uptake (21).

Strontium uptake by roots was affected by the presence of Al and also
Zn, but not that of Rb (Fig. 1). Zinc at 31 µmol/dm3 suppressed the uptake

204 Ozaki et al.

Biological Trace Element Research Vol. 84, 2001

Fig. 4. Relative uptake of Na by shoots with either of Zn (◆) and Rb (■)
added in the uptake solution. Values are normalized with those for 0 µmol/dm3
Zn or Rb. Error bars represent standard deviations for five to seven replications.

Fig. 5. Relative uptake of Be and Sr by shoots with either Al (●), Zn (◆), or Rb
(■) added in the uptake solution. Values are normalized with those for 0 µmol/dm3
Al, Zn, or Rb. Error bars represent standard deviations for five to seven replications.

Effect of Ionic Valency on Metal Ion Uptake 205

Biological Trace Element Research Vol. 84, 2001
F
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of Sr by approximately 0.3-fold compared to that without Zn. Aluminum
enhanced Sr uptake slightly in the concentration up to 0.74 µmol/dm3 and
then suppressed it to almost one-third at a concentration of 74 µmol/dm3.
Strontium is regarded as a beneficial element to plants because of its abil-
ity to perform the function of Ca to some extent (22). Most of the influence
on the uptake of Sr, therefore, is inferred as the interaction caused by Al
and Zn on the binding sites of Ca-transporting compounds, by which Sr2+
should be transported. Calcium stabilizes cell membranes by bridging
phosphate and carboxylate groups of phospholipids (23), preferentially at
membrane surfaces (24). Calcium can be replaced fairly readily from its
binding sites at the outer surface of the plasma membrane with metal
cations of high concentrations (25). The replacement of plasma membrane-
bound Ca by Al was suggested as the causative factor of Al toxicity
(26–28). The replacement of plasma membrane-bound Ca by high external
concentrations of Na is the main factor involved in salinity stress (25,29).
Based on these reports and our results, it is inferred that Zn also has the
ability to replace Ca, the degree of which is higher than Rb and smaller
than Al.

The effects of Al on the uptake of Mn, Co, and Zn are shown in Fig. 2.
The uptake of Zn was elevated by the presence of Al up to 0.074 µmol/dm3
and then decreased with increasing Al concentrations. A similar behavior
was also observed for Co uptake. In contrast, the uptake of Mn was almost
constant up to 0.074 µmol/dm3 Al concentration and then decreased with
the increase in Al concentrations. The influence of Zn on the uptake of Mn
and Co was also observed. The uptake of Mn and Co decreased with the
increase in Zn concentration; 31 µmol/dm3 of Zn suppressed the uptake of
Mn and Co to approximately 0.2-fold compared to that in the absence of
Zn. In the case of Zn, the relative uptake of Zn decreased with increasing
Zn concentration. However, the absolute amount of Zn absorbed by the
roots increased. The strong competition between Zn and Mn observed in
this study is in agreement with observations of Mn deficiency induced in
crop plants in the presence of extraordinarily high concentrations to Fe2+
(30); the uptake of Mg and Fe is inhibited by Zn. Concerning nonessential
elements, inhibition by Zn is also reported. Zinc inhibits Cd uptake
because of their similar physicochemical properties (31). The result
obtained in this investigation indicates that high amounts of Zn, in some
way, blocked the binding or transport sites for Co. The presence of Rb
showed no influence on the Mn, Co, and Zn uptake.

As seen in Fig. 3, no significant effect was observed on the uptake of
lanthanides (Ce, Pm, and Gd) in the case of Rb and Zn addition. On the
other hand, lanthanide uptake was enhanced by up to 7.4 µmol/dm3 Al
concentration and suppressed by 74 µmol/dm3 Al concentration. Lan-
thanides are regarded as neither essential nor beneficial elements for ordi-
nary plants and their uptakes into cells are considered to arise via
transporters of Ca, because of their physicochemical similarities to Ca,
such as in the ionic radius (32). It is deduced, therefore, that the enhance-

206 Ozaki et al.

Biological Trace Element Research Vol. 84, 2001

ment observed in the uptake of lanthanides was mainly attributable to the
uptake via Ca transporters, whose function and/or selectivity was deteri-
orated by Al.

Competition between monovalent ions has been reported: Physio-
logically, detrimental concentrations of Na is known to inhibit K uptake
(33). Rubidium and Cs were shown to partially reduce or block high-
affinity K transporter-mediated K+–Na+ uptake (34). Inhibition of
uptake of divalent ions was also reported: Potassium competes quite
effectively with Mg and strongly depresses the uptake rate of Mg (35).
In this study, however, inhibition of the root uptake of divalent and
trivalent ions by Rb was not observed. One of the possible reasons for
this is Rb concentration; rubidium at higher concentrations might
exhibit its inhibition effects.

Deviations (standard deviations) of relative uptakes obtained in the
presence of Al, Zn, and Rb from those in the absence of Al, Zn, and Rb
were calculated for roots to determine the extent of the influence of added
elements (Table 1). The deviations for root uptakes in the case of Rb addi-
tion were approximately one order of magnitude smaller than those for Zn
and Al addition, showing the small impact from Rb than those from Zn
and Al. The deviations for all the elements in the case of Zn addition were
smaller than those in the case of Al addition, especially with regard to
unbeneficial elements.

Effect of Ionic Valency on Metal Ion Uptake 207

Biological Trace Element Research Vol. 84, 2001

Table 1
Deviations (Standard Deviations) of Relative
Uptakes for Roots Obtained in the Presence
of Al, Zn, and Rb from Those in the Absence
of Al, Zn, and Rb, Calculated to Determine

the Extent of the Influence of Added Elements

Shoot Uptake

The uptake in shoots was observed for Na, Be, Sr, Mn, Co, and Zn. The
radioactivity of lanthanides was not detected in the shoots. It was reported
that many elements that are not regarded as useful for plant growth are
retained in the roots, not permitting their translocation into the shoots.
This corresponds with the observation for lanthanides, which are recog-
nized as neither essential nor beneficial for ordinary plants. However, lan-
thanides were determined in various kinds of plant grown under natural
conditions (36–38). A conceivable reason for the result, therefore, is that
this experiment was conducted for a relatively short period.

As seen in Fig. 4, Na uptake was observed in shoots in the case of Rb
or Zn addition. There were no data for Al where Na radioactivity was too
weak to be detected in the original multitracer solution. The uptake of
Na was decreased with increasing Zn concentration in the uptake solu-
tion, whereas Rb did not exhibit any effect on it. Considering the compe-
tition concept, competition is expected to occur, particularly between
ions with similar physicochemical properties. It is suggested that the dif-
ference in ionic radii between Na and Rb was so large for the transport
mechanisms in the plant species that no influence was exerted by Rb
addition, although they are both alkaline elements. Elements such as Cs
and Re were found to be absorbed by plants and transported to shoots
smoothly and only a very small portion remained in roots because of
their low interactions with the roots (5). In this research, Na was
observed only in shoots, suggesting a smooth uptake of the element by
the plant species. Sodium uptake from solutions by rice was studied, in
which about 20% of Na added in the uptake solution was absorbed by
roots, whereas 40% was transported to shoots after 130 d of cultivation
(39). These results suggest that the distribution of Na between shoots and
roots depends on the plant species, although differences in experimental
conditions, such as salt composition and concentration, and culture
period must be taken into consideration also.

As seen in Fig. 5, the elevation in the uptake by Al addition was not
observed for Be and Sr, even at Al concentrations at which the absorp-
tion into roots was elevated. The uptake of Be was reduced by the addi-
tion of Al to the uptake solution, giving almost the same uptake values
for all of the concentrations of Al. The effect of Zn addition on Be uptake
appeared only in the high concentration range. A 37-µmol/dm3 Zn
treatment indicated the occurrence of a heavily injured metabolism
associated with the disfunction of the mechanisms regulating the
translocation of Be from the roots to the shoots. It was also reported that
the uptake ratio of Be in turnip shoots decreased with an increase in the
nutrient concentration (5). Decreases in the uptake by shoots were
observed for Sr with increasing Al and Zn concentrations. At any con-
centration of Rb, the uptake of Be and Sr was almost the same as that
without Rb.

208 Ozaki et al.

Biological Trace Element Research Vol. 84, 2001

Figure 6 shows the effects of Al, Zn, and Rb concentrations on the
relative uptake of Mn, Co, and Zn. The relative uptake of Mn decreased
with the increase in the concentrations of Al and Zn, whereas it
remained almost same for all the concentrations of Rb. The addition of
Al and Zn reduced the relative uptake of Co markedly. In the case of Rb
addition, the decrease in the Co uptake was not evident because the
standard deviation for each value was large. The relative uptake of Zn
was reduced by the addition of Al, whereas it remained at the same level
with and without Rb.

In the presence of Zn, the relative uptake of Zn in the shoots
decreased with increasing Zn concentration. However, the absolute
uptake of Zn in the shoots increased with the Zn concentration, as
observed for the roots. The highest concentration of Zn (31 µmol/dm3)
used in this study corresponds to the concentration of Zn in a nutrient
solution. Zinc is an essential element. It is evident that the plants
cultured in an uptake solution with the Zn concentration less than
31 µmol/dm3 are deficient in Zn. The obtained results indicated that the
Zn uptake is restricted to some extent, in spite of the deficiency. This sug-
gests that the first important step in the ion uptake is chemical adsorp-
tion into the apoplast resulting from chemical equilibration between the
uptake solution and roots.

Deviations calculated for shoot uptakes are listed in Table 2. Those of
Be and Sr in the case of Rb addition are approximately one order of mag-
nitude smaller than those for Zn and Al. On the other hand, the differences
in Mn, Co, and Zn uptakes are much smaller compared with those for root
uptakes, suggesting complex physiological processes in translocating the
elements inside the cytoplasm.

Effect of Ionic Valency on Metal Ion Uptake 209

Biological Trace Element Research Vol. 84, 2001

Table 2
Deviations (Standard Deviations) of Relative
Uptakes for Shoots Obtained in the Presence
of Al, Zn, and Rb from Those in the Absence
of Al, Zn, and Rb, Calculated to Determine

the Extent of the Influence of Added Elements

ACKNOWLEDGMENTS

We are grateful to Dr. F. Ambe for his helpful suggestions. We are also
grateful to Dr. Y. Yano, Dr. M. Kase, and the staff of the RIKEN Accelerator
Research Facility for their cooperation in the beam irradiation.

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