Journal of Experimental Botany, Vol. 54, No. 381, pp. 349±354, January 2003
DOI: 10.1093/jxb/erg016
RESEARCH PAPER
The uptake and partitioning of cadmium in two cultivars of
potato (Solanum tuberosum L.)
K. R. Dunbar1, M. J. McLaughlin2 and R. J. Reid3,4
1
Department of Soil and Water, Adelaide University, Waite Campus, Private Bag 1, PO Glen Osmond, SA 5064,
Australia
2
CSIRO Land and Water, PMB 2, Glen Osmond, SA 5064, Australia
3
Department of Environmental Biology, Adelaide University, Adelaide 5005, Australia
Received 26 August 2002; Accepted 2 September 2002
Abstract
Introduction
The uptake and distribution of Cd in potatoes over
the course of a growing season was investigated in
two cultivars of potatoes that differed in tuber Cd
concentration. Plants were grown in soil with supplemental Cd. The concentrations of Cd in different tissues varied greatly in the order roots>shoots>>
tubers. After the initiation of tuber bulking, shoot
growth ceased and the increase in total plant Cd was
mostly due to accumulation in the tubers. The constancy of the Cd concentration in shoots suggested
that import of Cd via the xylem must be matched by
export in the phloem, which implied that Cd must
have signi®cant phloem mobility. It was found that
the differences in tuber Cd between cultivars
Wilwash and Kennebec were not due to differences
in total uptake or growth, but to differences in Cd
partitioning within the plant. This partitioning was
speci®c to Cd and was not observed for a range of
nutrient elements. Most of the differences in tuber Cd
concentration between the cultivars could be
accounted for by a 3-fold higher retention of Cd in
the roots of cv. Wilwash. The involvement of root
sequestration, and xylem and phloem pathways in
the loading of Cd into tubers is considered.
High cadmium concentrations in soils can arise naturally,
but more often are due to industrial contamination or
through application of agricultural fertilizers containing
high levels of Cd (Tiller et al., 1997). The possibility of
transfer of this contamination to humans through the food
chain has led food authorities to set a limit on the amount
of Cd allowed in foods for human consumption. Of
particular concern is the concentration in the tubers of
potatoes which may contribute more than 50% of the
dietary intake of Cd (Stenhouse, 1992). There is now an
imperative to ®nd ways of limiting the amount of Cd
accumulated in the tubers.
As with many other plants, potato cultivars have been
shown to differ in their ability to accumulate Cd, although
the differences between cultivars are not consistent. Harris
et al. (1981) found no differences in the tuber Cd
concentration of six cultivars grown in a metal-contaminated ®eld. McLaughlin et al. (1997), however, found that
cultivars grown commercially in Australia exhibited
signi®cant differences in tuber Cd concentration, with a
2±3-fold variation in tuber Cd concentration attributable to
cultivar alone.
It is not known how differences in tuber Cd arise,
whether it is due to increased uptake from the soil, or
to differences in partitioning of total Cd within the
plant. In maize, Florijn and Beusichem (1993) compared the uptake and distribution of Cd within six
inbred lines and found that distribution rather than
uptake was the factor most affecting genotypic differences in shoot Cd concentrations.
Key words: Cadmium, heavy metals, phloem translocation,
potato tuber, xylem transport.
4
To whom correspondence should be addressed. Fax: +61 8 8303 6222. E-mail: [email protected]
Journal of Experimental Botany, Vol. 54, No. 381, ã Society for Experimental Biology 2003; all rights reserved
350 Dunbar et al.
The aim of this study was to analyse the pattern of Cd
accumulation in potatoes and to try to determine the factors
that lead to differences in tuber Cd between different
cultivars.
Materials and methods
Plant material and growth conditions
Two cultivars of potato (Solanum tuberosum L.), cv. Wilwash and
cv. Kennebec, were grown in pots in a glasshouse in soil
supplemented with Cd. In previous ®eld trials (McLaughlin et al.,
1994) cv. Kennebec was shown to accumulate an average of 48 mg
Cd kg±1 fresh weight (FW) in tubers and was classi®ed as a high Cd
accumulator. By contrast, cv. Wilwash was classi®ed as a low
accumulator, having an average tuber Cd concentration of 34 mg kg±1
FW.
Plants were grown in free-draining pots containing 15 kg of Mt
Compass sand and watered daily with 1.0 l of nutrient solution. The
nutrient solution comprised (mM) 3.0 KNO3, 1.0 MgSO4, 0.5 NaCl,
2.5 CaNO3, 0.5 K2SO4, and 0.5 KH2PO4. Micronutrients (in mM)
were 20 B, 20 Mn, 10 Zn, 1.0 Cu, and 0.5 Mo. Iron (25 mM) was
added as a complex with DTPA. The solution was adjusted to a pH
of 5 with NaOH. Cadmium was added to the solution as CdCl2 at a
concentration of 10 nM to represent the concentration of Cd in the
soil solution of a non-polluted soil (McKenna et al., 1993).
Speciation calculations using GEOCHEM-PC (Parker et al., 1995)
indicated that all of the Cd in solution was free Cd2+ ion. Prior to
planting each pot of sand was leached with 2.0 l d±1 of nutrient
solution for 5 d to ensure saturation of the binding sites within the
sand.
Plant harvest
Plants were harvested once per week for a total of 10 weeks, with the
®rst harvest occurring 4 weeks after planting. Pots were arranged in a
randomized block design with four replicates per treatment. At
harvest, the plants were detopped at the base of the stem and divided
into new leaves (being the ®rst four leaves from the growing apex)
and old leaves (the remaining leaves). The roots and tubers were
collected by carefully washing away the sand. The leaves of each
plant were gently washed in a 0.1% solution of Decon to ensure
removal of any soil particles. They were then rinsed in RO water
followed by a rinse with distilled water and blotted dry. Roots were
thoroughly washed with tap water and desorbed for 10 min in a 5
mM solution of CaCl2, followed by rinsing in distilled water.
Results
Growth and development of potato tissues
The ®rst harvest was conducted approximately 6 weeks
after sprouting. At this stage much of the ®nal aboveground biomass was already in place and root development
was well advanced. Stolons were very short and some
tubers had started to develop. The main changes in
subsequent harvests were in the increase in stolon roots
and in the mass of the tubers. Tuber bulking began in both
varieties around 8 weeks after planting. The growth of cv.
Kennebec is shown in Fig. 1a. After about 6 weeks (harvest
3) the increase in plant weight was due entirely to the
increase in tuber weight. The pattern in cv. Wilwash was
almost identical (data not shown).
Comparison of Cd accumulation between cultivars
Kennebec and Wilwash
The accumulation of Cd in the different tissues of
Kennebec as a function of time is shown in Fig. 1b. In
the early stages, most of the plant Cd was found in the
shoots but after about 8 weeks, net Cd uptake was almost
entirely the result of increasing tuber Cd. It was surprising
to ®nd that the amount of Cd in the shoots did not continue
to increase after shoot maturity, over the 5 weeks of tuber
bulking. The overall pattern of Cd accumulation is easiest
to see by looking at the changes in concentration in the
tissues over time (Fig. 2). Comparison of the growth data
Plant analysis
Tubers were prepared for analysis as described by McLaughlin et al.
(1995). All plant material was oven dried at 75 °C for 2 d and ground
to less than 500 mm in a stainless steel mill. Dry material (~0.5 g) of
each sample was then digested in 5 ml of concentrated nitric acid
until clear and diluted to 20 ml with 0.016 M nitric acid.
The Cd concentration of each plant component was obtained by
atomic absorption spectroscopy with graphite furnace atomization.
The concentration of other elements was determined by inductivelycoupled plasma atomic emission spectroscopy (ICP).
Field trial
In addition to the glasshouse experiment, tubers of the two potato
varieties examined were also obtained from a ®eld trial in Victoria,
southern Australia. The tubers were analysed for mineral nutrients
and a comparison was made with the nutrient composition of the
glasshouse-grown tubers.
Fig. 1. Growth pattern of potato cv. Kennebec. Sprouted tuber
sections were planted at week 0. Values are mean 6SE of 4 plants.
Cd uptake in potatoes 351
Fig. 2. Uptake and partitioning of Cd into different tissues of potato
cultivars. Values are mean 6SE of 4 plants.
in Fig. 1a with Cd concentrations in the various tissues
shows that, in the case of shoots, once the tissue stopped
growing there was no further net input of Cd to that tissue,
hence the tissue concentration remained relatively constant. Similarly, in the case of tubers, the constancy of
concentration was due to the matching of Cd input to
tubers with increase in dry weight.
The striking difference between the two varieties was in
the concentration of Cd in roots. Whereas in Kennebec the
root Cd concentration remained steady after 6 weeks, the
concentration of Cd in the roots of Wilwash continued to
increase, except for the two weeks immediately after the
start of tuber bulking where the concentration plateaued.
The ®nal root Cd concentration in Wilwash was 9.0 mg g±1
DW compared to only 2.7 mg g±1 DW in Kennebec. In both
varieties the concentration of Cd in the roots greatly
exceeded that of the other tissues. The desorption
treatments were designed to remove most of the Cd
adsorbed onto the outside of the roots and, therefore, most
of the root Cd should have been symplastic rather than due
to binding in cell walls. On a dry weight basis, the
concentration of Cd in roots of Kennebec exceeded that in
tubers by more than a factor of 10 and was approximately
5-fold higher than the average shoot concentration. In
Wilwash, the root Cd concentration was more than 60-fold
higher than in the tubers and more than 15-fold higher than
in the shoots.
The differences in Cd concentrations in tissues other
than the roots is more clearly shown in Fig. 3. Whereas
Wilwash maintained higher Cd concentrations in all of the
components of the shoot, the concentration of Cd in tubers
was 60% higher in Kennebec, in agreement with previous
data from McLaughlin et al. (1993). The differences in Cd
concentration were established early in tuber development
and increased over time (data not shown).
The central question that this study sought to answer
was whether these differences in tuber Cd arose due to
naturally higher total plant uptake by cv. Kennebec, or to
differences in the distribution of Cd within the plant. Some
of the key parameters relating to growth and Cd accumulation in the two varieties are summarized in Table 1 for
the ®nal harvest. It can be seen that the growth habits of the
two varieties were similar, both in terms of total biomass
production and in tuber yield at ®nal harvest. The other
signi®cant features were the similarity in total Cd content
between the varieties and in the average plant Cd
concentration (Table 1). Thus the differences in tuber Cd
concentration could not be attributed to a difference in
growth or to a higher uptake of Cd into the plant as a
whole, nor to signi®cant differences in the yield of tubers.
Clearly the differences must have arisen through variation
in the partitioning of Cd between tubers and the rest of the
plant. The overall distribution of Cd in the two varieties at
®nal harvest is shown in Fig. 4. In Kennebec, 75% of the
total plant Cd was found in the tubers, whereas in Wilwash,
tuber Cd only accounted for 43%. On the other hand, roots
of Wilwash contained 42% of total Cd compared to only
14% in Kennebec. Shoots of Wilwash also contained
signi®cantly more Cd than Kennebec (Fig. 4).
These differences between varieties raise the question of
whether Cd is preferentially sequestered into non-tuber
tissues of cv. Wilwash, or whether the differences in
distribution arise coincidentally because of anatomical or
physiological factors that also dictate the partitioning of
Fig. 3. Comparison of the Cd concentration in tubers, leaves and
stems of cv Kennebec and cv Wilwash. Values are mean 6SE of 4
plants.
352 Dunbar et al.
Table 1. Comparison of growth, total plant Cd and concentrations of Cd in tubers and whole plant tissue of potato cvs Kennebec
and Wilwash
Values are the mean 6SE of 4 plants harvested 13 weeks after planting.
Total dry weight (g)
Total plant Cd (mg)
Plant Cd concentration (mg g±1 DW)
Tuber yield (g DW plant±1)
Tuber Cd concentration (mg g±1 DW)
Wilwash
Kennebec
Signi®cant difference
156615
47.664.3
0.30860.024
143614
0.14360.13
159610
48.963.1
0.28260.003
173610
0.23660.009
n.s.
n.s.
n.s.
n.s.
P <0.001
Fig. 4. Overall distribution of Cd in all tissues of potato plants after
13 weeks growth. Values are the mean of 4 plants.
other elements, notably nutrient elements. The pro®le of
mineral elements in leaves suggests that Cd is treated
differently. Comparison of the concentrations of mineral
elements in the two cultivars showed that, in leaves, the
concentrations in cv. Kennebec were similar (Mn, K, B,
Cu, S, Zn, P) or signi®cantly higher (Fe, Ca, Mg) than in
cv. Wilwash (Table 2). Cd did not conform to this pattern
and the concentration in cv. Kennebec was nearly half that
of cv. Wilwash. Concentrations of all elements, including
Cd, were higher in tubers of cv. Kennebec (Table 2). The
ratio of concentrations in leaves to concentrations in tubers
may be indicative of the ability of solutes to be mobilized
from leaves into the phloem, assuming the tuber does not
access signi®cant Cd through the tuber skin or stolon roots
(Reid et al., 2002). Certainly, in the case of Ca where the
ratios were 95 and 72 for cv. Wilwash and cv. Kennebec,
respectively, the results strongly support the view that
phloem is the major pathway for loading of mineral
elements into tubers. The ratios for all other elements were
much lower, but roughly consistent with the expected
mobility in phloem, with Mg, Mn and Fe displaying the
greatest differences between leaf and tuber concentrations
and Zn, S and P the lowest ratios (Table 2). Cd was
intermediate between these extremes.
The concentrations of all of the nutrient elements
examined was 1.5±2.2-fold higher in tubers of Kennebec
compared to Wilwash. As far as is known, such large
differences between cultivars have not previously been
reported for potatoes and the authors were interested to
discover whether this was a phenomenon peculiar to the
controlled glasshouse experiment or whether it was also
observed under ®eld conditions. Therefore, tubers from
both varieties were obtained from a ®eld trial in a potatogrowing region of southern Australia. Analysis of the
tubers showed that the concentration of nutrients in
Kennebec was 1.5±2.3-fold higher than in Wilwash (data
not shown) in good agreement with the glasshouse
experiments. The only exception was Ca which was
actually lower in Kennebec in the ®eld trial. The reason for
this is not known but may relate to differences in soil Ca.
The fresh weight to dry weight ratios of tubers gradually
decreased over the growth period but after 10 weeks the
values were quite similar for the two cultivars (Wilwash,
6.060.1; Kennebec, 5.560.1). Thus differences in nutrient
concentrations cannot be explained by differences in water
content of the tubers.
Discussion
The pathways for Cd movement around plants are poorly
understood. If it is accepted that little Cd is absorbed by
Cd uptake in potatoes 353
Table 2. Comparison of the concentrations of Cd and mineral nutrients in mature leaves and tubers of potato cvs Wilwash and
Kennebec
Concentrations are means 6SE (n=4) expressed as mg g±1 DW.
Element
Ca
Mg
Mn
Fe
Cd
K
B
Cu
S
Zn
P
Leaves
Tubers
Ratio leaves:tubers
Wilwash
Kennebec
Wilwash
Kennebec
Wilwash
Kennebec
227506479
81256281
34.060.6
53.461.6
0.5160.06
69 75063092
27.360.8
4.660.2
2175648
26.960.6
1518640
267506480
130256502
28.561.4
70.663.3
0.2860.03
70 50063476
26.361.8
4.060.3
2675685
23.460.7
1353623
238624
1245620
5.260.1
9.961.5
0.1560.01
23 2506750
10.160.3
3.060.2
19806108
25.261.1
22456108
370641
24256278
10.461.0
20.462.7
0.2460.01
41 75064347
22.263.4
6.160.4
33756202
36.961.4
37506357
95.4
6.5
6.5
5.4
3.5
3.0
2.7
1.5
1.1
1.1
0.7
72.3
5.4
2.7
3.5
1.2
1.7
1.2
0.7
0.8
0.6
0.4
direct uptake across the tuber periderm (Reid et al., 2002)
then input to the tuber must occur by redistribution of the
Cd absorbed by the basal roots. This could occur either in
the xylem or in the phloem. However, there is good
experimental evidence that functional xylem connections
to potato tubers do not exist, and that neither water nor Ca
are transferred directly from basal roots to tubers
(Wiersum, 1966; Baker and Moorby, 1969; Krauss and
Marschner, 1971; Gandar and Tanner, 1976; Kratzke and
Palta, 1985, 1986). Therefore inorganic nutrients and Cd
absorbed by basal roots must eventually be loaded into
tubers via the phloem. Since roots are sinks for
photosynthate, the direction of phloem movement would
be into rather than from roots. Therefore, the initial
traf®cking of mineral elements and Cd must occur via
xylem, at least until transfer into phloem tubes that are
connected to the tubers is possible. Reid et al. (2002)
showed using short-term experiments with 109Cd that rapid
exchange of Cd between stem and phloem was possible
and that Cd in leaves could be rapidly transferred to tubers.
On the basis of these previous studies, it seems
reasonable to conclude that the most likely pathway for
Cd movement into tubers is from the soil to basal roots to
shoots in the xylem, then back down to the tubers in the
phloem. A curious phenomenon that was uncovered in this
study was that once fully expanded, signi®cant net Cd
input into a tissue did not occur (with the exception of roots
in cv. Wilwash). In the case of leaves, this is dif®cult to
reconcile with the continued need for xylem input in order
to replace transpirational losses of water. Why then does
Cd not continue to be washed into leaves as a component
of the xylem ¯ow? It would seem a remarkable coincidence if the constancy of the Cd content of shoots were the
result of input via the xylem being exactly matched by its
export in the phloem. However, this seems to be the only
obvious conclusion that is consistent with the data. There
exist xylem connections between roots and leaves, and
phloem connections between leaves and tubers, as well as a
favourable concentration gradient for Cd ¯ow in this
direction (Figs 2, 3).
It has been clearly established in this study that the
genotypic differences in tuber Cd are due to differences in
partitioning and not to differences in total Cd uptake. The
principal difference between the genotypes was in the
proportion of total Cd that was retained in the roots and in
the leaves (Fig. 4). Comparison of the elemental composition of leaves between the two cultivars showed that while
the concentration of most elements was the same or lower
in cv. Wilwash, Cd was considerably higher. This suggests
that Cd is preferentially sequestered in cv. Wilwash, either
into physical compartments such as the vacuole or into
chemical complexes, thereby reducing its access to
transport in xylem and phloem. Previous studies on
intracellular Cd transport have established that Cd is
moved into the vacuole by two main routes, either by
complexation with phytochelatins (PCs) followed by
active transport of the PC±Cd complex across the tonoplast
(Vogeli-Lange and Wagner, 1990; Ortiz et al., 1995; Salt
and Rauser, 1995), or by H+/Cd2+ antiport (Salt and
Wagner, 1993). Cd tolerance has been shown to be related
to the ability to synthesize PCs (Rauser 1990; Zhu et al.,
1999; Cobbett, 2000) and there are several levels at which
variations in PC synthesis between cultivars might occur.
Firstly, PC synthase is rapidly induced by exposure to Cd
(Chen et al., 1997) and, therefore, natural variation in
response of the induction process may lead to signi®cant
differences in PC synthesis. Secondly, the level of PC
synthesis may also be controlled through modulation of the
biosynthetic pathway leading to the synthesis of glutathione, the immediate precursor of PCs (Yong et al.,
1999; Zhu et al., 1999). Alternatively higher accumulation
of Cd in vacuoles might occur through a greater activity of
the Mg-dependent ATPase that is believed to be responsible for the transport of the PC±Cd complex across the
354 Dunbar et al.
tonoplast (Salt and Rauser, 1995). Variations between the
cultivars in vacuolar acidity, for whatever reasons, would
also serve to stimulate sequestration through the H+/Cd2+
antiporter (Salt and Wagner, 1993) independently of any
contribution by phytochelatins. It remains to be established
if the inverse correlation between root and tuber Cd
concentration is a general pattern among potato cultivars.
If so, root Cd concentration might be a useful physiological
marker for the selection of low Cd tubers.
On a broader level, the higher import of Cd into tubers of
Kennebec occurs against a background of higher import of
all of the other nutrient elements examined. This demonstrates that there can be major differences between
genotypes in the ratio of sugars to inorganic nutrients in
phloem. At the same time these results highlight the lack of
understanding of the factors that control the loading into
the phloem of any solute other than photosynthate. On the
positive side, the results suggest that it may be possible to
®nd useful varietal differences in phloem composition that
lead to signi®cant increases in the micronutrient content of
other staple food crops. On the negative side, this may also
lead to higher concentrations of undesirable elements such
as Cd.
Acknowledgements
We are indebted to Dr Roger Kirkham of Agriculture Victoria for
providing tubers from his ®eld trial for comparison with the
glasshouse-grown tubers. This work was supported by the
Horticultural Research and Development Corporation. RJR acknowledges support from the Australian Research Council.
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