New Phytol.

(1992), 121, 81-88

Amelioration of aluminium toxicity in

wheat by fluoride

BY D. C. M A C L E A N , K. S. H A N S E N AND R. E. SCHNEIDER
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853,
USA
{Received 10 July 1991; accepted 12 December 1991)

SUMMARY

The deleterious effects of aluminiutn in the rhizosphere on growth, root morphology, ion uptake, and stomatal
conductance in wheat {Triticum aestivum L.) were prevented or attenuated hy the inclusion of fluoride in the
growth medium; the more fluoride present relative to the concentration of aluminium, the greater the alleviation.
Results support the conclusion that the ameliorative effects of fluoride were due to reductions in the concentration
of the rhizotoxic trivalent cation (Al^^) through the formation of aluminium-fluoride complexes that are neither
phytotoxic nor readily translocated from roots to shoots.

Key words: Aluminium, fluoride, rhizotoxicity, wheat {Triticum aestivum).

are not well understood. For these reasons, wheat

INTRODUCTION
seedlings were grown in nutrient solutions amended
Several factors prompted investigations on the joint with fluoride, aluminium or both to determine effects
effects on plants of fluoride and aluminium in the on growth and ion uptake.
rhizosphere. First, aluminium is a major constituent
of most soils and under acidic conditions it becomes
mobilized into rhizotoxic forms that limit plant
MATERIALS AND METHODS
growth (Foy, 1974; Moore, 1974). Indeed, alu-
minium toxicity is probably the most limiting factor Seeds of winter wheat {Triticum aestivum L, cv. Abe)
for plant productivity in acid soils (Foy, 1984). One were placed on seed germination paper moistened
current concern is the progressive increase in soil with deionized water. After 48 h the coleoptile, the
acidity from wet and dry deposition of air pollutants primary root, and two lateral (seminal) roots had
which exacerbates aluminium toxicity, possibly emerged from the caryopsis. Uniform seedlings were
contributing to forest declines in North America and selected and transferred to individual cells of a
Europe (Ulrich, 1983; McLaughlin, 1985). Second, recirculating nutrient culture system located in a
fluoride is also highly phytotoxic, widely distributed controlled-environment chamber that provided
in soils, and becomes more available for plant uptake day/night temperatures of 22/20 °C, relative humid-
as soils become more acidic (Weinstein, 1977). ities of 60/65%, and a 14-h photoperiod from an
Natural concentrations of fluoride in the upper equal mixture of sodium vapour and metal halide
horizons of soils may be increased in areas where lamps (PPFD of 670-730 //mol m - s^>).
industrial emissions of gaseous or particulate forms The recirculating nutrient culture system con-
occur from direct deposition or indirectly from the sisted of four 1-8 m long vinyl troughs that were
decomposition of fluoride-containing litter (Polom- slightly inclined (one end was elevated 4 cm).
ski, Fluhler & Blaser, 1982). Third, changes in the Separate nutrient/treating solutions for each trough
concentration or form of soilborne aluminium or were pumped from reservoirs to the elevated end at
fluoride may affect plants indirectly by altering the 1-2 dm^ min^\ drained by gravity to the lower end,
uptake of nutrients essential for plant growth and and collected in the same reservoir completing the
development. A fourth factor is that fluoride and circuit. In each trough there were 34 cells, each
aluminium readily react with each other to form containing one seedling. The depth of each cell was
complexes (Lindsay, 1979), and in the complexed adjusted to permit the roots to contact the surface of
form the toxicity of each would be altered. Finally, the solution in the trough below. The system was
the joint action on plants of aluminium and fluoride designed such that the recirculating nutrient/
ANP 121
82 D. C. MacLean, K. S. Hansen and R. E. Schneider
treating solutions were aerated, but not exposed to
light.
The basic nutrient solution used was a 0 25 x
modified Johnson's solution (Johnson, et al., 1957).
Concentrations of macronutrients were (in mM):
NO3-N, 2-0; NH4-N, 2-0; K, 16; Ca, 10; P, 0 1 ;
Mg, 0-25; and SO^, 2-0. The concentrations of
micronutrients were (in /iM): Cl, 25; B, 6-25; Zn,
1-0; Mn, 0-5; Cu, 0-25; Mo, 0-25; and Fe (as
FeHEDTA), 10-0.
Seedlings in the system were first grown for 3 d in
0-5 mM CaSO^, followed by 3 d in a pretreatment
dilute nutrient solution (0-125 x ) adjusted to pH 4-2.
The experimental treatments were started 8 d from
seed imbibition and continued for 8 d with re-
placement of the nutrient/treating solutions after 4
d. During the period of treatment, the nutrient
solutions were amended with fluoride (as NH^F),
aluminium (as Al2[SO^]3), or both. The pH of the
treating solutions was measured daily and, if necess-
ary, adjusted to pH 4-20 ±0-05 with H^SO^ or KOH.
Changes in pH were slight except during the last 2
d for treatments that permitted active root growth
(e.g. Huoride alone or with aluminium where the
concentration of fluoride was the same as or greater
than that of aluminium). At those times the pH
could decrease from 42 to 3-9 over 24 h.
Plants were harvested at 16 d of age, separated into
roots and shoots (entire tops), and dried in a force-
draft oven (80 °C) to a constant weight. After
measurements of dry mass, the tissues were ground
to pass a 40-mesh sieve and aliquots of roots and
shoots were analysed for fluoride by the semi-
automated method (AOAC, 1980) and for other
elements, inductively coupled argon plasma atomic
emission spectroscopy (IPC analysis) was used
(Thornton, Schaedle & Raynal, 1985). To clarify the
analytical results, values are presented (Tables 2—4)
as amount (/^g or mg) per plant rather than in terms
of concentration, because the latter (% or ppm on
dry matter basis) can be misleading, especially when
comparing plants with severely inhibited growth to
those in which growth was not affected.
The recirculating system permitted a maximum of
four treatments per experiment (one per trough).
Therefore, 16 experiments were carried out in which
treatments overlapped and replications were achi-
eved over time. The mean of 32 plants was used for
each replicate for growth; seedlings at the ends of the
trough were not included. For analyses of alu-
minium, fluoride, and other ions the number of
seedlings per determination was variable; in treat-
ments where growth (dry mass) was inhibited, plants
were pooled to provide enough tissue for analysis; n
= 4 for mean values given in Tables 1-4. Data for
growth and aluminium and Huoride uptake were
analysed using multivariate regression with the
concentrations of aluminium and of fluoride as
independent variables.
Stomatal conductance of leaf 3 of four plants per
treatment was measured with a steady state poro-
meter (Ll-1600, LI-COR Inc., Lincoln, Nebraska,
USA) at the end of the treatment period.
Formation of aluminium-fluoride complexes in
treating solutions was characterized by measuring
fluoride ion activity with a specific ion electrode
(Orion Research Inc., Cambridge, Massachusetts,
USA) in the presence and absence of TISAB IV, a
total ionic strength metal-complexing buffer
(Cameron, Ritchie & Robson, 1986). This buffer,
which is routinely used to remove interfering metals
in fluoride analysis, will complex ^lOOmgT^
aluminium in the presence of 1 mg T^ fiuoride
(Orion, 1983). Measurements of fiuoride activity
were made of nutrient solutions amended with 50 or
100/iM fluoride and concentrations of aluminium
from 0 to 100/^M. All solutions were adjusted to
pH 4-2 ±0-05 with 0-05 M-HNO3.
RESULTS
Growth
Concentrations of fiuoride in the nutrient medium of
from 50 to 200 /<M did not affect growth, whereas
treatment with aluminium had deleterious effects
on roots (Table 1). Root growth was significantly
reduced by aluminium at 25 fiyi, and even greater
inhibitions occurred at 50 and 100/<M aluminium.
Indeed, there was no significant increase in root dry
mass at the highest concentration of aluminium
during the 8 d period of treatment. The deleterious
effects of aluminium on root growth were amelior-
ated when aluminium and fluoride were supplied
together, and the degree of attenuation was a function
of the relative concentrations of fiuoride and alu-
minium. Fluoride at 50 and 100/iM prevented the
aluminium-induced inhibitions of root growth until
the concentration of aluminium reached 100//M. At
that concentration, 50/iM fluoride had no effect, 100
[iM fluoride partially prevented aluminium toxicity,
and the highest fluoride treatment (200 fiM) com-
pletely reversed the inhibitory effects of 100/tM
aluminium (Table 1).
The inhibitory effects of aluminium on growth
were greater for roots than for shoots. For example,
25 fiM aluminium reduced root growth by 50%, but
shoot growth was reduced by only 15%. Quali-
tatively, however, the responses of roots and shoots
to treatment were similar; statistically significant
differences tended to occur between the same
treatments for both shoots and roots. Plots of the
data from Table 1 for shoot and root growth (not
shown) resulted in curves that were very similar in
appearance to each other and to those shown in
Figure 1 for total plant growth. Similarities between
root and shoot responses to treatment are illustrated
by the relationship between values for root and shoot
mass over all treatments (Fig. 2). These significant
 Amelioration of aluminium toxicity by fluoride 83
240
Table 1. Mean values {n = 4) for growth (mg dry
mass) of roots and shoots of wheat fTriticum
aestivum) as affected by the concentrations of
aluminium and fluoride, alone and in combination, in
the nutrient medium

Fluoride Aluminium concentration (/tM)

0 25 50 100

:Shoots
0 144 121 108 105
50 154 152 145 106
100 142 151 151 113
25 50 200 144 153 148 151
75 100
Al concentration Roots
Figure 1. Total plant dry weight as affected by the 0 63 31 22 19
concentrations of aluminium and fluoride, alone and in 50 73 69 56 20
combination, in the nutrient medium. Fluoride concen- 100 72 76 72 38
trations, (in /<M): • , 0; A, 50; D, 100; O, 200. 200 74 77 71 63

Regression equations:
Dry mass (plant) = 193-75-O-642[A1]+O-3O8[F];
180 0-667; P < 0-001.
Dry mass (shoots) = 137-71-O-282[A1]-I-O-131[F];
0-509; P < 0-001.
160 Dry mass (roots) = 56-04-0-360[Al]-hO-177[F];
D 0-741; P < 0-001.

« 140
CO ment: morphological changes were moderate at 25
E
>• fjt,M aluminium and severe at 50 and 100/^M alu-
^ 120 minium. When aluminium and fluoride were sup-
o
o
plied together, there were no obvious effects on root
C/3
morphology if the concentration of fluoride was
100
greater than that of aluminium. If the fluoride
concentration was the same or less than the alu-
80 minium concentration, the aluminium-induced
0 20 40 60 80 100 morphological changes occurred, but were less
Root dry mass (mg) severe than when aluminium was supplied alone.
Figure 2. Regressions of dry mass of shoots on dry mass
of roots and of dry mass of roots on dry mass of shoots {W^
= 91-1 +0-816PF,; R^ = 0-761 and W^ = -7\-l Eluoride uptake
R^ = 0-761, respectively).
After 8 d of treatment the amount {/ig plant"^) of
fluoride in shoots was greater than that in roots. For
(P < 0-001) linear regressions for dry mass of shoots all treatments in which some fluoride was provided,
on root mass {W^ = 9M +0-816PF,; R^ = 0-761) and from 57 to 87% of the total amount of fluoride
for root mass on shoot mass {W^ = —71-7-1-O-933I^s; absorbed from the treating solutions was trans-
R^ = 0-761) indicated that the overall growth effects located to the shoots (Table 2). Where fluoride was
were on the 'size' rather than the 'shape' of plants. supplied alone, the only effect on the amount of
fluoride in roots was an increase at the highest
treatment concentration (200 /^M). If aluminium was
Morphological effects also present in the treating solutions, signiflcant
There were no apparent effects of treatment on the increases in the amount of fluoride in roots occurred
morphology of shoots due to aluminium or fluoride. at lower fluoride concentrations. The magnitude of
In roots, however, deleterious aluminium-induced this effect was related to the relative concentrations
alterations in morphology were observed. Flongation of aluminium and fluoride; at 100 and 200/iM
of primary roots was distorted, the size and number fluoride the presence of ^ 50 //M aluminium in-
of flbrous roots were markedly reduced, and lateral creased the amount of fluoride recovered in roots
root development was arrested resulting in short, (Table 2). For shoots the interacting effects of
thickened, peg-like laterals about 1-2 mm long. The fluoride and aluminium were the opposite. Fluoride
intensity of these aberrations was related to treat- in shoots increased with the concentration in the
6-2
84 D. C. MacLean, K. S. Hansen and R. E. Schneider

T a b l e 2. Mean values {n = 4) for fluoride (/ig F
plant'^) in roots and shoots of wheat (Triticum
aestivum) as affected by the concentrations of
aluminium and fluoride, alone and in combination, in
the nutrient medium
affect the total amount of fluoride accumulated
because the aluminium-induced increases in fluoride
in roots were offset by the aluminium-induced
decreases in the amount of fluoride in shoots.

Aluminium concentration Aluminium uptake

Fluoride {/IM)
concentration Most of the aluminium removed from the treating
(JMM) 0 25 50 100
solutions tended to remain in the roots. For all
Shoots treatments that included aluminium, only 8-13 % of
0 0-32 0-29 0-31 0-33 the total uptake was translocated to shoots (Table 3).
50 1-25 0-76 0-85 0-86 T h e amount of aluminium in roots increased with
100 1-96 1-51 1-41 1-68 increasing concentrations of aluminium in the rhizo-
200 3-16 2-47 2-24 2-43 sphere, but the increase was inhibited if fluoride was
Roots also included in the treatment. T h e degree of
0 0-34 0-31 0-26 0-29 inhibition became greater as the concentration of
50 0-37 0-39 0-45 0-65 fluoride increased (Table 3). T h e amount of alu-
100 0-29 0-41 0-63 1-25
minium in shoots also increased as the concentration
200 0-65 0-62 0-72 0-90
of aluminium in the treating solutions increased, but
Regression equations: there was no consistent effect of fluoride on the
Fluoride (shoots) = 0-489-O-OO3[A1]-f-0-011 [F]; amount of aluminium translocated to shoots.
0-906; P < 0-001.
Fluoride (roots) = 0-187-0-004[Al] + 0-002[F];
0-540; P < 0-001. Uptake of other ions

T h e effects of treatments on total uptake and

T a b l e 3. Mean values {n = 4) for aluminium (fig Al partitioning between roots and shoots were quali-
plant"^) in roots and shoots of wheat TTriticum tati^'ely the same for P, Ca, Mg and M n ; aluminium
aestivum) as affected by the concentrations of by itself reduced total uptake and the amounts
aluminium and fluoride, alone and in combination, in detected in both roots and shoots were less than in
the nutrient medium control plants (Table 4). T h e inhibitory effects of
aluminium on uptake of Ca and Mg were partially
Aluminium prevented by fluoride if the aluminium: fluoride
Fluoride concentration (//M) ratio was 1:2. For P, K and M g the aluminium-
concentration induced inhibition of uptake was completely over-
(//M) 0 50 100
come at a ratio of 1:1 (50 fiM of each). Tissue
Shoots analyses showed somewhat different effects for Fe.
0 1-0 3-4 5-1 Total uptake of Fe was not affected by any of the
50 1-1 5-0 6-8 treatments, but 50 /tM aluminium reduced the
100 1-1 3-2 6-2 amount of Fe recovered in shoots. This reduction
200 1-1 1-4 5-9 did not occur if fluoride ( ^ 50 ^,M) was also provided
Roots (Table 4). Fluoride by itself at concentrations of up
0 1-6 21-0 62-0 to 200 //M did not alter the uptake or partitioning
50 0-8 13-6 30-6 between roots and shoots of P, K, Ca, Mg, M n or Fe
100 1-2 6-5 24-4 (data not shown).
200 0-9 2-1 9-2

Regression equations: Stomatal conductance

Aluminium (shoots) = 1-301 +0-049[Al]-()-003[F]; R- =
0-845; P < 0-001.
Aluminium (roots) = 9-060 + 0-340[Al]-0-111[FJ; R'=
0-710; P < 0-001.
treating solutions, but at ^ 100//M fluoride, the co-
occurrence of aluminium reduced the amount of
fluoride in shoots relative to that in plants provided
fluoride by itself.
Total fluoride uptake per plant (roots plus shoots)
increased significantly as the concentration of
fluoride in the growth medium increased, but the
presence of aluminium in the rhizosphere did not
Measurements of stomatal conductance also revealed
the combined influences of aluminium and fluoride.
With increasing concentrations of aluminium, the
gas exchange capacity of leaves progressively de-
creased (Table 5). If fluoride was provided with
aluminium in the treating solutions, however, the
effects of aluminium were partially or completely
prevented, and the degree of attenuation was affected
by the relative concentrations of aluminium and
fluoride. When the concentration of fluoride was
greater than that of aluminium, the effects of
aluminium on stomatal conductance were prevented.
 Amelioration of aluminium toxicity by fluoride 85

Table 4. Uptake of P, K, Ca, Mg, Mn and Ee by wheat (Triticum aestivum) roots and transport to shoots as
affected by the relative concentrations of aluminium and fluoride in the treating solutions

Aluminium/fluoride concentrations (//.M)

Plant
Element fraction 0/0 50/0 50/50 50/100

mg plant '
P Shoot 1-13(0-029) 0-53(0-018) 1-25(0-028) 1-21(0-041)
Root 0-34(0-028) 0-12(0-011) 0-26(0-013) 0-31(0-017)
K Shoot 7-53(0-278) 3-78(0-196) 7-51(0-305) 8-12(0-563)
Root 3-39(0-164) 0-39(0-044) 2-92(0-161) 3-59(0-290)
fii g plant '
Ca Shoot 409 (32-1) 281 (8-0) 384 (24-5) 334 (25-8)
Root 53 (5-2) 23 (4-7) 44 (3-5) 46 (3-7)
Mg Shoot 213 (14-1) 68 (8-1) 102 (2-3) 172 (14-9)
Root 71 (10-0) 10 (2-6) 29 (4-0) 57 (11-6)
Mn Shoot 2-09(0-14) 1-00(0-09) 2-31(0-10) 2-32(0-34)
Root 0-97(0-13) 0-28(0-03) 0-96(0-05) 0-86(0-14)
Fe Shoot 19-2 (0-67) 7-6 (0-36) 14-6(0-38) 20-7(1-92)
Root 26-6 (2-75) 33-3 (6-86) 18-8(2-83) 22-7(4-41)

Values presented are means with standard errors in parentheses of 4 determinations; for one treatment, [A1]/[F] =
50/0 {n = 3).

120 r
Table 5. Stomatal conductance (mmol m '^ s ^) of leaf
3 of wheat (^Triticum aestivum) as affected by the o 100
concentrations of aluminium and fluoride in the 3

nutrient medium. Values are means {n = 4) with o

standard errors in parentheses

Fluoride Aluminium concentrations (/^M) c

concn o
0 25 50 100 0)
•D

0 222 (8-3) 125(10-6) 49(16-0) 31 (3-2) o

50 213(10-2) 224(11-4) 155(10-5) 55(11-0)
100 243(12-0) 239 (8-5) 242(12-0) 82 (7-8)
200 215(18-6) — 217(12-0) 200(13-9)
Complexing reactions
The various interacting effects of aluminium and
fluoride presented above suggested that aluminium
and fluoride were reacting to form complexes in the
nutrient solutions. Evidence to confirm this in-
ference was obtained by measuring the activity of
fluoride in nutrient solutions containing 50 or 100
//M fluoride and various concentrations of aluminium
in the presence and absence of a metal-complexing
buffer (TISAB-IV). The data in Figure 3 show that
if aluminium was complexed (by adding TISAB-IV)
and prevented from reacting with fluoride, there was
no effect of increasing aluminium concentrations on
fluoride activity. Conversely, in the absence of the
metal-complexing buffer, the percentage of total
fluoride as free fluoride ion decreased with increasing
concentrations of aluminium as aluminium-fluoride
complexes were formed. Complexation was essen-
tially complete at equimolar concentrations of alu-
minium and fluoride.
3
0) 20 -
CD
25 50 75 100
Aluminium concentration
Figure 3. Percentage of total fluoride as free fluoride ion in
nutrient solutions as affected by the concentration of
aluminium and the presence of a metal-complexing buffer
(TISAB IV). Fluoride concentrations were 100 (triangles)
and 50 //M (circles) with (open symbols) and without
(solid symbols) buffer. Each point is the mean of three
experiments.
DISCUSSION
Under the acidic (pH 4-2) experimental conditions
employed, aluminium existed mainly as the mono-
meric, highly charged cation, Al^^ (Wagatsuma &
Ezoe, 1985). In that form, aluminium was extremely
rhizotoxic and directly or indirectly responsible for
all of the deleterious effects of aluminium that were
observed (e.g., inhibited growth, altered root mor-
phology, reduced uptake of P, K, Ca, Mg, Mn and
Fe, and reductions in the gas exchange capacity of
leaves). The results clearly reveal that these harmful
effects were ameliorated or prevented if fluoride was
86 D. C. MacLean, K. S. Hansen and R. E. Schneider
also present in the growth medium at concentrations
equal to or greater than those of aluminium. Fluoride
is a powerful ligand for aluminium (Lindsay, 1979)
and at pH 4-2 their reaction would reduce the
concentration of the highly toxic trivalent cation
(Elrashidi & Lindsay, 1986 a, b). We conclude that
the amelioration of aluminium toxicity by fluoride in
wheat seedlings was due to reductions in the
concentration of Al ^^ in treating solutions through
the formation of aluminium-fluoride complexes (Fig.
3). Cameron et al. (1986) arrived at a similar
conclusion. They found that growth of barley roots
was highly correlated with the concentration of Al*^,
but not with the concentrations of total soluble
aluminium or of aluminium complexed with
fluoride.
The influence of fluoride on aluminium toxicity
has also been observed in other systems. For example,
the survival of fish in acidic (pH 4-4) water was
markedly increased by the addition of fluoride
concentrations equal to those of aluminium (Driscoll
et al, 1980). Similarly, aluminium-induced inhi-
bition of tea pollen growth in vitro was prevented by
adding NaF to the growth medium (Konishi &
Miyamoto, 1983). The formation of complexes
which reduce the toxicity of aluminium was used to
explain both of these examples. Thus the ameli-
oration of aluminium toxicity through the sequester-
ing of Al*"^ by fluoride appears to be a general
phenomenon and, because it is consistent with the
observations from the present study, it can be
used to explain the experimental results.
Fluoride was relatively mobile within plants.
Increasing concentrations of fluoride in the rhizo-
sphere resulted in corresponding increases in the
uptake of fluoride, most of which (77-87%) was
translocated to shoots (Table 2). Nevertheless,
fluoride by itself did not cause foliar symptoms or
affect the growth of roots or shoots. The presence of
aluminium did not affect the total amount of fluoride
accumulated, but translocation of fluoride to shoots
was reduced when fluoride and aluminium were
supplied together. The formation of relatively im-
mobile aluminium-fluoride complexes would ac-
count for the reduced translocation. In bean plants
provided with aluminium and fluoride as AIF3 at
pH 4-9, however, fluoride uptake and translocation
were enhanced relative to plants given the same
concentration of fluoride (as NaF) by itself (Takmaz-
Nisancioglu & Davison, 1988).
Analyses of wheat seedlings treated with alu-
minium showed signiflcantly elevated concentrations
of aluminium in roots and relatively low concen-
trations in shoots (Table 1), confirming the low
mobility of aluminium that has been reported by
others (Foy, 1974; Ohki, 1985). Ohki (1985) has
shown that only a small fraction of the aluminium
associated with roots occurred within the endo-
dermis; most was on surfaces and in cortical regions.
Nevertheless, that small internal fraction of alu-
minium was responsible for the most obvious effects
of aluminium in what seedlings: reduced root
growth, through inhibition of cell division in root
meristems and subsequent inhibition of elongation,
and altered root morphology (Pan, Hopkins &
Jackson, 1988). These responses were similar to
those described for wheat by Foy (1974). Roots were
more susceptible to aluminium-induced changes in
form than to growth inhibition (e.g. reduced dry
weight). Morphological aberrations were still ob-
vious at aluminium: fluoride ratios that did not affect
the dry mass of roots.
Although roots are the primary sites of aluminium
toxicity (Bennet, Breen & Fey, 1985 ; Kinrade, 1988),
the growth responses of shoots were qualitatively
similar to those of roots (Fig. 2). The same concen-
trations or combinations of fluoride and aluminium
that caused significant effects on root growth also
affected shoot growth (Table 1). Reductions in the
number and size of flne absorbing roots provide the
simplest explanation for these parallel effects, but
the impact of limiting concentrations of essential
nutrients or the accumulation of toxic levels of
aluminium in the aerial parts of plants cannot be
ignored.
The indirect effects were most probably related to
aluminium associated with root surfaces and free
space of roots. At pH values below 5-0, more than
half of the cation exchange sites may be occupied by
aluminium, preventing the uptake of other ions
(Evans & Kamprath, 1970). The effective binding of
aluminium to negative charges of the root apoplastic
space displaces ions of lower affinity such as K"*^,
Ca^^, Mg'+ and Mn^^ (Rengei & Robinson, 1989a-^;
Clarkson & Sanderson, 1971). Indeed, aluminium
toxicity is frequently expressed as foliar symptoms of
nutrient deficiencies (Foy, 1974; Rengel & Robinson,
1989 c), and it has been shown that differential
resistance of cultivars to aluminium toxicity are
often related to the internal concentrations of macro-
and micronutrients (Miyasaka et al, 1989; Ohki,
1985 ; Rengel & Robinson, 19896). In addition to the
effects of surface charges, altered uptake may result
from the precipitation by aluminium of Ca and P in
the soil solution (Foy, Chaney & White, 1978) or, in
the case of P, possibly within the root itself (Wright,
1948). The amelioration of aluminium-induced
inhibition of ion uptake by the inclusion of fluoride
in treating solutions (Table 4) is yet another
observation suggesting the formation of aluminium-
fluoride complexes that reduce the concentration of
Al^""", thereby freeing negative charges in the free
space for other cations. It is also possible that
aluminium-induced reductions in the size and num-
ber of absorbing roots contributed to the decreases in
the uptake of ions by wheat seedlings (Rengel &
Robinson, 1989«).
The inhibitory effects of aluminium on the gas
 Amelioration of aluminium toxicity by fluoride
exchange capacity of wheat leaves increased with
concentration. As found for other effects of alu-
minium, the inhibition was at least partially allevi-
ated by all concentrations of fluoride, and completely
prevented if the concentration of fluoride exceeded
that of aluminium (Table 5). Reduced stomatal
conductance due to high concentrations (2000 juwi at
pH 4-0) of aluminium in the nutrient medium has
also been reported for peach seedlings (Horton &
Edwards, 1976). The response in peach was not due
to changes in stomatal aperture or density, but was
closely related to reductions in root volume. The
relation between aluminium concentration and sto-
matal function observed for wheat in the present
study may be associated with the reduced concentra-
tions of K and P in shoots (leaves) of aluminium-
treated plants. Direct correlations between stomatal
aperture and the concentrations of K (MacRobbie,
1981) or P (Radin, 1984) in guard cells have been
reported. Water stress was not a factor; wheat
seedlings maintained in the various solution cultures
maintained turgor throughout the period of treat-
ment.
There were no deleterious effects of fluoride on
wheat at concentrations of up to 200 fiM. Even at 400
/iM (data not shown) there were no measurable
effects on root morphology or the growth of roots
and shoots. The absence of direct effects, however,
does not mean that fluoride in natural soils is
innocuous. In soils having elevated concentrations of
fluoride, either from natural or anthropogenic
sources, water soluble fluoride might perturb the soil
environment in other ways (Polomski et al., 1982).
For example, high levels of fluoride in the soil have
been shown to retard the rate of organic matter
decomposition (Dhruva & Dhirendra, 1978).
These experiments with wheat clearly demon-
strate the amelioration of aluminium toxicity by
fluoride in solution cultures. Similar responses
would be expected in natural soils at pH ^ 4-2 if the
concentrations of fluoride are sufficiently high.
However, the concentration of fluoride in most soils
is usually less than 10/iM (Moore & Richie, 1988).
The occurence of elevated concentrations suflicient
to overcome aluminium toxicity would most likely
be limited to areas of industrial pollution or to
certain soil types with naturally high fluoride
concentrations (Weinstein, 1977). The relative
abundance of other cations and the amount of organic
matter would also greatly affect the chemical equi-
libria of both fluoride (Elrashidi & Lindsay, 1986 a,
b, 1987) and aluminium (Kinrade & Parker, 1987).
A limited number of plant species naturally absorb
high concentrations of fluoride from the soil and
accumulate it in foliage without showing injury
(Weinstein, 1977). Many of these species also tend to
contain elevated foliar concentrations of aluminium
and do not exhibit toxicity symptoms (Davison,
1983). This kind of linkage between fluoride and
87
aluminium might represent an inherent defence
mechanism to reduce aluminium toxicity in some
plant species.
ACKNOWLEDGEMENT
We thank Dr J. A. Laurence for valuable help with
statistical analyses.
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