Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol15.1995:
Tree Physiology 15, 85--93
© 1995 Heron Publishing----Victoria, Canada
Growth and nutrition of birch seedlings at varied relative addition
rates of magnesium
TOM ERICSSON and MONIKA KÄHR
Department of Ecology and Environmental Research, Swedish University of Agricultural Sciences, P.O. Box 7072, S-750 07 Uppsala, Sweden
Received November 25, 1993
Summary Growth and nutrition of hydroponically cultivated
birch seedlings (Betula pendula Roth.) were investigated at
various magnesium (Mg) availabilities. Suboptimum Mg conditions were created by adding Mg once per hour in exponentially increasing amounts at one of four relative addition rates
(RMg): 0.05, 0.10, 0.15 or 0.20 day −1. Seedlings given free
access to Mg were used as controls. After an acclimation
period, the relative growth rate of the seedlings attained the
same value as the corresponding relative rate of Mg addition.
In all suboptimum Mg treatments, deficiency symptoms in the
form of chloroses and necroses developed in the older leaves,
both during and after the phase of growth acclimation. The
severity of these symptoms was correlated with the availability
of Mg. The relative growth rate of seedlings was linearly
correlated with plant Mg status. The root fraction of the total
biomass decreased from 22% in control plants to 8% in plants
receiving the lowest rate of Mg addition. A shift in Mg availability from free access to RMg = 0.05 day −1 decreased the
photosynthetically active leaf area per plant weight, despite a
concomitant increase in the leaf weight ratio (leaf dry
weight/plant dry weight) from 0.61 to 0.75. The loss in assimilating leaf area was mainly a consequence of enhanced leaf
mortality and formation of necroses, and to a minor extent
attributable to increased carbon costs for leaf area production.
A decrease in starch concentration was observed in leaves
showing Mg-deficiency symptoms, whereas the starch concentration in healthy leaves was unaffected by Mg availability. It
was concluded that shortage of carbohydrates constituted the
major growth constraint, particularly for roots, under Mg-limiting conditions.
Keywords: Betula pendula, dry matter distribution, leaf area
ratio, leaf weight ratio, net assimilation rate, nonstructural
carbohydrates, nutrient uptake rate.
Introduction
Nutrient uptake and growth are time-dependent processes and
the amount of nutrients taken up per unit of time is therefore
strongly coupled to both the size and growth rate of the plant.
Consequently, the quantitative nutrient requirement during the
course of an experiment increases more or less rapidly with
time. According to Ingestad (1982), full control over nutrient
uptake, plant nutrient status and growth can only be achieved
if the supply of nutrients is treated dynamically, i.e., by frequent nutrient additions (daily or hourly) in amounts adjusted
both to plant size and the desired growth rate.
The relative addition rate of nutrients has been used as a
treatment variable when studying the influence of plant nutrient status on physiological processes. Nitrogen fixation in gray
alder (Ingestad 1980), nitrogen nutrition in ectomychorrizal
Scots pine seedlings (Ingestad et al. 1986), carbohydrate dynamics in birch (McDonald et al. 1986), aluminum toxicity in
forest trees (Göransson and Eldhuset 1987, 1995), leaf chemistry and insect susceptibility in Salix (Waring et al. 1985,
Larsson et al. 1986), and leaf expansion (Taylor et al. 1993) are
examples of areas investigated under steady-state nutrition.
One of the most striking observations made with this technique
is the disappearance of deficiency symptoms after growth
acclimation to suboptimal supply rates of nitrogen (Ingestad
and Lund 1979) and phosphorus (Ericsson and Ingestad 1988).
Improved light conditions are generally associated with an
increase in the shoot/root ratio (Björkman 1981, Corré 1983),
but no significant effect of photon flux density on dry matter
partitioning was observed in experiments with small birch
plants where steady-state nutrition was maintained (Ingestad
and McDonald 1989). Similarly, elevated atmospheric CO2
concentration, which is often associated with a shift in the
carbon allocation pattern toward roots (Mousseau and Enoch
1989), caused no change in the shoot/root ratio of birch seedlings when the nutrient status of the test plants was carefully
controlled (Pettersson and McDonald 1992, Pettersson et al.
1993). Plant nutrient status, and its stability during the period
of investigation, thus has a strong impact on the results obtained and their interpretation.
The relationship between mineral nutrient status and growth
of birch seedlings has been extensively studied under conditions where the relative addition rate of nutrients has constituted the treatment variable. Nitrogen (Ingestad 1979),
phosphorus (Ericsson and Ingestad 1988), potassium (Ericsson
and Kähr 1993), iron (Göransson 1993) and manganese
(Göransson 1994) are the elements studied so far. The present
investigation is a continuation of these nutritional studies and
the element in focus this time was magnesium (Mg). Our
86
ERICSSON AND KÄHR
choice of element was based on recent interest in Mg deficiency as one of the factors causing forest dieback in areas of
central Europe and North America (Hüttl 1988, Schulze et al.
1988, Roberts et al. 1989). We hypothesized that disturbed
forest growth is associated with decreased carbohydrate availability in the tissues. Because Mg is essential for the activation
of many enzymes, including those required for CO2 fixation
(Marschner 1986), we were particularly interested in the influence of plant Mg status on the carbohydrate concentration of
tissues and on dry matter partitioning among root, stem and
leaves.
Material and methods
Growth conditions
The experiments were carried out in growth chambers with a
continuous photon flux density of 260 µmol m −2 s −1 (400 to
700 nm, Osram HQI R 250W/D). Both the air and root temperatures were 20 ± 0.5 °C and the vapor pressure deficit in the
air, VPD, was approximately 0.6 MPa.
Seedling culture
Birch seedlings (Betula pendula Roth.) were used as test material. Seeds were germinated on wet filter paper in petri dishes
under low light intensity, 50 µmol m −2 s −1, for about 10 days.
Seedlings at the same developmental stage were then planted
in growth units where the roots were continuously sprayed
with a circulating culture solution with a volume of 5 dm3. A
detailed description of the growth unit has been presented
elsewhere (Ingestad and Lund 1986). The culture solution
contained all essential mineral elements in the proportions
given by Ingestad and Lund (1986) (N = 100, K = 65, P = 13,
Ca = 7, Mg = 8.5, S = 9, Fe = 0.7, Mn = 0.4, B = 0.2, Zn = 0.06,
Cu = 0.03, Cl = 0.03, Mo = 0.007, Na = 0.003). Non-growthlimiting conditions were created by keeping the conductivity
of the culture solution between 250 and 350 µS cm −1, which is
equivalent to a nitrogen concentration of 3--4 mM. The pH of
the culture solution was maintained at 4.8--5.2. A computer
was used to control the hourly conductivity and pH titrations.
After pregrowth for 14 days under the culture conditions described, 60 uniform seedlings with a fresh weight (FW) of
40--50 mg per plant, were selected in groups of four for use in
each of the different treatments.
Treatments
Four relative addition rates of magnesium (RMg = 0.05, 0.10,
0.15 and 0.20 day −1) were used to induce a range of suboptimum plant Mg concentrations. These treatments corresponded to an approximate Mg restriction of 80 to 10%,
respectively, of the potential Mg requirement under the chosen
climatic conditions. The concentration of Mg in the seedlings
at the start of each treatment, 0.51 mg gFW−1, was used to
calculate the hourly Mg additions:
Mg t = Mg s(eR Mg /24 − 1)(eR Mg t/24 ),
where Mgs is the initial amount of magnesium in the seedlings,
and Mgt is the amount of magnesium added, together with
other essential nutrient elements, that is sufficient for one hour
of uptake at any time t hours from the beginning of the experiment at the desired RMg (Ingestad and Lund 1986). Conditions
that were not growth limiting with respect to availability of
other essential mineral elements were ensured by keeping the
conductivity of the culture solution above 70 µS cm −1. This
was achieved by automatic conductivity titrations with a Mgfree stock solution. The pH of the culture solution during the
experiments varied between 4.2 and 5.2.
A fifth treatment provided non-growth-limiting Mg conditions. All essential elements were supplied in the proportions
found optimal for birch (Ingestad and Lund 1986) and in free
access (FA). The magnesium concentration was kept in the
range of 0.1 to 0.2 mM by maintaining the conductivity of the
culture solution between 100 and 200 µS cm −1. The pH of the
solution varied between 4.2 and 5.2. All experiments were run
twice.
Harvesting
After an initial acclimation period of varying length, depending on the extent of Mg limitation, all plant groups in the 0.05,
0.10 and 0.15 day −1 treatments were reweighed, whereas
plants in the more short-term experiments, 0.20 day −1 and FA,
were left undisturbed. Groups of seedlings were then harvested
on four occasions during the exponential period of growth,
which lasted from 24 (FA) to 69 days (RMg = 0.05 day −1). Fresh
and dry weights (48 h at 70 °C) of roots, stems and leaves as
well as leaf area (LI 3310, Li-Cor Inc., Lincoln, NE) were
determined. The leaves were divided into three categories: 1 =
healthy, 2 = necroses covering less than 75%, and 3 = necroses
covering more than 75% of the leaf surface.
Analyses
Samples for macronutrient analyses were prepared by digestion in a solution of 10 ml concentrated HNO3 and 1 ml HClO4.
One ml of 2 M HNO3 was added to the digest and the solution
was diluted with water to 35 ml. Nitrogen was analyzed with
an elemental analyzer (Elemental Analyzer NA 1500, Rodano,
Italy). The macronutrients P, K, Ca, Mg and S were analyzed
by inductively coupled plasma spectrometry (Jobin Yvon JY70, Longjumeau, France).
Nonstructural carbohydrates were analyzed by the method
described by Steen and Larsson (1986) based on a two-step
extraction procedure. Glucose, fructose, sucrose, fructan and
soluble starch were determined in the first extract and residual
starch in the second extract.
Calculations
Growth was determined as relative growth rate, RG (day −1),
based on weights, W, on the four harvest dates, t, by fitting an
exponential curve:
W = W 0 eR Gt,
GROWTH AND MAGNESIUM NUTRITION IN BIRCH
where W0 is the weight of the seedlings at the beginning of the
treatments (RMg = 0.20 day −1 and FA) or after the acclimation
period (RMg = 0.05, 0.10, 0.15 day −1).
The net uptake rate of nutrients per root growth rate, dn/dWr
(mmol g −1 root growth), was calculated from:
n W C W 10 3
dn
=
=
,
M Wr
dW r W Wr
where n is the nutrient amount in the plant, C its tissue concentration, M the molecular weight, and W and Wr the dry weights
of the seedling and root system, respectively (cf. Ingestad and
Ågren 1988).
The net assimilation rate, NAR (kg plant dry weight (DW)
m−2 day −1), was calculated from:
NAR =
RG
,
LAR
where the leaf area ratio, LAR (m2 kgDW−1 plant), is the product
of specific leaf area, SLA (m2 kgDW−1 leaf), and leaf weight
ratio, LWR (leafDW plantDW−1):
LAR = SLA × LWR .
Statistical analyses
Statistical analyses were carried out by one-way ANOVA
(Statgraphics Inc., Rockville, Maryland, USA). The pair-wise
comparisons were made by the Least Significant Difference
method. The confidence level was 0.05.
87
Plant growth
The RG of the seedlings was similar to that of the treatment
variable, RMg, after an acclimation period of 14--29 days,
depending on the extent of Mg limitation (Figure 2). The
regression coefficients, r2, for the curve fitting of RMg with RG
were generally > 0.99. An RG of 0.23 day −1 was reached under
nonlimiting Mg conditions. The calculated net assimilation
rate, NAR, based on the area of leaves showing necroses on
less than 75% of their surface, decreased from 10.9 to 4.3 ×
10 −3 kg m −2 day −1 when the Mg supply was restricted from
free access to 0.05 day −1 (Table 1). The decline in NAR was
less pronounced, 10.9 to 8.8 × 10 −3 kg m −2 day −1, when only
the area of healthy leaves was considered to be photosynthetically active.
Dry matter partitioning
The proportional allocation of dry matter to roots decreased in
response to growth-limiting availability of Mg (Figure 1).
Roots made up about 8% of the standing biomass at RMg =
0.05 day −1 compared with 22% at free access. Concomitantly,
the fraction of leaves of the total biomass increased from 61 to
75% on a dry weight basis with increased Mg limitation
(Figure 1, Table 1). The leaf area per plant dry weight, LAR,
however, decreased from 21.0 to 11.2 m2 kg −1 (healthy + leaves
damaged on less than 75% of the leaf surface) or from 21.0 to
5.0 m2 kg −1 (healthy leaves) when Mg availability was reduced
from free access to 0.05 day −1 (Table 1). Leaf area production
Results
Plant appearance
Deficiency symptoms, in the form of chloroses and necroses,
developed in the older leaves at growth-limiting supply rates
of Mg, both during and after the phase of growth acclimation.
The severity of these symptoms was correlated with the extent
of Mg limitation (Figure 1). Pronounced increases in leaf
mortality rate and leaf fraction showing necroses on more than
75% of the leaf surface were obtained when RMg was reduced
from free access to 0.05 day −1 (Figure 1). This change occurred
at the expense of healthy leaves, the proportion of which
decreased from 100 to 20%. At the lowest rate of Mg addition,
only the uppermost three to four leaves remained undamaged,
although they exhibited slight interveinal chlorosis. The leaf
fraction showing damage to less than 75% of the leaf surface
constituted roughly 30% of the leaf biomass within the whole
range of suboptimum Mg availabilities studied. Both the size
of newly formed leaves and internode lengths were reduced at
RMg = 0.15 day −1 and lower. The branching pattern of the root
system was more or less unaffected by the supply rate of Mg.
The overall vigor of the roots, including characteristics such as
length and diameter, was reduced by a growth-limiting availability of Mg.
Figure 1. Dry matter distribution in birch seedlings grown in culture
solution at varied suboptimum relative addition rates of Mg, RMg
(day − 1), and at free access, FA. The leaf biomass fraction was divided
into three categories: 1 = healthy leaves (h), 2 = leaves with necroses
covering less than 75% of the leaf surface (< 75%), and 3 = leaves with
necroses covering more than 75% of the leaf surface (> 75%). Columns marked with the same letter within each biomass fraction are not
significantly different (LSD, 0.05 level, n = 5).
88
ERICSSON AND KÄHR
per unit of carbon used for leaf growth, SLA (m2 kg −1 leaf),
was not affected by the supply rate of Mg (Table 1).
Plant nutrient status
Figure 2. Influence of the relative Mg addition rate, RMg (day − 1), on
the relative growth rate, RG (day − 1), of birch seedlings grown in
culture solution. The linear regression and coefficient of determination, r2, are given. Filled symbols denote RG obtained under nonlimiting Mg-conditions; these data points are not included in the linear
regression.
Seedling RG was positively and linearly correlated with Mg
concentration of both the whole plant and the leaves (Figures
3a and 3b). The lowest tissue Mg concentration on a wholeplant basis that supported maximum growth rate (the intersection between the lines in Figure 3a) was 1.4 mg gDW−1. The
corresponding value for undamaged leaves was 1.8 mg gDW−1
(Figure 3b). About three times more Mg than required for
structural growth was taken up under nonlimiting Mg conditions (Figure 3a). At growth-limiting supply rates of Mg, a
strong gradient in foliar Mg concentration developed within
the shoot. The youngest leaves, without Mg-deficiency symptoms or with only weak symptoms, contained two to three
times more Mg within the range of suboptimum Mg availabilities studied than the older damaged leaves toward the base of
the shoot (Table 2). Visible deficiency symptoms in the form
of necroses were generally associated with foliar Mg concentrations below 1 mg gDW−1 at RMg = 0.20 day −1 and below 0.5
mg gDW−1 at RMg = 0.05 day −1 (Table 2). The difference in Mg
concentration between leaves with damage on more than 75%
of the surface and leaves with damage on less than 75% of the
surface was less pronounced.
Table 1. Mean values of net assimilation rate, NAR (kg m − 2 day−1 × 10 − 3), leaf weight ratio, LWR (kg kg − 1), leaf area ratio, LAR (m2 kg −1), and
specific leaf area, SLA (m2 kg − 1), of birch seedlings grown at various relative addition rates of Mg, RMg (day −1), and at free access, FA. The
projected leaf area of healthy leaves only, Lh, was used to calculate NAR, LAR and SLA. The parameters NAR and LAR were also calculated on
the basis of the leaf area of healthy leaves + leaves with necroses covering less than 75% of the leaf surface, Lh+75 , and FA where n = 3, 1 and 2, respectively).
Treatment RMg
0.05
0.10
0.15
0.20
FA
1
Carbohydrate
Starch
Soluble
Starch
Soluble
Starch
Soluble
Starch
Soluble
Starch
Soluble
Roots
1.2 ± 1.0 a
7.0 ± 2.9 a
1.5 ± 1.4 a
5.5 ± 2.2 a
1.5 ± 1.2 a
5.5 ± 2.2 a
2.0 ± 1.0 a
5.0 ± 1.7 a
1.5 ± 2.1 a
12 ± 2.8 b
Stems
2.5 ± 1.6 a
14 ± 2.1 a
3.5 ± 2.7 a
15 ± 6.4 a
3.5 ± 2.1 a
17 ± 3.9 a
6.0 ± 1.5 a
18 ± 3.1 a
7.5 ± 0.7 a
21 ± 2.8 b
Leaves
Lh
L75
42 ± 4.7 a,A
38 ± 3.1 a,A
45 ± 10.3 a,A
38 ± 6.3 a,A
45 ± 9.5 a,A
38 ± 4.2 a,A
53 ± 10.6 a,A
41 ± 8.4 a,A
57 ± 2.1
56 ± 1.4
7.5 ± 4.3 a,B
66 ± 8.3 a,B
14 ± 3.4 a,B
62 ± 9.4 a,B
23 ± 7.5 b,B
65 ± 2.4 a,B
40 ± 9.7 c,A
73 ± 8.3 a,A
---
6.0 ± 2.2 a,B
69 ± 6.7 a,B
9.0 ± 4.2 a,B
70 ± 6.4 a,B
16*1
72*
-----
An asterisk (*) denotes a single analysis.
roots generally contained less than 8 and 21 mg gDW−1 of starch
and soluble carbohydrates, respectively, over the range of Mg
availabilities studied (Table 4).
Discussion
Chlorosis, and particularly necroses, developed in the older
leaves of the Mg-limited birch seedlings as a consequence of
internal Mg cycling. These symptoms appeared once the leaf
Mg concentration had decreased to about half the value of
healthy leaves. This threshold value was higher under mild Mg
restriction, ≈ 1 mg gDW−1 leaf, than under strongly growth-limiting Mg conditions, ≈ 0.5 mg gDW−1 at RMg = 0.05 day −1
(Table 2). The difference in threshold values may be associated
with differences in the pool size of metabolically active and
inactive Mg. However, the difficulties associated with conducting an objective leaf sampling among the chosen leaf
categories offer a more likely explanation for the observed
discrepancy. The small difference in leaf Mg concentration
between the two categories of damaged leaves suggests that
most of the Mg available for resorption had already been
withdrawn before the deficiency symptoms became apparent.
Efficient retranslocation of limiting elements from old to
young foliage ensures the maintenance of physiological processes. About 80% of leaf biomass showed deficiency symp-
toms under severe Mg limitation (RMg = 0.05 day −1), whereas
30% of the leaf biomass showed deficiency symptoms when
the growth rate of the seedlings was only slightly suppressed
by Mg supply (RMg = 0.20 day −1) (Figure 1).
Luxury consumption of N was evident under Mg-limiting
growth conditions (Table 2). This phenomenon has also been
observed when Fe (Göransson 1993), Mn (Göransson 1994) or
Zn (Göransson, personal communication) constituted the
growth-limiting element. Nitrogen taken up in excess of
growth requirements is generally stored in the leaves in the
form of amino acids (Näsholm and McDonald 1990, Näsholm
1991) and acts as a sink for carbohydrates. Because the conversion of N to amino acids generally takes place in the roots
in trees, luxury uptake of N under growth-limiting Mg conditions may contribute to further decreases in the amounts of
carbohydrates available for root growth. We observed an antagonistic effect of Mg on Ca uptake. About three times more
Ca was found in stems and roots at the lowest rate of Mg supply
than at FA (Table 2). Conversely, the presence of a high Ca
concentration in the root medium is likely to exacerbate the
effects of Mg deficiency.
In contrast to previous reports for trees (e.g., Matzner et al.
1986) and herbaceous plants (e.g., Bottrill et al. 1970, Fischer
and Bussler 1988), starch did not accumulate in leaves at
suboptimum Mg tissue concentrations (Table 4). There was a
GROWTH AND MAGNESIUM NUTRITION IN BIRCH
significant decrease in starch concentration in all leaves showing Mg-deficiency symptoms that was independent of the
extent of Mg restriction. We also observed a small decrease in
the starch concentration of healthy leaves when Mg availability was reduced from free access to RMg = 0.05 day −1. We
conclude that the main constraint associated with a shortage of
Mg is a reduction in net carbon gain rather than impaired
assimilate transport in the phloem as suggested by Fink (1989),
because, although not observed in our study, a shortage of Mg
has a strong and negative impact on the rate of carbon fixation
(Beyschlag et al. 1987, Zimmermann et al. 1988). A possible
explanation of our results might be that the carbohydrate
analyses were carried out during the phase of steady-state
nutrition when both the growth rate and the tissue content of
Mg had acclimated to the Mg supply. In most studies, Mg
deficiency was induced by omitting Mg from the growth substrate and, as a result, the internal Mg concentration was
continuously decreasing, i.e., the plants never reached the
phase of steady-state growth.
The importance of the assimilate available for root growth
has already been pointed out by Pearsall (1923) and White
(1937). The balance between carbohydrates and nitrogen in
tissues plays a key role in determining the magnitude of aboveand belowground growth according to Brouwer (1962). When
there is a decrease in carbohydrate supply, the shoot retains a
larger fraction of assimilates than the root, thus increasing the
shoot/root ratio; the opposite occurs when mineral nutrients or
water supplies are decreased (cf. Thornley 1972, Dewar 1993).
Thus, Mg deficiency, which negatively affects carbon fixation,
has a negative impact on root growth. Under severe Mg limitation, the root made up only about 8% of the total biomass
(DW), whereas almost three times as much biomass was allocated to the root under non-growth-limiting Mg conditions
(Figure 1). Similar growth behavior in response to Mg shortage
is generally (e.g., Shear 1980, Marschner 1986, Matzner et al.
1986), but not always (e.g., Will 1961), observed.
If the allocation of biomass to roots is decreased in response
to a mineral shortage, the soil volume exploited by the plant
will also decrease. In turn, this will decrease the uptake of the
limiting element still further. This negative feedback could
lead to plant decline, unless the uptake per unit root growth,
dn/dWr, required to reach a new steady state decreases to a
larger extent than the flux of the limiting element. This condition is obtained if the limiting element exerts its growth regulatory role over a large concentration range in the tissue. We
found that the uptake of Mg per gram of root growth necessary
to achieve a new equilibrium between uptake and growth was
slightly higher after a fourfold reduction in Mg availability
(Table 5). It has previously been shown that for K (Ericsson
and Kähr 1993), Fe (Göransson 1993) and Mn (Göransson
1994), dn/dWr decreases to a lesser extent than the flux of these
elements (Table 5). For N (Ingestad 1979) and P (Ericsson and
Ingestad 1988), dn/dWr decreases almost seven to nine times,
respectively, in response to a fourfold reduction in their availabilities. Although, in the present study the uptake of Mg per
gram of root growth did not match the decrease in Mg flux
given to the plants, steady-state conditions of Mg uptake and
91
growth were established even in treatments where Mg was
severely limiting, probably because the spray technique brings
nutrients in direct contact with actively nutrient-absorbing root
surfaces. In a solid substrate, however, the size of the root
system in relation to shoot and root growth plays a dominant
role in nutrient acquisition (Clarkson 1985).
Shortage of Mg was expected to bring about a decrease in
the net assimilation rate, NAR, of the same magnitude as
reported for K (Ericsson and Kähr 1993), because both elements are essential for carbon fixation. However, we observed
only a small decrease in NAR in response to reduced Mg
availability (Table 1). In this respect, Mg shows similarities
with N and P (McDonald et al. 1991), although N and P more
directly interfere with the activity of the sinks (the meristems)
than of the source (carbon fixation). If the functional component of RG, NAR, is only slightly affected by a reduced nutrient
flux then the structural development of the plant must also
change (cf. Beadle 1985). This was the case under growth-limiting supply rates of Mg, but in contrast to N and P, more of the
assimilates available for growth were utilized in the shoot than
in the root (Figure 1). An increased allocation of biomass to
leaves generally implies an increase in the total leaf area per
plant weight, LAR, as has been shown for K under similar
cultural conditions (Ericsson and Kähr 1993). For Mg, however, the functioning leaf area was considerably decreased as a
result of the formation of necroses and reduced leaf longevity
(Table 1). When N or P limits growth, LAR is decreased
mainly because of root growth and increased costs for leaf
production (McDonald et al. 1991). We conclude that Mg
exerts its over-all growth regulatory role in birch seedlings in
a similar way to N and P, namely by affecting photosynthetically active leaf area. The uppermost and healthy leaves remained in a productive stage, regardless of the extent of Mg
restriction. The major difference between treatment extremes
was the proportion of leaves in the healthy category.
We assume that the establishment and maintenance of mycorrhizae are endangered when root growth is suppressed as a
result of decreased export of assimilates from the shoot (Meyer
et al. 1988), because the fungal component in this symbiosis is
totally dependent on host-derived carbon. Decreased fungal
Table 5. Net uptake rates of N, K, P, Mg, Fe and Mn per unit root
growth, dn/dWr (mmol g DW−1), in hydroponically grown birch seedlings during the phase of steady-state nutrition and the relative decrease in net uptake rates in response to a fourfold decrease in the
availability of these mineral elements (RA = relative addition rate,
day − 1). Data for N from Ingestad (1979), K from Ericsson and Kähr
(1993), P from Ericsson and Ingestad (1988), Mg from this study, Fe
from Göransson (1993a), and Mn from Göransson (1994). Mean
values are based on two to eight observations.
RA
N
K
P
(10 − 1)
Mg
(10 −1)
Fe
(10 − 3)
Mn
(10 −3)
0.20
0.05
11.5
1.7
1.5
0.5
6.9
0.8
2.8
3.0
4.7
2.4
1.3
1.6
3.1
8.7
0.9
2.0
0.8
Relative decrease
4
6.7
92
ERICSSON AND KÄHR
growth will, in turn, negatively affect the uptake of nutrients
still further. Our data suggest why Mg shortage under field
conditions is a greater threat to the health and productivity of
plants than a shortage of elements such as N and P.
Acknowledgments
We thank Annette Hovberg and Anette Carlsson for growing the test
plants, and the Analytical Laboratory of the Department of Ecology
and Environmental Research for the mineral analyses. We are also
grateful to Anita Flower-Ellis who helped us with carbohydrate determinations. Anders Göransson, Roger Pettersson, Lars Rytter and Fredrik Wikström offered valuable suggestions on the manuscript. The
investigation was financially supported by grants from the National
Council for Forestry and Agricultural Research in Sweden.
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© 1995 Heron Publishing----Victoria, Canada
Growth and nutrition of birch seedlings at varied relative addition
rates of magnesium
TOM ERICSSON and MONIKA KÄHR
Department of Ecology and Environmental Research, Swedish University of Agricultural Sciences, P.O. Box 7072, S-750 07 Uppsala, Sweden
Received November 25, 1993
Summary Growth and nutrition of hydroponically cultivated
birch seedlings (Betula pendula Roth.) were investigated at
various magnesium (Mg) availabilities. Suboptimum Mg conditions were created by adding Mg once per hour in exponentially increasing amounts at one of four relative addition rates
(RMg): 0.05, 0.10, 0.15 or 0.20 day −1. Seedlings given free
access to Mg were used as controls. After an acclimation
period, the relative growth rate of the seedlings attained the
same value as the corresponding relative rate of Mg addition.
In all suboptimum Mg treatments, deficiency symptoms in the
form of chloroses and necroses developed in the older leaves,
both during and after the phase of growth acclimation. The
severity of these symptoms was correlated with the availability
of Mg. The relative growth rate of seedlings was linearly
correlated with plant Mg status. The root fraction of the total
biomass decreased from 22% in control plants to 8% in plants
receiving the lowest rate of Mg addition. A shift in Mg availability from free access to RMg = 0.05 day −1 decreased the
photosynthetically active leaf area per plant weight, despite a
concomitant increase in the leaf weight ratio (leaf dry
weight/plant dry weight) from 0.61 to 0.75. The loss in assimilating leaf area was mainly a consequence of enhanced leaf
mortality and formation of necroses, and to a minor extent
attributable to increased carbon costs for leaf area production.
A decrease in starch concentration was observed in leaves
showing Mg-deficiency symptoms, whereas the starch concentration in healthy leaves was unaffected by Mg availability. It
was concluded that shortage of carbohydrates constituted the
major growth constraint, particularly for roots, under Mg-limiting conditions.
Keywords: Betula pendula, dry matter distribution, leaf area
ratio, leaf weight ratio, net assimilation rate, nonstructural
carbohydrates, nutrient uptake rate.
Introduction
Nutrient uptake and growth are time-dependent processes and
the amount of nutrients taken up per unit of time is therefore
strongly coupled to both the size and growth rate of the plant.
Consequently, the quantitative nutrient requirement during the
course of an experiment increases more or less rapidly with
time. According to Ingestad (1982), full control over nutrient
uptake, plant nutrient status and growth can only be achieved
if the supply of nutrients is treated dynamically, i.e., by frequent nutrient additions (daily or hourly) in amounts adjusted
both to plant size and the desired growth rate.
The relative addition rate of nutrients has been used as a
treatment variable when studying the influence of plant nutrient status on physiological processes. Nitrogen fixation in gray
alder (Ingestad 1980), nitrogen nutrition in ectomychorrizal
Scots pine seedlings (Ingestad et al. 1986), carbohydrate dynamics in birch (McDonald et al. 1986), aluminum toxicity in
forest trees (Göransson and Eldhuset 1987, 1995), leaf chemistry and insect susceptibility in Salix (Waring et al. 1985,
Larsson et al. 1986), and leaf expansion (Taylor et al. 1993) are
examples of areas investigated under steady-state nutrition.
One of the most striking observations made with this technique
is the disappearance of deficiency symptoms after growth
acclimation to suboptimal supply rates of nitrogen (Ingestad
and Lund 1979) and phosphorus (Ericsson and Ingestad 1988).
Improved light conditions are generally associated with an
increase in the shoot/root ratio (Björkman 1981, Corré 1983),
but no significant effect of photon flux density on dry matter
partitioning was observed in experiments with small birch
plants where steady-state nutrition was maintained (Ingestad
and McDonald 1989). Similarly, elevated atmospheric CO2
concentration, which is often associated with a shift in the
carbon allocation pattern toward roots (Mousseau and Enoch
1989), caused no change in the shoot/root ratio of birch seedlings when the nutrient status of the test plants was carefully
controlled (Pettersson and McDonald 1992, Pettersson et al.
1993). Plant nutrient status, and its stability during the period
of investigation, thus has a strong impact on the results obtained and their interpretation.
The relationship between mineral nutrient status and growth
of birch seedlings has been extensively studied under conditions where the relative addition rate of nutrients has constituted the treatment variable. Nitrogen (Ingestad 1979),
phosphorus (Ericsson and Ingestad 1988), potassium (Ericsson
and Kähr 1993), iron (Göransson 1993) and manganese
(Göransson 1994) are the elements studied so far. The present
investigation is a continuation of these nutritional studies and
the element in focus this time was magnesium (Mg). Our
86
ERICSSON AND KÄHR
choice of element was based on recent interest in Mg deficiency as one of the factors causing forest dieback in areas of
central Europe and North America (Hüttl 1988, Schulze et al.
1988, Roberts et al. 1989). We hypothesized that disturbed
forest growth is associated with decreased carbohydrate availability in the tissues. Because Mg is essential for the activation
of many enzymes, including those required for CO2 fixation
(Marschner 1986), we were particularly interested in the influence of plant Mg status on the carbohydrate concentration of
tissues and on dry matter partitioning among root, stem and
leaves.
Material and methods
Growth conditions
The experiments were carried out in growth chambers with a
continuous photon flux density of 260 µmol m −2 s −1 (400 to
700 nm, Osram HQI R 250W/D). Both the air and root temperatures were 20 ± 0.5 °C and the vapor pressure deficit in the
air, VPD, was approximately 0.6 MPa.
Seedling culture
Birch seedlings (Betula pendula Roth.) were used as test material. Seeds were germinated on wet filter paper in petri dishes
under low light intensity, 50 µmol m −2 s −1, for about 10 days.
Seedlings at the same developmental stage were then planted
in growth units where the roots were continuously sprayed
with a circulating culture solution with a volume of 5 dm3. A
detailed description of the growth unit has been presented
elsewhere (Ingestad and Lund 1986). The culture solution
contained all essential mineral elements in the proportions
given by Ingestad and Lund (1986) (N = 100, K = 65, P = 13,
Ca = 7, Mg = 8.5, S = 9, Fe = 0.7, Mn = 0.4, B = 0.2, Zn = 0.06,
Cu = 0.03, Cl = 0.03, Mo = 0.007, Na = 0.003). Non-growthlimiting conditions were created by keeping the conductivity
of the culture solution between 250 and 350 µS cm −1, which is
equivalent to a nitrogen concentration of 3--4 mM. The pH of
the culture solution was maintained at 4.8--5.2. A computer
was used to control the hourly conductivity and pH titrations.
After pregrowth for 14 days under the culture conditions described, 60 uniform seedlings with a fresh weight (FW) of
40--50 mg per plant, were selected in groups of four for use in
each of the different treatments.
Treatments
Four relative addition rates of magnesium (RMg = 0.05, 0.10,
0.15 and 0.20 day −1) were used to induce a range of suboptimum plant Mg concentrations. These treatments corresponded to an approximate Mg restriction of 80 to 10%,
respectively, of the potential Mg requirement under the chosen
climatic conditions. The concentration of Mg in the seedlings
at the start of each treatment, 0.51 mg gFW−1, was used to
calculate the hourly Mg additions:
Mg t = Mg s(eR Mg /24 − 1)(eR Mg t/24 ),
where Mgs is the initial amount of magnesium in the seedlings,
and Mgt is the amount of magnesium added, together with
other essential nutrient elements, that is sufficient for one hour
of uptake at any time t hours from the beginning of the experiment at the desired RMg (Ingestad and Lund 1986). Conditions
that were not growth limiting with respect to availability of
other essential mineral elements were ensured by keeping the
conductivity of the culture solution above 70 µS cm −1. This
was achieved by automatic conductivity titrations with a Mgfree stock solution. The pH of the culture solution during the
experiments varied between 4.2 and 5.2.
A fifth treatment provided non-growth-limiting Mg conditions. All essential elements were supplied in the proportions
found optimal for birch (Ingestad and Lund 1986) and in free
access (FA). The magnesium concentration was kept in the
range of 0.1 to 0.2 mM by maintaining the conductivity of the
culture solution between 100 and 200 µS cm −1. The pH of the
solution varied between 4.2 and 5.2. All experiments were run
twice.
Harvesting
After an initial acclimation period of varying length, depending on the extent of Mg limitation, all plant groups in the 0.05,
0.10 and 0.15 day −1 treatments were reweighed, whereas
plants in the more short-term experiments, 0.20 day −1 and FA,
were left undisturbed. Groups of seedlings were then harvested
on four occasions during the exponential period of growth,
which lasted from 24 (FA) to 69 days (RMg = 0.05 day −1). Fresh
and dry weights (48 h at 70 °C) of roots, stems and leaves as
well as leaf area (LI 3310, Li-Cor Inc., Lincoln, NE) were
determined. The leaves were divided into three categories: 1 =
healthy, 2 = necroses covering less than 75%, and 3 = necroses
covering more than 75% of the leaf surface.
Analyses
Samples for macronutrient analyses were prepared by digestion in a solution of 10 ml concentrated HNO3 and 1 ml HClO4.
One ml of 2 M HNO3 was added to the digest and the solution
was diluted with water to 35 ml. Nitrogen was analyzed with
an elemental analyzer (Elemental Analyzer NA 1500, Rodano,
Italy). The macronutrients P, K, Ca, Mg and S were analyzed
by inductively coupled plasma spectrometry (Jobin Yvon JY70, Longjumeau, France).
Nonstructural carbohydrates were analyzed by the method
described by Steen and Larsson (1986) based on a two-step
extraction procedure. Glucose, fructose, sucrose, fructan and
soluble starch were determined in the first extract and residual
starch in the second extract.
Calculations
Growth was determined as relative growth rate, RG (day −1),
based on weights, W, on the four harvest dates, t, by fitting an
exponential curve:
W = W 0 eR Gt,
GROWTH AND MAGNESIUM NUTRITION IN BIRCH
where W0 is the weight of the seedlings at the beginning of the
treatments (RMg = 0.20 day −1 and FA) or after the acclimation
period (RMg = 0.05, 0.10, 0.15 day −1).
The net uptake rate of nutrients per root growth rate, dn/dWr
(mmol g −1 root growth), was calculated from:
n W C W 10 3
dn
=
=
,
M Wr
dW r W Wr
where n is the nutrient amount in the plant, C its tissue concentration, M the molecular weight, and W and Wr the dry weights
of the seedling and root system, respectively (cf. Ingestad and
Ågren 1988).
The net assimilation rate, NAR (kg plant dry weight (DW)
m−2 day −1), was calculated from:
NAR =
RG
,
LAR
where the leaf area ratio, LAR (m2 kgDW−1 plant), is the product
of specific leaf area, SLA (m2 kgDW−1 leaf), and leaf weight
ratio, LWR (leafDW plantDW−1):
LAR = SLA × LWR .
Statistical analyses
Statistical analyses were carried out by one-way ANOVA
(Statgraphics Inc., Rockville, Maryland, USA). The pair-wise
comparisons were made by the Least Significant Difference
method. The confidence level was 0.05.
87
Plant growth
The RG of the seedlings was similar to that of the treatment
variable, RMg, after an acclimation period of 14--29 days,
depending on the extent of Mg limitation (Figure 2). The
regression coefficients, r2, for the curve fitting of RMg with RG
were generally > 0.99. An RG of 0.23 day −1 was reached under
nonlimiting Mg conditions. The calculated net assimilation
rate, NAR, based on the area of leaves showing necroses on
less than 75% of their surface, decreased from 10.9 to 4.3 ×
10 −3 kg m −2 day −1 when the Mg supply was restricted from
free access to 0.05 day −1 (Table 1). The decline in NAR was
less pronounced, 10.9 to 8.8 × 10 −3 kg m −2 day −1, when only
the area of healthy leaves was considered to be photosynthetically active.
Dry matter partitioning
The proportional allocation of dry matter to roots decreased in
response to growth-limiting availability of Mg (Figure 1).
Roots made up about 8% of the standing biomass at RMg =
0.05 day −1 compared with 22% at free access. Concomitantly,
the fraction of leaves of the total biomass increased from 61 to
75% on a dry weight basis with increased Mg limitation
(Figure 1, Table 1). The leaf area per plant dry weight, LAR,
however, decreased from 21.0 to 11.2 m2 kg −1 (healthy + leaves
damaged on less than 75% of the leaf surface) or from 21.0 to
5.0 m2 kg −1 (healthy leaves) when Mg availability was reduced
from free access to 0.05 day −1 (Table 1). Leaf area production
Results
Plant appearance
Deficiency symptoms, in the form of chloroses and necroses,
developed in the older leaves at growth-limiting supply rates
of Mg, both during and after the phase of growth acclimation.
The severity of these symptoms was correlated with the extent
of Mg limitation (Figure 1). Pronounced increases in leaf
mortality rate and leaf fraction showing necroses on more than
75% of the leaf surface were obtained when RMg was reduced
from free access to 0.05 day −1 (Figure 1). This change occurred
at the expense of healthy leaves, the proportion of which
decreased from 100 to 20%. At the lowest rate of Mg addition,
only the uppermost three to four leaves remained undamaged,
although they exhibited slight interveinal chlorosis. The leaf
fraction showing damage to less than 75% of the leaf surface
constituted roughly 30% of the leaf biomass within the whole
range of suboptimum Mg availabilities studied. Both the size
of newly formed leaves and internode lengths were reduced at
RMg = 0.15 day −1 and lower. The branching pattern of the root
system was more or less unaffected by the supply rate of Mg.
The overall vigor of the roots, including characteristics such as
length and diameter, was reduced by a growth-limiting availability of Mg.
Figure 1. Dry matter distribution in birch seedlings grown in culture
solution at varied suboptimum relative addition rates of Mg, RMg
(day − 1), and at free access, FA. The leaf biomass fraction was divided
into three categories: 1 = healthy leaves (h), 2 = leaves with necroses
covering less than 75% of the leaf surface (< 75%), and 3 = leaves with
necroses covering more than 75% of the leaf surface (> 75%). Columns marked with the same letter within each biomass fraction are not
significantly different (LSD, 0.05 level, n = 5).
88
ERICSSON AND KÄHR
per unit of carbon used for leaf growth, SLA (m2 kg −1 leaf),
was not affected by the supply rate of Mg (Table 1).
Plant nutrient status
Figure 2. Influence of the relative Mg addition rate, RMg (day − 1), on
the relative growth rate, RG (day − 1), of birch seedlings grown in
culture solution. The linear regression and coefficient of determination, r2, are given. Filled symbols denote RG obtained under nonlimiting Mg-conditions; these data points are not included in the linear
regression.
Seedling RG was positively and linearly correlated with Mg
concentration of both the whole plant and the leaves (Figures
3a and 3b). The lowest tissue Mg concentration on a wholeplant basis that supported maximum growth rate (the intersection between the lines in Figure 3a) was 1.4 mg gDW−1. The
corresponding value for undamaged leaves was 1.8 mg gDW−1
(Figure 3b). About three times more Mg than required for
structural growth was taken up under nonlimiting Mg conditions (Figure 3a). At growth-limiting supply rates of Mg, a
strong gradient in foliar Mg concentration developed within
the shoot. The youngest leaves, without Mg-deficiency symptoms or with only weak symptoms, contained two to three
times more Mg within the range of suboptimum Mg availabilities studied than the older damaged leaves toward the base of
the shoot (Table 2). Visible deficiency symptoms in the form
of necroses were generally associated with foliar Mg concentrations below 1 mg gDW−1 at RMg = 0.20 day −1 and below 0.5
mg gDW−1 at RMg = 0.05 day −1 (Table 2). The difference in Mg
concentration between leaves with damage on more than 75%
of the surface and leaves with damage on less than 75% of the
surface was less pronounced.
Table 1. Mean values of net assimilation rate, NAR (kg m − 2 day−1 × 10 − 3), leaf weight ratio, LWR (kg kg − 1), leaf area ratio, LAR (m2 kg −1), and
specific leaf area, SLA (m2 kg − 1), of birch seedlings grown at various relative addition rates of Mg, RMg (day −1), and at free access, FA. The
projected leaf area of healthy leaves only, Lh, was used to calculate NAR, LAR and SLA. The parameters NAR and LAR were also calculated on
the basis of the leaf area of healthy leaves + leaves with necroses covering less than 75% of the leaf surface, Lh+75 , and FA where n = 3, 1 and 2, respectively).
Treatment RMg
0.05
0.10
0.15
0.20
FA
1
Carbohydrate
Starch
Soluble
Starch
Soluble
Starch
Soluble
Starch
Soluble
Starch
Soluble
Roots
1.2 ± 1.0 a
7.0 ± 2.9 a
1.5 ± 1.4 a
5.5 ± 2.2 a
1.5 ± 1.2 a
5.5 ± 2.2 a
2.0 ± 1.0 a
5.0 ± 1.7 a
1.5 ± 2.1 a
12 ± 2.8 b
Stems
2.5 ± 1.6 a
14 ± 2.1 a
3.5 ± 2.7 a
15 ± 6.4 a
3.5 ± 2.1 a
17 ± 3.9 a
6.0 ± 1.5 a
18 ± 3.1 a
7.5 ± 0.7 a
21 ± 2.8 b
Leaves
Lh
L75
42 ± 4.7 a,A
38 ± 3.1 a,A
45 ± 10.3 a,A
38 ± 6.3 a,A
45 ± 9.5 a,A
38 ± 4.2 a,A
53 ± 10.6 a,A
41 ± 8.4 a,A
57 ± 2.1
56 ± 1.4
7.5 ± 4.3 a,B
66 ± 8.3 a,B
14 ± 3.4 a,B
62 ± 9.4 a,B
23 ± 7.5 b,B
65 ± 2.4 a,B
40 ± 9.7 c,A
73 ± 8.3 a,A
---
6.0 ± 2.2 a,B
69 ± 6.7 a,B
9.0 ± 4.2 a,B
70 ± 6.4 a,B
16*1
72*
-----
An asterisk (*) denotes a single analysis.
roots generally contained less than 8 and 21 mg gDW−1 of starch
and soluble carbohydrates, respectively, over the range of Mg
availabilities studied (Table 4).
Discussion
Chlorosis, and particularly necroses, developed in the older
leaves of the Mg-limited birch seedlings as a consequence of
internal Mg cycling. These symptoms appeared once the leaf
Mg concentration had decreased to about half the value of
healthy leaves. This threshold value was higher under mild Mg
restriction, ≈ 1 mg gDW−1 leaf, than under strongly growth-limiting Mg conditions, ≈ 0.5 mg gDW−1 at RMg = 0.05 day −1
(Table 2). The difference in threshold values may be associated
with differences in the pool size of metabolically active and
inactive Mg. However, the difficulties associated with conducting an objective leaf sampling among the chosen leaf
categories offer a more likely explanation for the observed
discrepancy. The small difference in leaf Mg concentration
between the two categories of damaged leaves suggests that
most of the Mg available for resorption had already been
withdrawn before the deficiency symptoms became apparent.
Efficient retranslocation of limiting elements from old to
young foliage ensures the maintenance of physiological processes. About 80% of leaf biomass showed deficiency symp-
toms under severe Mg limitation (RMg = 0.05 day −1), whereas
30% of the leaf biomass showed deficiency symptoms when
the growth rate of the seedlings was only slightly suppressed
by Mg supply (RMg = 0.20 day −1) (Figure 1).
Luxury consumption of N was evident under Mg-limiting
growth conditions (Table 2). This phenomenon has also been
observed when Fe (Göransson 1993), Mn (Göransson 1994) or
Zn (Göransson, personal communication) constituted the
growth-limiting element. Nitrogen taken up in excess of
growth requirements is generally stored in the leaves in the
form of amino acids (Näsholm and McDonald 1990, Näsholm
1991) and acts as a sink for carbohydrates. Because the conversion of N to amino acids generally takes place in the roots
in trees, luxury uptake of N under growth-limiting Mg conditions may contribute to further decreases in the amounts of
carbohydrates available for root growth. We observed an antagonistic effect of Mg on Ca uptake. About three times more
Ca was found in stems and roots at the lowest rate of Mg supply
than at FA (Table 2). Conversely, the presence of a high Ca
concentration in the root medium is likely to exacerbate the
effects of Mg deficiency.
In contrast to previous reports for trees (e.g., Matzner et al.
1986) and herbaceous plants (e.g., Bottrill et al. 1970, Fischer
and Bussler 1988), starch did not accumulate in leaves at
suboptimum Mg tissue concentrations (Table 4). There was a
GROWTH AND MAGNESIUM NUTRITION IN BIRCH
significant decrease in starch concentration in all leaves showing Mg-deficiency symptoms that was independent of the
extent of Mg restriction. We also observed a small decrease in
the starch concentration of healthy leaves when Mg availability was reduced from free access to RMg = 0.05 day −1. We
conclude that the main constraint associated with a shortage of
Mg is a reduction in net carbon gain rather than impaired
assimilate transport in the phloem as suggested by Fink (1989),
because, although not observed in our study, a shortage of Mg
has a strong and negative impact on the rate of carbon fixation
(Beyschlag et al. 1987, Zimmermann et al. 1988). A possible
explanation of our results might be that the carbohydrate
analyses were carried out during the phase of steady-state
nutrition when both the growth rate and the tissue content of
Mg had acclimated to the Mg supply. In most studies, Mg
deficiency was induced by omitting Mg from the growth substrate and, as a result, the internal Mg concentration was
continuously decreasing, i.e., the plants never reached the
phase of steady-state growth.
The importance of the assimilate available for root growth
has already been pointed out by Pearsall (1923) and White
(1937). The balance between carbohydrates and nitrogen in
tissues plays a key role in determining the magnitude of aboveand belowground growth according to Brouwer (1962). When
there is a decrease in carbohydrate supply, the shoot retains a
larger fraction of assimilates than the root, thus increasing the
shoot/root ratio; the opposite occurs when mineral nutrients or
water supplies are decreased (cf. Thornley 1972, Dewar 1993).
Thus, Mg deficiency, which negatively affects carbon fixation,
has a negative impact on root growth. Under severe Mg limitation, the root made up only about 8% of the total biomass
(DW), whereas almost three times as much biomass was allocated to the root under non-growth-limiting Mg conditions
(Figure 1). Similar growth behavior in response to Mg shortage
is generally (e.g., Shear 1980, Marschner 1986, Matzner et al.
1986), but not always (e.g., Will 1961), observed.
If the allocation of biomass to roots is decreased in response
to a mineral shortage, the soil volume exploited by the plant
will also decrease. In turn, this will decrease the uptake of the
limiting element still further. This negative feedback could
lead to plant decline, unless the uptake per unit root growth,
dn/dWr, required to reach a new steady state decreases to a
larger extent than the flux of the limiting element. This condition is obtained if the limiting element exerts its growth regulatory role over a large concentration range in the tissue. We
found that the uptake of Mg per gram of root growth necessary
to achieve a new equilibrium between uptake and growth was
slightly higher after a fourfold reduction in Mg availability
(Table 5). It has previously been shown that for K (Ericsson
and Kähr 1993), Fe (Göransson 1993) and Mn (Göransson
1994), dn/dWr decreases to a lesser extent than the flux of these
elements (Table 5). For N (Ingestad 1979) and P (Ericsson and
Ingestad 1988), dn/dWr decreases almost seven to nine times,
respectively, in response to a fourfold reduction in their availabilities. Although, in the present study the uptake of Mg per
gram of root growth did not match the decrease in Mg flux
given to the plants, steady-state conditions of Mg uptake and
91
growth were established even in treatments where Mg was
severely limiting, probably because the spray technique brings
nutrients in direct contact with actively nutrient-absorbing root
surfaces. In a solid substrate, however, the size of the root
system in relation to shoot and root growth plays a dominant
role in nutrient acquisition (Clarkson 1985).
Shortage of Mg was expected to bring about a decrease in
the net assimilation rate, NAR, of the same magnitude as
reported for K (Ericsson and Kähr 1993), because both elements are essential for carbon fixation. However, we observed
only a small decrease in NAR in response to reduced Mg
availability (Table 1). In this respect, Mg shows similarities
with N and P (McDonald et al. 1991), although N and P more
directly interfere with the activity of the sinks (the meristems)
than of the source (carbon fixation). If the functional component of RG, NAR, is only slightly affected by a reduced nutrient
flux then the structural development of the plant must also
change (cf. Beadle 1985). This was the case under growth-limiting supply rates of Mg, but in contrast to N and P, more of the
assimilates available for growth were utilized in the shoot than
in the root (Figure 1). An increased allocation of biomass to
leaves generally implies an increase in the total leaf area per
plant weight, LAR, as has been shown for K under similar
cultural conditions (Ericsson and Kähr 1993). For Mg, however, the functioning leaf area was considerably decreased as a
result of the formation of necroses and reduced leaf longevity
(Table 1). When N or P limits growth, LAR is decreased
mainly because of root growth and increased costs for leaf
production (McDonald et al. 1991). We conclude that Mg
exerts its over-all growth regulatory role in birch seedlings in
a similar way to N and P, namely by affecting photosynthetically active leaf area. The uppermost and healthy leaves remained in a productive stage, regardless of the extent of Mg
restriction. The major difference between treatment extremes
was the proportion of leaves in the healthy category.
We assume that the establishment and maintenance of mycorrhizae are endangered when root growth is suppressed as a
result of decreased export of assimilates from the shoot (Meyer
et al. 1988), because the fungal component in this symbiosis is
totally dependent on host-derived carbon. Decreased fungal
Table 5. Net uptake rates of N, K, P, Mg, Fe and Mn per unit root
growth, dn/dWr (mmol g DW−1), in hydroponically grown birch seedlings during the phase of steady-state nutrition and the relative decrease in net uptake rates in response to a fourfold decrease in the
availability of these mineral elements (RA = relative addition rate,
day − 1). Data for N from Ingestad (1979), K from Ericsson and Kähr
(1993), P from Ericsson and Ingestad (1988), Mg from this study, Fe
from Göransson (1993a), and Mn from Göransson (1994). Mean
values are based on two to eight observations.
RA
N
K
P
(10 − 1)
Mg
(10 −1)
Fe
(10 − 3)
Mn
(10 −3)
0.20
0.05
11.5
1.7
1.5
0.5
6.9
0.8
2.8
3.0
4.7
2.4
1.3
1.6
3.1
8.7
0.9
2.0
0.8
Relative decrease
4
6.7
92
ERICSSON AND KÄHR
growth will, in turn, negatively affect the uptake of nutrients
still further. Our data suggest why Mg shortage under field
conditions is a greater threat to the health and productivity of
plants than a shortage of elements such as N and P.
Acknowledgments
We thank Annette Hovberg and Anette Carlsson for growing the test
plants, and the Analytical Laboratory of the Department of Ecology
and Environmental Research for the mineral analyses. We are also
grateful to Anita Flower-Ellis who helped us with carbohydrate determinations. Anders Göransson, Roger Pettersson, Lars Rytter and Fredrik Wikström offered valuable suggestions on the manuscript. The
investigation was financially supported by grants from the National
Council for Forestry and Agricultural Research in Sweden.
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