Journal of Experimental Botany, Vol. 50, No. 336, pp. 1169–1177, July 1999
The modular character of growth in Nicotiana tabacum
plants under steady-state nutrition
A. Walter and U. Schurr1
Department of Botany, University of Heidelberg, Im Neuenheimer Feld 360, D-69120 Heidelberg, Germany
Received 8 December 1998; Accepted 25 February 1999
Abstract
The impact of different plant growth rates on biomass
allocation and growth distribution in tobacco was
studied on the whole plant, total leaf area and single
leaf level. On the whole plant level, constant relationships were found between the total leaf area and
the biomass allocation to leaves and the nonphotosynthetic organs (roots and stem) independent
from the overall growth rate and the nutrient addition
rate to the plants. On the level of total leaf area, plants
grown at lower nutrient supply reached a distinct distribution of leaf area later than those grown at higher
nutrient supply, but the normalized distribution of leaf
area along the stem at a certain plant size did not
differ between plants growing at different nutrient
supply and growth rates. On the leaf blade level,
growth rates declined, initially linearly, from the leaf
base to the leaf tip. Distinct gradients within the side
veins were not observed, but the growth rates of the
side veins were closely correlated to the adjacent midvein segments. These gradients flattened with increasing size of the leaf. The modular character of growth
in tobacco is discussed in the context of basic growth
analysis and as a framework for physiological, cytological, biochemical, and molecular studies in growing
plants.
Key words: Nicotiana tabacum, whole plant, total leaf area,
leaf growth, growth rate, biomass.
Introduction
Growth occurs simultaneously at a number of sites of the
plant exerting different functions like nutrient or carbon
supply that need to be co-ordinated on the whole plant
level. As a consequence of this co-ordination, growth
patterns evolve that determine the typical habitus for a
certain species. Their basis is the organization of the plant
from modules like leaves, internodes and roots arranged
in a characteristic way (phytomers) (Scanlon, 1998).
Underlying principles in these patterns represent the
functional balance between different parts of the plant
and can only be understood from a multiscale approach:
whole plant processes need to be coupled mechanistically
to the underlying growth process in the individual modules to understand growth regulation. On the other hand,
analysis of growth on the level of the organs and on
smaller scales needs to be related to the framework of
the whole plant.
Quantitative analysis of the patterns requires the use
of adequate co-ordinate systems. The higher complexity
inherent to areal growth of dicot leaves has hampered
progress in this field significantly, in contrast to linearly
arranged monocot leaves or roots (Schurr, 1997). Often
cartesian (rectangular) co-ordinate systems are used to
analyse spatial aspects of growth (Avery, 1933; Poethig
and Sussex, 1985; Granier and Tardieu, 1998). They are
useful for the description of Euclidean geometric objects
(or models), or for spatio-temporal movements of points
like in classical mechanics, but hardly for natural objects.
The physical description of movement or growth processes of natural objects subjected to natural conditions/
constraints can more adequately be described within
‘natural’ co-ordinate systems (Hejnowicz and Karczewski,
1993). It is therefore essential to determine suitable
co-ordinate systems for the respective scale that can be
interrelated to higher and lower scales. It is proposed that
such a natural co-ordinate system for the description of
leaf growth could be the vein system of the leaf.
The functional approach to plant growth in its simple
form is only valid if the parameters determining the
physiological function remain constant. This allows the
plant to gain a structure, in which the functional balance
1 To whom correspondence should be addressed. Fax: +49 6 221 545 859. E-mail: [email protected]
© Oxford University Press 1999
1170 Walter and Schurr
can actually be seen. If environmental conditions, like
nutrient supply, change during growth the evolving functional imbalances can typically not be translated directly
into a new architecture, since already formed modules
cannot be restructured to meet the new requirements
(Schurr, 1997). Therefore, a prerequisite to identify functionally related patterns is to maintain external growth
conditions initially as constant as possible, prior to understanding the complex, dynamic responses as they obviously are common in the field.
Growth cabinets allow maintenance of temperature,
humidity and light conditions, but in many cases nutrient
supply, as one of the most important environmental
constraints governing growth, is less controlled. Often
nutrients are added to plants in nutrient solutions at a
constant concentration irrespective of the increase in
nutrient demand with the increase in growing biomass
(Ingestad and Agren, 1992; Hellgren and Ingestad, 1995).
Therefore, nutrient supply at constant concentrations
contains the risk that plants are subjected to decreasing
availability of nutrients and thus the architecture of the
plant can not attain a steady-state. Steady-state nutrition
can be achieved by adding nutrients in relation to growth
rate. Plants subjected to non-maximal nutrient addition
rates adjust their growth rate to the nutrient supply
(Ingestad and Agren, 1992).
In the present study, patterns of growth in tobacco
plants grown in steady-state nutrition are presented,
starting from the whole plant perspective and leading
down to the distribution of growth on a single leaf.
Further analysis from the single leaf level to biochemical
data will be presented in a forthcoming paper (A Walter,
U Schurr, unpublished results).
the basis that the fresh weight of the seedlings contained 0.5%
N. The nutrient proportions by weight with respect to nitrogen
were: NO− 61.5%, NH+ 38.5%, K+ 65%, PO3− 13%, Ca2+
3
4
4
7%, Mg2+ 8.5%, SO2− 9%, Fe 0.7%, Mn 0.4%, Cu 0.03%, Zn
4
0.06%, B 0.2%, Mo 0.07%, Na+ 0.034%, Cl− 0.033%. Each day
2 h after onset of the light, the sand in each pot was thoroughly
percolated with distilled water to remove any nutrients.
Immediately after percolation the nutrient solution was added
with a pipette in volumes between 1 and 10 ml.
When leaf 10 (cotyledons were numbered as ‘leaf 1’ and ‘leaf
2’) had reached an area of 2 cmO, three plants from each
population were harvested every second/third day over a period
of 16 d and plants were dissected into root, stem and individual
leaves. The fresh weight of the excised plant parts was
determined immediately with a balance (Sartorius; sensitivity
0.1 mg). Dry weight was determined after drying the samples
for 2 d at 80 °C.
Materials and methods
Distribution of growth on the leaf blade
For analysis of growth distribution on leaf blades, the vein
system was used as a natural co-ordinate system (Hejnowicz
and Karczewski, 1993). Ink marks were placed on class II veins
(Ding et al., 1988) of 2–3 cm long leaf blades (n=4). The
longitudinal growth of these segments and of the class I veinsegments enclosed by them was measured with a slide caliper
(precision 0.1 mm) daily 8 h after the onset of the light.
Unidirectional relative growth rates were calculated as given
above for the relative growth rates of the leaf area. Relative
growth rates of the areas enclosed by a class I vein segment
and its adjacent class II vein were calculated by adding the
unidirectional growth rates of the two elements because the
angle between them did not change significantly from day to day.
Cultivation, nutrition and harvests
Tobacco (Nicotiana tabacum L. cv. Samsun) seeds were
germinated on sand and transplanted into 15 cm diameter pots
containing a 151 mixture of sand of different grain size
(0.6–0.8 mm and 0.6–1.2 mm). Three populations with different
nutrient supply (see below, n=22 per treatment) were grown in
a walk-in growth chamber ( Weiss, Giessen) with a 12/12 h
photoperiod (180–220 mmol photons m−2 s−1 at the uppermost
leaf ), a constant air temperature of 25 °C and a constant
relative humidity of 60%.
For a period of 11 d after transplanting, the seedlings received
a constant concentration of nutrients. Thereafter the amount
of nutrients added per day was increased to match the increase
of the nutrient demand with increase in growing biomass (cf.
Ingestad and Lund, 1979). All nutrients were added in fixed
proportions relative to nitrogen. The relative nutrient addition
rates (nutrients added per nutrients already present in the plant)
were constant for each treatment over the entire experiment
(Fig. 1A) at 40% d−1 (high: H ), 24% d−1 (medium: M ) and
18% d−1 ( low: L), respectively. The amount of nitrogen to be
added at the start of the Ingestad treatment was calculated
from the fresh weight of seedlings 11 d after transplanting on
Measurements and calculation of growth rates
The length and width of all leaves of each plant were measured
1 h after the onset of light with a ruler during the last 20–30 d
of each experiment. Leaf area (A) was calculated by the
biometric relation between leaf area, the length of the leaf blade
(L) and the maximal width of the leaf blade (W) as A=
0.75×L×W (Schurr, 1997). This relation was determined on
the basis of 125 leaves from all studied positions at the stem
and from all treatments without significant differences between
treatments or leaf positions. The total leaf area of each plant
was calculated as the sum of all individual leaf areas.
Relative growth rates (RGR) were calculated as:
RGR [%/d ]=100×( ln(A /A ))/(t2–t1)
t2 t1
where A is the area at day t2 and A is the area at day t1.
t2
t1
Relative growth rates for fresh weight and dry weight as well
as relative addition rates (RAR) for nutrient addition were
calculated analogously.
Normalized properties
Normalized distribution functions of leaf area were calculated
as percentages by dividing the area of each leaf by the total
leaf area on a daily basis. The same procedure was done with
leaf growth rates: the difference in area of each leaf at successive
days was divided by the difference of the total leaf area during
the same time interval and expressed as a percentage value.
Modular growth in tobacco 1171
Results
Whole plant growth
The total leaf area of the plants increased almost parallel
to the nutrient addition ( Fig. 1A) over the entire range
of plant sizes (2 cm2 up to 1000 cm2). Relative growth
rates (Fig. 1B) of the treatments with low (L) and medium
(M ) nutrient addition rate were almost constant during
the entire experiment, while the treatment supplied with
a high nutrient addition rate (H ) initially showed lower
relative growth rates of the leaf area (RGR). RGR in this
treatment increased when the nutrient amount was supplied in a bigger volume, decreasing the concentration of
the nutrient solution. The mean total leaf area at high
and medium nutrient availability was three times higher
than at low nutrient supply (Fig. 1C ). Mean relative
growth rates of leaf area of the populations during the
harvest interval were calculated to be 13% d−1 for low
nutrient availability and 18% d−1 in conditions of medium
and high nutrient supply (Fig. 1D). Means of relative
growth rates on a fresh and dry weight basis were identical
(data not shown) indicating constant relative water content of all treatments, but standard deviations of relative
growth rates of leaf area were smaller due to higher
numbers of replicates
measurements.
from
the
non-destructive
Biomass allocation
Plant fresh weight increased linearly ( Fig. 2A–C, cumulative plots) with total leaf area (FW
=
plant
0.060 g cm−2×area leaf
). This relationship was contotal
served with a mean error of 9% in all treatments and for
all harvested plants in a range of plant fresh weights
between 2 and 100 g. This relation was independent of
the growth rate and the nutrient supply to the plants.
Moreover, the fresh weight of leaves, stem (including
petioles) and root increased linearly with the total leaf
area (Fig. 2). Fifty per cent of the fresh weight of each
plant were located in leaves (specific leaf mass:
30 mg cm−2); the other 50% were allocated to root and
shoot axis. With increasing plant size, the share of the
shoot axis rose at the cost of the root. Again these
relations were identical for plants grown at different
growth rates due to different nutrient addition rates. The
ratio between fresh and dry weight was constant throughout the harvesting period for stem and root at relative
water contents of 93.5% and 94%, respectively (data not
Fig. 1. Characterization of Nicotiana plants grown at high (H, 40% d−1), medium (M, 24% d−1) or low (L, 18% d−1) rates of nutrient addition in
an Ingestad culture. (A) Increase in total leaf area and nitrogen-addition in the medium nutrition treatment. (B) Relative growth rates of leaf area
during the period of harvest in treatment H, M and L. (C ) Mean total leaf area during the harvest period in treatment H, M and L and (D) mean
relative growth rates during the harvest interval for all three treatments.
1172 Walter and Schurr
Fig. 2. Cumulative plots of the fresh weight of the total leaf area, the
stem (including the petiole) and the root system in relation to the total
leaf area in Nicotiana tabacum plants subjected to high (H: A and B),
medium (M: C and D) and low (L: E ) nutrient addition rates. The
insets show the plots over the entire range of total leaf area studied in
the experiments.
shown). For individual leaves the proportion of dry
weight at the fresh varied with the position at the stem
between 5% and over 20% with a maximum at the central
leaf positions.
Distribution of growth within the total leaf area
The exponential growth of the total leaf area is achieved
by individual leaves increasing their leaf area sigmoidally,
reaching different final leaf sizes and initiated at different
times ( Fig. 3). Relative contribution of individual leaves
to the total leaf area followed a slightly asymmetrical
binomial distribution along the stem during the entire
experiment (Fig. 4A). With increase in plant size the
distribution broadened as more leaves contributed to the
total leaf area. The maximum of this distribution declined
almost linearly, while moving to higher positions at the
stem with increasing plant size. Differences in the total
growth rate between plants subjected to different relative
growth rates and different nutrient supply were solely due
to the fact that slower growing plants reached particular
stages later than faster growing plants, as indicated by
the absence of differences in the maximum of the binomial
Fig. 3. Cumulative plot of the exponential development of the total
leaf area as composed from sigmoidally growing individual leaves in
Nicotiana tabacum of treatment M (medium nutrient supply rate).
distributions between the three different treatments
( Fig. 4A).
The share of a particular leaf to the daily gain of leaf
area followed a binomial distribution that was narrower
and shifted by one to two leaf positions upwards on the
stem ( Fig. 4B) compared to the distribution of leaf areas.
Again the distribution broadened with increasing size of
the plant and the maxima became lower. Standard deviations were larger for the share on growth than for the
distribution of areas. Therefore, differences between
plants growing at different growth rates of the maximum
of the distribution were not significant. These results
show that the total distribution of leaf area and growth
in plants growing at different overall growth rate at
steady-state nutrition is not altered, but the time needed
to reach a certain size is influenced by the nutrient supply.
The uniformity of the normalized distributions of leaf
area causes the linear correlation of the area of the biggest
leaf at a certain time to the total leaf area at that time
( Fig. 5A) with the biggest leaf always corresponding to
35% of the total leaf area. When the plants left the rosette
state at a total leaf area of about 15 cm2 the share of the
biggest leaf on the total leaf area declined with plant size
and caused an upward bending of the fit (Fig. 5B). By
analogy, the area gain of the total leaf area and the
biggest gain of an individual leaf were strongly correlated
Modular growth in tobacco 1173
Fig. 4. (A) Distribution along the stem of the share of individual leaf positions at the total leaf area (normalized leaf area distribution) expemplarily
for days 49, 62 and 68 from Nicotiana tabaccum grown with medium nutrient addition rate and the position and share of the biggest leaf during
the harvest period of the experiments from plants grown with high (H ), medium (M ) and low (L) nutrient addition rate. (B) Distribution of the
share of individual leaf positions at the total gain of leaf area per day (normalized gain distribution) exemplarily for days 49, 62 and 68 of Nicotiana
tabacum grown with medium nutrient addition rate and the position and share of the leaf with the biggest increase in leaf area per day for the days
of the harvest periods of plants grown at high, medium and low nutrient addition rate.
growth rate and those growing at a lower relative growth
rate than the overall total leaf area was constant at 0.5,
irrespective of the overall growth rates and nutrient
availability ( Fig. 6). The apparent scatter is due to the
binary principle in the classification of a certain leaf to
one or the other class. In plants growing at different
constant nutrient addition/growth rates, 50% of the biomass was located in the leaves with 1/3 allocated to leaves
growing faster and 2/3 to leaves growing at lower than
Fig. 5. (A) Relationship between the total leaf area and the leaf area
of the biggest leaf of Nicotiana tabacum grown at high (H ), medium
(M ) and low (L) nutrient addition rates. Part A is an enlargement of
part B. (C ) Relationship between the maximal increase of a single leaf
and the increase of total leaf area at the same day for Nicotiana
tabacum grown at high, medium and low nutrient addition rates. Part
C is the enlargement of part D.
(Fig. 5C, D), again irrespective of the nutrient supply
and growth rate of the plants. This indicates that the area
below the binomial normalized distribution functions for
area and growth remains constant with plant size.
The ratio between leaves growing at a higher relative
Fig. 6. Relationship between the area of leaves growing faster (‘biomasssink leaf area’) and the area of leaves growing slower (‘biomass-source
leaf area’) than the total leaf area for Nicotiana tabacum plants grown
at high (H ), medium (M ) and low (L) nutrient addition rate.
1174 Walter and Schurr
average (Fig. 7). The remaining 50% of the biomass was
located in stems and roots with the stem gaining a higher
percentage with increasing plant size.
Distribution of growth within a single leaf
A distinct gradient of growth rate was present along the
mid-vein of tobacco leaves ( Fig. 8A): The basal segments
of the mid-vein grew faster than the apical segments. In
contrast, the side veins did not show significant gradients
of growth rates from the midrib to the leaf margin
(Fig. 8B). However, the mean elongation rate of the class
II veins followed closely the tip-to-base gradient of growth
rates along the mid-vein ( Fig. 8B) and the relative growth
rate of a side vein was identical to the one of the adjacent
mid-vein segments (Fig. 9).
The growth rate of the leaf area enclosed by a midvein segment and the adjacent side vein was calculated
and plotted versus the distance of this area from the leaf
tip ( Fig. 10). With increase in leaf size, the tip-to-base
gradient of growth rates flattens significantly in parallel
to the decline in the overall growth rate of the leaf. By
analogy to the observation on the level of total leaf area
approximately 1/3 of the leaf area grew faster and 2/3
grew slower than the average.
Discussion
The allocation of biomass in tobacco plants to leaves,
root and stem, when subjected to growth-adjusted nutrient supply, followed distinct patterns independent from
the total growth rate. This fact indicates that the plants,
Fig. 7. Biomass allocation to leaves, stem and roots as a percentage of
the total biomass for Nicotiana tabacum plants grown at high, medium
and low nutrient addition rate in relation to plant size. Leaves are
further separated in leaves growing faster and slower than the total leaf
area of the plant. Dark shaded areas indicate biomass-source, while
light areas indicate biomass sinks.
given enough time for adaptation, adjust their biomass
allocation to meet certain set points. The patterns confirm
results in hydroponically grown tobacco ( Wakhloo and
Ruppenthjal, 1990). The evolving patterns are likely to
be linked to the functional optimum of the plant under a
given set of conditions. The fact that the ratio between
the leaf biomass and the biomass of the non-assimilating
parts of the plant was constant, while the root-to-shoot
ratio changed with plant size, has important consequences. First, the often observed alterations in rootto-shoot ratio in response to nutrient conditions may at
least in some cases be linked to plant size effects rather
than to specific responses to different nutrient availability.
Second, sink tissues compete directly and in response to
the overall architecture of the plant. The increased partitioning towards the stem is likely to be due to increased
demand for biomass in stems for statical reasons (Niklas,
1992) with increasing plant height.
The constancy of the allocation patterns was not only
observed on the whole plant level, but also within the
total leaf area and within single leaves. In both cases 1/3
of the leaf area was growing faster and 2/3 grew slower
than average, an apparently inherent property of the
tobacco variety used. As the specific leaf weights (on a
fresh and dry weight basis) were identical for the different
nutrient supply rates, the relations were not only due to
leaf area. Specific leaf weight remained constant after
leaves/leaf parts had finished expansion growth, in agreement with the finding that tobacco leaves do not thicken
after the end of the longitudinal expansion (Avery, 1933;
Dose, 1914). This is in contrast to monocot leaves that
increase leaf weight and thickness significantly during
post-elongation differentiation (Groeneveld et al., 1998).
Thus variation of nutrient supply in the Ingestad sense
does accelerate/decelerate the speed of plant development,
but the overall plant architecture remains constant. This
closely resembles findings on the leaf level in castor bean
where removal of the nitrogen supply accelerated leaf
maturation in those parts of the total leaf area with active
cell division activity (Roggatz et al., 1999).
In the reported experiments total leaf area increased
(a) by an increase in the final leaf area of the leaves and
(b) by an increase in the number of leaves contributing
to leaf growth. Growth distribution along the stem of
tobacco can be described as an acropetally moving wave,
which flattens and broadens with increasing plant size.
Leaves at lower positions are released from the shoot
apical meristem earlier than leaves of higher positions.
Thus leaves of different positions show a temporal shift
in their development processes and courses of growth
rates relative to each other. This is in contrast to monocot
species, in which only a few leaves contribute to the
increase in total leaf area at any one time (Groeneveld et
al., 1998). Leaf initiation gains a crucial role in adjusting
the growth rate to the nutrient supply under these steady-
Modular growth in tobacco 1175
Fig. 8. Distribution of relative growth rates of mid-vein segments (A) and side vein segments (B) on leaf 10 of Nicotiana tabacum for a single leaf
during a discrete day.
state conditions by determining the speed of initiation of
new modules, while the duration of cell division determines the end size of the leaves (Roggatz et al., 1999).
Distribution of the leaf growth
Leaf growth and differentiation proceeds as a basipetally
moving wave (Maksymowych, 1973; Van Volkenburgh,
1987; Granier and Tardieu, 1998). The apical parts of the
leaf are released from the shoot axial meristem some days
earlier than the basal parts of the leaf (Poethig, 1997).
This time-lag corresponds to the temporal shift in differentiation processes of the leaf blade (Avery, 1933; Poethig
and Sussex, 1985; A Walter, U Schurr, unpublished
results) causing gradients of growth rate along the midrib.
To quantify the impact of environmental or internal
(genetic) constraints on leaf development, a suitable
reference system has to be defined. From these results it
is proposed that the veinal system of the leaf is a proper
natural co-ordinate system for leaf growth. Hejnowicz
and colleagues (Hejnowicz and Hejnowicz, 1991;
Hejnowicz and Karczewski, 1993) have already proved,
for growing root tips, that the natural co-ordinate system
of the cell files is superior to a rectangular basis for
quantitative analysis. Clonal analysis of the origin of cells
on tobacco leaves indicate that cell files that originated
from a single mother cell, lie parallel to class II veins
(Poethig and Sussex, 1985). Within this co-ordinate
system, growth processes can be quantified more clearly
than in a rectangular co-ordinate system since they are
isotropic in this co-ordinate system. The reason for the
advantage of the natural over the artificial system is that
leaves do not grow in perpendicular x ( length) and y
(width) direction, but along their veins. The use of the
artifical rectangular grid has led to the conclusion that
1176 Walter and Schurr
as the veins are the transport routes for growth substrates
and areal expansion not balanced by vein expansion will
cause buckling of interveinal areas rather than increase
in projected leaf area.
Growth analysis as a framework
Fig. 9. Relationship between the relative growth rate of the mid-vein
and its basipetally adjacent side vein segment in leaf 10 of Nicotiana
tabacum.
The conserved growth patterns can practically be used as
a framework for analysis of growing plants, as, first, they
provide the functional background, to which a certain
cellular, physiological, biochemical, and molecular process is related. The steady-state nutrition thereby provides
the basis for sensible analysis because the structure of the
plant can be expected to be actually related to internal
functions. Therefore, apparent changes in the growth
patterns, e.g. in transgenic plants, indicate significant
interference of treatments with sink–source relationships.
Second, the stability of the patterns can be used to test
developmental versus specific responses to environmental
or genetic impact. Repetitive growth patterns, like the
Leaf Plastochron Index (LPI ), are the basis for developmental indices (Silk and Erikson, 1979). However, the
application of LPI is risky in leaf canopies, as in tobacco,
with apparent differences in the final size of the leaves,
as the LPI is based on the time when a leaf reaches a
certain absolute size. As this leaf size is chosen arbitrarily,
it can correspond to very different stages of leaf differentiation in leaves reaching different final leaf size.
Normalization will provide a more general approach to
developmental indices than the classical LPI ( U Schurr,
unpublished results).
Acknowledgements
The authors thank Uwe Roggatz for valuable discussion and
help during the experiments. The work was funded by the
Deutsche Forschungsgemeinschaft (DFG) in SFB 199 ( TP C1).
Fig. 10. Distribution of the relative growth rate of mid-vein segments
over a period of 13 d on leaf 10 of Nicotiana tabacum. The thick line
indicates the site of the leaf, which showed the same growth rate as the
entire leaf.
tobacco leaf growth would be anisotropical (Avery, 1933).
The reason for this conclusion is solely the application of
an unadapted co-ordinate system that has nothing to do
with the physiology of growth. This approach is still
widely used (Granier and Tardieu, 1998), but recent
developments of image analysis techniques based on
natural landmarks (Schmundt et al., 1998) have the
potential to substitute them. The 151 correlation of
growth rates of midrib segments and adjacent class II
veins may prove to ease analysis and modelling of dicot
leaf growth considerably, when based on vein branching
and growth of veinal segments. Besides these technical
reasons the veinal system is a natural reference for growth
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