Tree Physiology 19, 933--942
© 1999 Heron Publishing----Victoria, Canada
Growth adaptation of leaves and internodes of poplar to irradiance,
day length and temperature
G. A. PIETERS, M. E. VAN DEN NOORT and J. A. VAN NIJKERKEN
Department of Plant Physiology, Agricultural University of Wageningen, Wageningen, The Netherlands
Received November 13, 1998
Summary The adaptation of absolute growth rate of leaves
and internodes of Populus euramericana (Dode) Guinier cv.
‘Robusta’ to irradiance and day length proceeds by increases
in the volume of the apex. Diameter and height of the apex
increase linearly with time, resulting in linear increases in rates
of leaf initiation and stem height growth that can be described
by an acceleration factor. The acceleration factor is proportional to day length. The relationship between the acceleration
factor and irradiance is curvilinear and saturates at irradiances
above about 300 W m −2. Absolute stem height growth rate is
the product of mean relative growth rate in stem height and the
length of the growing part of the stem. The temperature-dependent growth pattern of each individual leaf or internode reflects
a specific relationship between its relative growth rate and
organ age that is independent of irradiance and plant age;
however, it is dependent on day length during the primordial
phase. The constancy of the growth patterns and the correlation
between leaf length and leaf initiation rate indicate that growth
of primordia is predetermined in the apex, presumably by the
precisely structured vascular system.
Keywords: acceleration factors, apex, height growth, internode extension, leaf growth, Populus euramericana ‘Robusta’,
vascular system.
Introduction
Poplar is an ideal model growth system because of its large
genetic variation and the ease with which it can be propagated
vegetatively. If cuttings are taken in summer and grown under
optimal nutrient conditions, only irradiance and temperature
determine their rate of development. In the macroscopic phase
of growth in such plants, relative growth rates of leaf length
and internode length at half-mature length (RGR50 = 0.15 and
0.22 day −1, respectively; see Appendix for symbol definitions)
are nearly independent of irradiance and plant height (Pieters
1974, 1986). Thus, although plants grow much faster at high
than at low irradiance, mean RGRs of leaves and internodes are
almost constant. The slight dependence of RGR on irradiance
is the result of temperature increases associated with high
irradiances (Pieters 1974, 1975). Similarly, in Populus tremuloides Michx. plants growing in open-top chambers, the relative growth rates at half-mature length, RGR 50 , of leaves
(0.15 day −1) and stem height (0.26 day −1) were dependent on
temperature but not on irradiance (Pieters 1996).
At constant temperature, relative growth rate of the length
(L) of an individual leaf (RGRleaf) or internode (RGRinternode ),
defined as dL/(Ldt), seems to follow an organ-specific pattern
with organ age, irrespective of final length of the organ (Pieters
1974, 1986). Because RGR is a measure of the mean absolute
growth rate of unit cell length, it is an important physiological
property of growing cells. Furthermore, because leaf length is
correlated with both leaf width and leaf area (Pieters 1974,
1983, 1984, 1986), the growth of a leaf can be described by the
growth pattern of leaf length. Differences in the full-grown
length and absolute growth rates among leaves can, thus, be
explained by differences in the mass of cells supplied by the
apex to the primordia.
In many plants, plots of the lengths of successive growing
leaves against leaf number (plastochron) yield (descending)
slopes (∆L/∆N) that remain constant at successive measurement times. The constancy of this slope implies that the difference in lengths of successive leaves at about half of their
mature length (∆L) is constant, irrespective of mature leaf
length (Lm) (Pieters 1974). This difference in length can be
calculated as: ∆L = 0.5Lm(RGR50)P, where P is plastochron
duration. Because ∆L and RGR50 are constant, Lm /(1/P) must
be constant; i.e., mature leaf length is coupled to leaf initiation
rate (1/P). The finding that leaf length and leaf initiation rate
are correlated is consistent with the observation of a precisely
regulated pattern of anatomical development in the apical
vascular system, as described by Larson (1975, 1977, 1980).
The growing part of the stem, GS, is defined as the axis
above an internode (GSi) or leaf (GSL) that just reached its final
length. The basal diameter of GSL is correlated with final leaf
length (Pieters 1974, Pieters and van den Noort 1988). A
similar situation is found for stem elongation. The length of the
growing part of the stem (GSi) is directly related to the rate of
stem elongation growth (Pieters and van den Noort 1988),
indicating that absolute growth rate is determined by the mass
of contributing cells, whereas mean RGR of those cells
(0.25 day −1) remains unchanged. Neither irradiance nor photosynthesis influences the absolute growth rate of cells. The
mean internode length (Lint) can be calculated as: Lint =
(GSi)(RGR internode )P. Because GSi and 1/P are linearly correlated, mean length of an internode is constant, irrespective of
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PIETERS, VAN DEN NOORT AND VAN NIJKERKEN
leaf length. This phenomenon has been observed in many other
plants.
Adaptation of absolute growth to irradiance proceeds by
way of the apex. Because leaves and internodes of poplar grow
according to a predetermined pattern, the increasing size of the
apex is reflected in the size of GS. Because length and diameter
of GS increase linearly with time, final leaf length (Lm) and leaf
initiation rate also increase linearly with time (Pieters 1986).
If it is possible to determine accurately the rate of growth of
GS, it is also possible to predict the moments of initiation of
successive leaves and their final lengths. If we then measure
the lengths of successive primordia in an apex, we can calculate the age of each primordium in relation to the leaf that has
just reached its final length. Correcting the measured length of
each primordium for the increase in GS, together with the age
data, give the leaf length--leaf age curve throughout the growth
of the leaf from initiation to maturation. The relative growth
curve of a leaf at a given irradiance can then be calculated from
this curve. Because plant temperatures increase with increasing irradiance, these relative growth curves should be corrected
for the temperature increase. Neither the difference in length
of successive leaves (∆L) nor the final length of successive
leaves (Lm), nor the final lengths of the internodes, is changed
by temperature (Pieters 1974). This indicates that temperature
only changes the time scale of the growth process; i.e., it
increases leaf initiation rate and mean RGR of leaf and internode growth, and decreases the duration of growth of the
individual organs proportionally.
We have used published data to examine the effects of
irradiance, day length and temperature on the rate and duration
of growth of the growing part of the stem (GS) of euramericana
poplar (Populus euramericana (Dode) Guinier). Specifically,
we studied apex-mediated effects of irradiance on poplar leaf
and stem growth on the basis of initial growth parameters and
a single irradiance-dependent variable. We also constructed
relative growth curves of leaves to evaluate the hypothesis that
irradiance does not influence the form of these growth curves.
Model development
ments. At t = 0, the rate of leaf production is aNtN and the
number of leaves is 0.5aNtN2. These relationships are also valid
for stem height, where the constants aN and tN are replaced by
aH and tH.
Materials and methods
Experiments and plant numbers
The experiments reported in this paper are listed in Table 1.
Each plant has a code. The first digits indicate the experiment
number, the following character indicates the plant material,
the digit after this indicates irradiance and the last digit indicates the plant. The code 13R33 means: Experiment 13 with
Populus euramericana cv. ‘Robusta’, lowest irradiance (in this
experiment 15 W m −2), plant number 3.
During measurements on plants in Experiment 11R, we
discovered that the wrong plant material had been taken. This
undefined poplar clone is called Clone 2.
Growth room
All experiments, except where noted otherwise, were done in
a 6 × 4.68 × 2 m growth room of the phytotron of the Laboratory of Plant Physiological Research, Wageningen, the Netherlands. Irradiance in the growth room was regulated by lamp
type, the number of lamps, and by moving vertical screens in
the horizontal direction. The plants were irradiated from two
sides and from above to ensure uniform irradiance with 7.5, 15,
30 and 60 W m −2 of photosynthetically active radiation (PAR;
32.5, 65, 130 and 260 µmol m −2 at 400--700 nm). Irradiances
of 7.5 and 15 W m −2 were provided by Philips TLM(F)-33
65-W fluorescent tubes, and irradiances of 30 and 60 W m −2
were provided by 140-W fluorescent tubes of the same lamp
type. The photoperiod was 16 h. Room temperature was maintained at 22 ± 0.5 °C and relative humidity was kept between
40 and 60%. For further details see Pieters (1974, 1975).
Experiment 15R was done in a growth room of the Department of Plant Physiology. The climate conditions were similar
to those of the phytotron growth room, except that irradiance
was only from above and temperature was 19.5 °C. Maximum
A linear increase in the basal diameter of GSL is accompanied
by a linear increase in leaf initiation rate (dN/dt), thus:
dN/dt = aN(tN + t) ,
(1)
where N = the number of a specific leaf, counting acropetally,
aN = leaf acceleration factor (day −2), tN = a constant (days), and
t = time (days).
For each initiated leaf, plant age t is increased by the duration of one plastochron. The relationship between total number
of leaves and time is:
N(t) = 0.5aN (tN + t)2 ,
(2)
The constant tN describes the developmental stage of the
apex with respect to leaf production at the start of the measure-
Table 1. Summary of experiments discussed in this paper. Details
provided include experiment number and year, irradiances used, day
length, and the number of plants per treatment.
Experiment no. Year
Irradiance
(W m −2)
Photoperiod No. of plants
(h)
1R
5R
9R
10R
11R1
13R
15R2
7.5, 15, 30
7.5, 15, 30
7.5, 15, 30, 60
30, 60
7.5, 15, 30, 60
15, 30, 60
60
16
16
16
16
16
24
16
1981
1985
1992
1992
1993
1993
1994
1 Unknown clone designated Clone 2.
2 No lateral illumination.
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4
3
3
3
3
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GROWTH ADAPTATION TO ENVIRONMENTAL CONDITIONS
irradiance was about 80 W m −2 supplied by high-frequency
58-W fluorescent tubes (Philips, TLD-50W/HF, color 33).
Plant cultivation
Populus euramericana cv. ‘Robusta’ cuttings were cultivated
in gravel culture in rectangular polyethylene containers (250 ×
250 × 300 mm). The plants were subirrigated every 30 min
with 50% Hoagland A-Z solution, modified after Steiner
(1968). To prevent nitrate deficiency, this concentration was
increased to 100% for plants growing at 60 W m −2 with a 16-h
photoperiod, and to 150% for plants growing at 60 W m −2 with
a 24-h photoperiod. One shoot was allowed to grow on each
plant. At the end of the experiment, each shoot consisted of
about 50--60 mature leaves, nodes and internodes.
For Experiment 15R, in which irradiance was from above
only, the tops of the growing plants were maintained about
10 cm under the light ceiling to ensure an irradiance of about
60 W m −2 at the plant tops.
Measurements
Lengths of successive leaves and internodes (+ node) were
measured to the nearest 0.5 mm. Stem diameters at the middle
of successive internodes (mid-internode diameter) were measured to the nearest 0.1 mm with calipers held parallel with the
base of the attached leaf. Plant height was measured directly
or calculated by summing the lengths of internodes (+ nodes).
Measurements were made three times a week. Plant age is the
number of days after the start of the measurements.
Data evaluation
Several secondary growth parameters were calculated from the
original data. Because the time of the end of leaf growth is
difficult to determine, we calculated the moment when each
leaf and internode reached 90% of its final length, by linear
interpolation between the two closest measurement points.
The acceleration factors aN and aH and the constants tN and
tH were determined by fitting leaf number (N) to the calculated
time of reaching 90% of mature leaf length (t), or successive
heights (H) to t with Equation 2.
Relationship between RGRleaf and leaf age
The acceleration factor was used to calculate the growth pattern of individual primordia and leaves, on the basis of continuous measurements of the visible leaves and destructive
measurements of primordia length at the end of the experiment. The time at which a leaf N reaches 90% of its final length
was calculated with Equation 2. The age of leaf N + n (n places
above leaf N) was then calculated by subtraction of the calculated times. However, because of the increase in apical size, the
length of leaf N + n is greater than the length of leaf N at the
same age. Because leaf production rate at time t (Equation 1)
and final leaf length are correlated, the length of leaf N + n was
corrected by dividing it by the ratio of the initiation rates of
leaves N and N + n. In this way, a standardized pattern of leaf
development was established through the relationship between
RGR and leaf age. To minimize variability, successively calculated RGRs were averaged.
935
Effect of temperature on growth pattern
Plant temperature was more than 2 °C higher at an irradiance
of 30 than at 7.5 W m −2 (Pieters, 1975); the temperature
difference between plants in 30 W m −2 and plants in the dark
was about 2.5 °C. A correction for the temperature increase
caused by high irradiances was calculated from the relationship between RGR of leaves at half of mature length (RGR50)
and temperature (Pieters 1974):
RGR 50 = 0.242 − 0.717 exp −T/10.577 ,
(3)
where T = temperature (°C).
The temperature-induced increase in RGR50 causes a proportional decrease in growth duration, because neither the
full-grown length of successive leaves, nor the difference in
length of two successive leaves about half-final length, nor
internode length, is changed by temperature (Pieters 1974).
This means that, in each individual leaf, the temperature-induced increase in RGR is compensated for by a decrease in the
duration of growth. If it is assumed that the relative effect of a
temperature change is similar for all growth processes, the
relative effect of a temperature change on RGR50 and other
temperature-dependent processes can be calculated with Equation 3. To account for the difference in the duration of irradiance (16-h versus 24-h photoperiod) the relative effect (e) of
temperature was approximated as:
e = 24eL / (16eL + 8eD) ,
(4)
where eL and eD express the relative temperature effect in light
and darkness.
Estimation of internode length
The model used to estimate internode length was based on
stem height growth and leaf initiation. Height growth is the
product of the length of GSi and mean RGRinternode. Because of
periodic leaf initiation, the length of the stem is divided into
internodes. When the developmental stages of the apex for leaf
production and for height growth are in steady state, the length
of an internode is the ratio between the rates of height growth
and leaf production. At the start of growth of a plant, however,
neither process is at steady state. Under such conditions, the
final length of internode N is determined as follows: the time
at which leaf N reaches 90% of full-grown length can be
calculated with Equation 2 plus the acceleration factor aN and
the constant tN of that particular plant. The corresponding
internode N reaches 90% of its final length 6.5 days earlier than
under steady-state conditions (Pieters 1974). Stem height can
be calculated with Equation 2, plus the acceleration factor aH
and the constant tH of the same plant and the time internode N
reaches 90% of its final length. Rate of height growth at the
same moment can be calculated with Equation 1. Because
mean RGRstem corresponds with 25% of the length of the stem
undergoing extension growth (GSi), this length can be taken as
four times the rate of height growth (Pieters and van den Noort
1988). Subtracting the length of GSi from calculated total plant
height gives the length of the full-grown part of the stem at the
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936
PIETERS, VAN DEN NOORT AND VAN NIJKERKEN
end of elongation growth by internode N. The difference between this stem length and the length of the full-grown stem at
the end of extension growth of internode N − 1, yields the
full-grown length of internode N.
Destructive measurements of primordial length and
primordial stem diameter
At harvest, the shoot apex was excised. To prevent drying, it
was inserted in an elastic, water filled polyethylene tube that
fitted the stem tightly. The length of a primordium and the
diameter of the internode were measured with the aid of a
binocular stereo-microscope. After measurement, the primordium was carefully removed to get access to the next one. The
smallest measured primordium was about 50 µm in length.
Leaf weight per unit area
At the end of the experiment, the areas of all leaves were
measured with a video camera area meter (Pieters 1984). The
weight per area ratio of each leaf (WAR) was determined by
dividing the fresh weight of each leaf (without petiole) by its
area.
Results and discussion
Leaf initiation and leaf growth
Figure 1A shows the time course of leaf number (N) for three
plants, grown at three irradiances. The leaf data fit Equation 2
with high correlation coefficients (r 2). Because absolute rate of
leaf initiation differed among plants of the same age grown at
different irradiances, our hypothesis that irradiance primarily
affects the rate of increase of the growing part of the stem (GS)
(aNt) was fully corroborated. Figure 1B shows that the data on
plant height also fit Equation 2 well.
Aadaptation of plant growth to irradiance or day length can
be described with a limited number of parameters. Thus, tN and
tH define the developmental stage of the apex of the plant at the
start of the experiment, and the acceleration factors aN and aH
define its developmental rate. The acceleration factor aN was
linearly related to the weight area ratio (WAR) of the leaves
(Figure 2), suggesting that aN and WAR have a similar physiological basis.
Dependence of the acceleration factor aN on irradiance and
clone
The acceleration factor aN was also related to growth irradiance. Figure 3A shows this relationship for Robusta plants and
for Clone 2 grown at different irradiances and day lengths. In
all cases, the relationship between aN and irradiance was curvilinear. The increase in aN was nearly proportional to day
length, indicating that the plants were growing optimally with
no limitations in the root environment.
Experiment 1R produced a different relationship between aN
and irradiance as a result of root constrictions. In this experiment, we reused stubs from a preceding experiment. Consequently, the root system had already filled the pot and new root
growth was pressed against the walls of the pot. This limited
Figure 1. (A) Examples of measured and simulated production of
leaves at 90% of final length versus plant age for individual plants
grown at 7.5, 15 or 30 W m −2 in a 16-h photoperiod. Simulated leaf
production versus plant age t, N(t), was calculated according to Equation 2: N(t) = 0.5aN(tN + t)2 in which aN is the acceleration factor for
leaf production and tN a time factor, indicating the developmental state
of the plant at the start of the experiment. (B) Examples of measured
and simulated growth in stem height versus plant age for individual
plants grown at 7.5, 15 or 30 W m −2 in a 16-h photoperiod. Simulated
height growth versus plant age t, H(t), was calculated according to
Equation 2: H(t) = 0.5aH(tH + t)2 in which aH is the acceleration factor
and tH a time factor, indicating the developmental state of the plant at
the start of the experiment.
growth of the plant because uptake of water or ions was
impeded. The only plant that was growing vigorously in Experiment 1R was a new cutting that was included as a replacement for a dead cutting. Note that the acceleration factor of the
new cutting (filled circle, in the middle curve in Figure 3A) lies
in line with those for other plants in the same photoperiod.
Subsequently, fresh plant material was always used for each
experiment.
The response of aN to irradiance differed for Clone 2, indicating that the relationship between aN and irradiance is also
determined by genetic properties of the plant, because there
were no limitations in the root environment during experiment
11R.
A plot of the acceleration factor against total daily irradiance
(Figure 3B) indicated that the effect of day length can be
ascribed largely to the increase in the total daily energy supply.
The temperature-corrected relationship between aN and irradiance is also shown in Figure 3B.
TREE PHYSIOLOGY VOLUME 19, 1999
GROWTH ADAPTATION TO ENVIRONMENTAL CONDITIONS
937
loides, Pieters 1996), the acceleration factors were negligibly
affected by a doubling of the atmospheric CO2 concentration.
This finding provides further circumstantial evidence that photosynthesis does not directly control the growth rate of GS
(or the apex); however, there is considerable variation in the
growth responses of different tree species to elevated CO2
(Ceulemans et al. 1992, 1995, 1996). Furthermore, elevated
CO2 influences not only photosynthesis, but also transpiration,
and may have other direct or indirect effects on plant functioning (Jarvis 1989). Thus, it is not clear whether photosynthates
or hormones direct the growth of GS. A detailed knowledge of
the energy balances in the GS and apex may help elucidate
whether photosynthates or hormones direct their growth.
Figure 2. Linear relationship between the acceleration factor for leaf
initiation (aN) and leaf weight area ratio (WAR) for poplar plants
grown at irradiances of 7.5, 15 or 30 W m −2 in a 16-h photoperiod and
15, 30 or 60 W m −2 in a 24-h photoperiod.
The curvilinear relationship between aN and irradiance (Figures 3A and 3B) supports the idea that the response of aN to
irradiance is determined by the photosynthetic production of
assimilates. Light saturation occurs at about 300 W m −2 and
lies between the light saturation of an individual leaf and a
canopy (Monteith 1965, Ceulemans 1990, Ceulemans and
Saugier 1990). The value of aN is not a direct measure of the
absolute growth response of the plant. Although a larger aN
leads to a faster increase in apical size, there will be a delay
before the increase in aN causes a substantial increase in
absolute growth rate. Based on the study of Doorenstouter et
al. (1985), we conclude that the linear relationship between the
acceleration factor and weight area ratio of the leaves (WAR in
Figure 2) is unlikely to be a result of a direct relationship
between photosynthesis and the growth of the apex. Doorenstouter et al. (1985) found that chlorotic, Mg-deficient leaves
grown at 7.5 or 30 W m −2 had similar WAR as Mg-sufficient
leaves, indicating that WAR is determined by irradiance, not
by photosynthesis. However, the relation between aN and WAR
depends strongly on temperature (at higher temperature aN
increases and WAR decreases), shifting to the left with higher
temperature; indicating that the relationship between aN and
WAR is indirect. In an experiment with aspen (Populus tremu-
Relationship between the acceleration factors for leaf
initiation and stem elongation
The relationship between the acceleration factors for leaf initiation rate and height growth is approximately linear: aN =
−0.0026 + 0.352aH, with a correlation coefficient of 0.88.
Thus, there is some independence between the factors aN and
aH, which differ by a factor of three. This difference arises
because they have different dimensions (aN has the dimension
leaves × day −2, whereas aH has the dimension cm × day −2)
reflecting that each leaf produced corresponds to an increase
in stem length (internode length) of about 3 cm.
The relationship between tN and tH is less clear than that
between aN and aH. The values of tN and tH are mainly determined by leaf number and stem height at the start of the
experiment. The variable tN/tH ratio indicates that, at the beginning of the experiment, there exists some variability in the
developmental stage of the apex with respect to leaf initiation
(the diameter of the apex) and to the rate of stem extension
growth (the height of the apex).
Independence of the acceleration factor aN from plant age
and plant size
A doubling of the length of a newly-matured leaf (Lm) roughly
corresponds to an eightfold increase in leaf area production per
day (Pieters 1974). Also, the total area of growing leaves is
correlated with Lm3 (Pieters 1974). The ratio of rate of leaf area
production per day and area of growing leaves present along
the stem is approximately constant; i.e., at a constant, all-sided
irradiance, the ratio between use and production of assimilates
for leaf area production remains approximately constant. This
Figure 3. (A) Relationship between acceleration factor for leaf
initiation (aN) and irradiance in a
16-h or 24-h photoperiod. (B) Relationship between acceleration
factor for leaf production (aN) and
the total daily irradiance both corrected and uncorrected for temperature for Experiments 9R, 10R
and 13R. The temperature-corrected values of aN are fitted to a
photosynthesis curve with a correlation coefficient of r 2 = 0.94.
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PIETERS, VAN DEN NOORT AND VAN NIJKERKEN
may explain why the acceleration factors aN and aH are independent of plant age and, consequently, of plant size and the
ever increasing leaf area. The growing shoot seems to be
self-sufficient for assimilates. It is known that older leaves do
not contribute substantially to the assimilates needed in shoot
development in other plant species (Milthorpe and Moorby
1974). In poplar, the shift from acropetal to basipetal transport
of assimilates occurs just before the leaf reaches its full length
(Larson 1969); however, this observation contrasts with the
report that photosynthesis of mature leaves contributes to the
development of poplar plants (Ceulemans et al. 1995).
Based on an experiment with an irradiance of 60 W m −2 from
above only, we calculated a temperature-corrected leaf acceleration factor of aN = 0.016 day −2, which is comparable with a
three-sided, uniform irradiance of about 45 W m −2. Because
length of the growing part of the shoot (GS) increases from
about 5 to 24.0 cm, the average irradiance received by the GS
declines with time. Although we do not know how to calculate
the average irradiance in this changing light climate, some
indication about effective irradiance can be found in the WAR
of successive leaves on plants. On plants grown with lateral
irradiance, we observed a remarkable constancy of WAR. In
contrast, on plants grown with irradiance from above only,
WAR declined from 0.03 to 0.025 g cm −2 during the experiment, suggesting that, by the end of the experiment, the effective irradiance had dropped from 60 to below 30 W m −2. This
means that the acceleration factor declines with increasing
plant size and that, in this situation, aN is not correctly defined
by Equations 1 and 2. These results also demonstrate the
importance of using a uniform irradiance for growth analysis
studies.
Growth patterns
Temperature-corrected growth patterns for leaves of three
plants grown at 30 W m −2 in a 16-h photoperiod are shown in
Figure 4A. Average growth patterns for plants grown at 7.5 and
30 W m −2 in a 16-h photoperiod, and at 15, 30 and 60 W m −2
in a 24-h photoperiod are shown in Figure 4B; each graph
comprises data for three or four plants. The temperature-corrected growth patterns of plants in the 16-h photoperiod are
similar, whereas those of plants in the 24-h photoperiod show
some variability in the primordial phase of growth, although
no systematic effect of irradiance was evident. Based on the
macroscopic phase of growth, we calculated the duration of
leaf growth in a 16-h photoperiod as 32 days (Pieters 1986),
excluding the primordial phase. The durations of growth before and after temperature correction are given in Table 2.
Compared with the RGR in a 16-h photoperiod, a 24-h photoperiod increases the RGR of the primordium in the early phase
of growth, but at the same time decreases the duration of
growth. These changes in RGR and growth duration probably
compensate each other, because the difference in lengths of
successive leaves remained similar (∆L, Table 3) in both photoperiods. This finding also implies that photosynthesis does
not affect final leaf length or internode length in plants grown
in a 24-h photoperiod. The increase in RGR with increasing
photoperiod is consistent with the absence of an effect of
Figure 4. (A) The fixed growth patterns of leaves on four plants grown
in a 16-h photoperiod at 30 W m −2. The growth patterns were calculated on the basis of the acceleration factor and the measured lengths
of successive primordia and corrected for a temperature of 22 °C. The
RGR for leaf length is fitted to leaf age with a polynomial equation.
One standard deviation is indicated by a bar. (B) The averaged, fixed
growth patterns of leaves on plants grown in a 16-h photoperiod at
irradiances of 7.5 or 30 W m −2 (n = 4) or in a 24-h photoperiod at
irradiances of 15, 30 or 60 W m −2 (n = 3). The growth patterns were
corrected for a temperature of 22 °C. The standard deviation is indicated for each curve.
irradiance, because the ratio of the rate of leaf area production
per day and the area of growing leaves present along the stem
remained constant, but carbohydrate production per day increased. It is not known why day length increased RGR in the
primordial phase of leaf growth but irradiance did not.
The constancy of the growth patterns indicates that final leaf
length depends on the length of the initiated primordium, but
is independent of irradiance or temperature; i.e., extension and
division growth are determinate in poplar. Because primordia
of similar length are not necessarily at a similar developmental
stage, the plastochron index conceived by Erickson and
Michelini (1957) does not adequately define the developmental stage of leaves and internodes of poplar. The length of the
primordium is already determined before initiation in the apical system, suggesting that the developing vascular system
plays an important role in this determination.
The constancy of the growth patterns in the various irradiances also indicates that pruning of axillary buds has no effect
on growth of the growing part of the shoot (GS). In a 16-h
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Table 2. Calculated mean duration of leaf growth before and after
temperature correction for four plants grown at 7.5 or 30 W m −2 in a
16-h photoperiod and for three plants grown at 15, 30 or 60 W m −2 in
a 24-h photoperiod.
Day length
Irradiance
(W m −2)
Duration
before
correction
(days)
Duration
after
correction
(days)
(h)
16
16
24
24
24
7.5
30
15
30
60
33.5 ± 0.3
31.0 ± 1.1
27.4 ± 0.7
23.5 ± 0.2
21.6 ± 0.6
35.9 ± 0.1
35.9 ± 0.7
31.2 ± 0.0
31.4 ± 0.0
31.5 ± 0.0
Table 3. Mean values for the difference in length of successive growing
leaves at about half mature length (∆L; cm), their standard error (SE)
and the number of measurements (n) for Experiments 9R (16-h photoperiod), 10R (16-h photoperiod), and 13R (24-h photoperiod).
Irradiance Experiment
(W m −2)
7.5
15
30
60
9R (16 h)
10R (16 h)
13R (24 h)
∆L
SE
n
∆L
SE
n
∆L
SE
n
2.06
2.25
2.10
−
0.23
0.28
0.30
−
51
44
6
−
−
−
1.83
1.92
−
−
0.11
0.22
−
−
29
52
−
2.29
2.43
2.30
−
0.51
0.40
0.37
−
41
37
33
photoperiod, no buds started growth at irradiances lower than
30 W m −2 and the acceleration factors were correlated with
WAR, which in itself is independent of side branches.
Mature leaf length (Lm) and leaf initiation rate
The acceleration factor can be used to estimate rate of leaf
production of a plant at the moment of maturation of a leaf.
Calculated leaf production rate, corrected for temperature, is
plotted against Lm in Figure 5. The correlation coefficient for
the relationship between Lm and leaf initiation rate is 0.99.
Only at the start of cutting growth is Lm lower than the expected
value, probably because of imbalances between shoot and root
growth of the new cutting.
Internode formation
Internode formation is principally dependent on rates of stem
elongation and leaf initiation. The rate of height growth divided by the leaf production rate determines internode length,
which is usually about 30 mm.
At the start of cutting growth, short internodes are formed.
As in leaves, this is probably a result of an imbalance between
shoot and root growth. (The first internodes of a side branch,
growing on a vigorously growing main shoot, are normally
about 30 mm long.) Internode length gradually increases to a
more or less constant length (steady state). The lengths of the
successive internodes during this period of adaptation can be
calculated as the ratio of actual stem elongation to leaf initia-
Figure 5. Linear relationship between temperature-corrected leaf initiation rates (1/P) and full-grown leaf lengths (Lm). The leaf initiation
rate for leaf N is calculated from Equation 1: dN/dt = aN(tN + t), where
aN is the acceleration factor for leaf production, tN a time factor
indicating the developmental state of the plant at the start of the
experiment, and t is the time at which leaf N reached 90 % of its final
length. The calculated leaf initiation rates were corrected for a temperature of 22 °C.
tion rate (see Materials and methods). A comparison of such a
calculation with measured internode lengths is presented in
Figure 6A. There was agreement between the measured and
modeled data during the adaptation period; however, internode
lengths in the steady state were somewhat underestimated,
because calculated leaf production rate was accurate, but calculated height growth was lower than actual height growth.
This deviation occurred in all of the plants in this experiment.
Relationship between RGRinternode and internode age
We analyzed the relation between RGRinternode and internode
age (M) for the period where it could be measured nondestructively. We set RGRinternode at half of mature length to Day 20,
which was the mean date on which this occurred. Linear
relationships between RGRinternode and internode age are presented in Figure 6B, and the slope of the relationship and the
standard deviation of the mean are given in Table 4 for the
different irradiances. Values both corrected for temperature
and uncorrected for temperature are given. Values of M depended only slightly on irradiance.
Mean RGRstem of the growing stem part is 0.25 day −1 (Pieters
and van den Noort 1988). On the basis of this value, mean
RGR in the primordial phase was calculated as the maximum
RGRinternode . Values are listed in Table 4 and again show little
dependence on irradiance.
Primordium length, initiation rate and vascular system
development
The finding that leaf length and leaf initiation rate are correlated indicates that the apex of GS is precisely structured.
Remarkable parallels exist between the increasing size of the
growing part of the stem and the change in architecture of the
vascular system in the apex (Larson 1975, 1977 and 1980). The
number of vascular traces and the diameter of GS gradually
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940
PIETERS, VAN DEN NOORT AND VAN NIJKERKEN
Figure 6. (A) Comparison of
measured (●) and modeled ()
internode lengths. The first internodes are short, but successive internodes gradually increase in
length to between 20 and 30 mm.
The length of GSi (-- --) is plotted
against internode number as a
measure of plant age. Internode
length is underestimated in the period after adaptation, because the
actual rate of height growth was
greater than the calculated mean
rate. (B) Example of the fixed
growth pattern of all internodes of
one plant during the macroscopic
phase of growth (●).
Table 4. Estimated slope of the relationship between RGRinternode and internode age in the macroscopic phase (M) of all growing internodes (see
Figure 6B). The calculated maximum RGRinternode in the primordial phase and the duration of growth are also given. Values are means ± standard
error.
Irradiance (W m −2)
Slope uncorrected for temperature
Maximum RGR (day −1)
Growth duration (day)
Slope corrected for temperature
Maximum RGR (day −1)
Growth duration (day)
Total no. of observations
No. of internodes measured
No. of plants measured
7.5
15
30
−0.034 ± 0.003
0.304 ± 0.006
25.4 ± 0.14
−0.037 ± 0.002
0.297 ± 0.003
25.2 ± 0.18
−0.045 ± 0.005
0.288 ± 0.005
24.7 ± 0.31
0.033 ± 0.003
0.295 ± 0.006
24.6 ± 0.1
0.035 ± 0.002
0.279 ± 0.002
23.7 ± 0.2
0.040 ± 0.005
0.256 ± 0.004
21.9 ± 0.3
191
41
3
increase during the development of the plant. Also, the lengths
of the procambial traces increase proportionally, as well as the
length of GS. By increasing the number of traces from two to
thirteen, the phyllotactic order increases from 1/2, 1/3, 2/5, 3/8
to 5/13, as is also evident in in the enlarging GS. Because the
procambial traces develop acropetally long before the primordium that they will feed is initiated (Larson 1975), the change
in vascular architecture anticipates the change in GS. In poplar
clone Robusta, the time-span between the initiation of two
successive primordia on the same vessel (one orthostichy) was
about 13 days at 22 °C. If the number of traces is five, leaf
production is about one leaf per 13/5 = 2.8 days, if the number
of traces is 13 about one leaf per 13/13 = 1 day is produced by
GS. These estimates compare well with our observations on
leaf production and phyllotactic order (data not shown).
264
72
3
142
49
2
tions of time. Total leaf production is a cubic function of the
length of the youngest matured leaf. In contrast, total biomass
production of a shoot is not an exponential function of time and
shoot RGR is a physiologically meaningless parameter. Relative growth rate is a meaningful physiological parameter only
for the growth capacity of cells during primary extension
growth of leaves, internodes or roots. It cannot be used for
whole plants because the increasing proportion of plant mass
that does not participate in growth causes a continuous decline
in RGR, which is called ontogenetic drift (Lord et al. 1993). To
calculate absolute growth, it is necessary to know at least mean
RGR and the cell capital participating in growth (Lambers
1987). For a plant that can branch freely, the use of RGR may
have significance when related to the number of developing
buds over the years.
Relative growth rate
Growth of the apex, development of final leaf length and of rate
of leaf initiation or height growth proceed linearly with time.
Leaf production and height growth are both quadratic func-
Conclusions
Because leaves and internodes follow characteristic relative
growth patterns, constant gradients of RGRinternode and RGRleaf
TREE PHYSIOLOGY VOLUME 19, 1999
GROWTH ADAPTATION TO ENVIRONMENTAL CONDITIONS
exist along the growing part of the stem that are related to the
relative distance from the shoot apex. The developmental characteristics of the growing cells are coupled through their age to
a specific location on the GS. Our model for leaf and internode
growth is based exclusively on the age of each individual
organ. Growth response to irradiance occurs by simultaneous
increases in leaf length and leaf initiation rate, according to a
growth pattern predetermined in the apex.
Constant internode lengths, together with increasing leaf
lengths, are often observed in other plant species, indicating
that their growth is probably regulated by mechanisms similar
to those in poplar. Future research should concentrate on how
physiological cell age regulates organ development. We also
need to determine whether the architecture of the vascular
system plays a fundamental role in regulating cell numbers in
the shoot apex, leading to simultaneous increases in rates of
leaf elongation and initiation.
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Appendix
Symbol
Definition and units
aN
aH
dN/dt
∆L
e
eD
eL
GS
GSi
GSL
H
Lint
Lm
M
N
n
P
RGRx
RGR50
t
tH
tN
T
WAR
Acceleration factor for leaf initiation (proportional to the growth rate of apical diameter) in N day −2
Acceleration factor for height growth (proportional to the growth rate of apical length) in cm day −2
Leaf production rate in leaves day −1
Difference in length (cm) of two successive leaves at half final length
Relative temperature effect
Relative temperature effect in the dark
Relative temperature effect in the light
The growing part of the shoot
Part of the stem with growing internodes (cm)
Part of the stem with elongating leaves (cm)
Shoot height (cm)
Final internode length (cm)
Final leaf length (cm)
Slope of the relation between RGRinternode and internode age during macroscopic growth
Number of a leaf or internode, counting acropetally
Number of a leaf or internode, counted from the youngest mature leaf
Plastochron duration (days)
Relative growth rate of the indicated organ (dL/(Ldt)) (day −1)
Relative growth rate at half of final organ length (day −1)
Plant age (days)
Developmental stage of height growth or of apical height (days at the start of the experiment).
Developmental stage of leaf initiation or of apical diameter (days at the start of the experiment).
Temperature (°C)
Leaf weight to leaf area ratio (g cm −2)
TREE PHYSIOLOGY VOLUME 19, 1999