Journal of Experimental Botany, Vol. 55, No. 402, pp. 1549–1556, July 2004
DOI: 10.1093/jxb/erh169 Advance Access publication 4 June, 2004
RESEARCH PAPER
Hydraulic architecture of plants of Helianthus annuus
L. cv. Margot: evidence for plant segmentation in herbs
M. A. Lo Gullo1, L. Castro Noval2, S. Salleo3,* and A. Nardini3
1
Dipartimento di Scienze Botaniche, Università di Messina, Salita Sperone 31, 98166 Messina S. Agata, Italia
2
UD Anatomia y Fisiologia Vegetal, ETS Ingenieros de Montes (UPM), Ciudad Universitaria s/n, 28040 Madrid,
España
3
Dipartimento di Biologia, Università di Trieste, Via L. Giorgieri 10, 34127 Trieste, Italia
Received 9 March 2004; Accepted 7 April 2004
Abstract
The hydraulic architecture of sunflower (Helianthus
annuus L. cv. Margot) was studied in terms of the
partitioning of the hydraulic conductance (Kleaf) of
leaves inserted at progressively more apical nodes
both in growing plants (GP) and in plants at full
anthesis (mature plants, MP). Leaf conductance to
water vapour (gL), leaf water potential (WL), leaf water
potential at zero turgor (Wtlp), and leaf osmotic potential at full turgor (p0) were also measured. Sunflower
plants showed gL and Kleaf values significantly increasing in the acropetal direction, while WL of basal
leaves was significantly more negative than that of
distal leaves; Wtlp markedly decreased in the acropetal
direction in MP so that leaves of MP retained increasingly more turgor the more apical they were. This
hydraulic pattern, already present in very young plants
(GP), strongly favours apical leaves. These data suggest that the progressive leaf dieback starting from the
stem base, as observed when the inflorescence of
sunflower reached maturity, might be due to timedependent loss of hydraulic conductance. In fact, Kleaf
loss was correlated with WL drop and stomatal closure.
Leaf dehydration was aggravated by solute exportation
from the basal towards the apical leaves, as revealed
by the acropetal decrease of p0. Kleaf was shown to be
linearly and positively related to the prevailing ambient
irradiance during plant growth, thus suggesting that
leaf hydraulics is very sensitive to environmental conditions. It was concluded that the pronounced apical
dominance of some sunflower cultivars is determined,
among other factors, by plant hydraulic architecture.
Key words: Apical dominance, Helianthus annuus L., hydraulic
architecture, leaf hydraulics, senescence, sunflower.
Introduction
Almost a quarter of a century ago, Zimmermann (1978,
1983) first introduced the concept of ‘hydraulic architecture’ of plants. He intended, with this term, to outline the
physiological importance of the partitioning of the hydraulic conductances (K) in a plant. In this framework,
Zimmermann extensively discussed his idea of ‘plant
segmentation’ according to which hydraulic barriers would
exist between different parts of the plant body such as leaf
insertions and stem nodal regions (Larson and Isebrands,
1978; Salleo et al., 1982; Lo Gullo et al., 1995). These
relative hydraulic separations between organs would allow
plants to favour certain parts at the expense of others. Plant
segmentation was also proposed to act as ‘vulnerability
segmentation’ (Tyree et al., 1993; Tsuda and Tyree, 1997).
As an example, these authors found that leaf petioles of
walnut were consistently more prone to cavitation-induced
embolism than stems. As a consequence, leaves would drop
under excessive transpiration thus preventing the stem’s
embolization and saving older parts where larger amounts
of metabolic energy had been invested. Similar leaf versus
stem vulnerability to cavitation has been described (Salleo
et al., 2000, 2001). Even if Tyree and Alexander (1993)
have computed that the hydraulic bottlenecks at the stem
nodes would have little impact on the whole plant hydraulics, nodal regions have been shown to be more resistant to
embolism than internodes (Salleo and Lo Gullo, 1986) and
now it is generally agreed that the hydraulic barriers
* To whom correspondence should be addressed. Fax: +39 040 568855. E-mail: [email protected]
Journal of Experimental Botany, Vol. 55, No. 402, ª Society for Experimental Biology 2004; all rights reserved
1550 Lo Gullo et al.
existing at the leaf traces (Zimmermann and Sperry, 1983),
leaf petioles (Tyree et al., 1993), and leaf veins (Salleo
et al., 2001) may play a crucial role in the leaf vulnerability
to cavitation (Nardini et al., 2001; Salleo et al., 2001;
Brodribb and Holbrook, 2003b) and leaf senescence (Salleo
et al., 2002; Brodribb and Holbrook, 2003a).
The hydraulic resistance of the leaf (Rleaf =1/Kleaf) has
been reported to represent 60–80% of that of the shoot
(Yang and Tyree, 1994; Nardini and Tyree, 1999; Nardini
and Salleo, 2000). As a consequence, both spatial and
temporal variability in Rleaf can be expected to have a strong
impact on shoot water relations. In turn, leaf conductance to
water vapour (gL) has been reported to be a positive, linear
function of plant hydraulic conductance as scaled per unit
leaf surface area in Betula occidentalis (Saliendra et al.,
1995) and in Pinus ponderosa (Hubbard et al., 2001).
Environmental factors such as light and leaf temperature
have been shown to cause Kleaf to vary consistently in
some species depending on stomatal behaviour (Sack et al.,
2002) or on aquaporin new expression/activation (Morillon
and Chrispeels, 2001).
The hydraulics of different species and organs have been
measured extensively using several different techniques
including vacuum chamber (Kolb et al., 1996; Nardini
et al., 2001), high pressure flow meter (Tyree et al., 1995;
Nardini and Tyree, 1999), evaporative flux (Tsuda and
Tyree, 2000; Nardini et al., 2001; Sack et al., 2002) and
others, so that there is now a sufficiently clear idea of
how complex the K partitioning in a plant can be, not only
during the course of plant’s life but even within a single
day. As an example, leaves receive variable irradiances
depending on their orientation and phyllotaxis: sun leaves
of several trees have been shown to have higher Kleaf than
shade leaves (Sack et al., 2003) and the timing of leaf
shedding was also influenced by changes in Kleaf (Brodribb
and Holbrook, 2003a).
If some parts of the plant are favoured over others in
terms of water balance and nutrient flow, it can be expected
that variability in Kleaf along a plant may also have an
impact on plant growth form. In the present study, the
hydraulic conductance was measured of leaves inserted at
different nodes of growing and mature plants of a cultivar
(see below) of sunflower characterized by a pronounced
apical dominance. Some sunflower varieties, in fact, produce only one stem (i.e. lateral buds do not grow into
shoots) and only the apical floral bud develops into one
inflorescence. Because anthesis occurs in this species near
the end of the plant’s life, the inflorescence can be expected
to be (and really is) strongly favoured in terms of water and
nutrient flow which would occur at the expense of leaves.
The aim of this study was to investigate the impact of
different Kleaf values along the stem between the plant’s base
and the apical inflorescence on leaf water relations. This
might elucidate the physiological significance of changes in
this variable during plant growth and development.
Materials and methods
All experiments were conducted on plants of Helianthus annuus L.
cv. Margot at 4 weeks old (growing plants, GP) and 7 weeks old
(mature plants, MP). In particular, GP had heights about two-thirds
those of MP (Table 1); GP had leaves inserted at the most apical node
still actively expanding while MP were in full anthesis, i.e. the
inflorescence was mature and all the leaves as well (except for the
most apical two leaf pairs that remained quite small all the time and
were not considered in the present study).
Seeds were planted in 2.5 l pots filled with a mixture (1:1, v:v) of
peat and sand (one seed per pot). Ten days after germination, each
plant received 7.5 g of fertilizer (Nitrophoska Top, BASF Italia SpA,
15% N, 10% P2O5, 15% K2O, 2% MgO, 12% SO3, 0.02% B, and
0.01% Zn). Plants were grown in a growth room where air
temperature was adjusted to vary between 25 8C and 19 8C (during
the day and night, respectively), relative humidity was set at 5565%,
and light was provided by mercury halide and high pressure sodium
lamps. The distance between lamps and the apical portion of the plant
was kept constant at 1.0 m by moving lamps upward during plant
growth. The photoperiod was set at 14 h (lights were turned on at
05.30 h and turned off at 19.30 h). Plants were well irrigated and each
plant received about 400 ml of water every 2 d before experiments
started and 200 ml of water every day during the experiments.
All measurements were performed on mature leaves starting from
the second-formed pair of leaves (node 2, node 1 bearing the
cotyledons) up to node 7 in GP and node 11 in MP, i.e. only fully
expanded leaves were used for measurements, except for leaves at
node 7 of GP which were still expanding (Table 1).
Water relations parameters
Leaf conductance to water vapour (gL) and water potential (WL) of
one leaf per node were measured on 10 plants, 3 h after lights were
turned on. The opposite leaf of each node was used for hydraulic
experiments (see below). Leaf conductance to water vapour and water
potential were measured using a steady-state porometer (LI1600, LiCor Inc., Lincoln, NE, USA) and a pressure chamber (mod. 1000,
PMS Instrument Company, Corvallis, OR, USA), respectively. When
measuring gL, the photosynthetically active radiation (PAR) incident
on each leaf was also measured using the quantum sensor built in the
porometer (LI-190S-1, Li-Cor Inc.).
The leaves used for WL measurements were rehydrated in distilled
water for 1 h in the dark and then used to measure leaf water potential
isotherms (PV curves, Tyree and Hammel, 1972; Salleo, 1983), thus
Table 1. Leaf surface area (one side only) measured in growing
plants of sunflower and in plants in full anthesis (mature plants)
The heights of the two groups of plants are reported as h. The node
numbers refer to leaf pairs starting from node 2, node 1 bearing the
cotyledons. Means are given 6SD (n=5).
Node number
from the base
2
3
4
5
6
7
8
9
10
11
Leaf surface area (cm2)
Growing plants
(h=67.768.5 cm)
Mature plants
(h=102.564.9 cm)
73.265.8
95.369.9
116.5620.1
128.5620.5
111.2620.3
97.867.9
–
–
–
–
69.468.8
100.166.0
115.767.1
138.6614.1
146.0618.7
159.3621.2
143.6620.8
155.1618.5
110.3624.5
95.267.8
Hydraulic architecture of sunflower 1551
obtaining the leaf water potential at the turgor loss point (Wtlp) and
osmotic potential at full turgor (p0). At least five leaves per node
number of both GP and MP were measured for water potential
isotherms. These measurements were intended to give information of
leaf turgor at given WL values in terms of (WLÿWtlp) as well as of
changes in the mean leaf solute concentration in terms of p0.
Leaf hydraulic conductance
Whole-leaf hydraulic conductance (KL) was measured using the
vacuum chamber technique introduced by Kolb et al. (1996) and
modified for leaf blades by Nardini et al. (2001). Further validation of
the vacuum chamber technique for measuring Kleaf has been provided
by Sack et al. (2002). In particular, the vacuum chamber method has
proved to be an effective tool for measuring actual values of leaf
hydraulic conductance in that the perfusion of leaves under vacuum
does not cause the refilling of cavitated vessels (Trifilò et al., 2003a).
The vacuum chamber was an 8.0 l PVC flask. The petiole was
connected to rigid PEEK (polyetheretherketone) tubing using a 5 mm
length of Tygon tubing. The PEEK tubing passed through the rubber
seal of the vacuum flask to a beaker of solution (50 mM KCl) resting
on a digital balance (Ohaus Explorer, Switzerland). A vacuum pump
was used to reduce the pressure in the vacuum flask in steps of 20 kPa
and at each pressure a computer measured the weight of the beaker on
the digital balance at 30 s intervals to compute flow. All flow readings
were made at a temperature of 2261 8C and under normal laboratory
irradiance (PAR<6 lmol mÿ2 sÿ1). At least 10 flow readings were
made at each pressure ranging from atmospheric to depressions of
20 kPa in four steps starting from 80 kPa below atmospheric and
continuing at 60, 40, and 20 kPa. Volume flow rates were recorded
until the flow became stable (i.e. the SD of the mean of the last 10
readings was less than 3% of the mean). The flows (F) were plotted
versus the pressures applied (P) and leaf hydraulic conductance was
computed from the slope of the F to P linear relationship.
At the end of each experiment, leaf surface area (AL) was measured
using a leaf area meter (LI3000A, Li-Cor Inc.) and KL was scaled by
leaf surface area thus obtaining leaf area-specific hydraulic conductance (Kleaf). At least five leaves per node number of both GP and MP
were measured for their Kleaf.
Fig. 1. Photosynthetically active radiation (PAR) incident on leaves
inserted at progressively more apical nodes, starting from the base, as
measured in both growing (black columns) and mature (white columns)
plants. Vertical bars represent SD of the mean (n=10).
Results
Under the prevailing experimental conditions of the present
study, apical leaves experienced levels of photosynthetically active radiation (PAR; Fig. 1) which were up to five
times higher with respect to basal leaves, both in growing
and mature plants. Accordingly, sunflower plants still
actively growing (GP; Table 1) showed gL values significantly increasing in the acropetal direction (Fig. 2A).
Leaves inserted at nodes 2 and 3 (basal leaves) had gL of
40–70 mmol mÿ2 sÿ1 while distal leaves (at nodes 5, 6, and
7) had fully open stomata (gL was about 240 mmol mÿ2
sÿ1). Mature flowering plants (MP; Fig. 2B) showed the
same gL spatial pattern as GP, with basal leaves with gL
values up to six times less than those measured for distal
leaves. Furthermore, stomata of leaves inserted at the same
node numbers appeared to undergo progressive closure
with the time so that, for example, gL of leaves inserted at
nodes 4, 5, and 6 decreased from 160, 240, and 235 mmol
mÿ2 sÿ1, respectively, to 95, 100, and 150 mmol mÿ2 sÿ1,
respectively, between the phase of active plant growth and
that of maturity. In other words, gas exchange of these
leaves (that were located near the middle of the stem of GP
Fig. 2. Leaf conductance to water vapour (gL) measured on leaves
inserted at progressively more apical nodes, starting from the base.
Vertical bars represent SD of the mean (n=10). Different letters indicate
significant differences (P<0.05) for Tukey pairwise comparisons.
but had become basal in MP) decreased by 40–60% during
plant growth and development. Fully expanded leaves
inserted at the four most apical nodes of MP, by contrast,
had highest gL of over 250 mmol mÿ2 sÿ1.
1552 Lo Gullo et al.
Leaf water potential (WL) of basal leaves was significantly more negative than that of distal leaves (Fig. 3A, B).
It can be noted that the difference in WL between leaves
inserted at node 2 (most basal) and 7 (most apical) in GP
(Fig. 3A) was of ÿ0.55 to ÿ0.35 MPa. In MP, this difference was even larger (ÿ0.78 to ÿ0.40 MPa for leaves
inserted at node 2 with respect to those inserted at node 11,
the most apical one). In other words, leaves were experiencing time-dependent progressive dehydration, decreasing
in the acropetal direction. Leaf water potential at zero turgor
(Wtlp) of GP leaves (Fig. 3A) was only slightly (but still
significantly) more negative in distal versus basal leaves,
while it showed a more marked decrease in the acropetal
direction in MP (Fig. 3B). In this case, WL of the most basal
leaves dropped near the turgor loss point (Wtlp= ÿ0.9 MPa;
WL= ÿ0.79 MPa). Leaves located at the most apical nodes,
by contrast, showed WL= ÿ0.40 MPa and Wtlp as negative
as ÿ1.27 MPa. In other words, leaves of MP retained
increasingly more turgor the more apical they were. This
also occurred in GP because WL was increasingly higher
Fig. 3. Leaf water potential (WL, dashed columns) and leaf water
potential at the turgor loss point (Wtlp, black columns) measured on leaves
inserted at progressively more apical nodes, starting from the base.
Vertical bars represent SD of the mean (n=10 for WL; n=5 for Wtlp).
Different letters indicate significant differences (P<0.05) for Tukey
pairwise comparisons.
(less negative) in the acropetal direction, but to a much
lesser extent because leaf Wtlp was more or less constant
along the stem.
The osmotic potential at full turgor (p0) of leaves (Fig.
4A) was about 0.05 MPa more negative for the most distal
than for the most basal leaves of GP (this difference,
although quite small, was statistically significant); in MP,
however, the difference in p0 (Fig. 4B) was as large as 0.25
MPa between the most basal and the most apical leaves,
these last leaves having the highest solute concentration
(most negative p0). In other words, solute export from basal
to apical leaves was just starting in GP and increased
noticeably in MP (the difference in p0 between basal and
apical leaves was only 5% in GP but as high as over 33% in
MP). The still expanding leaves of GP (at node 7, Fig. 4A)
showed, as expected, WL values less negative than those
measured in fully expanded leaves and less negative
osmotic potentials.
Leaf-area-specific hydraulic conductance (Kleaf) is reported, for all the leaves studied, in Fig. 5. Growing plants
(Fig. 5A) showed Kleaf increasing sharply in the acropetal
direction so that apical leaves had Kleaf about three times
higher than that measured for basal leaves (Kleaf of the two
Fig. 4. Leaf osmotic potential at full turgor (p0) measured on leaves
inserted at progressively more apical nodes, starting from the base.
Vertical bars represent SD of the mean (n=5). Different letters indicate
significant differences (P<0.05) for Tukey pairwise comparisons.
Hydraulic architecture of sunflower 1553
Fig. 6. Leaf hydraulic conductance (KL) as a function of leaf surface area
as measured for both growing (solid symbols) and mature plants (open
symbols). The solid and dashed lines represents linear regression and
95% confidence intervals, respectively. The regression coefficient (r) and
the P value (Pearson Product Moment Correlation) are also reported.
Fig. 5. Leaf area specific hydraulic conductance (Kleaf) measured on
leaves inserted at progressively more apical nodes, starting from the base.
Vertical bars represent SD of the mean (n=5). Different letters indicate
significant differences (P<0.05) for Tukey pairwise comparisons.
most apical leaves was of the order of 2.1 e-4 versus 0.7 e-4
kg sÿ1 mÿ2 MPaÿ1 as measured for basal leaves).
On a temporal scale, Kleaf of MP was found to have
decreased slightly in leaves inserted between node 3 and
node 6 with respect to the same variable measured in leaves
of GP (Fig. 5). On a spatial scale, leaves of MP inserted
between node 7 and node 11 (at which the most apical leaves
studied were inserted) had fairly high Kleaf (of the order
of over 2.0 e-4 kg sÿ1 mÿ2 MPaÿ1). When KL (i.e. leaf
hydraulic conductance not scaled to leaf surface area) was
plotted versus the corresponding leaf surface area, a highly
significant linear relationship appeared to exist between the
two variables (Fig. 6) thus suggesting that no ‘size effect’
on Kleaf was superimposed on spatial and temporal effects.
The hydraulic conductance of leaves has been reported to
be sensitive to light (Sack et al., 2002, 2003). When Kleaf, as
measured in both GP and MP, was plotted to the PAR measured at the upper surface of leaves still attached to the plant
before they were collected for measurements, a linear positive
relationship was found to exist between the two variables (Fig.
7) with a high correlation coefficient (r2=0.805) and high
significance (P<0.01). In other words, leaves shaded by others
(which occurred mostly to basal leaves) had significantly
lower Kleaf than leaves more exposed to light.
Fig. 7. Leaf area specific hydraulic conductance (Kleaf) as a function of
the prevailing irradiance applied during plant growth (photosynthetically
active radiation, PAR). Black circles refer to growing plants; open circles
refer to mature plants. Vertical and horizontal bars represent SD of the
mean (n=5). The correlation coefficient r2 and the P-value (Pearson
Product Moment Correlation) are reported.
Stomata are well known to be quite sensitive to several
factors among which are light and bulk leaf water potential.
To investigate the possible relationship between stomatal
conductance to water vapour and leaf hydraulic conductance, gL and Kleaf both measured on leaves of GP and MP
were plotted to each other (Fig. 8). Again, a linear positive
relationship was found to exist between the two variables
with a correlation coefficient r2 of 0.808 and P<0.01.
Discussion
It is well known that, when the inflorescence of sunflower
reaches maturity and produces fruits and seeds, leaves
progressively die starting from the stem base. These data
1554 Lo Gullo et al.
suggest that leaf dieback might be related to the progressive
loss of hydraulic conductance that would cause stomata to
close progressively both on a spatial and on a temporal
scale (i.e. the measured progressive decrease of gL, Fig. 2A,
B). On the basis of the Ohm’s law hydraulic analogue, leaf
water potential at a given stem xylem water potential (Wx)
is the result of the ratio of transpiration rate to Kleaf.
Stomatal closure has been reported to ensure the homeostasis of leaf water potential, which typically occurs in
species with a good stomatal control of transpiration
(Nardini and Salleo, 2003; Trifilò et al., 2003b). In the
present case, the reduction of gL was linearly related to the
Kleaf loss. Stomatal closure, however, was not effective in
preventing the dehydration of basal leaves. Leaf turgor was
found to increase in the acropetal direction in terms of
the difference between WL and Wtlp (Fig. 3A, B) both in
growing and in mature plants. In summary, the water status
of basal leaves was likely to be altered by dehydration as
well as by solute export from the basal towards the apical
leaves (which was more consistent in MP, Fig. 4B) both
processes typically accompanying leaf senescence.
Leaf hydraulic conductance (Fig. 5) of basal leaves was,
in both GP and in MP, over 60% less than that measured for
apical leaves. In principle, this might be related either to the
increasing shadowing of the basal leaves by the more apical
ones or to senescence initiating from the plant base. Some
of these data are in favour of the former hypothesis because:
basal leaves of actively growing plants (GP) were only
slightly less turgid than apical leaves (Fig. 3A) and
seemingly green and healthy. In spite of this, Kleaf of
these leaves was 60% less than Kleaf of apical ones. Leaf
senescence (although not yet visible) is known to be
accompanied by solute export (Patakas and Noitsakis,
2001; Wang et al., 2003). In this case, the osmotic potential
at full turgor (p0, Fig. 4A) measured from basal leaves of
GP was only 5% less negative than that of apical leaves (i.e.
for leaves inserted between node 2 and node 6). Therefore,
it can be assumed that senescence of basal leaves was
just beginning in GP, but that it had been preceded by
a consistent drop in Kleaf. Moreover, Kleaf was shown to be
linearly and positively related to the PAR measured at the
upper surface of leaves that were still attached. Hence, it
was concluded that the possible sequence of events leading
to leaf dieback was: Kleaf drop as the primary event, causing
WL and leaf turgor to decrease leading to stomatal closure
and later to leaf senescence. However, it has to be pointed
out that causal relationships between these physiological
traits were not specifically investigated in the present study,
so that the above conclusion has to be considered as a
tentative hypothesis for further studies addressed at elucidating the sequence of events possibly linking impairment
of plant hydraulic functioning to leaf ageing.
Both gL and Kleaf are light-dependent (Sack et al., 2003)
and, in fact, these two variables were found to be positively
and linearly related to each other (Fig. 8) in accordance with
Fig. 8. Leaf conductance to water vapour (gL) as a function of leaf
hydraulic conductance (Kleaf). Black circles refer to growing plants; open
circles refer to mature plants. Vertical and horizontal bars represent SD of
the mean (n=10 for gL; n=5 for Kleaf). The correlation coefficient r2 and
the P value (Pearson Product Moment Correlation) are reported.
other studies (Lo Gullo et al., 2003). It has to be noted,
however, that all Kleaf measurements were performed under
ambient irradiance (PAR<6 lmol mÿ2 sÿ1), so that Kleaf
correlated with the prevailing ambient irradiance during plant
growth and development (Fig. 7) and not to the irradiance at
the time of measurement. This suggests that stomatal conductance to water vapour and leaf hydraulic conductance may
be regulated by two different light-dependent mechanisms,
Kleaf being possibly regulated by aquaporins (Morillon and
Chrispeels, 2001) whose expression has been reported to
change on a diurnal basis (Henzler et al., 1999) as a possible
result of light-mediated circadian regulation (Moshelion
et al., 2002). In turn, the relationship between Kleaf and gL
might be an effect of hydraulic architecture in that higher
water availability would be assured to leaves with higher
hydraulic conductance, thus allowing stomata to open while
maintaining leaf water potential within critical threshold
levels (Trifilò et al., 2003b).
The sunflower plants, well before they reached maturity,
had a shoot hydraulic architecture consisting of an intrinsically low-resistance water pathway (the stem; see
Tsuda and Tyree, 2000) to which several lateral water paths
(the leaves) are connected, the basal leaves having K three
times less than apical ones. This hydraulic pattern strongly
favours apical leaves. The K of the inflorescence has not
been measured, but it would be expected to have an even
larger K than apical leaves have. Because both GP and MP
showed the same partitioning of leaf hydraulic conductances, the conclusion is that the sunflower cv. Margot (and
many others with the same typically ‘monopodial’ growth
form) is hydraulically designed in such a way that the distal
leaves of the plant (and probably the inflorescences too) are
at any time favoured in terms of water balance with respect
to leaves located at the base and that this hydraulic
architecture is already present in young plants. Experimental
Hydraulic architecture of sunflower 1555
evidence for an influence of plant hydraulic properties on
final leaf size and shape has been recently provided by
Nardini (2002) and by Zwieniecki et al. (2004). Moreover, it
is of interest to note that trees with typically strong apical
dominance (e.g. Abies sp.) tend to have a hydraulic dominance, too, with large increases in leaf specific hydraulic
conductance towards the dominant apex (Huber, 1928;
Zimmermann, 1983; Tyree and Zimmermann, 2002). On
the basis of the above, it is suggested that the pronounced
apical dominance of this cultivar of sunflower was determined, among other factors, by its hydraulic architecture.
The authors are aware that the hydraulic properties of
other important compartments, like the root system and the
stem, might influence plant growth form. These, were not
investigated in the present study. However, Tsuda and
Tyree (2000) have reported the partitioning of hydraulic
resistances between roots, stem, and leaves of sunflower
showing that about 50% of plant hydraulic resistance was
located in the shoot. In turn, leaves represented about 70%
of shoot hydraulic resistance. Hence, leaves represent an
important hydraulic limitation in sunflower which is likely
to have profound effects on plant growth form.
The only other strongly monopodial species studied in
this respect are palms (Zimmermann and Sperry, 1983).
The possibility that the growth form of herbs is closely
dependent upon their hydraulic construction deserves, in
the authors’ opinion, more studies in the view of its
relevance in the agricultural practice.
Acknowledgements
The present study was funded by the University of Messina (Finanziamenti di Ateneo per Progetti di Ricerca). The visit of L Castro Noval
to the Department of Botanical Sciences, University of Messina, was
made possible by a grant from the Ministerio de Educaciòn, Cultura y
Deporte de España. We are very grateful to Maisadour Sementi Italia
SpA for providing seeds of sunflower cv. Margot.
References
Brodribb TJ, Holbrook NM. 2003a. Changes in leaf hydraulic
conductance during leaf shedding in seasonally dry tropical forest.
New Phytologist 158, 295–303.
Brodribb TJ, Holbrook NM. 2003b. Stomatal closure during leaf
dehydration, correlation with other leaf physiological traits. Plant
Physiology 132, 2166–2173.
Henzler T, Waterhouse RN, Smyth AJ, Carvajal M, Cooke DT,
Schäffner AR, Steudle E, Clarkson DT. 1999. Diurnal variations
in hydraulic conductivity and root pressure can be correlated with
the expression of putative aquaporins in the roots of Lotus
japonicus. Planta 210, 50–60.
Hubbard RM, Ryan MG, Stiller V, Sperry JS. 2001. Stomatal
conductance and photosynthesis vary linearly with plant hydraulic
conductance in ponderosa pine. Plant, Cell and Environment 24,
113–121.
Huber B. 1928. Weitere quantitative Untersuchungen über das
Wasserleitungssystem der Pflanzen. Jahrbuch Wissenschaftliche
Botanik 67, 877–959.
Kolb KJ, Sperry JS, Lamont BB. 1996. A method for measuring
xylem hydraulic conductance and embolism in entire root and
shoot systems. Journal of Experimental Botany 47, 1805–1810.
Larson PR, Isebrands JG. 1978. Functional significance of the
nodal constricted zone in Populus deltoides. Canadian Journal of
Botany 56, 801–804.
Lo Gullo MA, Nardini A, Trifilò P, Salleo S. 2003. Changes in leaf
hydraulics and stomatal conductance following drought stress and
irrigation in Ceratonia siliqua (Carob tree). Physiologia Plantarum 117, 184–196.
Lo Gullo MA, Salleo S, Piaceri EC, Rosso R. 1995. Relations
between vulnerability to xylem embolism and xylem conduit
dimensions in young trees of Quercus cerris. Plant, Cell and
Environment 18, 661–669.
Morillon R, Chrispeels MJ. 2001. The role of ABA and the
transpiration stream in the regulation of the osmotic water
permeability of leaf cells. Proceedings of the National Academy
of Sciences 98, 14138–14143.
Moshelion M, Becker D, Biela A, Uehlein N, Hedrich R, Otto B,
Levi H, Moran N, Kaldenhoff R. 2002. Plasma membrane
aquaporins in the motor cells of Samanea saman: diurnal and
circadian regulation. The Plant Cell 14, 727–739.
Nardini A. 2002. Relations between efficiency of water transport and
duration of leaf growth in some deciduous and evergreen trees.
Trees 16, 417–422.
Nardini A, Salleo S. 2000. Limitation of stomatal conductance by
hydraulic traits: sensing or preventing xylem cavitation? Trees 15,
14–24.
Nardini A, Salleo S. 2003. Effects of the experimental blockage of the
major veins on hydraulics and gas exchange of Prunus laurocerasus
L. leaves. Journal of Experimental Botany 54, 1213–1219.
Nardini A, Tyree MT. 1999. Root and shoot hydraulic conductance of seven Quercus species. Annals of Forest Science 56,
371–377.
Nardini A, Tyree MT, Salleo S. 2001. Xylem cavitation in the leaf
of Prunus laurocerasus and its impact on leaf hydraulics. Plant
Physiology 125, 1700–1709.
Patakas A, Noitsakis B. 2001. Leaf age effects on solute accumulation in water-stressed grapevines. Journal of Plant Physiology
158, 63–69.
Sack L, Cowan PD, Jaikumar N, Holbrook NM. 2003. The
‘hydrology’ of leaves: co-ordination of structure and function in
temperate woody species. Plant, Cell and Environment 26, 1343–
1356.
Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM. 2002. The
hydraulic conductance of the angiosperm leaf lamina: a comparison
of three measurement methods. Journal of Experimental Botany
53, 2177–2184.
Saliendra NZ, Sperry JS, Comstock JP. 1995. Influence of leaf
water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis. Planta 196, 357–
366.
Salleo S. 1983. Water relations parameters of two Sicilian species of
Senecio (groundsel) measured by the pressure bomb technique.
New Phytologist 95, 179–188.
Salleo S, Lo Gullo MA. 1986. Xylem cavitation in nodes and
internodes of whole Chorisia insignis H.B. et K. plants subjected
to water stress: relations between xylem conduit size and cavitation. Annals of Botany 58, 431–441.
Salleo S, Lo Gullo MA, Raimondo F, Nardini A. 2001. Vulnerability to cavitation of leaf minor veins: any impact on leaf gas
exchange? Plant, Cell and Environment 24, 851–859.
Salleo S, Nardini A, Lo Gullo MA, Ghirardelli LA. 2002. Changes
in stem and leaf hydraulics preceding leaf shedding in Castanea
sativa L.. Biologia Plantarum 45, 227–234.
1556 Lo Gullo et al.
Salleo S, Nardini A, Pitt F, Lo Gullo MA. 2000. Xylem cavitation
and hydraulic control of stomatal conductance in laurel (Laurus
nobilis L.). Plant, Cell and Environment 23, 71–79.
Salleo S, Rosso R, Lo Gullo MA. 1982. Hydraulic architecture of
Vitis vinifera L. and Populus deltoides Bartr. 1-year-old twigs. II.
The nodal regions as ‘constriction zones’ of the xylem system.
Giornale Botanico Italiano 116, 29–40.
Trifilò P, Gascó A, Raimondo F, Nardini A, Salleo S. 2003a.
Kinetics of recovery of leaf hydraulic conductance and vein
functionality from cavitation-induced embolism in sunflower.
Journal of Experimental Botany 54, 2323–2330.
Trifilò P, Nardini A, Lo Gullo MA, Salleo S. 2003b. Vein cavitation
and stomatal behaviour of sunflower (Helianthus annuus L.) leaves
under water limitation. Physiologia Plantarum 119, 409–417.
Tsuda M, Tyree MT. 1997. Whole-plant hydraulic resistance and
vulnerability segmentation in Acer saccharinum. Tree Physiology
17, 351–357.
Tsuda M, Tyree MT. 2000. Plant hydraulic conductance measured
by the high pressure flow meter in crop plants. Journal of
Experimental Botany 51, 823–828.
Tyree MT, Alexander JD. 1993. Hydraulic conductivity of branch
junctions in three temperate tree species. Trees 7, 156–159.
Tyree MT, Cochard H, Cruiziat P, Sinclair B, Ameglio T.
1993. Drought-induced leaf shedding in walnut: evidence for
vulnerability segmentation. Plant, Cell and Environment 16,
879–882.
Tyree MT, Hammel HT. 1972. The measurement of the turgor
pressure and the water relations of plants by the pressure-bomb
technique. Journal of Experimental Botany 23, 267–282.
Tyree MT, Patiño S, Bennink J, Alexander J. 1995. Dynamic
measurements of root hydraulic conductance using a high-pressure
flowmeter in the laboratory and field. Journal of Experimental
Botany 46, 83–94.
Tyree MT, Zimmermann MH. 2002. Xylem structure and the
ascent of sap, 2nd edn. New York: Springer Verlag.
Wang WQ, Wang M, Lin P. 2003. Seasonal changes in element
contents in mangrove element retranslocation during leaf senescence. Plant and Soil 252, 187–193.
Yang S, Tyree MT. 1994. Hydraulic architecture of Acer saccharum
and A. rubrum: comparison of branches to whole trees and the
contribution of leaves to hydraulic resistance. Journal of Experimental Botany 45, 179–186.
Zimmermann MH. 1978. Hydraulic architecture of some diffuseporous trees. Canadian Journal of Botany 56, 2286–2295.
Zimmermann MH. 1983. Xylem structure and the ascent of sap, 1st
edn. New York: Springer Verlag.
Zimmermann MH, Sperry JS. 1983. Anatomy of the palm Raphis
excelsa. IX. Xylem structure of the leaf insertion. Journal of the
Arnold Arboretum 64, 599–609.
Zwieniecki MA, Boyce CK, Holbrook NM. 2004. Hydraulic limitations imposed by crown placement determine final size and shape of
Quercus rubra L. leaves. Plant, Cell and Environment 27, 357–365.