JXB Advance Access originally published online on June 4, 2004
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Journal of Experimental Botany, Vol. 55, No. 402, pp. 1549-1556, July 2004
Journal of Experimental Botany, Vol. 55, No. 402, © Society for Experimental Biology 2004; all rights reserved
RESEARCH PAPER |
Hydraulic architecture of plants of Helianthus annuus L. cv. Margot: evidence for plant segmentation in herbs
1Dipartimento di Scienze Botaniche, Università di Messina, Salita Sperone 31, 98166 Messina S. Agata, Italia
2UD Anatomia y Fisiologia Vegetal, ETS Ingenieros de Montes (UPM), Ciudad Universitaria s/n, 28040 Madrid, España
3Dipartimento di Biologia, Università di Trieste, Via L. Giorgieri 10, 34127 Trieste, Italia
* To whom correspondence should be addressed. Fax: +39 040 568855. E-mail: salleo{at}univ.trieste.it
Received 9 March 2004; Accepted 7 April 2004
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Abstract |
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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 (
L), leaf water potential at zero turgor (tlp), and leaf osmotic potential at full turgor (
0) were also measured. Sunflower plants showed gL and Kleaf values significantly increasing in the acropetal direction, while L of basal leaves was significantly more negative than that of distal leaves; tlp 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 time-dependent loss of hydraulic conductance. In fact, Kleaf loss was correlated with L 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 0. 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
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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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 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.
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Materials and methods |
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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).
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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 °C and 19 °C (during the day and night, respectively), relative humidity was set at 55±5%, 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 (L) 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, Li-Cor 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 L 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 obtaining the leaf water potential at the turgor loss point (tlp) and osmotic potential at full turgor (0). 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 L values in terms of (L–tlp) as well as of changes in the mean leaf solute concentration in terms of 0.
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 22±1 °C and under normal laboratory irradiance (PAR<6 µmol m–2 s–1). 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.
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Results |
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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 m–2 s–1 while distal leaves (at nodes 5, 6, and 7) had fully open stomata (gL was about 240 mmol m–2 s–1). 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 m–2 s–1, respectively, to 95, 100, and 150 mmol m–2 s–1, 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 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 m–2 s–1.
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Leaf water potential (
L) of basal leaves was significantly more negative than that of distal leaves (Fig. 3A, B). It can be noted that the difference in L between leaves inserted at node 2 (most basal) and 7 (most apical) in GP (Fig. 3A) was of –0.55 to –0.35 MPa. In MP, this difference was even larger (–0.78 to –0.40 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 (tlp) 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, L of the most basal leaves dropped near the turgor loss point (tlp= –0.9 MPa; L= –0.79 MPa). Leaves located at the most apical nodes, by contrast, showed L= –0.40 MPa and tlp as negative as –1.27 MPa. In other words, leaves of MP retained increasingly more turgor the more apical they were. This also occurred in GP because L was increasingly higher (less negative) in the acropetal direction, but to a much lesser extent because leaf tlp was more or less constant along the stem.
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The osmotic potential at full turgor (
0) 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 0 (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 0). In other words, solute export from basal to apical leaves was just starting in GP and increased noticeably in MP (the difference in 0 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, L values less negative than those measured in fully expanded leaves and less negative osmotic potentials.
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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 most apical leaves was of the order of 2.1 e-4 versus 0.7 e-4 kg s–1 m–2 MPa–1 as measured for basal leaves).
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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 s–1 m–2 MPa–1). 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.
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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.
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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.
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Discussion |
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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 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 (
x) 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 L and tlp (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 (0, 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 L 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 other studies (Lo Gullo et al., 2003). It has to be noted, however, that all Kleaf measurements were performed under ambient irradiance (PAR<6 µmol m–2 s–1), 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 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.
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Acknowledgements |
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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.
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References |
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