Journal of Experimental Botany, Vol. 53, No. 374, pp. 1651-1657,
July 1, 2002
© 2002 Oxford University Press
Light-regulated leaf expansion in two Populus species: dependence on developmentally controlled ion transport
Received 8 August 2001; Accepted 19 March 2002
1 Botany Department, Box 35-5325, University of Washington, Seattle, WA, 98195-5325, USA
Abbreviations: Em, membrane potential; TEA, tetraethylammonium.
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Abstract |
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Leaf growth responses to light have been compared in two species of Populus, P. deltoides and P. trichocarpa. These species differ markedly in morphology, anatomy, and dependence on light during leaf expansion. Light stimulates the growth rate and acidification of cell walls in P. trichocarpa but not in P. deltoides, whereas leaves of P. deltoides maintain growth in the dark. Light-induced growth is promoted in P. deltoides when cells are provided 50–100 mM KCl. In both species, light initially depolarizes, then hyperpolarizes mesophyll plasma membranes. However, in the dark, the resting Em of mesophyll cells in P. deltoides, but not in P. trichocarpa, is relatively insensitive to decade changes in external [K+]. Results suggest that light-stimulated leaf growth depends on developmentally regulated cellular mechanisms controlling ion fluxes across the plasma membrane. These developmental differences underlie species-level differences in growth and physiological responses to the photoenvironment.
Key words: Key words: Ion transport, leaf expansion, light, Populus.
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Introduction |
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Light influences the growth of dicotyledonous leaves throughout the developmental process, from determining the timing of leaf initiation and de-etiolation to controlling the rate and duration of cell division, cell expansion and thus leaf shape (Dale, 1988; Francis, 1998; Keller and Van Volkenburgh, 1998). Specifically, it is known that light acts through red- and blue-light-stimulated pathways, apart from but augmented by photosynthesis, to increase cell expansion rates (Van Volkenburgh, 1999). The targets of these pathways increase H+ efflux into the apoplast, acid-induced cell wall loosening, and solute accumulation for turgor maintenance, thus driving cell expansion. The ‘acid-growth’ mechanism, proposed originally by Rayle and Cleland (1970, 1972, 1992) to explain the stimulatory effect of auxin on cell expansion, also applies to light-stimulated growth of dicotyledonous leaves including bean (Phaseolus vulgaris L.) (Van Volkenburgh and Cleland, 1980), pea (Pisum sativum L. var. Argenteum) (Stahlberg and Van Volkenburgh, 1999), and birch (Betula) (Taylor and Davies, 1985).
Two closely related species of Populus, P. trichocarpa and P. deltoides, display markedly different leaf morphology, anatomy, and dependence on light for growth. Previously, it was shown that biomass productivity, as measured by stem volume, in these two species and their fast-growing hybrids is correlated not only with total leaf area but also with the rate of leaf expansion (Ridge et al., 1986). Here, the physiological response to light in growing leaves of P. trichocarpa and P. deltoides has been compared. The focus of the investigation was on the characterization of H+ and K+ transport across the plasma membrane, their regulation by the photoenvironment and contribution to growth. The results indicate that a fundamental difference in the regulation of membrane transport and conductance to K+ underlies the contrasting growth behaviours of these two species. Further, leaves of P. trichocarpa cease cell division when 10–20% expanded, but P. deltoides leaves continue cell division until they are 80–90% expanded (Van Volkenburgh and Taylor, 1996). The results presented here, from comparative studies of leaves 30% and 90% full size, suggest that growth and physiological differences are related to the developmental state of growing leaf cells.
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Materials and methods |
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Plant material and growing conditions
Hardwood cuttings of P. trichocarpa (clone 93–968) and P. deltoides (clone ILL-129) were harvested yearly in February from a clone bank (Farm 5, Washington State University Agricultural Experiment Station, Puyallup WA) and planted in 2.2 l pots containing a nutrient- and pH-adjusted commercial soil mix of peat and perlite. Cuttings were alternately fertilized with solutions containing N-P-K concentrations of 15:0:15 or 20:10:20 at 100 ppm N, both supplemented with Mg and micronutrients. Cuttings were grown in a greenhouse with temperatures controlled between 18 °C and 23 °C (day) and 13 °C and 16 °C (night). During the winter months, natural light was supplemented with metal halide lamps to provide a minimum 17 h daylength with PAR
175 µmol m–2 s–1. To maintain a fresh supply of young leaves, plants were cut back when they reached a height of approximately 1 m to stimulate production of new shoots and leaves. All leaves selected for experiments were taken from the first 10 leaves produced by newly expanding shoots. Growing leaves at 30% and 90% full size were selected for the experiments. Relative size was estimated based on the leaf length to leaf area relationship for each genotype as previously described (Ridge et al., 1986).
Measurement of leaf growth
Diurnal variation in the extension rate of intact leaves was measured using position transducers (RVDT, RD 30; Schaevitz, Pennsauken, Pa., USA). Plants were moved from the greenhouse to a light- and temperature-controlled growth chamber (150 µmol m–2 s–1, 12 h photoperiod at constant 25 °C) for 24 h before extension rates were measured in order to minimize the effects of variable greenhouse temperatures on growth measurements. Leaves 30–50% full size were clamped in a fixed position at the middle of the midvein, and a mobile arm connected to the axis of the rotary position transducer was clamped 5 cm distal from the fixed clamp at an angle parallel to the secondary veins. A 2 g load was applied to the mobile clamp to keep the leaf tissue under constant tension.
Growth of isolated leaf tissue was measured on discs excised with a cork borer (7.1 mm diameter) from growing leaves and floated on solutions containing varying concentrations of KCl. Discs were incubated in 150 µmol m–2 s–1 white light or dark for 24 h at 25 °C, after which the change in disc diameter was measured with a ruler under a dissecting microscope.
Measurement of leaf surface pH
All experiments were conducted on leaf tissue isolated from greenhouse-grown plants (see above for greenhouse conditions). Leaves were harvested between 12.00 h and 16.00 h and experiments were begun within 15 min after leaf harvest. The abaxial surface of leaves 30% and 90% full size was abraded lightly with abrasive powder (89 µm aluminum oxide; K.C. Abrasive Co., Kansas City, KS). Strips 5 mm wide were cut from the entire length of the leaf and laid abaxial side down on pH indicator plates containing 0.7 mM bromcresol purple, 0.4% phytagel, 10 mM KCl adjusted to pH 6.0 with NaOH (Mulkey et al., 1981). Due to the puncture of the cuticle and wounding of the epidermal layer by abrasion, the observed pH changes are considered to reflect the long-term changes in the apoplastic pH of the mesophyll. Plates were placed in the dark or under white light (150 µmol m–2 s–1) for 24 h at 25 °C.
Continuous recordings of apoplastic pH responses to light and dark in 30% expanded leaves were made using a flat-tipped combination pH electrode. Squares of leaf tissue were cut from the basal region of the leaf, the abaxial side abraded and placed abraded side up on filter paper dampened with 10 mM KCl. Ten µl of the same solution was used to cover the abraded section and a flat-tipped pH electrode (MI-410 Combination pH electrode; Microelectrodes, Inc., Bedford, NH., USA) was placed in contact with the drop of solution for continuous recording of the pH in response to light/dark transitions. White light (150 µmol m–2 s–1) was supplied with a projector lamp directly to the leaf tissue through a fibreglass light guide.
Measurement of Em of mesophyll cells
All experiments were conducted on leaf tissue isolated from greenhouse-grown plants (see above for greenhouse conditions). Leaf strips (0.5x2.0 cm) were cut parallel to secondary veins from the basal region of leaves 30% and 90% full size. Strips were floated on the experimental solution, 1–100 mM KCl and 1 mM CaCl2 adjusted to pH 6.0 with NaOH, overnight in white light (150 µmol m–2 s–1) or dark to allow recovery of the Em after strip excision. Leaf strips were then secured to a Plexiglas strip using Terostat (Teroson Werke, Heidelberg, Germany) and placed into a perfusion chamber holding a reference electrode and mounted onto a microscope stage. The leaf strip was continuously bathed with the experimental solution using a gravity-fed perfusion system. A microelectrode was inserted into mesophyll cells under microscopic control using perpendicular green light of less than 1 µmol m–2 s–1. Microelectrodes were pulled from borosilicate glass capillaries (Kwik-Fil; World Precision Instruments, Sarasota, Fl, USA), backfilled with 0.3 M KCl and used if tip potentials were less than ±10 mV. The Em of the second or third mesophyll cell encountered upon insertion of the microelectrode was recorded continuously throughout light-on/light-off transitions. White light (150 µmol m–2 s–1) was supplied with a projector lamp directly to the leaf tissue through a fibreglass light guide as described in Stahlberg and Van Volkenburgh (1999).
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Results |
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Effect of light on leaf growth in P. trichocarpa and P. deltoides
Exposure to light (150 µmol m–2 s–1 white light) increased the growth rate of P. trichocarpa leaves 2–3-fold. P. deltoides leaves responded only slightly to light. Although the growth rates of P. trichocarpa and P. deltoides leaves may be similar to each other in the light (Fig. 1a) or in the dark (Fig. 1b), P. trichocarpa leaves always showed a significant light-stimulation of growth, whereas leaves of P. deltoides did not (Fig. 1c). Light caused the extension rate of P. trichocarpa leaves to increase from an average of 3.8 µm mm–1 h–1 to 10 µm mm–1 h–1 within 3 h. The removal of light slowed extension to the dark rate within an hour. By contrast, P. deltoides leaves grew on average only slightly faster in light (7.3 µm mm–1 h–1) than in dark (5.5 µm mm–1 h–1).
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Effect of exogenous KCl on light-stimulated growth of excised leaf tissue
In order to isolate direct effects of light on leaf growth from possible indirect effects of light resulting from changes in whole plant water relations, experiments were conducted with leaf discs floated on water or dilute KCl. When provided with water or low [KCl]ext (<10 mM), isolated discs of P. trichocarpa grew up to three times faster in light than dark, while P. deltoides leaf discs grew little in response to light (Fig. 2a, b). This result is similar to that found in intact leaves (Fig. 1). However, at higher concentrations of KCl, discs of P. deltoides exhibited light-stimulated expansion rates similar to those observed in P. trichocarpa (Fig. 2a). The concentration at which KCl enhanced growth in the light varied with the time of year. P. deltoides leaves harvested late in the summer responded to KCl concentrations of 1–5 mM (Fig. 2b) while early in the summer, an effect was only observed with KCl concentrations greater than 10 mM (Fig. 2a).
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Apoplast acidification and electrical responses (Em) to light and KCl
The ability of leaf cells to excrete acid, thus acidifying the apoplast and external medium, was tested using two methods. First, leaf tissue was excised, lightly abraded, and placed onto agar containing KCl and a pH indicator dye. Acidification was scored 24 h later by visual inspection of the colour of the agar under the leaf tissue. The second method monitored leaf surface pH over short periods before and after illumination using a flat-tipped pH electrode.
Tissue excised from young (30% full size) leaves of P. trichocarpa acidified the external medium in light, but not in dark, when incubated on 10 mM KCl (data summarized in Table 1). By contrast, P. deltoides leaves alkalinized the external medium in the light, and acidified it in the dark when provided with low, 1 or 10 mM, [KCl]ext. In a very few cases, when provided with 10 mM KCl (but never at 1 mM), some acidification was observed in young P. deltoides in response to light, as well as in the dark for young P. trichocarpa leaves. Leaf tissue isolated from older (90% full size) leaves of both species acidified the external medium in response to light. However, older P. trichocarpa showed reduced light-induced acidification when compared to younger leaves of the same species whereas older leaves of P. deltoides showed increased light-stimulated acidification relative to their younger counterparts.
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Data collected using a flat-tipped pH electrode to monitor the short-term effects (0–2 h) of light on apoplastic pH in young (30% full size) leaves are consistent with data on the long-term (24 h) effect of light on apoplastic pH in both species. Apoplastic pH of P. trichocarpa in the dark was initially around 6.0 (initial pH of 6.4 in Fig. 3a). Upon illumination, there was frequently a transient alkalization (not present in the trace in Fig. 3a), followed by a sustained acidification. In P. deltoides, light caused leaf cells to alkalinize the apoplast, shifting the pH from an initial value of ±6.0 in the dark (initial pH of 6.2 in Fig. 3b) approximately +0.5 pH units to a more alkaline pH within 20 min.
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Changes in Em can be expected when H+ efflux is stimulated. Acidification of the leaf surface in response to light is a result of light-activation of a H+ pump, and is associated with hyperpolarization of the plasma membrane in other species (i.e Stahlberg and Van Volkenburgh, 1999). The electrical response of mesophyll cells in these two poplar species was measured in an attempt to explain the differences observed in light-induced changes in apoplastic pH. The transient Em response to light-on, light-off transitions was similar in both species (Fig. 4a, b). These responses in poplar were similar both in magnitude, and in the sequence of oscillations, to Em responses reported in pea (Stahlberg and Van Volkenburgh, 1999) and other species (Lüttge and Higinbotham, 1979).
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Experiments testing the Em response to changes in external KCl concentrations (an assay of membrane conductance) reveal a difference between the two species. Table 2 shows the average change in the resting Em in response to 10-fold changes in external KCl. In the dark, young P. deltoides leaves (30% full size) underwent a transient depolarization, but returned to the initial Em following each 10-fold increase in external KCl (over the range of 1–100 mM) (Fig. 4c; Table 2). In the light, however, after a large initial depolarization similar to that seen in the dark, the resting Em of young P. deltoides leaves shifted ±8 mV in response to 10-fold changes in [KCl]ext (Table 2) rather than returning to the initial resting Em. This prolonged shift in the resting Em was similar to the response of young (30% full size) P. trichocarpa leaves to changes in [KCl]ext in the light (Table 2). However, P. trichocarpa leaves showed a considerably larger long-lasting shift in the resting Em in response to changes in [KCl]ext (30 mV per 10-fold change) when incubated in the dark (Table 2; traces not shown but the Em response is similar to that shown for older P. deltoides leaves in Fig. 4d).
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Leaf developmental pattern and responsiveness to light and KCl
It has previously been reported that leaves of P. trichocarpa and P. deltoides differ in their pattern of development. Based on non-destructive measurements of epidermal cell size and number throughout leaf blade expansion, Clum (as cited in Van Volkenburgh and Taylor, 1996) found that P. trichocarpa leaves complete the phase of cell division when leaves are 10–20% full size. P. deltoides leaves continue cell division until leaves are 80–90% expanded. Since the experiments reported above were carried out with leaves 30% full size, the comparison of species is confounded by developmental differences, as leaves of P. deltoides were still undergoing cell division but P. trichocarpa leaf cells were growing by cell expansion alone. The following results compare the growth responses of young (30% full size) and older, but still expanding (90% full size) leaves of the two species to light and [KCl]ext.
Light-induced acidification of the apoplast (and agar in contact with abraded leaf surfaces) was observed in both young and older leaf tissue from P. trichocarpa in the presence of low, 1 or 10 mM, KCl (Table 1). As stated previously, young leaves of P. deltoides showed no acidification response to light when provided 1–10 mM KCl. However, older (90% full size) leaves of P. deltoides acidified the external medium in response to light, similar to younger (30% full size) leaves of P. trichocarpa (Table 1). By contrast, older leaves of P. trichocarpa had almost completely lost the ability to acidify the medium in response to light.
Young and older leaves of both species showed similar transient and long-lasting Em oscillations in response to light-dark transitions (Fig. 4a, b; data for older leaves were similar but are not shown). By contrast, whereas 
Em in response to 10-fold changes in [KCl]ext was similar in young and older leaves of P. trichocarpa (Table 2 traces are similar to Fig. 4d; data not shown), the Em response of P. deltoides depended on the age of the leaf. Young leaves show no, or very little, long-lasting changes in Em in response to 10-fold changes in [KCl]ext (Fig. 4c; Table 2), but older leaves respond with a ±20 mV change in Em per 10-fold step in [KCl]ext (Fig. 4d; Table 2). The apparent conductance to K+, as measured by change in Em per 10-fold change in [K+]ext, is similar, ±20 mV per 10-fold change in [KCl]ext, for older leaves of both species (Fig. 4d; Table 2).
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Discussion |
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Young leaves of P. trichocarpa grew considerably faster in the light than in the dark, whereas P. deltoides leaves grew relatively rapidly in the dark and were less stimulated by light. This difference was observed both in intact leaves (Fig. 1) and in leaf discs incubated in water or dilute KCl (Fig. 2). However, the difference in growth response between the species was overcome when the exogenous KCl level rose above 10 mM (Fig. 2), suggesting that the species differ in ion transport physiology or membrane conductance. Light-stimulated growth in P. trichocarpa leaves was associated with light-stimulated H+ efflux, whereas no light-stimulated acidification was observed in young P. deltoides. However, as P. deltoides leaves matured and cell division ceased, their physiological response to light looked increasingly like that of P. trichocarpa leaves: light-stimulated wall acidification increased (Table 1; Fig. 3), and the membrane conductance to K+ increased (Fig. 4). The physiology of light-stimulated growth is based on H+ efflux, solute accumulation (K+ when available), wall extension and turgor maintenance (Van Volkenburgh, 1999). The results presented here show that the contrasting growth responses to light in the two poplar species are correlated with a difference in membrane conductance to K+, which itself is a reflection of the developmental state of the leaf. Further, the results suggest that the species and developmental differences in the membrane K+ conductance are associated with similar differences in light-stimulated acidification.
To date, most research investigating the physiological and biochemical mechanisms that drive and regulate tissue expansion has been carried out in experimental systems, such as expanding leaves of Phaseolus (Van Volkenburgh and Cleland, 1979), that have been specifically designed to isolate cell expansion from the complications introduced by cell division. This includes research on the role of light in leaf cell expansion. The duration of cell division in expanding leaves is variable (Dale, 1988; Francis, 1998). In P. trichocarpa, cell division has ceased by the time leaves are 10–20% full size whereas in P. deltoides, cell division persists throughout most of leaf expansion until leaves are 80–90% full size (Van Volkenburgh and Taylor, 1996). Results presented here show that the apparent interspecific differences in the physiology of young Populus leaves disappeared when leaves of the two species were compared at similar developmental stages; i.e. when cell division ceased and leaf growth was driven by cell expansion alone.
Perhaps the strongest support for developmental differences underlying species differences in the growth response to light lies in the developmental shift in the quality of the Em response to external KCl. Young leaves of P. deltoides showed a ‘recovery response’ to changes in external KCl concentrations which was absent in older tissue (Fig. 4). Initially, the Em of cells in young leaves responded to changes in external KCl with a depolarization or hyperpolarization, indicating the presence of open K+-channels in the plasma membrane. However, in contrast to responses in other species (including P. trichocarpa) and in older P. deltoides, after initial oscillations in response to changing [KCl]ext, the Em of young leaves of P. deltoides returned to the original value. The ability to recover a pre-established Em, even in the presence of widely varying external KCl concentrations, suggests that an ion transporter is functioning in the plasma membrane of young leaf tissue, allowing the cells to restore or maintain a fixed Em. This mechanism could be an ATPase, ion co-transporter or ion channel whose expression or activity is developmentally-regulated. Such a ‘recovery’ mechanism might help dividing cells maintain the resting potential within a narrow, desirable range and might also prevent large, potentially signal-carrying oscillations (Elzenga et al., 1995) in the Em.
One possible explanation for the differences in young leaves and later similarities in older leaves of Populus is that the environment in and around dividing cells differs from that in and around expanding cells (those no longer undergoing mitosis) due to differences in the concentrations of growth hormones associated with cell division, such as auxin and cytokinins. These hormones influence multiple components of both intra- and intercellular signalling pathways, thus determining the cellular and growth responses to environmental factors such as light. Recent work on the role of auxin in developing dicot leaves suggests that not only are leaves an important source of auxin for the rest of the plant, but leaves themselves depend on a tight regulation of auxin content throughout development to maintain optimal division and expansion rates (Chen et al., 2001; Ljung et al., 2001; for a review see Chen, 2001).
Results from P. deltoides showing high growth rates in the absence of light-stimulated wall acidification call into question the role of H+ efflux in the cell expansion process. A similar absence of acidification associated with light-stimulated growth has been found previously in Acer pseudoplatanus (Taylor and Davies, 1985). The activity of the H+-pump in the plasma membrane and the resulting acidification of the apoplast have been considered important for acidifying and increasing the extensibility of the cell wall, thus allowing an increased cell expansion rate (Cosgrove, 1997). However, in P. deltoides leaves, acidification of the apoplast does not occur in response to light and is not necessary for maximal expansion rates. Either there is no light-induced increase in pump activity and H+ efflux (unlikely since the light-induced Em hyperpolarization probably reflects H+-pump activation; Stahlberg and Van Volkenburgh, 1999) or H+ fail to accumulate in the cell wall, perhaps due to the scavenging of available H+ for solute co-transport back into the cell. In young tissue, particularly that which is still sink tissue, it is possible that the role of H+ as a co-transporter of sucrose and other solutes back into the cell is equally, if not more important than the role of H+ in the regulation of wall extensibility. Whichever the case, the results suggest that an acidification of the cell wall may not always be required for maximal tissue expansion.
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