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Annals of Botany 89: 221-226, 2002
© 2002 Annals of Botany Company

Heterogeneity in Bean Leaf Mesophyll Tissue and Ion Flux Profiles: Leaf Electrophysiological Characteristics Correlate with the Anatomical Structure

SERGEY SHABALA*,1, LISA J. SCHIMANSKI2 and ANTHONY KOUTOULIS2

1School of Agricultural Science, University of Tasmania, GPO Box 252–54 and 2School of Plant Science, University of Tasmania, GPO Box 252–55, Hobart, TAS 7001, Australia

 * For correspondence: E-mail: Sergey.Shabala{at}utas.edu.au

Received: 18 July 2001; Returned for revision: 8 October 2001; Accepted: 7 November 2001.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 

It has been suggested for some time that the architectural properties of leaf venation are related to leaf functions; however, experimental evidence is scant and, when present, mainly investigates water or carbohydrate transport patterns. Transport of inorganic nutrients in relationship to leaf anatomical structure remains, to a large extent, an unexplored area in plant physiology. In this study, we correlated ion flux profiles with the anatomical structure of bean (Vicia faba L.) leaf mesophyll tissue using a non-invasive ion flux measuring technique (microelectrode ion flux estimation) and scanning electron microscopy. Quasi-periodic patterns of net H+ and K+ flux distributions were found when the mesophyll surface was scanned along the longitudinal axis with 0·1–0·2 mm increments. These patterns showed a high correlation with anatomical features of the mesophyll tissue (i.e. the distribution of vascular bundles). The observed flux profiles were not time-dependent, showed qualitative similarity in both light and dark conditions, and resulted in heterogeneous plant physiological responses. The possible physiological role of the observed findings, specifically in relation to stomatal ‘patchiness’ and phloem loading mechanisms, is discussed.

Key words: Ion fluxes, leaf scan, hydrogen, potassium, venation system, mesophyll, phloem, stomata, bean, Vicia faba, heterogeneity.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 
Plant leaves are complex heterogeneous structures designed to provide the optimal balance between fluxes of light, CO2, water, nutrients and carbohydrates into and out of the leaf. The leaf venation system supplies the leaf lamina with water and solutes via the xylem, and facilitates the export of carbohydrates to other plant organs via the phloem. It is not surprising, therefore, that it has been suggested for some time that the architectural properties of the leaf venation system are related to physiological leaf functions (see recent review by Roth-Nebelsik et al., 2001).

The transport properties of the vascular bundle system have been investigated, mostly, from the point of view of water flux (Altus and Canny, 1985; Jeje, 1985; Kull and Herbig, 1994; Roth-Nebelsik et al., 2001). Additionally, numerous studies report the link between leaf anatomical features and carbohydrate transport processes (Gamalei, 1989; Reismeier et al., 1993; Van Bel, 1993; Patrick, 1997; Wood et al., 1997, 1998; Schobert et al., 1998). Transport and re-distribution of inorganic nutrients in relation to leaf anatomical structure remains, to a large extent, an unexplored area in plant physiology.

The heterogeneous nature of leaf physiological characteristics is obvious. In beans (Vicia faba L.), up to 80 % of leaf expansion is caused solely by the growth of preformed cells (Dale, 1988). As growth patterns of the apical and basal regions of the leaf are strikingly different, it is reasonable to suggest that K+ distribution (the major osmoticum required for the extension growth) might vary significantly between these regions. On a smaller scale, ‘stomatal patchiness’ is another example of heterogeneity of leaf physiological characteristics. It has been demonstrated that in many species and under various experimental conditions, stomatal conductance and behaviour differ between regions of the leaf, forming patches up to several millimetres across (Mott and Buckley, 1998). In some cases, stomata may stay fully open for prolonged periods of time in some patches, whilst in nearby regions they may exhibit pronounced oscillatory behaviour (Cardon et al., 1994; Siebke and Weis, 1995). Local production and distribution of chemical ‘signals’ (including K+ ions) have been suggested as facilitators of these differences (Mott and Buckley, 1998), but direct experimental evidence is lacking. Importantly, a quasi-periodic distribution pattern of surface electric potentials was found in tomato and bean leaves measured in situ using a miniature tritium ionization electrode (Shabala et al., 1993).

In this study, we have attempted to correlate leaf electrophysiological characteristics (specifically, net fluxes of H+ and K+) with the anatomical structure of bean leaf mesophyll, using the non-invasive microelectrode ion flux measuring technique in conjunction with scanning electron microscopy. We report a close correlation between electrophysiology and anatomy, and discuss possible underlying mechanisms as well as their physiological significance.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 LITERATURE CITED
 
Plant material
Broad beans (Vicia faba L. cv Coles Dwarf; Cresswell’s Seeds, New Norfolk, Australia) were grown from seed in 0·5 l plastic pots in the glasshouse. The potting mixture included 70 % composted pine bark, 20 % coarse sand and 10 % sphagnum peat (pH 6·0). A fertilizer mixture (1·8 kg m–3 Limil, 1·8 kg m–3 dolomite, 6·0 kg m–3 Osmocote Plus and 0·5 kg m–3 ferrous sulfate) was added to each pot, and the plants were watered daily with tap water. Leaves were harvested from 20–30-d old plants, and mesophyll tissue segments were isolated essentially as described by Shabala and Newman (1999). Mature, but still expanding, leaves (7–10-d old) were used in experiments.

Ion selective flux measurements
Net fluxes of H+ and K+ were measured non-invasively using ion-selective vibrating microelectrodes [the microelectrode ion flux estimation (MIFETM) technique; University of Tasmania, Australia] generally as described in our previous publications (Shabala et al., 1997; Shabala, 2000). The theory of the MIFE technique has been described in a recent review (Newman, 2001). Commercially available ionophore cocktails were used [H+ (catalogue number 95297) and K+ (catalogue number 60031); Fluka, Switzerland]. The electrodes were calibrated in sets of standards before and after use. Electrodes with a response of <50 mV per decade and a correlation <0·999 were discarded. We maintained our sign convention for ion influx as being positive.

Experimental protocol
Isolated mesophyll segments were cut and floated peeled side (abaxial surface) down on the experimental solution (10 mM KCl, 1 mM MgCl2 and 0·1 mM CaCl2; unbuffered pH approx. 5·5) for 4–5 h. Forty to fifty minutes prior to measurement, each segment was mounted in a Perspex holder (peeled side up) and placed in the measuring chamber under dim green microscope light (Fig. 1). The ionic composition of the measuring solution was 0·1 mM KCl + 0·1 mM CaCl2. A low-level K+ solution was used in an attempt to maximize signal-to-noise ratio for K+ liquid ion exchanger (LIX).



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  		Fig. 1. Schematic diagram of experimental set-up for flux measurements. Full details are provided in Materials and Methods.

 
Before the leaf scan started, a test for the absence of endogenous oscillations was routinely undertaken. Electrodes were positioned 50 µm above the leaf mesophyll surface, with their tips separated by 2–3 µm and aligned parallel to the surface. Ion fluxes were measured for 15– 20 min to make sure that steady-state conditions were reached, thereby eliminating the potentially confounding effects of wounding, solution replacement or changes in light conditions.

After the ‘test for stability’ was completed, electrodes were positioned at one end of the cut segment, close to the edge, and net ion fluxes of H+ and K+ were measured for 1–1·5 min. The electrodes were then re-positioned, along the longitudinal axis, to another spot (100–200 µm from the initial one), and flux measurements were repeated. In most experiments, the ‘grid size’ for re-positioning was 200 µm, and 25–30 different spots were measured for segments, typically with lengths of 5–6 mm. Each scan took 30–45 min to complete.

In some experiments, several repetitive scans were performed to determine whether endogenous processes confounded ion flux profiles; this was not the case in any circumstance. In some experiments the light conditions were changed and scans were performed under bright (150 W m–2) microscope light. In the latter experiments, scans were started 1 h after light treatment was given, to ensure the completion of any light-induced changes in net ion fluxes (Shabala and Newman, 1999).

Scanning electron microscopy
On completion of the flux scans, leaf samples remained in the experimental solution to prevent desiccation. The leaf samples were removed from the Perspex holder and placed onto an aluminium stub covered with graphite tape. The stubs were placed immediately into an Electroscan 2020 environmental scanning electron microscope operated in environmental mode using water vapour as the imaging medium. The microscope was maintained at 15 kV, and approx. 5 torr at ambient room temperature (approx. 20 °C). Secondary electron images were acquired using the proprietary Electroscan gaseous secondary electron detector (GSED). The start position of the flux scans was marked before the sample was removed from the holder, and the path of the flux scan was serially photographed. Consequently, vascular bundles were differentiated from mesophyll cells and the distances between vascular bundles were measured.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
LITERATURE CITED
 
When steady state values of net ion fluxes are measured from the same tissue under the same conditions and following the same experimental protocol, a normal distribution curve is expected. This was not the case when net H+ fluxes were measured from the surface of isolated bean mesophyll segments (Fig. 2A). Instead, the frequency distribution curve was significantly skewed towards high negative values. This cannot be explained by methodological problems of ion flux measurements. A more likely scenario is that the observed phenomenon was due to biological variability. Similar results were also obtained for net K+ fluxes (data not shown).



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  		Fig. 2. A, Frequency distribution of net H+ fluxes (inward positive) measured from the surface of isolated bean mesophyll segments. Overall, 420 measurements were made using 43 individual leaves. The number of samples was plotted at the mid-point of each 20 nM m–2 s–1 range flux interval. B, Kinetics of net H+ flux measured near the leaf mesophyll surface in response to onset of illumination. Responses from ‘group 1’ samples (open symbols) (steady state dark values close to zero). Responses from ‘group 2’ samples (closed symbols) whose steady-state dark H+ flux values were significantly more negative. Data are average ± s.e. (n = 5 and 7, respectively).

 
Initial heterogeneity of steady net flux values results in significantly different patterns of leaf physiological responses. The kinetics of net H+ flux measured near the leaf mesophyll surface in response to the onset of illumination is shown in Fig. 2B. When initial H+ values were close to zero (where most of the measured samples fell), dark to light transition caused initial net H+ efflux, peaking at approx. 7 min after light treatment (Fig. 2B; open symbols), similar to our previous report (Shabala and Newman, 1999). These typical, so-called ‘group 1’, H+ flux responses are consistent with literature reports on light-induced stimulation of H+ pump in leaves (Marre et al., 1989; Linnemeyer et al., 1990; Okazaki et al., 1994; Remis et al., 1994). However, very often (in approx. 30–40 % of cases), light onset caused an immediate shift towards net H+ uptake (Fig. 2B, closed symbols; a so-called ‘group 2’ response). For the latter samples, the initial steady net H+ flux values were, as a rule, significantly more negative than those for the ‘group 1’ type responses. Both response groups showed similar kinetics at the later stages, but differed significantly during the first 5–7 min of light treatment.

A possible explanation for the observed phenomenon might be that it is due to different rates of CO2 uptake by different parts of the mesophyll segment. In our early studies we have suggested that the apparent inconsistency between observed light-induced pH and H+ flux changes might be caused by simultaneous activation of H+ pumps (leading to net H+ efflux) and increased CO2 uptake by photosynthesizing leaf tissues (leading to medium alkalinization and interpreted as net H+ influx by the MIFE technique) (Shabala and Newman, 1999). Therefore, the qualitative difference and, ultimately, the two different types of light-induced H+ flux kinetics reported in this study (Fig. 2B) may be attributed to either different rates of H+ pump activation by light, or to different rates of CO2 uptake into photosynthesizing mesophyll cells. In both cases, such a difference may be attributed to the heterogeneous structure of the bean mesophyll tissue.

In order to further investigate this issue, we looked at ion flux profiles along the longitudinal axis of mesophyll segments (Fig. 1) and tried to correlate them with the anatomical structure of the measured tissue. A close association between positions of ‘peaks’ and ‘troughs’ in ion flux profiles and the distribution of the vascular bundles in leaf mesophyll was found. One typical example (out of five) is shown in Fig. 3. Three obvious vascular bundles are present in this sample (Fig. 3A) and the corresponding H+ flux profile had major peaks (minimal efflux) at these exact positions (Fig. 3B). This phenomenon is further illustrated in Fig. 4, where another example is shown at a higher magnification. Both net H+ and K+ fluxes were significantly higher close to the vascular bundle of the leaf (Fig. 4B).



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  		Fig. 3. A, Composite of scanning electron micrographs of abaxial leaf mesophyll surface. B, Corresponding net H+ flux profiles measured along the scan axis (shown as a dashed line in panel A) at 200 µm intervals. One (out of five) representative example is shown. The diagonal lines drawn on the micrographs represent the position of veins.

 


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  		Fig. 4. A, Composite of scanning electron micrographs of the leaf mesophyll surface. B, Corresponding H+ (open symbols) and K+ (closed symbols) flux profiles. Note the clear dependence of the net H+ and K+ fluxes on the distance from the major vein present.

 
A high correlation (R > 0·7) between H+ and K+ flux profiles was observed in all experiments. Figure 5 shows two examples (from two individual segments with different venation patterns); one for net K+ and H+ fluxes (Fig. 5A), and another for concentration of these ions in the bathing solution (Fig. 5B). A degree of similarity is obvious. The qualitative similarity of ion flux profiles and close stoichiometry of H+/K+ for most of the measured region (Fig. 5A) suggests the possible mediation of the same transport system. This issue requires further investigation using a pharmacological approach.



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  		Fig. 5. Traces illustrate the similarity in profiles of net H+ and K+ flux (A) or their concentrations in the apoplasm near the tissue (B). Two individual examples (one for flux and another one for concentration data) are shown. Troughs and peaks in the flux/concentration distribution reflect the morphology of leaf mesophyll segment measured. H+ (open symbols); K+ (closed symbols).

 
Differential accumulation of inorganic solutes between epidermal and mesophyll cells is a widely reported phenomenon. Karley et al. (2000a, b) showed that this difference could not be explained by the simple presence or absence of ion transporters, and suggested the differential regulation of ion channels. Keunecke and Hansen (2000) have found a striking difference between K+ transporter properties in the bundle sheath and mesophyll cells of maize leaves. Here we report the heterogeneity of ion flux profiles near the mesophyll surface and demonstrate that this difference in electrophysiological characteristics is determined, essentially, by the distance of the measured cell from the vascular bundles.

To demonstrate that ion flux profiles are associated with leaf spatial, but not temporal, organization, we have performed a series of repetitive scans on the same leaf segment. One such example is shown in Fig. 6. No qualitative difference in net H+ and K+ (data not shown) flux profiles was found between two consecutive scans, which were performed 1 h apart (closed circles and squares in Fig. 6). Moreover, qualitatively similar ion flux profiles were found even after leaf segments were exposed to a bright light for 1 h (open circles in Fig. 6). Taken together, these data suggest that the observed heterogeneity of ion flux profiles are not caused by variation in nutrient transport rates due to some endogenous process, but are relevant to mesophyll anatomical structure; specifically, venation system patterns.



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  		Fig. 6. Net H+ flux profiles measured near the bean mesophyll surface at different times and at different light conditions. Initial scan (closed circles) (dark); measurements taken 1 h after the initial scan (closed squares) (still in the dark); measurements taken from the same segment 1 h after the light was switched on (open circles). Note the qualitative similarity of ion flux profiles between three consecutive scans.

 
Possible physiological implications of these findings are at least two-fold. First, there is an issue of heterogeneity in leaf photosynthesis (Siebke and Weis, 1995). K+ movement between subsidiary and guard cells is central for stomata aperture control. As guard cells lack plasmodesmatal connections, this interaction is mediated by significant changes in ionic concentrations in the apoplasm. Uneven distribution of apoplasmic K+ concentrations above the mesophyll surface, caused by complex K+ fluxes profiles reported in this study (Figs 4, 5), might be responsible for differential availability of K+ for epidermal cells and, ultimately, produce ‘patchiness’ in guard cell responses. This idea is consistent with (1) suggestions that some chemical signals (ABA or K+) might be responsible for the latter phenomenon (Mott and Buckley, 1998) and (2) observations that stomatal patches are usually bound by veins (Pospisilova and Santrucek, 1994).

Secondly, complex ion flux profiles and their association with the leaf anatomical structure might be relevant to solute and nutrient transport from the leaf. In some species, up to 90 % of total K+ absorbed by roots and delivered to leaves via xylem may be translocated in the phloem and therefore cycled within the vascular tissue (Jeschke and Pate, 1991; Marschner, 1995). The highest K+ influx, observed in the vascular bundles regions (Fig. 4), is consistent with this idea. As for H+ flux profiles, a possible link is photoassimilate export from the leaf lamina. In some species, including broad beans, phloem loading is known to be predominantly apoplasmic (Bourquin et al., 1990; Laloi et al., 1993). This process might often be energy-dependent (Marschner, 1995) and a H+-coupled carrier-mediated transport mechanism has been suggested (Giaquinta, 1977; Komor et al., 1977; Laloi et al., 1993). Importantly, the phloem loading of sucrose is significantly affected by external K+ levels (Schobert et al., 1998), which might explain the close correlation between the net H+ and K+ flux profiles observed in our experiments (Figs 4B, 5).


   ACKNOWLEDGEMENT
 
This work was supported by the ARC Large Grant (A00001144) to Dr S. Shabala.


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