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JXB Advance Access originally published online on July 26, 2006
Journal of Experimental Botany 2006 57(12):2937-2942; doi:10.1093/jxb/erl053
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© The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

RESEARCH PAPER

Thermodynamics of the water permeability of plant cuticles: characterization of the polar pathway

Markus Riederer*

Julius-von-Sachs-Institut für Biowissenschaften, Universität Würzburg, Julius-von-Sachs-Platz 3, D-97082 Würzburg, Germany

*E-mail: riederer{at}uni-wuerzburg.de

Received 28 November 2005; Accepted 12 May 2006


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
The water permeability of cuticles isolated from the leaves of 14 plant species was measured at temperatures from 10 °C to 55 °C at 5 K intervals. Permeances increased slightly with temperatures ≤35 °C and drastically in the higher temperature range. The data were analysed according to the Arrhenius formalism which led to distinct plots for the lower and higher temperature range, respectively. Activation energies of permeation for the lower temperature range were estimated to amount to 15.2–52.5 kJ mol–1, at higher temperature activation energies ranged from 52.2–117.3 kJ mol–1. This thermodynamics approach is used for further elucidating the pathway taken by water across the plant cuticle. Based on the results of this study it is hypothesized that the diffusion of water occurs along polysaccharide strands crossing the cuticle and that the transport properties of these polar pathways change with temperature.

Key words: Activation energy, cuticle, permeability, polysaccharides, temperature dependence, thermodynamics, water


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Protection against uncontrolled water loss from the above-ground parts of terrestrial plants is one of the most important functions of the plant cuticle (Schönherr, 1982; Burghardt and Riederer, 2003, 2006). This function is based on very low permeabilities to water which, for comparison, are equal or even lower than those of technical polymeric membranes of equal thickness (Riederer and Schreiber, 2001). The low water permeability of the plant cuticle originates from the chemical and physical nature of this barrier membrane (Riederer and Schreiber, 1995). The cuticle is, in principle, made up of the biopolymer cutin and associated cuticular waxes. For further information on the chemical composition and physical properties of the plant cuticle see the volume edited by Riederer and Müller (2006).

Over the years contradicting hypotheses have been put forward concerning the nature of the diffusion pathway of water and small polar molecules across the cuticle. Now, there is a consensus that inorganic and small organic ions can move across the cuticle by a special pathway which can not be analysed by the formalisms used to describe and quantify the pathway for lipophilic organic compounds (Schreiber, 2005; Riederer and Friedmann, 2006). However, the nature and the properties of the pathway for small polar non-electrolytes and ions (Schönherr, 2000, 2001, 2002; Schönherr and Luber, 2001; Schreiber and Schönherr, 2004; Schlegel et al., 2005; Popp et al., 2005) and water (Popp et al., 2005; Schreiber, 2005) have only recently become the focus of quantitative experimental analysis. The present state of knowledge is that the water permeating the cuticle takes (a) polar pathway(s) and that (b) the dissolution/diffusion pathway across the cuticular wax barrier may not have the relevance formerly attributed to it (Riederer and Schreiber, 2001). The polar pathway is considered to consist of polysaccharides and to have a mean apparent pore radius of 0.3 nm with a standard deviation of 0.02 nm in Hedera helix leaf cuticular membranes (Popp et al., 2005).

The objective of the present study was to use a thermodynamics approach for further elucidating the pathway taken by water across the plant cuticle. It will be shown that this technique leads to new insights into the physico-chemical nature of this pathway, the energetics of water transport, and the nature of sharp temperature-dependent changes in cuticular permeability.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Plant material and isolation of cuticles
Healthy fully expanded leaves from Camellia sinensis Kuntze (Theaceae), Citrus aurantium L. (Rutaceae), Cydonia oblonga Mill. (Rosaceae), Euonymus europaeus L. (Celastraceae), Ficus benjamina L. (Moraceae), Ficus elastica Roxb. (Moraceae), Forsythiaxintermedia Zabel (Oleaceae), Garcinia acuminata Wall. (Clusiaceae), Hedera helix L. (Araliaceae), Liriodendron tulipifera L. (Magnoliaceae), Monstera deliciosa Liebm. (Araceae), Nerium oleander L. (Apocynaceae), Prunus laurocerasus L. (Rosaceae), Pyrus communis L. var. ‘Williams Christ’ (Rosaceae) were used in this study. C. sinensis, C. aurantium, F. benjamina, F. elastica, G. acuminata, and M. deliciosa were grown in the greenhouses and the remaining species in the fields of the Botanic Garden of the University of Würzburg. Care was taken that the leaves harvested had previously not undergone treatment with agrochemicals. Cuticular membranes (CM) were isolated enzymatically from the upper astomatous surfaces of the leaves by the method described earlier by Schönherr and Riederer (1986).

Permeability measurements
Cuticular permeances were determined by the measurement of water loss through adaxial, astomatous CM. The CM were mounted in transpiration chambers made out of stainless steel with the upper side orientated towards the atmosphere (Schönherr and Lendzian, 1981; Burghardt and Riederer, 2003). The donor compartment of the transpiration chamber was filled with 1 cm3 water. The transpiration chambers were placed upside down into plastic boxes containing silica gel and were stored in growth cabinets at temperatures from 10–55 (±0.5) °C. The water loss across the exposed area of the transpiration chamber was measured by weighing the chambers at regular time intervals using a semi-micro balance (SBC 21; Scaltec, Göttingen, Germany; ±0.1 mg). In all cases the plots of the weight loss versus the time were linear, as shown previously for this type of experimental setup (Schreiber and Riederer, 1996).

The transpiration rate at maximum driving force J was calculated from the slope of the regression line of weight loss versus time divided by the exposed area (1.13 cm2). The cuticular permeance (p) was obtained from the cuticular transpiration rate divided by the concentration difference of water across the cuticular membrane acting as driving force:

Formula 1(1)

Since the transpiration chambers were filled with pure water, the corresponding water activity in the chamber (achamber) is equal to unity. The humidity of the air was controlled by silica gel resulting in a water activity (aair) close to zero. Therefore, the driving force for transpirational water loss is identical to the density of water vapour at saturation in the air ({rho}) (Nobel, 1991). Calculating water permeances on vapour-based concentration gradients eliminates the effect of temperature on the driving force (Kerstiens, 1996) and, when estimating thermodynamic properties, the energetic cost of evaporation.

Statistics
Ten to 20 replicates from each plant species were used for measuring permeances at one temperature. At temperatures ≤30 °C the same set of CM was used for experiments at different temperatures. Above this temperature range new sets of CM were used for each temperature. Permeances were calculated for each CM separately with the median of the whole sample estimated afterwards. For statistical calculations SPSS 13.1 for Windows and SigmaStat 3.10 were used.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
The permeances for water were measured for the cuticular membranes from the leaves of 14 species at temperatures from 10–55 °C. Within a species the data for replicates at one temperature varied considerably and were not normally distributed (Fig. 1). At 25 °C the median permeances ranged from 1.07x10–6 (Ficus elastica) to 1.42x10–4 m s–1 (Liriodendron tulipifera) thus varying over more than two orders of magnitude (Fig. 1).


Figure 1
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  		Fig. 1 Box plots (percentiles at 10, 25, 75, and 90%; medians, outliers) of permeances for water across the isolated leaf cuticular membranes from 14 plant species measured at 25 °C. Full systematic names of the species are given in the Materials and methods, numbers accompanying each box indicate N. Letters on the right side of the species names give the results of a two-sided multiple comparison of the permeances using the Kruskal–Wallis test [H (13, N=205)=184.4, P=0.000].

 
Temperature had a significant effect on water permeances (Fig. 2). For instance, the medians of water permeances of Hedera helix leaf CM increased from 5.24x10–7 (10 °C) to 1.21x10–4 (55 °C) m s–1. In the temperature range ≤35 °C permeances for all species increased only slightly while at higher temperatures drastic increases of permeances were observed (Fig. 2).


Figure 2
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  		Fig. 2 Effect of temperature on the permeance of water across the isolated leaf cuticles of 14 plant species. Full systematic names of the species are given in the Materials and methods. Medians from 10–20 replicates each are plotted vs. temperature.

 
When the medians at the different temperatures were plotted as Arrhenius graphs (logarithm of permeances versus the inverse of the absolute temperature) straight lines were obtained. For each species two Arrhenius graphs resulted: one for the low temperature range (≤35 °C) and one for temperatures higher than that value (Fig. 3).


Figure 3
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  		Fig. 3 Arrhenius plots of the permeances for water across isolated leaf cuticular membranes. Full systematic names of the species are given in the Materials and methods. The logarithm of medians from 10–20 replicates at each temperature are plotted versus the inverse absolute temperature.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
In general, temperature has a pronounced effect on diffusion and on the permeation of membranes by water. This behaviour was also observed with isolated plant cuticular membranes and leaf discs (Schönherr et al., 1979; Schreiber, 2001). The present study, based on an unprecedented broad spectrum of species (cuticular membranes isolated from the leaves of 14 plant species), confirmed the previous findings and showed that considerable variability exists between the temperature-dependent variation of cuticular water permeation of different species (Fig. 2). Plant cuticular water permeances versus temperature exhibited significant but comparably small increases at temperatures from 10–35 °C while, in contrast, very steep increases were observed at temperatures above 35 °C. This behaviour was also observed previously when the temperature dependence of CM water permeance from a much smaller range of species was investigated (Schönherr et al., 1979; Schreiber, 2001).

Temperature dependence of membrane permeability can be used to obtain information on the energetics and molecular mechanisms of transport (Vieth, 1991). Prominent biological examples for this type of study have been carried out with the wax-based barriers of the cuticles of arthropods where abrupt changes of water permeance as a function of temperature have similarly been observed (Hadley, 1989; Gibbs, 1998, 2002). In some cases, the thermal dependence of water permeability of arthropod cuticles showed geographic and altitudinal variations and adaptations (Rourke, 2000) which have been explained by the energetics of water transport and phase behaviour of cuticular lipids varying accordingly.

The temperature dependence of rate phenomena like diffusion is best analysed and interpreted by the Arrhenius formalism. The Arrhenius equation for diffusion states that

Formula 2(2)
where D (m2 s–1) is the diffusion coefficient at temperature T (K), D0 the pre-exponential factor which is equal to D at infinite temperature, ED (J mol–1) the activation energy of diffusion, and R (J mol–1 K–1) the gas constant. ED is a measure of the energy expended against the cohesive forces of the medium in which diffusion occurs. In the special case of diffusion in polymers, cohesive forces between polymer chains must be overcome in order to open up gaps into which the diffusing molecules can jump.

Permeance according to equation 1 can also be expressed by

Formula 3(3)
where K is the dimensionless partition coefficient of the diffusing molecule between the membrane and the adjacent phase and l (m) the thickness of the membrane or that of its transport-limiting barrier. The partition coefficient is also temperature-dependent according to

Formula 4(4)
with K0 standing for the partition coefficient at infinite temperature and {Delta}HK for the enthalpy of phase transfer during partitioning.

From equations 3 and 4, it follows that the temperature dependence of permeance is given by

Formula 5(5)
where

Formula 6(6)
Linear regression analysis of ln p versus 1/T yields Ep from the slope and p0 from the y-intercept (Fig. 3; Tables 1, 2). In Arrhenius plots of the water permeances measured in this study for the CM isolated from 14 plant species, two clearly distinct relationships between permeance and temperature can be observed: one at lower temperatures (10–35 °C) and one at higher temperatures ranging from 35–55 °C. The activation energies Ep of water permeance range from 21.1 (Cydonia oblonga) to 52.5 (Ficus elastica) kJ mol–1 in the lower-temperature range (Table 1) and from 52.2 (Citrus aurantium) to 117.3 (Ficus elastica) kJ mol–1 at temperatures above 35 °C (Table 2).


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  		Table 1 Activation energies obtained from Arrhenius plots of water permeance for plant cuticular membranes in the temperature range from 10–35 °C

 

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  		Table 2 Activation energies obtained from Arrhenius plots of water permeance for plant cuticular membranes in the temperature range from 35–55 °C

 
According to equation 6 the activation energy of permeance derived from Arrhenius plots is a compound quantity incorporating the activation energy of diffusion in the pathway the water molecules take across the membrane ED and the enthalpy released or consumed by the transfer of water into the material of the diffusion pathway {Delta}HK. Recent evidence suggests that water preferentially permeates plant cuticles through polar pathways which presumably consist of polysaccharide strands extending from the epidermal cell wall to the outer surface of the cuticle or of permanent charges in the cutin (Schreiber and Schönherr, 2004; Shi et al., 2005; Popp et al., 2005; Schreiber, 2005). Assuming that water preferentially uses the polysaccharide pathway, Ep adds up the activation energy of diffusion in the aqueous phase of the polysaccharide strands and the enthalpy of water/polysaccharide interactions. Water/polysaccharide interactions are exothermic which can be inferred from the determination of heats of wetting of dry wood. The enthalpy change accompanying wetting was found to be in the range of –80 kJ kg–1 (Kelsey and Clarke, 1955) which means that the water content of polysaccharide material decreases with increasing temperature. Approximately 80% of the sorbed water in wood is associated with the cellulose and hemicellulose fractions (Christensen and Kelsey, 1958). This implies that the interaction of water with the polysaccharide strands of plant cuticles will release energy, while the diffusion of water molecules within the strands consumes energy. As ED and {Delta}HK can be assumed to have opposite signs, the activation energy of the permeation process EP will be lower than ED and can even reach 0 when ED= –{Delta}HK.

The values of Ep can be compared to the activation energy of the self-diffusion of water which amounts to approximately 19–22 kJ mol–1 (Glasstone et al., 1941; Wang et al., 1953; Pruppacher, 1972). The activation energy would equal this value if water diffused across the cuticle unhindered in a wide continuous aqueous pore and did not interact with the walls of the pore. As activation energies measured for the permeation of water across CM are larger than this value (with the exception of Nerium oleander; Table 1), the pathway of diffusion can not be envisaged as a pore that is large with respect to the dimensions of a water molecule where the walls do not interact physically or chemically with the diffusing molecule. This is even more the case as the activation energies of permeation are reduced by the counteracting effect of water sorption to the polysaccharides. This finding implies that water diffusion is sterically hindered and that the water molecules chemically interact with the strand material. It is therefore questionable whether the term ‘pore’ adequately describes the pathway water takes across plant cuticles.

Abrupt changes of the activation energies of permeation in all species were observed at a given temperature (Tables 1, 2). It may be speculated that this fact is due to a progressive swelling with increasing temperature of the polysaccharide material, presumably making up the preferential pathway of diffusion in plant CM. Such temperature-dependent degrees of swelling were observed for wood (Stamm and Longborough, 1935). There may be a critical degree of swelling reached at a critical temperature (in this case approximately 35 °C) which opens new and ‘stiffer’ regions of the polysaccharides for the diffusion of water (Damstra, 1986). These new pathways may contribute to higher water permeances since the diffusion cross-section increases. The additional pathways for diffusion can be accessed only at a higher cost of activation energy Ep.

The differences in activation energies between different fractions of the polysaccharide strands may not only be due to differences in the physical properties of the polymers but also to the strength of water binding. There are several fractions of water within a polysaccharide network which are made up of either free, freezing bound or non-freezing bound water molecules (Berthold et al., 1996). At high water activities, depending on the polar group and the counter-ion involved, up to 14 water molecules are hydrogen-bonded to single polar group of the polysaccharide. It is imaginable that above the critical temperature an additional water fraction (probably one of the bound fractions) is set free to produce additional mobile water taking part in diffusion. The activation energy for diffusion ED in the polysaccharide strands is therefore suggested to be composed both of a term related to the opening of gaps between the polysaccharide polymers and of a term related to the breaking of additional hydrogen bonds (Zhou and Lucas, 1999).

The hypothesis proposed for the nature and the temperature-dependent behaviour of the polar pathways across the plant cuticle can now be put into perspective with potential phase-transitions of the lipid material making up a major part of the plant cuticular membrane. The phase behaviours of cutin (Schreiber and Schönherr, 1990; Matas et al., 2004) and of cuticular waxes (Reynhardt and Riederer, 1991, 1994; Merk et al., 1998) have been studied in the past. In the case of cuticular waxes, in no case did the observed phase transition temperatures coincide with the temperatures where the sharp bends in the Arrhenius graphs of permeance occurred. Schreiber and Schönherr (1990), however, observed a sharp change in the thermal expansion coefficient of water-saturated cuticles at about 35 °C which they ascribed to (volume) changes in the polysaccharide fraction(s). The mechanical strain exerted by these changes may open up additional polar pathways in plant cuticular membranes. This conclusion agrees with the view presented here that changes in the swelling behaviour of the polysaccharides associated with the cuticle occur at this temperature. Recent work with arthropods has also shown that the formerly proposed phase transitions of cuticular lipids do not explain the abrupt changes in the water permeability of the arthropod cuticle at higher temperatures (Yoder et al., 2005).


   Acknowledgements
 
This work was supported by grants from the Coordinated Research Centres 251 and 567 and the Fonds der Chemischen Industrie. The author is indebted to Ellen Kilian and Ursula Hoffman for skilful technical assistance. The support by the staff of the Botanic Garden of the University of Würzburg is gratefully acknowledged.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
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