Journal of Experimental Botany, Vol. 57, No. 11, pp. 2493–2499, 2006
doi:10.1093/jxb/erl017 Advance Access publication 5 July, 2006
FOCUS PAPER
Water transport in plant cuticles: an update
Gerhard Kerstiens*
Lancaster Environment Centre/Biological Sciences, Lancaster University, Lancaster LA1 4YQ, UK
Received 18 November 2005; Accepted 11 April 2006
Abstract
The scale, mechanism, and physiological importance
of cuticular transpiration were last reviewed in this
journal 5 and 10 years ago. Progress in our basic
understanding of the underlying processes and their
physiological and structural determinants has remained frustratingly slow ever since. There have
been major advances in the quantification of cuticular
water permeability of stomata-bearing leaf and fruit
surfaces and its dependence on leaf temperature in
astomatous surfaces, as well as in our understanding
of the respective roles of epicuticular and intracuticular
waxes and molecular-scale aqueous pores in its physical control. However, understanding the properties
that determine the thousand-fold differences between
permeabilities of different cuticles remains a huge
challenge. Molecular biology offers unique opportunities to elucidate the relationships between cuticular
permeability and structure and chemical composition
of cuticles, provided care is taken to quantify the
effects of genetic manipulation on cuticular permeability by reliable experimental approaches.
Key words: Aqueous pores, cuticular water permeance,
epicuticular, epidermal transpiration, leaf conductance,
lipophilic pathway, wax.
Introduction
There is no question that creating a good water barrier, and
hence allowing a plant to control water loss through
regulation of its stomatal conductance, represents the major
physiological role of plant cuticles. However, permeabilities for water (Kerstiens, 1996b; Riederer and Schreiber,
2001) and other compounds (Buchholz et al., 1998;
Niederl et al., 1998) differ by up to about three orders of
magnitude between different types of cuticles. It is likely
that this huge variation is due, at least in part, to the
cuticle’s involvement in many other processes, ranging
from reflecting or absorbing radiation to providing information on microbes and insects arriving on a leaf surface
and possibly affecting stomatal patterning (Bird and Gray,
2003; Barnes and Cardoso-Vilhena, 1996; Jackson and
Danehower, 1996; Kerstiens, 1996a; Chassot and Métraux,
2005). Our understanding of the totality of evolutionary
pressures acting on the formation of the cuticle, in past and
present environments, is poor. Without it and an appreciation that the biosynthesis of many cuticular components is
tied up with other metabolic processes that have been
subjected to further pressures and constraints, it will remain
difficult to determine why different plants have such vastly
different cuticles, in terms of ultrastructure and chemical
composition, and how to improve them in crop plants with
regard to desirable traits such as drought or pest resistance
without impairing others.
Recent progress in the more applied areas relevant to
cuticular permeability, particularly the study of foliar
uptake of lipophilic, hydrophilic, and ionic agrochemicals,
has been impressive, but there is still quite a poor understanding of some of the most basic physiological questions,
such as why different species put so very different amounts
of resources into building a cuticle, why there are so many
different types of cuticles, differing not just between species but between different organs of a species (i.e. stems
and leaves, which may respond quite differently to manipulation of the same gene) and even between abaxial and
adaxial leaf surfaces, and how their permeabilities can
differ by up to three orders of magnitude. The structural and
compositional variability is of particular importance for
the cuticular permeability to water, as this compound is
likely not only to use the lipophilic pathway (i.e. random
diffusion in the lipophilic polymer and accessible wax
domains) but, to some unknown extent probably depending
on circumstances, aqueous pores as well (Schreiber, 2005).
Cuticular permeability to water is usually characterized
by the variable permeance (P), which is the ratio of water
* E-mail: [email protected]
ª The Author [2006]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
For Permissions, please e-mail: [email protected]
2494 Kerstiens
flow rate density to driving force, the latter being expressed
as a concentration difference (Kerstiens, 1996b; Riederer
and Schreiber, 2001). In the case of water, the concentration
is often expressed as density of liquid water, but there are
advantages in using the equivalent concentration of water
vapour in the gas phase, in particular with respect to
temperature effects (Kerstiens, 1996b). When liquid water
is present on one side of the cuticle, the equivalent is the
water vapour saturation concentration at the respective
temperature (Becker et al., 1986). All else being equal, the
flow rate is independent of the phase in which water is
present. At 25 8C and standard pressure, the density of
liquid water is 43 384 times greater than the saturation
water vapour concentration in air and, correspondingly,
values of P referenced to the gas phase are greater by this
same factor than values referenced to the liquid phase
(provided the experiment was carried out at 25 8C, which
is mostly the case). Values of P given in this paper are
referenced to the gas phase.
Water transport in lipophilic pathways and
aqueous pores and its dependence on
humidity and temperature
The two pathways
It is a well-established fact that cuticles act as solutiondiffusion membranes (also variably known as solubility
or solubility/mobility membranes) for water (Kerstiens,
1996b; Schreiber and Riederer, 1996; Niederl et al., 1998;
Riederer and Schreiber, 2001; Buchholz, 2006). This
means that individual water molecules follow a random
path across the cuticle in a mostly lipophilic chemical
environment, in the same way as would a freshly synthesized wax molecule, a dioxin molecule taken up from the
air, or some foliarly applied systemic herbicide.
Diffusion across a simple lipophilic polymer membrane
is governed by two parameters, namely the degree of
partitioning between the adjoining external phases and the
polymer (i.e. how many diffusant molecules enter it at
a given external concentration), and the diffusant’s mobility
within the polymer, which depends on the rate at which
molecular motion of polymer chains causes sufficiently
large random openings in the network to occur that allow
a diffusant molecule to move to another position. As parts
of the cuticle’s polymer network are taken up by highly
ordered domains that show little chain motion and hence
are inaccessible to diffusants, amplified tortuosity of the
diffusion path plays an important role as well. The main
barrier properties of the cuticle reside in a thin region at
its outer surface (the so-called limiting skin), and it is
the partitioning into, mobility within, and tortuosity of this
region that largely determine the diffusion properties of the
lipophilic cuticular pathway (Kerstiens, 1996b; Buchholz,
2006; Schönherr, 2006).
For a long time there have been suggestions that there is
an additional network of paths across the cuticles, which
would be much more hydrophilic in nature (Kerstiens,
1996b). Recent work on the transport of salts has demonstrated that such pathways—called aqueous pores—exist in
intact cuticles (Schönherr, 2000, 2006; Schönherr and
Schreiber, 2004; Schlegel et al., 2005; Schreiber, 2005).
While reasonably good estimates of pore diameter (in the
order of 1–2 nm) and number of pores per unit surface area
(in the order of 1015 per m2 after removal of waxes, but
probably fewer in intact cuticles) are possible (Schönherr,
2006), it is not known how tortuous and hence how long
they effectively are, what the mobility of water molecules
is in these very narrow channels with their hydrophilic
and hence ‘sticky’ sides, and how persistent they are in the
face of perpetual molecular motion. Even ‘porous’ membranes often behave as solution-diffusion membranes when
pore width is in the order of 1 nm or less (Wijmans and
Baker, 1995).
While at present these issues prevent any sensible
theoretical estimate of the quantitative contribution of pores
to water transport, an ingenious experiment has recently
provided direct measurements (Schreiber et al., 2006). As
ions are only transported in pores, the study used diffusion of silver and chloride ions from opposite sides into
isolated cuticles to let the resulting precipitate of AgCl
presumably block all pores. It was found that following
this treatment P decreased by between 0% and 37% in leaf
or fruit cuticles from 15 species, in an experimental set-up
where the morphologically inner side of the cuticle faced
a 0.01 M aqueous solution of NaCl and the outer one air
nearly devoid of water vapour. There was a weak positive
correlation between P in the untreated cuticle and the extent of the effect. The (presumptive) blockage of pores did
not lead to similar P across the range of different cuticles.
While P ranged from 3.08310ÿ6 to 1.44310ÿ4 m sÿ1 before
the treatment, the spread still amounted to 3.18310ÿ6 to
6.81310ÿ5 m sÿ1 thereafter.
Figure 1 shows the percentage decrease of P by this
treatment in some cuticles, which were also used in a
previous experiment that found a close correlation between
P in isolated leaf or fruit cuticles from 24 species and the
diffusion coefficient (D) of a lipophilic molecule (octadecanoic acid) in reconstituted cuticular waxes from the
same cuticles, demonstrating the importance of the lipophilic pathway for water diffusion in cuticles (Schreiber
and Riederer, 1996). One might expect that the cuticles that
had similar values of D but differed in P would also differ
in the degree to which pore blocking reduces P, bringing it
down to comparable values at similar D. This was clearly
not the case (Fig. 1). Surprisingly, the cuticles that did not
respond to the AgCl treatment at all had relatively high
values of P for their values of D. Unfortunately, the cuticles
where the strongest effects of the AgCl treatment were
found had not been included in the earlier experiment
20.00
P (10-5 m s-1)
10.00
7.00
5.00
32
·
3.00
2.00
·
21
1.00
0.70
0.50
·
0.30
0.20
0.10
0.07
0.05
·
·
0
·
37
·
·
·20 34
31
34
·
·
2
·
·
2
3
5
7
10
20 30
D
(10-19
50 70 100
m2
200 300 500
s-1)
Fig. 1. Diffusion coefficients D of a lipophilic probe in reconstituted
cuticular waxes (means), and water permeances P (medians) of leaf or
fruit cuticles from 24 species (replotted from Schreiber and Riederer,
1996), with percentage decrease of P after AgCl precipitation inside
cuticles superimposed (numbers; Schreiber et al., 2006). Bars represent
95% confidence intervals (D) and 25–75 percentiles (P), respectively.
(Schreiber and Riederer, 1996) and, therefore, could not be
included in Fig. 1.
P was determined gravimetrically in both of the above
experiments (Schreiber and Riederer, 1996; Schreiber
et al., 2006) by mounting isolated cuticles on so-called
transpiration chambers, which are small water-filled containers sealed by the cuticle. They are placed in an
atmosphere of near 0% relative humidity at 25 8C and
weighed repeatedly over a period of several weeks. In
a different experiment that demonstrated a close relationship between concurrently measured permeabilities to
water and a lipophilic compound across a wide spectrum
of cuticles, P was measured by diffusion of tritiated water
(as a tracer for water) in a system where the isolated cuticles were placed between two aqueous solutions (Niederl
et al., 1998). Figure 2 shows values of P from the gravimetric and tracer experiments for cuticles from the same
species plotted against each other. While P obtained with
the gravimetric method was lower for all cuticles, there was
a clear trend for the relative difference to increase with
rising P. It is possible that this was caused by a large
contribution of diffusion in aqueous pores to overall water
flow, especially in the most permeable cuticles, when there
was liquid water in contact with both surfaces of the
isolated cuticles. This would suggest that, if water is present
on the outside of the cuticle, the relative contribution of
diffusion in pores could be much higher than the 64%
maximum found when pores were blocked by AgCl and the
outside of the cuticle subsequently exposed to dry air; it
might in fact be as high as 95% (Fig. 2).
Results by Beyer et al. (2002) and Weichert et al. (2004),
obtained by application of aqueous solutions containing
one of a wide variety of different salts to the outside of
P from gravimetric experiments (10-5 m s-1)
Water transport in plant cuticles
5.0
2495
1:1 line
3.0
LYCOPERSICON
GINGKO
JUGLANS CITRUS
LIRIODENDRON
EUONYMUS
2.0
1.0
PYRUS
0.7
0.5
0.3
CAMELLIA
PHILODENDRON
HEDERA
0.2
0.1
0.3
PRUNUS
MONSTERA
1:20 line
0.5 0.7
1
2
3
5
7
10
20
30
50 70
P from co-permeability experiments (10-5 m s-1)
Fig. 2. Cuticular permeances to water (P) for leaf or fruit cuticles from
12 species obtained from gravimetric experiments (all values from
Schreiber and Riederer, 1996, except for Pyrus, which is from Riederer
and Schreiber, 2001) or co-permeability experiments (Niederl et al.,
1998). In the gravimetric experiments, isolated cuticles were in contact
with liquid water on the inside and very dry air on the outside. In the copermeability experiments, the cuticles were in contact with liquid water
on both sides. The continuous lines represent 1:1 and 1:20 ratios between
P values from the two types of experiments, and the dotted line the linear
regression.
excised cherry (Prunus avium L.) exocarp segments,
showed that some salts had a large effect (up to 80%
reduction) on cuticular permeability to water moving across
it from the outside (with an aqueous solution of high
osmolality—1.14 OsM—present on the inside to provide
a driving force). However, where it was tested, no effect on
permeability to water moving from the inside (with the
outside facing dry air) was found (Beyer et al., 2002).
While it is not clear what mechanism was responsible for
the different effects observed—it was suggested it might
have been precipitation of iron, aluminium, and copper
oxides and hydroxides, or other precipitates in the cuticle’s
‘polar pathways’ (i.e. aqueous pores)—it again indicates
that the presence or absence of liquid water on the outside
of the cuticle can make a large difference to its behaviour
towards water.
It is worth noting that cuticular permeabilities to both
water and lipophilic compounds are usually log-normally
distributed (Baur, 1997). This, therefore, appears to be
a feature related to the lipophilic pathway.
Effect of humidity
It would appear that water diffusion along lipophilic and
non-lipophilic pathways differs very strongly with regard
to its dependence on temperature and relative humidity of
the air. Diffusion of salts in pores shows very little temperature dependence compared with that of similar-sized
lipophilic molecules (Schönherr, 2006). The frequently
observed increase in cuticular permeability to water with
increasing air humidity (Hoad et al., 1997; Schreiber et al.,
2496 Kerstiens
2001; for a review of the older literature, see Kerstiens,
1996b) is much more plausibly explained by changes in the
degree of hydration of the polar groups giving rise to the
aqueous pores (Schönherr, 2006). These differences may
hold the clue to an experimental assessment of the relative
importance of the two pathways for cuticular transpiration
under different environmental conditions and in different
cuticles in the future. For instance, it would be interesting to
see whether (and by how much) the temperature dependence of P increases, and humidity dependence decreases,
after AgCl treatment, as one would expect if all our ideas
are correct.
Effect of temperature
A substantial body of data has been produced over the past
few years characterizing the temperature dependence of P
in more cuticles and under a wider range of conditions
(Knoche et al., 2000; Riederer and Schreiber, 2001;
Schreiber 2001, 2002; for a review of the older literature,
see Kerstiens, 1996b). In general, increasing temperature
reduces the amounts of any diffusants sorbed by the cuticle
but increases their mobility (cf. Kerstiens, 2006), with the
overall effect being positive in the case of water. The
temperature dependence of permeation is quantified by its
activation energy; the stronger the temperature dependence,
the higher is the activation energy. It is the sum of a positive
term (activation energy of diffusion) and a negative term
(enthalpy of sorption). If liquid water is present on the highconcentration side of the cuticle but no aqueous continuum
exists across the cuticle, a third term—the latent heat of
vaporization—adds to the overall energy required for
transport across the cuticle, as water molecules must sever
hydrogen bonds to break free from the liquid phase before
they can diffuse in the lipophilic environment of the cuticle.
When P is referenced to water vapour concentration in the
gas phase, the temperature dependence of the saturation
value in equilibrium with pure liquid water reflects the
influence of the latent heat of vaporization, and the
activation energy of permeation equals the sum of activation energy of diffusion and enthalpy of sorption as stated
above. However, when permeance is referenced to the
liquid phase (using water density rather than water vapour
concentration as the driving force), and water is present in
the liquid phase on one side of the cuticular membrane and
in the gas phase on the other, the apparent activation energy
of permeation should exceed the latent heat of vaporization
(Kerstiens, 1996b).
It is intriguing that in some experiments the activation
energy in cuticles from certain species was found to be well
below the latent heat of vaporization (Schreiber, 2001)—an
‘impossible’ result in the traditional view because it would
appear to imply that the sum of activation energy of
diffusion and enthalpy of sorption is negative. In those
experiments, the outside of the isolated cuticle faced a gas
phase saturated with water vapour (the receiver volume),
whereas the inside was in contact with liquid water (the
donor). While there was no gradient in chemical potential
of water across the cuticles, the liquid water was enriched
with tritiated water, and the accumulation of the tritiated
water molecules in the receiver volume was used to quantify
P. The concentration of tritiated water in the liquid phase
was used as the driving force. There were probably some
condensation droplets present on the outside of the cuticle,
and it can only be speculated at present that this might have
allowed some water to cross the cuticle in an aqueous continuum associated with a very low activation energy. One
could argue that those water molecules that traversed the
cuticle by diffusion in the lipophilic phase and ended up in
water droplets on the outside would also have regained
the energy required to separate them from the liquid phase of
the donor, and hence that the latent heat of vaporization
should not have contributed to the activation energy of
permeation. However, whether condensation heat released
on the outside of the cuticle would flow back into the donor
compartment to balance out the latent heat of vaporization
consumed, rather than being lost to the air in the receiver
compartment, seems doubtful. It would be interesting to test
whether the same ‘impossibly’ low temperature dependence
were still observed in a system where no droplets are present
on the outside of the cuticle, for example, when the air in the
receiver volume is unsaturated or droplets are made to slide
off through vibrating and tilting the chambers.
Role of epicuticular waxes
There are two quite common (and mutually exclusive)
misconceptions regarding intrinsic determinants of cuticular permeability: firstly, that thicker cuticles make better
transport barriers and, secondly, that ‘epicuticular’ and
overall ‘cuticular’ waxes—waxes being the actual agents
responsible for slowing down diffusion to the very low
values observed in cuticles—are interchangeable terms,
implying that the bulk of the diffusion resistance rests with
the epicuticular portion of the waxes. There are now three
sets of quantitative results of the relative importance of
epicuticular and intracuticular waxes for water transport
across the cuticle to put this view to the test.
Baur (1998) reported that stripping away epicuticular
waxes with a film of cellulose acetate formed after
evaporation of the solvent acetone did not significantly
affect P of leaf and fruit cuticles from 12 species. Using the
same stripping technique, Knoche et al. (2000) found that
removal of epicuticular waxes from cherry fruit raised P
by a factor of 3.6 and repeated extraction of cuticular
waxes with a 1:1 mixture of chloroform and methanol by
a factor of 49. Finally, Vogg et al. (2004), using the more
advanced stripping technique of applying gum arabic in
water, measured an increase in P of tomato fruit by a factor
of 2 after removal of epicuticular waxes and a factor of
10 after extraction of all cuticular waxes.
Water transport in plant cuticles
What may not be immediately apparent here is that, even
though the relative increase of P following wax extraction
was much greater than after stripping, by treating the
strippable epicuticular waxes and the rest of the underlying
cuticle (i.e. polymeric matrix and intracuticular waxes) as
two diffusion resistances in series (the resistance being
the inverse of P), it turns out that the resistance of the
epicuticular waxes (RECW) in cherries amounts to 72% of
the total cuticular resistance RCM (Knoche et al., 2000),
the corresponding value for tomatoes coming to 50%.
The general expression for the relationship is RECW/
RCM=(1ÿfÿ1), with f being the factor by which P is
increased after stripping epicuticular waxes. This analysis
demonstrates that even a quite small relative increase in
P after removal of epicuticular waxes may indicate a substantial contribution of this fraction of cuticular waxes to
the overall diffusion barrier properties. It appears unlikely
that this is produced by the wax crystallites visible by
scanning electron microscopy in many species, as diffusion
around these discrete structures in the air phase would be
fast. A visually ‘amorphous’ and continuous layer of
epicuticular waxes that may be difficult to observe seems
to be a better, but still somewhat speculative, candidate.
Quantification of cuticular water permeability of
stomatous plant surfaces
The inability properly to quantify cuticular water transport
in plant surfaces with stomata has for a long time placed
a very significant limitation on the selection of objects for
research. The traditional way to measure P when stomata
are present has been to use conditions that promote stomatal
closure (e.g. darkness or water deficit after leaf excision)
and measure water loss gravimetrically or by other means.
However, the assumption of complete stomatal closure is
always a highly uncertain one, and model calculations have
shown that even minuscule residual stomatal gaps in the
order of 0.1 lm are likely to cause transpirational losses of
a magnitude similar to that of typical cuticular transpiration rates (Kerstiens, 1996b, c). It is a very welcome
development that three new avenues of experimentation
have been opened up which allow P of stomata-bearing
surfaces to be estimated with a greater degree of reliability.
Schreiber and co-workers have shown that it is possible,
in principle, to quantify P via the measurement of cuticular
permeability to lipophilic substances of moderate water
solubility and low volatility by establishing an apparently
universal empirical relationship between the permeabilities to water and the test compound (Niederl et al.,
1998; Schreiber, 2002). This method is also applicable to
stomatous plant surfaces as discussed in some detail
elsewhere in this issue (Kerstiens et al., 2006). Knoche
et al. (2000, 2001) quantified P of cherry fruit by analysing
the linear regression between stomatal density and overall
2497
surface conductance to water and extrapolating the curve to
a stomatal density of zero. This simple method requires that
stomatal opening is constant, as is the case with the nonfunctional stomata in cherries. Finally, Santrucek et al.
(2004) measured water diffusion through isolated stomatous cuticles in artificial atmospheres of widely differing
diffusivities owing to different molecular masses of the
gases making up the bulk of the different atmospheres, and
used the dependence of diffusion through stomatal pores on
the diffusivity of water molecules in the atmosphere to
distinguish between stomatal and cuticular transport.
Values for P of abaxial stomatous leaf cuticles of Hedera
helix obtained with different methods were found to be in
good agreement with each other (Kerstiens et al., 2006).
The experiment by Santrucek et al. (2004) allows
a glimpse into another puzzle related to heterogeneity in
cuticular permeability, namely lateral heterogeneity at
cellular and subcellular scales. As mentioned above,
Schreiber and Riederer (1996) demonstrated a positive
correlation between the mobility of a lipophilic probe in
reconstituted cuticular waxes and P of cuticles (Fig. 1).
Intriguingly, the probe mobility was 2.6 times greater in
reconstituted waxes extracted from the adaxial leaf surface
of Hedera than in waxes extracted from the abaxial surface,
contrary to the pattern observed for P. The authors
tentatively suggested that this was due to much higher
permeability of relatively small areas of the abaxial surface
that contributed little to the wax load; the most likely
candidates for which being guard cells, based on findings
using histochemical methods (Schreiber, 2005; Schönherr,
2006). This could also explain the conundrum that cuticular transpiration seems to play a role in the response of
stomatal pores to changes in air humidity (more precisely,
the transpiration rate) even though ‘typical’ values of P, i.e.
ones determined with isolated astomatous cuticles, are so
low that mechanistic explanations have remained inconclusive (Kerstiens, 1996b, 1997).
This advance in methodology is of particular importance
to studies estimating the relative limitations of stomatal
transport and biochemical potential for photosynthesis
under conditions of low stomatal conductance, such as
drought. These estimates rely on calculations of leaf
internal concentration of CO2, and those in turn depend
on data for stomatal water loss and CO2 uptake. Cuticular
transpiration cannot automatically be assumed to be
negligible and may need to be deducted from total leaf
transpiration to obtain a sufficiently good estimate of
stomatal transpiration (Boyer et al., 1997; Meyer and
Genty, 1998; Flexas et al., 2002).
Outlook
A plethora of ecophysiologically relevant questions remains unresolved. To name a few: What drives wax
2498 Kerstiens
composition, in phylogenetic, ontogenetic, and environmental terms, and how does it relate to cuticular permeability? What is the temperature dependence of P in situ?
How large is lateral variability in P at the cellular and subcellular levels, and how does it affect stomatal behaviour?
Which factors are responsible for the huge differences in
permeability between cuticle types? The manipulation tools
provided by molecular biological studies hold much
promise, especially for resolving the mystery concerning
relationships of P with cuticular ultrastructure and chemical
composition. However, to date, advancements in this field
have been greatly hampered by the problem of quantifying
cuticular permeability in Arabidopsis and other species
typically used in these experiments (Kerstiens et al., 2006).
It remains to be seen whether this central problem holding
back cuticular research can be successfully overcome.
Acknowledgement
I would like to thank Jörg Schönherr for stimulating and critically
commenting on this article, and especially for teaching me how to
‘do Science’ in the first place.
References
Barnes JD, Cardoso-Vilhena J. 1996. Interactions between electromagnetic radiation and the plant cuticle. In: Kerstiens G, ed.
Plant cuticles: an integrated functional approach. Oxford: BIOS
Scientific Publishers, 157–174.
Baur P. 1997. Lognormal distribution of water permeability and
organic solute mobility in plant cuticles. Plant, Cell and Environment 20, 167–177.
Baur P. 1998. Mechanistic aspects of foliar penetration of
agrochemicals and the effect of adjuvants. Recent Research
Developments in Agricultural and Food Chemistry 2,
809–837.
Becker M, Kerstiens G, Schönherr J. 1986. Water permeability of
plant cuticles: permeance, diffusion and partition coefficients.
Trees 1, 54–60.
Beyer M, Peschel S, Weichert H, Knoche M. 2002. Studies on
water transport through the sweet cherry fruit surface. 7. Fe3+ and
Al3+ reduce conductance for water uptake. Journal of Agricultural
and Food Chemistry 50, 7600–7608.
Bird SM, Gray JE. 2003. Signals from the cuticle affect epidermal
cell differentiation. New Phytologist 157, 9–23.
Boyer JS, Wong SC, Farquhar GD. 1997. CO2 and water vapor
exchange across leaf cuticle (epidermis) at various water potentials. Plant Physiology 114, 185–191.
Buchholz A. 2006. Characterization of the diffusion of nonelectrolytes across plant cuticles: properties of the lipophilic
pathway. Journal of Experimental Botany 57, 2501–2513.
Buchholz A, Baur P, Schönherr J. 1998. Differences among plant
species in cuticular permeabilities and solute mobilities are not
caused by differential selectivities. Planta 206, 322–328.
Chassot C, Métraux JP. 2005. The cuticle as source of signals for
plant defense. Plant Biosystems 139, 28–31.
Flexas J, Bota J, Escalona JM, Sampol B, Medrano H. 2002.
Effects of drought on photosynthesis in grapevines under field
conditions: an evaluation of stomatal and mesophyll limitations.
Functional Plant Biology 29, 461–471.
Hoad S, Grace J, Jeffree C. 1997. Humidity response of cuticular
conductance of beech (Fagus sylvatica L.) leaf discs maintained at
high relative water content. Journal of Experimental Botany 48,
1969–1975.
Jackson DM, Danehower DA. 1996. Integrated case study:
Nicotiana leaf-surface components and their effects on insect
pests and diseases. In: Kerstiens G, ed. Plant cuticles: an
integrated functional approach. Oxford: BIOS Scientific Publishers, 231–254.
Kerstiens G. 1996a. Signalling across the divide: a wider perspective
of cuticular structure–function relationships. Trends in Plant
Science 1, 125–129.
Kerstiens G. 1996b. Cuticular water permeability and its physiological significance. Journal of Experimental Botany 47,
1813–1832.
Kerstiens G. 1996c. Diffusion of water vapour and gases across
cuticles and through stomatal pores presumed closed. In: Kerstiens
G, ed. Plant cuticles: an integrated functional approach. Oxford:
BIOS Scientific Publishers, 121–134.
Kerstiens G. 1997. In vivo manipulation of cuticular water
permeance and its effect on stomatal response to air humidity.
New Phytologist 137, 473–480.
Kerstiens G. 2006. Parametrization, comparison, and validation of
models quantifying relative change of cuticular permeability with
physicochemical properties of diffusants. Journal of Experimental
Botany 57, 2525–2533.
Kerstiens G, Schreiber L, Lendzian KJ. 2006. Quantification of
cuticular permeability in genetically modified plants. Journal of
Experimental Botany 57, 2547–2552.
Knoche M, Peschel S, Hinz M, Bukovac MJ. 2000. Studies on
water transport through the sweet cherry fruit surface: characterizing conductance of the cuticular membrane using pericarp
segments. Planta 212, 127–135.
Knoche M, Peschel S, Hinz M, Bukovac M. 2001. Studies on water
transport through the sweet cherry fruit surface. II. Conductance of
the cuticle in relation to fruit development. Planta 213, 927–936.
Meyer S, Genty B. 1998. Mapping intercellular CO2 mole fraction
(Ci) in Rosa rubiginosa leaves fed with abscisic acid by using
chlorophyll fluorescence imaging: significance of Ci estimated
from leaf gas exchange. Plant Physiology 116, 947–957.
Niederl S, Kirsch T, Riederer M, Schreiber L. 1998. Copermeability of 3H-labeled water and 14C-labeled organic acids
across isolated plant cuticles. Plant Physiology 116, 117–123.
Riederer M, Schreiber L. 2001. Protecting against water loss:
analysis of the barrier properties of plant cuticles. Journal of
Experimental Botany 52, 2023–2032.
Santrucek J, Simanova E, Karbulkova J, Simkova M, Schreiber L.
2004. A new technique for measurement of water permeability of
stomatous cuticular membranes isolated from Hedera helix leaves.
Journal of Experimental Botany 55, 1411–1422.
Schlegel TK, Schönherr J, Schreiber L. 2005. Size selectivity of
aqueous pores in stomatous cuticles of Vicia faba leaves. Planta
221, 648–655.
Schönherr J. 2000. Calcium chloride penetrates plant cuticles via
aqueous pores. Planta 212, 112–118.
Schönherr J. 2006. Characterization of aqueous pores in plant
cuticles and permeation of ionic solutes. Journal of Experimental
Botany 57, 2471–2491.
Schönherr J, Schreiber L. 2004. Size selectivity of aqueous pores in
astomatous cuticular membranes isolated from Populus canescens
(Aiton) Sm. leaves. Planta 219, 405–411.
Schreiber L, Skrabs M, Hartmann KD, Diamantopoulos P,
Simanova E, Santrucek J. 2001. Effect of humidity on cuticular
water permeability of isolated cuticular membranes and leaf disks.
Planta 214, 274–282.
Water transport in plant cuticles
Schreiber L. 2001. Effect of temperature on cuticular transpiration of
isolated cuticular membranes and leaf discs. Journal of Experimental Botany 52, 1893–1900.
Schreiber L. 2002. Co-permeability of 3H-labelled water and 14Clabelled organic acids across isolated Prunus laurocerasus cuticles: effect of temperature on cuticular paths of diffusion. Plant,
Cell and Environment 25, 1087–1094.
Schreiber L. 2005. Polar paths of diffusion across plant cuticles: new
evidence for an old hypothesis. Annals of Botany 95, 1069–1073.
Schreiber L, Elshatshat S, Koch K, Lin J, Santrucek J. 2006.
AgCl precipitates in isolated cuticular membranes reduce rates of
cuticular transpiration. Planta 223, 283–290.
Schreiber L, Riederer M. 1996. Determination of diffusion
coefficients of octadecanoic acid in isolated cuticular waxes and
2499
their relationship to cuticular water permeabilities. Plant, Cell and
Environment 19, 1075–1082.
Vogg G, Fischer S, Leide J, Emmanuel E, Jetter R, Levy AA,
Riederer M. 2004. Tomato fruit cuticular waxes and their effects
on transpiration barrier properties: functional characterization of
a mutant deficient in a very-long-chain fatty acid b-ketoacyl-CoA
synthase. Journal of Experimental Botany 55, 1401–1410.
Weichert H, von Jagemann C, Peschel S, Knoche M, Neumann D,
Erfurth W. 2004. Studies on water transport through the sweet
cherry fruit surface. VIII. Effect of selected cations on water uptake
and fruit cracking. Journal of the American Society for Horticultural Science 129, 781–788.
Wijmans JG, Baker RW. 1995. The solution-diffusion model:
a review. Journal of Membrane Science 107, 1–21.