Physiol. Plant. 40: 255-260. 1977
CELL SIZE AND WATER RELATIONS
255
The Importance of Cell Size in the Water Relations of Plants
By
J. M. CUTLER, D. W. RAINS and R. S. LOOMIS
Department of Agronomy & Range Science, University of California, Davis, CA 95616, U.S.A.
(Received 30 November, 1976; revised 25 March, 1977)
Abstract
Several structural changes in cotton {Gossypium hirsutum L.)
leaves attendant on development under conditions of water deficit
were examined. Cell size was less and cell wall thickness greater in
the leaves of stressed plants than in leaves of well-watered plants. A
short review of the literature suggested that the lesser cell size is a
fairly general observation and that it may contribute to plant
resistance to moisture stress.
A simple model is developed to investigate the influence of the
reduction of cell size on cellular water relations. The predictions
which can be drawn from simulations with this model are that
snjialler cells should maintain turgor to lower values of water
potential than larger cells. Rather large changes in cell water
relations are predicted for small changes in cell size. These effects
are related principally to the changing proportion of cell water
which resides in the cell wall and is external to the plasmalemma
and the osmotic adjustment system. This prediction is in agreement
with several observerations on the behavior of stress-hardened
plants and supports the hypothesis that plants or tissues with the
smaller cell size will be more tolerant of low water potential.
Introduction
Early studies of drought resistance in plants largely
emphasized the structural, anatomical, and ecological
characteristics of plants adapted to conditions of aridity
(Maximov 1929). Most recent studies on drought tolerance,
on the other hand, have emphasized physiological adaptations (Henckel 1964, Hsiao 1973) and few efforts have
been directed towards integrating the structural and functional aspects of this problem.
It has long been known that many plants, when subjected
to conditions of water sti^ess during development, exhibit a
reduced sensitivity to subsequent drought; the phenomenon
of "hardening" (Levitt 1972). It is of interest to examine
whether structural alterations in response to water deficits
might play a role in the reduced sensitivity of hardened
plants. In this paper, experimental evidence for structural
alterations in plant leaves in response to water deficits is
reviewed and some of their possible implications to drought
resistance and hardening are evaluated. Emphasis is given to
the influences of cell size on solute and turgor potentials.
Abbreviatiotis: V, water potential
turgor potential; i//^, matric potential.
osmotic potential;
Materials and Methods
This paper is devoted largely to the development of a
conceptual and mathematical model by which the sensitivity
of cellular water relations to changes in cell structure is
examined. This model is supplemented with critical data
gathered in the following way.
Plant tnaterials. Upper, recently expanded, fully exposed
leaves of field-grown cotton {Gossypium hirsutum L.) were
excised at 1500 h on 20 July, 1976, 111 days after planting
at the University of California Westside Eield Sation. The
leaves, after excision, were sealed into plastic bags and
refrigerated until measurements were made.
Plants from two treatments, differentiated by the frequency of irrigation, were chosen for comparison. The dry
treatment received a preirrigation only, and plants were
severely stunted at the time of sampling. The wet treatment
had received a preirrigation and three subsequent irrigations
at the time of sampling and had a normal appearance. No
significant rainfall fell during the growth period.
Measuretnents. Fifteen individual cells chosen at random
in each of ten microscope fields were examined and
measured in fresh peeled strips of the lower epidermis of 15
leaves from each treatment. Cell length, cell wall thickness,
and cell density were determined with a calibrated optical
micrometer at a magnification of 256 or 640. Leaf area was
determined with a photoelectric leaf area meter and leaf dry
weight was measured after drying to constant weight in a
forced-draft oven at 70°C. The differences between treatments was analyzed by a t-test and differences stated to be
significant were statistically significant at the 5% confidence
level.
256
J, M, CUTLER, D, W, RAINS AND R, S, LOOMIS
Turgor Maintenance
Physiol, Plant, 40,
Table 1, The effect of irrigation frequency on weight and dimensional characteristics of cotton leaves and the structure of the lower
epidermis of these leaves. Numbers followed by * in the dry
treatment are significantly different (at the 5% level) from
corresponding values in the wet treatment. The thickness of the
walls was determined by measuring the distance between the
plasmalemma of two adjacent cells and dividing by two.
One important aspect of drought hardiness in plants is the
ability to maintain cell turgor in spite of tissue water deficits.
Adequate turgor is known to be critical for the elongative
growth of plant cells, providing the internal "push" for
expansive growth (Cleland 1971, Hsiao 1973), Adequate
turgor is also critical for the asymmetric swelling of guard
Treatment
A
cells which causes stomata to open and allows for gas
exchange (Raschke 1975), In most plants, turgor decreases
Wet
Characteristic
Dry
very rapidly as plant water deficits develop (Hsiao and
77,6
64,0*
Acevedo 1974) and cell elongation and stomatal opening are Area/leaf, cm^
Dry wt/leaf, g
0,26
0,29
inhibited with only small levels of water deficits (Hsiao
Area/dry weight, cmVg
298,5
237,0*
1973), Drought-hardy plants, however, appear to maintain
Lower epidermis
V/p and turgor-mediated processes despite reductions in tissue
Cell length, //m
37,1
32,0*
Cell density, mm~^
727
924*
water content or water potential (Cutler and Rains 1977),
Cell wall thickness, //m
0,68
0,76*
Several mechanisms have been hypothesized to allow for
the maintenance of i//p in plants subjected to water deficits:
decreases in vacuolar osmotic potential through the ac- to severe water deficits was 69% less than that of wellcumulation of solutes; high cell wall elasticity allowing the watered control plants, Tumanow (Ordin 1966) observed
cells to shrink in response to water loss; and, as water is lost, that the density of cells of the lower epidermis of Helianthus
decreases in matric potential according to the nature and annuus was 28 to 51% greater in plants subjected to periodic
quantity of protoplasmic and cell wall matrix (Weatherley wilting than in controls, Ashby (1948), in an extensive study
on several species of Ipotnoea, found that the density of cells
1966, Noy-Meir and Ginzburg 1969),
Good evidence is now available for osmotic adjustment in of the adaxial epidermis was 5 to 42% greater in the leaves of
leaves in response to water deficits in corn and sorghum plants subject to water deficits than in well-watered controls.
(Hsiao et al. 1976) and in cotton (Brown et al. 1976, Cutler Morton and Watson (1948) observed 9 to 22% greater
and Rains 1976), Cell wall elasticity as a factor in drought palisade cell density in stressed leaves of Beta vulgaris and
adaptation has not been directly evaluated although dif- McCree and Davis (1974) found an 18 to 20% lesser planar
ferences in elasticity have been hypothesized to account for area of upper epidermal cells of Sorghum bicolor subject to
the different drought sensitivity of corn and sorghum water deficits in comparison with well-watered controls. As
(Sanchez-Diaz and Kramer 1971), The results of several illustrated in Table 1, we found in the field that the length of
investigators suggest that the infiuence of v^m '^ negligible cells of the lower epidermis of stressed cotton leaves was
until much of the tissue water is lost (Wiebe 1966, Boyer 11% less than in plants receiving normal irrigation.
Despite the generally held view that the cell walls are
1967), It is of interest to examine how structural alterations
attendant on water stress might infiuence these cellular level thickened in plants subjected to water stress (Maximov 1929,
Shields 1950, Stocker 1960) there is a paucity of quantitative
adaptations.
data on the effects of water stress on the quantity, thickness,
and mechanical properties of cell walls, Schloesing (MacStructural Changes
Dougal and Spoehr 1918) found that the cellulose content on
Morphological and anatomical alterations, often a dry weight basis of the leaves of stressed tobacco plants
xeromorphic in character, are commonly observed in plants was 62% greater than in moist controls. However, Rippel
which develop under conditions of water stress (Maximov (Stocker 1960) found a reverse trend for the leaves of
1929, Stocker 1960), Leaf structure is especially plastic to Sinapis alba. Effects of water stress on the cell walls of
water deficiency, exhibiting decreases in epidermal and structural and conducting elements of plants have been
mesophyll cell size, increases in cell wall thickness, increases observed (Penfound 1931, Barss 1930), and such effects may
in length of veins, and the number of stomates per unit leaf confound interpretation of bulk leaf analyses. As illustrated
area, increases in cutinization, and increases in the number of in Table 1, walls of cells of the lower epidermis of leaves of
layers of palisade parenchyma (Shields 1950), Of particular stressed cotton plants were 12% thicker than those of
interest are those changes which might contribute to altered normally irrigated plants.
cellular water relations — the decreases in cell size and
increases in cell wall thickness,
Implications of Structural Changes to Internal Water
A reduction in cell size is one of the most general
Relations
anatomical observations with leaves which develop under
Information on the compartmentation of water in the
water stress (Henckel 1964), Rippel (Stocker 1960) found
that the area of leaf epidermal cells of Sinapis alba subjected various cellular phases (cell wall, protoplast, and vacuole) is
Physiol, Plant, 40, 1977
CELL SIZE AND WATER RELATIONS
scant and controversial (Weatherley 1966), Since the
vacuole and cytoplasm constitutes the primary osmotically
active portions of the cells, it is critical to estimate the
fraction of the total cell water in these cellular compartments. Crafts et al. (1949) suggested that determination
of the volume of each cellular phase would give a rough
indication of the partition of water. That method would
presumably result in little error for the vacuole but is more
questionable with the cell wall and cytoplasmic compartments.
Estimates of the fraction of cell water held in the cell walls
vary with the technique of measurement (Weatherley 1966),
and dramatically with the species, Boyer (1967) found with
three species that the estimated fractional volume of water
outside the protoplast ranged from 0,75 to 0,93 of the cell
wall volume, Slatyer (1967) suggests that the volumetric
water content of cell walls may fall below 0,5 where substantial amounts of non-cellulosic materials are included in
the wall. Gaff and Carr (1967) estimated that 40% of the
total cell water of leaves of Eucalyptus globusus was
confined in the wall volume at turgidity while Boyer's (1967)
estimates were that wall volume equalled 9% (sunfiower) to
26% (Rhodadendron) of total cell water volume.
To estimate the effect which alterations in leaf structure
might have on the water relations of leaves we have
constructed a simple model. We first examined the effect of
cell size and cell wall thickness on the fraction of total cell
volume occupied by the cell wall (w/v). If one assumes
spherical geometry and uniform cell wall thickness, then:
Wall volume = w = 4n(,3R^t-iRl^ + t^)/3
Cell volume = y =
- 2Rt
Here I is the thickness of the cell wall and R is the radius of
the cell to the middle lamella. The total diameter of the cell
will then be 2R. Spherical geometry represents the most conservative case since w/v (for a given volume) is minimized in
this instance. For any case, we may now define the cellular
osmotic volume as o = v — w. The ratio w/v is plotted as a
function of total cell length and wall thickness in Figure 1,
It is clear that cell geometry, cell size, and cell wall
thickness can all significantly affect the fractional volume of
the cell wall. As cell size decreases or wall thickness
increases, the wall constitutes a larger fraction of the total
cell volume. Deviations from spherical shape (volume held
constant) will also increase the fractional volume of wall.
One would thus suspect that the cells of leaves developed
under conditions of water deficits would have a larger w/v,
and this is the case for cotton leaves (assuming spherical
geometry, uniform wall thickness, and uniform response to
stress) as indicated by the points in Figure 1 for leaves from
the wet and dry treatments. Even larger changes would be
expected in species which show a greater sensitivity of cell
water deficits than does cotton.
257
UJ
0.16 - ^ \ > ^ ^
DRV
UJ
u
2
o
0.14 -
^
WET
'0.8^Jm
U] O.IZ
3
0.10 -
• ~
0,7 pm
SPHERICAL
0,6p.
0,08
30
1
1
1
32
34
36
TOTAL CELL LENGTH
38
40
Figure 1, The effects of cell length and cell wall thickness (t) on the
ratio of cell wall volume to total cell volutne. The points indicated as
"Dry" and "Wet" correspond to values computed for leaves of
cotton plants.
In our assumption of o = u — w, we still must deal with
one further issue in partitioning, namely the relative role of
organelle space. The vacuole is clearly principally solution
volume and is largely pure osmotic space. Mitochondria and
other organelles have significant volume occupied by solid
structures (e,^,, proteins and lipids) and these agents may
contribute to adsorptive water binding (/,e,, to some matric
potential). The actual solid volume of the cytoplasmic
constituents is here considered to be negligible. In considering osmotic relations, we then need to establish what fraction
of the osmotic volume is involved in solution relations, A
variety of evidence suggests that the matric potentials of a
variety of biocoUoidal and plant materials are quite small
until their water content is reduced to levels much lower than
normally experienced by plants (Wiebe 1966, Boyer 1967),
Hence, we feel justified in neglecting this component of water
potential and will consider the entire volume internal to the
cell wall as the cellular osmotic volume,
A similar problem exists with the capacity of the cell wall
to absorb and hold water. As a first approximation, we
assume that the wall phase will contain a fraction of cell
water in proportion to its relative volume. In real plants, solid
material is a significant fraction of the wall volume, and
changes in wall composition and structure affect the capacity
of this volume to hold water. In Figure 2, the effects of cell
size and the capacity of the wall to absorb water on cell
osmotic volume are illustrated. In this analysis, we have
assumed, in addition to the previous assumptions, that the
osmotic volume of the cell is equal to the fraction of cell
water internal to the cell wall.
Two hypotheses, illustrating the sensitivity of osmotic
volume to the absorption capacity of the wall are illustrated
in Figure 2: 1) the wall contains a fraction of total cell water
that is equal to its relative volume (1/1); 2) the wall contains
a fraction of total cell water that is equal to half its relative
258
J, M, CUTLER, D, W, RAINS AND R, S, LOOMIS
Physiol, Plant, 40, 19 77
of 40 //m to 0,64 x 10^'" mmol/cell at 30 ftm (decreasing
content); 3) the case where cellular solute content increases
linearly from 1,27 x 10"'° mmol/cell at a diameter of 40 fuxi
to 2,54 X 10~'° mmol/cell at a diameter of 30 fim (increasing
content); and 4) a case where cellular solute content
decreases with cell volume as estimated with our data from
real plants.
For case 4), cell solute index is calculated for hardened
and unhardened leaves with the following equation:
30
32
34
36
TOTAL CELL LENGTH
38
Figure 2, The effect of cell length and two hypotheses concerning
the capacity of the eell wall to absorb water on the osmotic volume
of a cell. The cases where the wall contains a fraction of total cell
water equal to, respectively half of its relative volume are shown by
the curves labelled 1/1 and 1/2,
volume (1/2), As can be seen, the capacity of the cell wall to
absorb water can affect the cellular osmotic volume, A 100%
increase (1/2 to 1/1) in the wall absorption capacity will
decrease the calculated osmotic volume about 6% for cells
40 fim in diameter and about 9% for cells 30 ftm in diameter.
The infiuence of wall absorptive capacity on the cellular
osmotic volume is small relative to the dominating infiuence
of cell size but may be significant. To simplify comparisons
in the subsequent calculations, we have used the 1/1 wall
absorption ratio.
We can now procede to examine the infiuence of w/v
partitioning on the osmotic potential of plant cells. The
purpose is to consider the extent to which osmotic
adjustments may be dependent on cell size. The osmotic
potential may be established from the Van't Hoff approximation in terms ofv — w:
nRT
where n is the number of moles of osmotically active solutes
in the cell osmotic volume, R the gas constant, T the absolute
temperature (here assumed to be 278 °K), and y — w the
cellular osmotic volume.
In order to investigate the influence of cell size on cellular
osmotic potential, we must first make some deductions or
assumptions about the content of solutes per cell. In Figure
3A, we have presented the relationship between cell solute
concentration and cell diameter and illustrated the sensitivity
of this to several hypotheses conceming the solute content
per cell. These hypotheses represent: 1) the case where cell
solute content is constant at 1,27 x 10"'" mmol/cell
(constant content); 2) the case where cell solute content
decreases linearly from 1,27 x 10"'° mmol/cell at a diameter
solute content
solute content
cell
dry weight
dry weight
cell
In a previous study (Cutler 1976), we found that leaves of
hardened and unhardened cotton plants had essentially the
same solute concentration (of the major solutes) on a dry
weight basis and we have thus reasoned that changes in the
solute content/cell are likely to be dominated by changes in
the dry weight/cell term. The effect of moisture history may
be estimated from the data and the calculations presented in
Table 2, In Table 2, relative cell density is calculated as the
relative volumetric density of cells of the two treatments
assuming all space is occupied by cells (no intercellular
spaces). The relative dry weight per cell is calculated by
dividing the dry weight per leaf by the respective relative cell
densities. By assuming that all the tissue volume is filled with
cells, we overestimate the cell density and hence underestimate the dry weight/cell.
As illustrated in Table 2, the relative dry weight per cell is
about 27% less in the leaves of the dry treatment than in
leaves of the wet treatment. If we assume that dry weight/cell
is a linear function of cell volume, we arrive at the equation
for the regression for data (Table 2) gathered for the two
treatments
Dry weight/cell (g) = 0,029 -\- 8,64 x 10"'* x (v - w)
If we then assume a constant solute content per unit dry
weight of 3,13 x lO"'" mmol/g, the solute content/cell may
be described by the equation:
Solute content/celli(mmol) =
-i
3,13 X lO-'o X 0,029 + 8,64 x lO""* x (y - w)
The results of computations for all four cases are
illustrated in Figure 3A, It is clear from this figure that cell
size can dramatically infiuence the cellular concentration of
solutes. The infiuence will depend, in large part on the effect
of stress hardening on the solute content/cell and can range
from a difference of 23 to 390% between cells of diameter 40
^m and 30 fim for the "decreasing content" and "increasing
content" hypothesis respectively. The curve based on the cell
solute index predicts a 56% greater cellular solute concentration in cells 30 fim in diameter than in cells 40 ^m in
diameter. It is an easy step then to predict the infiuence of
cell size on cellular osmotic potential.
In Figure 3B, the effects of cell size and the same
hypotheses on the cell osmotic potential are illustrated. In
this figure, we have assumed the validity of the Van't Hoff
CELL SIZE AND WATER RELATIONS
Physiol, Plant, 40, 1977
259
2.0
INCREASING
CONTENT
cc
ca
O
a
o
<
UJ
u
(5
10
32
34
36
38
TOTAL CELL LENGTH pm
40
30
DECREASING /
CONTENT
32
34
36
38
40
TOTAL CELL LENGTH
Figure 3, The effect of celt length and several hypotheses concernitig the effect of hardening stress on the cell solute content (dry wt, basis)
on (a) the concentration of solutes in the vacuole and on (b) the ostnotic potential of the cell. Further explanation is provided in the text.
Table 2, The effect of irrigation frequency on the calculated cell
volume, calculated relative cell density, and calculated relative dry
weight per cell of the lower epidermis of cotton leaves. Further
explanation provided in text.
Treatment
Characteristic
Leaf dry weight, g
Cell volume, lOVm'
Relative cell density
Relative dry weight/cell
Wet
Dry
0,26
2,67
1
0,26
0,29
1,86
1,44
0,19
equation and the explicit assumptions of the previous
arguments. It is clear that cell size can have a dramatic effect
on cellular osmotic potential. The effect is strongly influenced
by the assumptions regarding solute content/cell and points
to this relationship as a key to our understanding of the
infiuence of structural changes on hardening. The cell index
curve predicts that the osmotic potential of a 30 fan cell
would be about 5 bars less than that of a 40 fim cell, a
difference likely to be significant to the leaf in terms of turgor
maintenance.
Weatherley (1966) reasoned that a cell with lower osmotic
potential could maintain turgor and turgor-mediated processes to lower values of water potential than a cell with a
higher osmotic potential. We have observed that the leaves of
hardened cotton plants continue growth and maintain open
stomata to lower values of water potential than unhardened
plants (Cutler and Rains 1977), Brown et al. (1976) have
observed that the leaves of prestressed cotton plants
maintained open stomata to lower values of water potential
and had a lower osmotic potential than leaves on plants not
previously stressed, Simmelsgaard (1976) has made similar
observations on wheat.
Our conclusion is that such differences can be mediated
simply by the smaller cell size of hardened leaves. The idea
that cell size can affect the internal water relations and
responses to water deficits of plants is not a new one, Iljin
(1957) and others have found that cell size and an
organism's ability to survive drought are inversely correlated,
Iljin proposed that this might be explained by a lower
susceptibility of small-celled tissues to mechanical damage
on dehydration and attendant shrinkage. The observation
might equally well be explained by a lower osmotic potential
of small cells as we have deduced, although the capacity to
260
J, M, CUTLER, D, W, RAINS AND R, S, LOOMIS
accumulate solutes can affect this dramatically, A recent
publication by Steudle and co-workers (1977) has discussed
the relationship between cell size, turgor pressure and wall
elasticity. They suggest that smaller cells require less turgor
to achieve their growth potential than do larger cells and that
much more turgor pressure is necessary to stretch the cell
wall to initiate extension growth in the larger cells. They did
not discuss these observations in terms of drought tolerance
or hardening although the implications are clear.
This concept may be extended to comparison of different
tissues within the same plant. Numerous data cited in
Maximov (1929) suggest that the youngest leaves of plants
show the least susceptibility to damage from water stress, an
observation which might be explained by the smaller cell size
of young leaves. Similarly, the ability of meristematic tissues
to continue somewhat normal activity despite severe water
deficits which greatly reduce activity in more mature
tissues, might be explained by the small size of meristematic
cells.
Conclusions
Haldane (1956), in an essay on the size of organisms,
suggested that there is an optimum size for an organism
which depends on its mode of life and environment. Every
student of ecology is aware of the importance of size in
influencing the nature and magnitude of heat exchange,
gaseous and liquid diffusion, mechanical support, and a
multitude of other life-influencing processes.
In this paper we have investigated some of the effects of
size on the volumetric and water relations of plant cells. We
came to the conclusion that the commonly observed
reduction in cell size attendant on development under
conditions of water stress may, of itself, be advantageous in
terms of permitting a lower cellular osmotic potential, and
hence increased capacity for turgor maintenance. Several
assumptions explicit in this" paper are yet to be thoroughly
tested, and generalization of the conclusions will require
further accumulation of experimental data. It is clear,
however, that lesser cell size can be advantageous to plants
under conditions creating water deficits and that it may
provide an explanation for the different behavior of hardened
and non-hardened plants, small and large-celled plants of
different species, and small and large-celled tissues within the
same plant.
Contribution from the Department of Agronomy and Range
Science, V.C. Davis, CA 95616, Supported in part by a USDA
grant (CSRS 316-15-36),
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