Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol15.1995:
Tree Physiology 15, 379--385
© 1995 Heron Publishing----Victoria, Canada
Offsetting effects of reduced root hydraulic conductivity and osmotic
adjustment following drought
M. RIEGER
Department of Horticulture, University of Georgia, Athens, GA 30602, USA
Received February 28, 1994
Summary Root hydraulic conductivity (Lp) and leaf osmotic
potential at full turgor (Ψπ,o) were measured in young, droughtstressed and nonstressed peach (Prunus persica (L.) Batsch),
olive (Olea europaea L.), citrumelo (Poncirus trifoliata Raf. ×
Citrus paradisi Macf.) and pistachio (Pistachia integerrima
L.). Drought stress caused a 2.5- to 4.2-fold reduction in Lp,
depending on species, but Ψπ,o was reduced only in citrumelo
and olive leaves by 0.34 and 1.4 MPa, respectively. No differences existed in Lp among species for nonstressed plants. A
simple model linking Lp to osmotic adjustment through leaf
water potential (Ψ) quantified the offsetting effects of reduced
Lp and osmotic adjustment on the hypothetical turgor pressure
difference between drought-stressed and nonstressed plants
(∆Ψp). For olive, the 2.5-fold reduction in Lp caused a linear
decrease in ∆Ψp such that the effect of osmotic adjustment was
totally negated at Ψ = −3.2 MPa. Thus, no stomatal closure
would be required to maintain higher turgor in drought-stressed
olive plants than in nonstressed plants over their typical diurnal
range of Ψ (−0.6 to −2.0 MPa). For citrumelo, osmotic adjustment was offset by reduced Lp at Ψ ≈ −0.9 MPa. Unlike olive,
stomatal closure would be necessary to maintain higher turgor
in drought-stressed citrumelo plants than in nonstressed plants
over their typical diurnal range of Ψ (0 to −1.5 MPa). Regardless of species or the magnitude of osmotic adjustment, my
analysis suggests that a drought-induced reduction in Lp reduces or eliminates turgor maintenance through osmotic adjustment.
Key words: citrumelo, leaf osmotic potential, Olea europaea,
olive, peach, pistachio, Pistacia integerrima, Poncirus trifoliata × Citrus paradisi, Prunus persica, stomatal closure, turgor,
water relations.
Introduction
Drought stress produces a variety of changes in the physiological behavior of plants. Responses such as stomatal closure and
osmotic adjustment have been documented in leaves of many
tree crops (Jones et al. 1985). Less is known about the effects
of drought on roots, although parameters such as root hydraulic conductivity (Lp) are important in determining leaf water
potential (Ψ) at a given rate of transpiration (Weatherley
1982). Most studies have focused on organ-specific responses
to drought, whereas interactions among factors affecting plant
water relations are less frequently considered. For example, if
drought stress results in reduced leaf conductance (g) and
osmotic adjustment, then leaf turgor pressure (Ψp) may be
increased. Simultaneously, drought stress may reduce Lp (Nobel and Huang 1992), potentially causing reductions in Ψ and
Ψp depending on the extent to which changes in Lp, osmotic
potential and g offset each other. Because Ψp is the driving
force for cell expansion and ultimately the growth of plant
organs (Cosgrove 1984), understanding the interaction among
factors that affect turgor maintenance is important.
I examined the interaction of drought-induced changes in Lp,
leaf osmotic potential (Ψπ) and g in four economically important tree crops: olive, peach, pistachio and citrumelo. Peach
and olive represent the extremes in drought tolerance seen in
tree crops: peach is native to humid, temperate regions, and
olive is native to arid, Mediterranean regions. Larsen et al.
(1989) showed that olive tolerates lower water potentials than
peach. Furthermore, olive has been cultivated for centuries in
Mediterranean countries without irrigation on sites that would
not support other tree crops (Romano 1977). Pistachio is native
to the same region as olive and can be grown without irrigation
in arid climates, provided that rainfall is at least 300--450 mm
per year (Duke 1989). Olive is probably more tolerant than
pistachio because it is grown commercially in Northern Africa,
where only 200--300 mm of rain falls each year (Romano
1977), and olive tolerates lower predawn and midday Ψ than
Pistacia species in Mediterranean climates (Duhme and
Hinckley 1992). Citrus requires irrigation and often wind protection for economic production in dry climates that support
olive or pistachio production (Chandler 1950). However, citrus
trees can survive leaf water potentials of −5 MPa (Fereres et al.
1979), whereas peach trees die after reaching −3 MPa
(Proebsting and Middleton 1980). Thus, these crops may be
ranked from most to least drought tolerant as olive > pistachio
> citrumelo > peach.
Based on preliminary findings that drought stress causes a
reduction in Lp and Ψπ, I developed a data set and a simple
analytical model to test the hypothesis that drought-stressed
plants maintain higher turgor pressure through osmotic adjustment than nonstressed plants, given that the stressed plants
must generate lower Ψ to maintain water uptake at reduced Lp.
380
RIEGER
Materials and methods
Plant material
Commonly used rootstocks for peach, olive, pistachio and
citrus were chosen: ‘Nemaguard’ peach (Prunus persica (L.)
Batsch), ‘Manzanillo’ olive (Olea europaea L.), Pistacia integerrima L., and ‘Swingle’ citrumelo (Poncirus trifoliata Raf.
× Citrus paradisi Macf.), respectively. Olives were grown from
rooted cuttings, but other species were propagated from seed.
Plants were grown in 15-cm diameter pots containing coarse
sand and fertilized with a soluble fertilizer. Coarse sand was
used because it provided good drainage and facilitated accurate root length measurements. Plants were 6--12 months old
when data were collected in September--October 1992. Greenhouse conditions varied with season, with minimum temperatures of ≈ 15 °C in winter and maxima of ≈ 35 °C in summer.
Integrated daily solar radiation was about 70% of outdoor
values.
Experimental design
Twenty or more plants of each species were arranged randomly
on two greenhouse benches. On August 29, 1992, plants of
each species were divided into a nonstressed control group and
a drought-stressed group. Nonstressed plants were irrigated
every other day to run-off with 200--300 ml of water or nutrient
solution. Drought-stressed plants received limited irrigation
over a 25- to 45-day period according to the following scheme.
Containers of drought-stressed plants were placed in pans that
retained 90 ± 10 ml of water. Plants were examined daily for
visible wilting or leaf cupping, and occasionally the appearance of the roots was observed by inverting the plant and
removing the container. Plants exhibiting wilting, leaf cupping
or root shrinkage had their pans filled; the water was rapidly
absorbed by the medium. Roots in the upper portion of the
containers of drought-stressed plants were exposed continuously to dry soil because subirrigation rewetted the lower half
of the medium only. Drought-stressed plants required irrigation at intervals of 3 to 12 days; the period between irrigations
varied with species, leaf area per container and weather conditions. Average weekly irrigation rates for drought-stressed
plants were: olive = 64 ± 12 ml, pistachio = 107 ± 29 ml,
citrumelo = 198 ± 59 ml, and peach = 128 ± 17 ml. Periodic
measurements of Ψ (pressure chamber, PMS Instruments, Corvallis, OR) and g (LI-1600 steady-state porometer, Li-Cor Inc.,
Lincoln, NE) quantified the extent of the drought stress imposed during a drying cycle. Average midday Ψ was −1.5 to
−1.9 MPa in drought-stressed plants before irrigation, whereas
the Ψ of nonstressed plants was − 0.6 to − 0.9 MPa. Leaf
conductance of wilted plants during the drought-stress period
was highly variable, but generally 2- to 10-fold lower than that
of nonstressed plants (200--400 mmol m −2 s −1).
Measurements
Root hydraulic conductivity (Lp) and the minimum Ψ gradient
required for water flow into roots (hereafter referred to as
‘‘intercept’’) were estimated on six intact plants per species per
drought-stress treatment by the technique of Rieger and Motisi
(1990). Briefly, plants were brought to the laboratory and
watered thoroughly the night before measurement. The canopy
of each plant was enclosed in its own 42-l gas exchange
chamber with the container and one basal side shoot left
outside the chamber. Chamber conditions were: PAR ≥ 1000
µmol m −2 s −1, VPD = 2.0 ± 0.2 kPa, temperature = 27 ± 2 °C,
and [CO2] = 350 ± 10 µl l −1. The container was placed in 1 cm
of distilled water to ensure that the soil water potential was
nearly zero. Leaves on the basal shoot outside the chamber
were wrapped in parafilm and foil, and allowed to equilibrate
with the water potential of the stem base. The water potential
gradient across the root system was assumed equal in magnitude, but opposite in sign, to the water potential of the wrapped
leaf at steady state. Total water flow through the plant was
measured by pumping chamber air through a desiccant column
at a rate that maintained a constant dewpoint. After steady
values of transpiration and Ψ were obtained, the lights were
turned off, and the VPD was reduced to < 1.0 kPa to induce a
lower flow through the plant. A regression equation was developed for water potential gradient (y) versus water flow on a
root length basis (x) from the two points obtained for each
plant, assuming linearity (Rieger and Motisi 1990). The y-intercept of the regression gives the minimum gradient required
for flow through the root system (Passioura and Munns 1984,
Rieger and Motisi 1990), and the reciprocal of the slope gives
Lp (in g H2O h −1 MPa −1 m −1).
Because Lp measurements were time consuming, data were
collected over a 20-day period. The measurement sequence
was blocked by replication to enable comparisons among
species and between stress treatments despite variations imposed by time of drought exposure. Regression analysis determined the effects of time of drought exposure on Lp and
intercept.
Leaf conductance was calculated from transpiration and
vapor pressure gradient data under the conditions given above
on whole plant canopies during Lp measurement. Boundary
layer conductance and leaf temperature were measured as
described by Rieger and Motisi (1990). Length of living roots
≤ 2 mm in diameter was estimated by the line intersect method
of Tennant (1975).
Osmotic potentials at full hydration (Ψπ,o) of mature and
expanding leaves were measured on October 1, 1992, 33 days
after drought stress was imposed. Two mature and two expanding leaves were removed from each of five plants in each
species × stress treatment combination just after sunrise.
Leaves, which were wrapped in parafilm and aluminum foil
with only the petiole protruding, were placed on ice and
transported to the laboratory. The samples were placed in
beakers, with enough distilled water to cover the exposed
petiole, and stored at 4 °C overnight to become fully hydrated.
Samples were then incubated at − 80 °C to destroy membranes
and eliminate turgor, and Ψπ,o was then measured with a
thermocouple psychrometer (SCA-10, Decagon Devices, Pullman, WA). Standard NaCl solutions with Ψπ of −1.0, −2.0 and
− 3.0 MPa were used to generate a regression that converted µV
output to Ψπ in MPa. No correction was made for the dilution
of symplastic water by mixing with apoplastic water after
MODELING ROOT HYDRAULIC CONDUCTANCE AND OSMOTIC POTENTIAL
freezing, so the Ψπ,o values reported here are probably overestimates for living cells. The dilution effect was assumed to be
similar between drought-stressed and nonstressed samples.
Several samples of mature, drought-stressed olive leaves gave
erroneously low values of Ψπ,o (i.e., −6.0 to − 20.0 MPa),
presumably because of insufficient rehydration or desiccation
during storage; these data were omitted. A t-test was used to
separate means between stress treatments within a species.
Analysis of offsetting effects
The flow of water through plants at steady state (Jv) can be
approximated by:
Jv = L ∆Ψ,
(1)
where ∆Ψ is the water potential gradient between the root
surface and the evaporating sites of the leaves. The L in Equation 1 represents whole-plant hydraulic conductance, but for
simplicity, I will assume that L = Lp because most of the
resistance to flow in plants resides within the root system
(Kramer 1983, Rieger 1989). Assuming soil water potential
approaches zero, ∆Ψ becomes simply −Ψleaf , because Ψ at the
root surface should be negligible when plants are rooted in
moist soil. The comparison between previously droughtstressed and nonstressed plants was made assuming a favorable soil water status. Although the relationship between Jv and
−Ψleaf was linear, it did not go through the origin (Rieger and
Motisi 1990):
−1
Ψ = Jv + intercept ,
Lp
(2)
and rearranging,
Jv = −Lp(Ψ − intercept ),
(3)
Setting Jv equal in previously drought-stressed and nonstressed plants (denoted by subscripts s and n, respectively):
−Lp,n(Ψ n − intercept n ) = −Lp,s (Ψs − intercept s),
(4)
and solving for Ψs:
Lp,n
Ψs = (Ψn − interceptn)
+ intercept s ,
Lp,s
(5)
allows calculation of Ψs relative to Ψn as a function of the
change in root water uptake characteristics following drought.
Drought stress often causes a reduction in stomatal opening
that persists after rewatering (e.g., Fereres et al. 1979, Tan and
Buttery 1982). This would reduce Jv,s and, in turn, increase Ψs.
To consider unequal rates of water flow in drought-stressed
and nonstressed plants, the left-hand side of Equation 4 can be
multiplied by Jv,s /Jv,n to give a modification of Equation 5 on
rearrangement:
Lp,n Jv,s
Ψ s = (Ψn − interceptn)
+ intercept s .
Lp,s Jv,n
381
(6)
This equation considers the interaction of reduced g with
changes in Lp. If drought stress reduces Jv,s (by stomatal closure) and Lp,s by proportionately the same amount, then Equation 6 predicts that drought-stressed and nonstressed plants
will have the same Ψ, provided that any change in intercept is
proportional to the change in Lp.
The effects of osmotic adjustment on Ψp and Ψ were calculated by means of a mathematical description of leaf pressure-volume (PV) curves (Cheung et al. 1976). The BASIC code for
this program is available from the author.
Several simplifying assumptions were made to permit the
analysis. First, the relationship between the bulk modulus of
elasticity (ε) and Ψp was assumed to be asymptotic, equivalent
to the ‘‘Type II’’ response of ε to Ψp given in Roberts et al.
(1981) and to theoretical relationships presented by Cheung et
al. (1976). A search of available literature on the four species
used here found the ε versus Ψp relationship documented for
peach only (Andersen and Brodbeck 1988), where a linear
(‘‘Type I’’ of Roberts et al. 1981) relationship for expanding
leaves and a curvilinear (‘‘Type II’’) response for expanded
leaves were observed. Second, a maximum value of ε of 20
MPa (εmax) was assumed based on data for peach (Andersen
and Brodbeck 1988) and apple (Jones et al. 1985). Third, the
exponential coefficient relating ε to Ψp (β) was estimated as
− 2.25, which allowed ε to approach within ≈ 10% of εmax at a
Ψp of 1.0 MPa; this was derived by inspection of curves
presented in Jones et al. (1985) and Cheung et al. (1976).
Fourth, an apoplastic water content of 30% of relative water
content (RWC) was used, which was a compromise between
values of 40% (Santakumari and Berkowitz 1989) and 15-20% (Hardegree 1989) obtained for drought-stressed spinach
leaves, and close to the value of 31% obtained for droughtstressed orange leaves (Fereres et al. 1979). Fifth, the slope of
the linear portion of the PV curve (RWC versus Ψπ−1) was
calculated assuming that Ψπ−1 approaches zero when the RWC
reaches 30% (i.e., Ψπ approaches infinity when the symplastic
water content reaches zero), and Ψπ−1 at 100% RWC equaled
the reciprocal of Ψπ,o measurements for each species. The Lp
and intercept values used in the model were obtained from
actual measurements. The turgor loss point was simply the
RWC or Ψ where Ψp reached zero, obtained by inspection of
the program output.
The program was run assuming relative flow rates (Jv,s/Jv,n)
of 0.2, 0.4, 0.6, 0.8 and 1.0. The Ψs required to maintain each
relative flow was calculated by Equation 6, and values of Ψp at
the respective Ψ in drought-stressed and nonstressed plants
were calculated from separate runs of the model with corresponding parameters. The difference in turgor pressure between drought-stressed and nonstressed plants (∆Ψp = Ψp,s −
Ψp,n) was calculated and plotted versus Ψs to examine the range
of Ψs over which ∆Ψp was positive.
382
RIEGER
Results and discussion
Influence of drought stress on Lp, Ψπ,o and g
There were no significant effects of time of drought exposure
on Lp or intercept for any species during the 20-day measurement period (data not shown). Lack of correlation of Lp with
time suggests that the drought-induced change in Lp occurred
within 25 days of withholding water.
Drought stress caused a 2.5- to 4.2-fold reduction in Lp,
depending on species, but reduced intercept for citrumelo only
(Table 1). In nonstressed plants, values of Lp were not significantly different among species, but drought-stressed olive
plants had significantly higher Lp than drought-stressed peach
or pistachio plants. Whether differences in Lp among droughtstressed plants were due to genetic variation in drought response or to differing levels of drought stress experienced by
each species is unclear. Although all plants reached similar
minimum values of Ψ before rewatering, olive used water
more slowly than the other species, and as a result, probably
had a more favorable soil water status overall. The decrease in
Lp in response to drought in whole root systems of intact plants
was similar to the response of Lp to drought obtained with
excised roots of desert succulents (Nobel and Huang 1992).
Similar Lp values among nonstressed plants that differ
widely in drought adaptation support previous work with
Prunus where it was found that Lp could not be used to
discriminate drought tolerance (Rieger and Duemmel 1992).
Table 1. Root hydraulic conductivity (Lp), the minimum water potential required for flow (intercept), and leaf conductance (g) for previously drought-stressed and nonstressed ‘Swingle’ citrumelo,
‘Nemaguard’ peach, ‘Manzanillo’ olive and Pistacia integerrima seedlings following a 25- to 45-day drought period. All measurements
were made 12 to 24 h after rewatering drought-stressed plants.
Treatment
Peach
Unstressed
Stressed
P > F2
Citrumelo
Unstressed
Stressed
P>F
Olive
Unstressed
Stressed
P>F
Pistachio
Unstressed
Stressed
P>F
1
2
Lp
(g m − 1 h − 1 MPa −1)
Intercept
(MPa)
g
(mmol m − 2 s−1)
0.217 a1
0.052 b
0.0219
−0.32 b
−0.33 a
0.9151
107
60
0.0607
0.196 a
0.076 ab
0.0089
−0.43 b
−0.65 b
0.0213
106
61
0.0606
0.246 a
0.100 a
0.0371
−0.20 a
−0.33 a
0.1332
61
36
0.0732
0.144 a
0.034 b
0.0499
−0.31 ab
−0.23 a
0.6303
65
58
0.7802
The lack of variation among species and the apparent sensitivity of Lp to soil drying suggest that the environment modulates
Lp to a greater extent than genetics in tree crops.
After rewatering, leaf conductance was not significantly
affected by previous drought stress in any of the species (Table 1). Reduced g after rewatering drought-stressed peach and
citrumelo trees has been reported (Fereres et al. 1979, Tan and
Buttery 1982); however, the severity of drought-stress imposed
in this study (Ψmin ≈ − 2.0 MPa) was less than that imposed in
previous studies (Ψmin ≈ −3.0 to −5.0 MPa).
Osmotic adjustment occurred only in mature leaves of citrumelo and expanding leaves of olive (Table 2). The difference
in Ψπ,o between drought-stressed and nonstressed plants was
greater in olive than in citrumelo, i.e., 1.4 versus 0.34 MPa,
respectively. Generally, olive leaves had lower Ψπ,o values than
those of other species, and citrumelo leaves had the highest
Ψπ,o values regardless of stress treatment or leaf type. The
values of Ψπ,o reported here agree closely with those reported
by others for olive, citrus and peach (Abdel-Rahman and
El-Sharkawi 1974, Syvertsen et al. 1981, Rieger 1992). Values
of Ψπ,o for P. integerrima were 0.5 to 1.0 MPa higher than
osmotic potentials at the turgor loss point reported for Pistacia
terebinthus L. (Duhme and Hinckley 1992). The magnitude of
osmotic adjustment found for citrumelo (0.34 MPa) agrees
with previous reports for tree crops (Jones et al. 1985) and
herbaceous crops (Morgan 1984), and the magnitude of adjustment found for olive (1.4 MPa) was comparable to the seasonal
Table 2. Osmotic potential at full hydration (Ψπ,o) of mature and
expanding leaves of drought-stressed and nonstressed ‘Swingle’ citrumelo, ‘Nemaguard’ peach, ‘Manzanillo’ olive and Pistacia integerrima seedlings 33 days after imposing drought-stress treatments.
Leaf type
Peach
Mature
Expanding
Citrumelo
Mature
Expanding
Olive
Mature
Expanding
Pistachio
Mature
Expanding
Means followed by the same letter are not significantly different
from those of other species within a stress treatment; Duncan’s
multiple range test, 5% level.
Significance of the comparison of means between stress treatments
within a species.
1
Treatment
Ψπ,o (MPa)
Significance1
Unstressed
Stressed
Unstressed
Stressed
−2.95
−2.86
−2.72
−2.33
0.6399
Unstressed
Stressed
Unstressed
Stressed
−1.50
−1.84
−1.95
−2.11
Unstressed
Stressed
Unstressed
Stressed
−3.46
-−2.82
−4.25
--
Unstressed
Stressed
Unstressed
Stressed
−2.71
−2.41
−2.78
−3.02
0.3126
0.0639
0.0034
0.3972
0.0067
0.1826
Probability of a greater F value for the comparison of means between drought-stressed and nonstressed plants within the same species and leaf type classes.
MODELING ROOT HYDRAULIC CONDUCTANCE AND OSMOTIC POTENTIAL
change in Ψπ,o reported by Duhme and Hinckley (1992).
A relative ranking of sensitivity to drought stress among the
three parameters measured in this study arises from the data.
In all species, Lp was reduced, yet Ψπ,o was reduced in only two
of the four species, and g (post-stress) was not significantly
reduced for any species. If the changes in g were significant,
the percent reductions would rank 60--76% for Lp, 23--50% for
Ψπ,o, and 11--44% for g. This is important in the subsequent
analysis because a decrease in Lp would be expected if osmotic
adjustment occurred in response to drought.
Analysis of offsetting effects of reduced Lp and osmotic
adjustment
Turgor pressures calculated by the model were sensitive to εmax
(data not shown). For example, a 50% reduction in εmax yielded
a 97% reduction in Ψ at the turgor loss point. In contrast, the
model was relatively insensitive to changes in β and apoplastic
water content (50% change in these parameters produced < 2%
change in Ψ at the turgor loss point). As εmax was not measured
in this study, the quantities presented here are realistic only if
there is close agreement between the assumed and actual εmax
values; however, the qualitative nature of the relationships
described below was conserved at all values of εmax.
The output from the PV curve model compared favorably to
published pressure--volume data. Values of Ψπ,o and Ψπ at the
turgor loss point for olive growing in Beskonak, Turkey, were
Figure 1. The difference in turgor pressure (∆Ψp) between previously
drought-stressed and nonstressed leaves of citrumelo plotted as a
function of water potential of previously drought-stressed leaves (Ψs).
The line labeled ‘‘OA only’’ (osmotic adjustment only) shows the
relationship when Ψ of drought-stressed and nonstressed leaves is the
same, and Lp and intercept are not reduced in stressed plants, i.e., the
effect of osmotic adjustment alone. Line labels 1.0 through 0.2 indicate the relative flow rate of water in drought-stressed plants versus
nonstressed plants (Jv,s /Jv,n); this simulates the effect of stomatal
closure. The ‘‘intercept’’ (indicated by the dotted vertical line) is the
maximum water potential that previously stressed citrumelo plants
achieved when flow was zero and the soil was saturated with water.
383
− 2.98 and −3.57 MPa, respectively (Hinckley et al. 1980); the
corresponding values from the model were −2.8 and −3.66
MPa, respectively. Also, data of Hinckley et al. (1980) show
the turgor loss point at a RWC of about 77% for olive; the RWC
at turgor loss from the model was 80%. Andersen and Brodbeck (1988) published Ψπ,o and Ψπ values at the turgor loss
point of −2.1 and −2.7 MPa, respectively, for expanded peach
leaves, and −1.7 and − 2.0 MPa, respectively, for expanding
peach leaves. Using their Ψπ,o data, the model predicted a Ψπ
value at turgor loss of −2.74 MPa (1.5% error) for expanded
peach leaves, and − 2.14 MPa (7.0% error) for expanding peach
leaves. Abrams (1988) compiled Ψπ,o and Ψπ values at the
turgor loss point from 37 North American tree species. Using
his values of Ψπ,o for seven broad-leaved trees as input, the
model predicted the corresponding Ψπ at the turgor loss point
with an average error of 11%.
The offsetting effects of decreased Lp and osmotic adjustment are illustrated using data for citrumelo and olive (Figures 1 and 2). The relationships in Figures 1 and 2 do not
extend to 0 MPa along the x-axis because both species have
nonzero intercepts (Table 1), i.e., zero flow occurred at
nonzero water potentials. For citrumelo, when water flow is
the same for drought-stressed and nonstressed plants, droughtstressed plants maintained higher Ψp than nonstressed plants
at Ψs values from −0.65 to ≈ − 0.9 MPa (following line for
relative flow = 1.0 in Figure 1). At Ψs < − 0.9 MPa, droughtstressed plants would have lower Ψp than nonstressed plants,
Figure 2. Relationships between ∆Ψp and Ψs for olive. The line
labeled ‘‘OA only’’ (osmotic adjustment only) shows the relationship
when Ψ of drought-stressed and nonstressed leaves is the same, and
Lp and intercept are not reduced in stressed plants, i.e., the effect of
osmotic adjustment alone. Line labels 1.0 through 0.2 indicate the
relative flow rate of water in drought-stressed plants versus nonstressed plants (Jv,s/Jv,n ); this simulates the effect of stomatal closure.
The ‘‘intercept’’ (indicated by the dotted vertical line) is the maximum
water potential that previously stressed olive plants achieved when
flow was zero and the soil was saturated with water.
384
RIEGER
because the decrease in Lp would more than offset the decrease
in Ψπ,o in terms of turgor maintenance. As flow is reduced by
stomatal closure (relative flows of 0.8 to 0.2), the range of Ψs
over which a turgor advantage is maintained in droughtstressed plants increases, such that when ∆Ψp = 0, Ψs is moved
progressively toward the turgor loss point of Ψs = −2.3 MPa.
The line marked ‘‘OA only’’ in Figure 1 illustrates the effect
of osmotic adjustment on ∆Ψp without a change in Lp or
intercept. Along this line, the Ψ values of drought-stressed and
nonstressed plants are equal, and osmotic adjustment confers
a turgor advantage at all Ψs values down to the turgor loss
point. The difference between the ‘‘OA only’’ line and lines
representing relative flows of 1.0, 0.8, 0.6 or 0.4 at any given
Ψs therefore represents the offsetting effect of reduced Lp and
intercept on osmotic adjustment. When relative flow in
drought-stressed plants is reduced to 20% of that in nonstressed plants, the turgor advantage produced by osmotic
adjustment increases above the ‘‘OA only’’ line. This results
from the combined effects of two turgor-maintaining processes
(stomatal closure and osmotic adjustment) over-compensating
for the turgor-reducing effect of low Lp. Hence, ∆Ψp is greater
than would be predicted from inspection of the change in Ψπ,o
when the relative flow falls below about 0.4.
The analysis suggests that partial stomatal closure must
accompany osmotic adjustment if a turgor advantage is to be
maintained in drought-stressed citrumelo plants through their
reported diurnal range of Ψ (0 to −1.5 MPa, Syvertsen et al.
1981). Because flow would have to be reduced by 40 to 60%
in drought-stressed plants to allow Ψ to reach −1.5 MPa
(Figure 1), a reduction in CO2 assimilation may also be expected. The reduction in g of ≈ 40% due to drought stress,
although not statistically significant (P > 0.05) for citrumelo
(Table 1), would not have reduced flow to the extent necessary
to allow ∆Ψp to remain positive at all expected values of Ψs.
In olive, the response of ∆Ψp to Ψs was similar to that of
citrumelo (Figure 2). However, in the absence of stomatal
closure, the large decrease in Ψπ,o would offset the 2.5-fold
decline in Lp at all Ψs values above ≈ −3.0 MPa (see Figure 2
where relative flow = 1.0). Thus, unlike citrumelo, the turgor
advantage due to osmotic adjustment would likely be maintained in olive throughout the diurnal range of Ψ (−0.6 to−2.0
MPa, Larsen et al. 1989). However, this magnitude of osmotic
adjustment (1.4 MPa) is uncharacteristically high for tree species and serves to illustrate an extreme rather than a typical
case.
One factor not considered in this analysis is reduced axial
conductance in the xylem due to cavitation and embolism
during moderate drought stress (Tyree and Sperry 1988). The
assumption was made that whole-plant hydraulic conductivity,
L, was equal to Lp, when in reality, L also includes stem
conductivity. A reduction in stem conductivity would reduce
the turgor advantage due to osmotic adjustment even more than
predicted here. Therefore, the amount of stomatal closure
required to counter-balance the reduction in plant conductivity
would be greater than that shown in Figures 1 and 2.
I conclude that the turgor advantage conferred by osmotic
adjustment is reduced by decreased Lp following drought
stress. Because Lp is more sensitive to drought than Ψπ,o, the
effect of osmotic adjustment on turgor maintenance is less than
that estimated from pressure--volume analyses alone. The
adaptive value of osmotic adjustment has also been questioned
by others (see Munns 1988), because evidence suggests that
growth must decrease for osmotic adjustment to occur. Although Ψp drives cell expansion and growth, cell wall properties such as yield threshold and extensibility may change in
response to drought to negate an increase in Ψp (Van Volkenburgh and Cleland 1984). Thus, the translation of osmotic
adjustment into increased growth or physiological function is
at best limited by Lp reduction, and at worst unobtainable as a
result of reduced Lp combined with other negative impacts of
drought stress.
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© 1995 Heron Publishing----Victoria, Canada
Offsetting effects of reduced root hydraulic conductivity and osmotic
adjustment following drought
M. RIEGER
Department of Horticulture, University of Georgia, Athens, GA 30602, USA
Received February 28, 1994
Summary Root hydraulic conductivity (Lp) and leaf osmotic
potential at full turgor (Ψπ,o) were measured in young, droughtstressed and nonstressed peach (Prunus persica (L.) Batsch),
olive (Olea europaea L.), citrumelo (Poncirus trifoliata Raf. ×
Citrus paradisi Macf.) and pistachio (Pistachia integerrima
L.). Drought stress caused a 2.5- to 4.2-fold reduction in Lp,
depending on species, but Ψπ,o was reduced only in citrumelo
and olive leaves by 0.34 and 1.4 MPa, respectively. No differences existed in Lp among species for nonstressed plants. A
simple model linking Lp to osmotic adjustment through leaf
water potential (Ψ) quantified the offsetting effects of reduced
Lp and osmotic adjustment on the hypothetical turgor pressure
difference between drought-stressed and nonstressed plants
(∆Ψp). For olive, the 2.5-fold reduction in Lp caused a linear
decrease in ∆Ψp such that the effect of osmotic adjustment was
totally negated at Ψ = −3.2 MPa. Thus, no stomatal closure
would be required to maintain higher turgor in drought-stressed
olive plants than in nonstressed plants over their typical diurnal
range of Ψ (−0.6 to −2.0 MPa). For citrumelo, osmotic adjustment was offset by reduced Lp at Ψ ≈ −0.9 MPa. Unlike olive,
stomatal closure would be necessary to maintain higher turgor
in drought-stressed citrumelo plants than in nonstressed plants
over their typical diurnal range of Ψ (0 to −1.5 MPa). Regardless of species or the magnitude of osmotic adjustment, my
analysis suggests that a drought-induced reduction in Lp reduces or eliminates turgor maintenance through osmotic adjustment.
Key words: citrumelo, leaf osmotic potential, Olea europaea,
olive, peach, pistachio, Pistacia integerrima, Poncirus trifoliata × Citrus paradisi, Prunus persica, stomatal closure, turgor,
water relations.
Introduction
Drought stress produces a variety of changes in the physiological behavior of plants. Responses such as stomatal closure and
osmotic adjustment have been documented in leaves of many
tree crops (Jones et al. 1985). Less is known about the effects
of drought on roots, although parameters such as root hydraulic conductivity (Lp) are important in determining leaf water
potential (Ψ) at a given rate of transpiration (Weatherley
1982). Most studies have focused on organ-specific responses
to drought, whereas interactions among factors affecting plant
water relations are less frequently considered. For example, if
drought stress results in reduced leaf conductance (g) and
osmotic adjustment, then leaf turgor pressure (Ψp) may be
increased. Simultaneously, drought stress may reduce Lp (Nobel and Huang 1992), potentially causing reductions in Ψ and
Ψp depending on the extent to which changes in Lp, osmotic
potential and g offset each other. Because Ψp is the driving
force for cell expansion and ultimately the growth of plant
organs (Cosgrove 1984), understanding the interaction among
factors that affect turgor maintenance is important.
I examined the interaction of drought-induced changes in Lp,
leaf osmotic potential (Ψπ) and g in four economically important tree crops: olive, peach, pistachio and citrumelo. Peach
and olive represent the extremes in drought tolerance seen in
tree crops: peach is native to humid, temperate regions, and
olive is native to arid, Mediterranean regions. Larsen et al.
(1989) showed that olive tolerates lower water potentials than
peach. Furthermore, olive has been cultivated for centuries in
Mediterranean countries without irrigation on sites that would
not support other tree crops (Romano 1977). Pistachio is native
to the same region as olive and can be grown without irrigation
in arid climates, provided that rainfall is at least 300--450 mm
per year (Duke 1989). Olive is probably more tolerant than
pistachio because it is grown commercially in Northern Africa,
where only 200--300 mm of rain falls each year (Romano
1977), and olive tolerates lower predawn and midday Ψ than
Pistacia species in Mediterranean climates (Duhme and
Hinckley 1992). Citrus requires irrigation and often wind protection for economic production in dry climates that support
olive or pistachio production (Chandler 1950). However, citrus
trees can survive leaf water potentials of −5 MPa (Fereres et al.
1979), whereas peach trees die after reaching −3 MPa
(Proebsting and Middleton 1980). Thus, these crops may be
ranked from most to least drought tolerant as olive > pistachio
> citrumelo > peach.
Based on preliminary findings that drought stress causes a
reduction in Lp and Ψπ, I developed a data set and a simple
analytical model to test the hypothesis that drought-stressed
plants maintain higher turgor pressure through osmotic adjustment than nonstressed plants, given that the stressed plants
must generate lower Ψ to maintain water uptake at reduced Lp.
380
RIEGER
Materials and methods
Plant material
Commonly used rootstocks for peach, olive, pistachio and
citrus were chosen: ‘Nemaguard’ peach (Prunus persica (L.)
Batsch), ‘Manzanillo’ olive (Olea europaea L.), Pistacia integerrima L., and ‘Swingle’ citrumelo (Poncirus trifoliata Raf.
× Citrus paradisi Macf.), respectively. Olives were grown from
rooted cuttings, but other species were propagated from seed.
Plants were grown in 15-cm diameter pots containing coarse
sand and fertilized with a soluble fertilizer. Coarse sand was
used because it provided good drainage and facilitated accurate root length measurements. Plants were 6--12 months old
when data were collected in September--October 1992. Greenhouse conditions varied with season, with minimum temperatures of ≈ 15 °C in winter and maxima of ≈ 35 °C in summer.
Integrated daily solar radiation was about 70% of outdoor
values.
Experimental design
Twenty or more plants of each species were arranged randomly
on two greenhouse benches. On August 29, 1992, plants of
each species were divided into a nonstressed control group and
a drought-stressed group. Nonstressed plants were irrigated
every other day to run-off with 200--300 ml of water or nutrient
solution. Drought-stressed plants received limited irrigation
over a 25- to 45-day period according to the following scheme.
Containers of drought-stressed plants were placed in pans that
retained 90 ± 10 ml of water. Plants were examined daily for
visible wilting or leaf cupping, and occasionally the appearance of the roots was observed by inverting the plant and
removing the container. Plants exhibiting wilting, leaf cupping
or root shrinkage had their pans filled; the water was rapidly
absorbed by the medium. Roots in the upper portion of the
containers of drought-stressed plants were exposed continuously to dry soil because subirrigation rewetted the lower half
of the medium only. Drought-stressed plants required irrigation at intervals of 3 to 12 days; the period between irrigations
varied with species, leaf area per container and weather conditions. Average weekly irrigation rates for drought-stressed
plants were: olive = 64 ± 12 ml, pistachio = 107 ± 29 ml,
citrumelo = 198 ± 59 ml, and peach = 128 ± 17 ml. Periodic
measurements of Ψ (pressure chamber, PMS Instruments, Corvallis, OR) and g (LI-1600 steady-state porometer, Li-Cor Inc.,
Lincoln, NE) quantified the extent of the drought stress imposed during a drying cycle. Average midday Ψ was −1.5 to
−1.9 MPa in drought-stressed plants before irrigation, whereas
the Ψ of nonstressed plants was − 0.6 to − 0.9 MPa. Leaf
conductance of wilted plants during the drought-stress period
was highly variable, but generally 2- to 10-fold lower than that
of nonstressed plants (200--400 mmol m −2 s −1).
Measurements
Root hydraulic conductivity (Lp) and the minimum Ψ gradient
required for water flow into roots (hereafter referred to as
‘‘intercept’’) were estimated on six intact plants per species per
drought-stress treatment by the technique of Rieger and Motisi
(1990). Briefly, plants were brought to the laboratory and
watered thoroughly the night before measurement. The canopy
of each plant was enclosed in its own 42-l gas exchange
chamber with the container and one basal side shoot left
outside the chamber. Chamber conditions were: PAR ≥ 1000
µmol m −2 s −1, VPD = 2.0 ± 0.2 kPa, temperature = 27 ± 2 °C,
and [CO2] = 350 ± 10 µl l −1. The container was placed in 1 cm
of distilled water to ensure that the soil water potential was
nearly zero. Leaves on the basal shoot outside the chamber
were wrapped in parafilm and foil, and allowed to equilibrate
with the water potential of the stem base. The water potential
gradient across the root system was assumed equal in magnitude, but opposite in sign, to the water potential of the wrapped
leaf at steady state. Total water flow through the plant was
measured by pumping chamber air through a desiccant column
at a rate that maintained a constant dewpoint. After steady
values of transpiration and Ψ were obtained, the lights were
turned off, and the VPD was reduced to < 1.0 kPa to induce a
lower flow through the plant. A regression equation was developed for water potential gradient (y) versus water flow on a
root length basis (x) from the two points obtained for each
plant, assuming linearity (Rieger and Motisi 1990). The y-intercept of the regression gives the minimum gradient required
for flow through the root system (Passioura and Munns 1984,
Rieger and Motisi 1990), and the reciprocal of the slope gives
Lp (in g H2O h −1 MPa −1 m −1).
Because Lp measurements were time consuming, data were
collected over a 20-day period. The measurement sequence
was blocked by replication to enable comparisons among
species and between stress treatments despite variations imposed by time of drought exposure. Regression analysis determined the effects of time of drought exposure on Lp and
intercept.
Leaf conductance was calculated from transpiration and
vapor pressure gradient data under the conditions given above
on whole plant canopies during Lp measurement. Boundary
layer conductance and leaf temperature were measured as
described by Rieger and Motisi (1990). Length of living roots
≤ 2 mm in diameter was estimated by the line intersect method
of Tennant (1975).
Osmotic potentials at full hydration (Ψπ,o) of mature and
expanding leaves were measured on October 1, 1992, 33 days
after drought stress was imposed. Two mature and two expanding leaves were removed from each of five plants in each
species × stress treatment combination just after sunrise.
Leaves, which were wrapped in parafilm and aluminum foil
with only the petiole protruding, were placed on ice and
transported to the laboratory. The samples were placed in
beakers, with enough distilled water to cover the exposed
petiole, and stored at 4 °C overnight to become fully hydrated.
Samples were then incubated at − 80 °C to destroy membranes
and eliminate turgor, and Ψπ,o was then measured with a
thermocouple psychrometer (SCA-10, Decagon Devices, Pullman, WA). Standard NaCl solutions with Ψπ of −1.0, −2.0 and
− 3.0 MPa were used to generate a regression that converted µV
output to Ψπ in MPa. No correction was made for the dilution
of symplastic water by mixing with apoplastic water after
MODELING ROOT HYDRAULIC CONDUCTANCE AND OSMOTIC POTENTIAL
freezing, so the Ψπ,o values reported here are probably overestimates for living cells. The dilution effect was assumed to be
similar between drought-stressed and nonstressed samples.
Several samples of mature, drought-stressed olive leaves gave
erroneously low values of Ψπ,o (i.e., −6.0 to − 20.0 MPa),
presumably because of insufficient rehydration or desiccation
during storage; these data were omitted. A t-test was used to
separate means between stress treatments within a species.
Analysis of offsetting effects
The flow of water through plants at steady state (Jv) can be
approximated by:
Jv = L ∆Ψ,
(1)
where ∆Ψ is the water potential gradient between the root
surface and the evaporating sites of the leaves. The L in Equation 1 represents whole-plant hydraulic conductance, but for
simplicity, I will assume that L = Lp because most of the
resistance to flow in plants resides within the root system
(Kramer 1983, Rieger 1989). Assuming soil water potential
approaches zero, ∆Ψ becomes simply −Ψleaf , because Ψ at the
root surface should be negligible when plants are rooted in
moist soil. The comparison between previously droughtstressed and nonstressed plants was made assuming a favorable soil water status. Although the relationship between Jv and
−Ψleaf was linear, it did not go through the origin (Rieger and
Motisi 1990):
−1
Ψ = Jv + intercept ,
Lp
(2)
and rearranging,
Jv = −Lp(Ψ − intercept ),
(3)
Setting Jv equal in previously drought-stressed and nonstressed plants (denoted by subscripts s and n, respectively):
−Lp,n(Ψ n − intercept n ) = −Lp,s (Ψs − intercept s),
(4)
and solving for Ψs:
Lp,n
Ψs = (Ψn − interceptn)
+ intercept s ,
Lp,s
(5)
allows calculation of Ψs relative to Ψn as a function of the
change in root water uptake characteristics following drought.
Drought stress often causes a reduction in stomatal opening
that persists after rewatering (e.g., Fereres et al. 1979, Tan and
Buttery 1982). This would reduce Jv,s and, in turn, increase Ψs.
To consider unequal rates of water flow in drought-stressed
and nonstressed plants, the left-hand side of Equation 4 can be
multiplied by Jv,s /Jv,n to give a modification of Equation 5 on
rearrangement:
Lp,n Jv,s
Ψ s = (Ψn − interceptn)
+ intercept s .
Lp,s Jv,n
381
(6)
This equation considers the interaction of reduced g with
changes in Lp. If drought stress reduces Jv,s (by stomatal closure) and Lp,s by proportionately the same amount, then Equation 6 predicts that drought-stressed and nonstressed plants
will have the same Ψ, provided that any change in intercept is
proportional to the change in Lp.
The effects of osmotic adjustment on Ψp and Ψ were calculated by means of a mathematical description of leaf pressure-volume (PV) curves (Cheung et al. 1976). The BASIC code for
this program is available from the author.
Several simplifying assumptions were made to permit the
analysis. First, the relationship between the bulk modulus of
elasticity (ε) and Ψp was assumed to be asymptotic, equivalent
to the ‘‘Type II’’ response of ε to Ψp given in Roberts et al.
(1981) and to theoretical relationships presented by Cheung et
al. (1976). A search of available literature on the four species
used here found the ε versus Ψp relationship documented for
peach only (Andersen and Brodbeck 1988), where a linear
(‘‘Type I’’ of Roberts et al. 1981) relationship for expanding
leaves and a curvilinear (‘‘Type II’’) response for expanded
leaves were observed. Second, a maximum value of ε of 20
MPa (εmax) was assumed based on data for peach (Andersen
and Brodbeck 1988) and apple (Jones et al. 1985). Third, the
exponential coefficient relating ε to Ψp (β) was estimated as
− 2.25, which allowed ε to approach within ≈ 10% of εmax at a
Ψp of 1.0 MPa; this was derived by inspection of curves
presented in Jones et al. (1985) and Cheung et al. (1976).
Fourth, an apoplastic water content of 30% of relative water
content (RWC) was used, which was a compromise between
values of 40% (Santakumari and Berkowitz 1989) and 15-20% (Hardegree 1989) obtained for drought-stressed spinach
leaves, and close to the value of 31% obtained for droughtstressed orange leaves (Fereres et al. 1979). Fifth, the slope of
the linear portion of the PV curve (RWC versus Ψπ−1) was
calculated assuming that Ψπ−1 approaches zero when the RWC
reaches 30% (i.e., Ψπ approaches infinity when the symplastic
water content reaches zero), and Ψπ−1 at 100% RWC equaled
the reciprocal of Ψπ,o measurements for each species. The Lp
and intercept values used in the model were obtained from
actual measurements. The turgor loss point was simply the
RWC or Ψ where Ψp reached zero, obtained by inspection of
the program output.
The program was run assuming relative flow rates (Jv,s/Jv,n)
of 0.2, 0.4, 0.6, 0.8 and 1.0. The Ψs required to maintain each
relative flow was calculated by Equation 6, and values of Ψp at
the respective Ψ in drought-stressed and nonstressed plants
were calculated from separate runs of the model with corresponding parameters. The difference in turgor pressure between drought-stressed and nonstressed plants (∆Ψp = Ψp,s −
Ψp,n) was calculated and plotted versus Ψs to examine the range
of Ψs over which ∆Ψp was positive.
382
RIEGER
Results and discussion
Influence of drought stress on Lp, Ψπ,o and g
There were no significant effects of time of drought exposure
on Lp or intercept for any species during the 20-day measurement period (data not shown). Lack of correlation of Lp with
time suggests that the drought-induced change in Lp occurred
within 25 days of withholding water.
Drought stress caused a 2.5- to 4.2-fold reduction in Lp,
depending on species, but reduced intercept for citrumelo only
(Table 1). In nonstressed plants, values of Lp were not significantly different among species, but drought-stressed olive
plants had significantly higher Lp than drought-stressed peach
or pistachio plants. Whether differences in Lp among droughtstressed plants were due to genetic variation in drought response or to differing levels of drought stress experienced by
each species is unclear. Although all plants reached similar
minimum values of Ψ before rewatering, olive used water
more slowly than the other species, and as a result, probably
had a more favorable soil water status overall. The decrease in
Lp in response to drought in whole root systems of intact plants
was similar to the response of Lp to drought obtained with
excised roots of desert succulents (Nobel and Huang 1992).
Similar Lp values among nonstressed plants that differ
widely in drought adaptation support previous work with
Prunus where it was found that Lp could not be used to
discriminate drought tolerance (Rieger and Duemmel 1992).
Table 1. Root hydraulic conductivity (Lp), the minimum water potential required for flow (intercept), and leaf conductance (g) for previously drought-stressed and nonstressed ‘Swingle’ citrumelo,
‘Nemaguard’ peach, ‘Manzanillo’ olive and Pistacia integerrima seedlings following a 25- to 45-day drought period. All measurements
were made 12 to 24 h after rewatering drought-stressed plants.
Treatment
Peach
Unstressed
Stressed
P > F2
Citrumelo
Unstressed
Stressed
P>F
Olive
Unstressed
Stressed
P>F
Pistachio
Unstressed
Stressed
P>F
1
2
Lp
(g m − 1 h − 1 MPa −1)
Intercept
(MPa)
g
(mmol m − 2 s−1)
0.217 a1
0.052 b
0.0219
−0.32 b
−0.33 a
0.9151
107
60
0.0607
0.196 a
0.076 ab
0.0089
−0.43 b
−0.65 b
0.0213
106
61
0.0606
0.246 a
0.100 a
0.0371
−0.20 a
−0.33 a
0.1332
61
36
0.0732
0.144 a
0.034 b
0.0499
−0.31 ab
−0.23 a
0.6303
65
58
0.7802
The lack of variation among species and the apparent sensitivity of Lp to soil drying suggest that the environment modulates
Lp to a greater extent than genetics in tree crops.
After rewatering, leaf conductance was not significantly
affected by previous drought stress in any of the species (Table 1). Reduced g after rewatering drought-stressed peach and
citrumelo trees has been reported (Fereres et al. 1979, Tan and
Buttery 1982); however, the severity of drought-stress imposed
in this study (Ψmin ≈ − 2.0 MPa) was less than that imposed in
previous studies (Ψmin ≈ −3.0 to −5.0 MPa).
Osmotic adjustment occurred only in mature leaves of citrumelo and expanding leaves of olive (Table 2). The difference
in Ψπ,o between drought-stressed and nonstressed plants was
greater in olive than in citrumelo, i.e., 1.4 versus 0.34 MPa,
respectively. Generally, olive leaves had lower Ψπ,o values than
those of other species, and citrumelo leaves had the highest
Ψπ,o values regardless of stress treatment or leaf type. The
values of Ψπ,o reported here agree closely with those reported
by others for olive, citrus and peach (Abdel-Rahman and
El-Sharkawi 1974, Syvertsen et al. 1981, Rieger 1992). Values
of Ψπ,o for P. integerrima were 0.5 to 1.0 MPa higher than
osmotic potentials at the turgor loss point reported for Pistacia
terebinthus L. (Duhme and Hinckley 1992). The magnitude of
osmotic adjustment found for citrumelo (0.34 MPa) agrees
with previous reports for tree crops (Jones et al. 1985) and
herbaceous crops (Morgan 1984), and the magnitude of adjustment found for olive (1.4 MPa) was comparable to the seasonal
Table 2. Osmotic potential at full hydration (Ψπ,o) of mature and
expanding leaves of drought-stressed and nonstressed ‘Swingle’ citrumelo, ‘Nemaguard’ peach, ‘Manzanillo’ olive and Pistacia integerrima seedlings 33 days after imposing drought-stress treatments.
Leaf type
Peach
Mature
Expanding
Citrumelo
Mature
Expanding
Olive
Mature
Expanding
Pistachio
Mature
Expanding
Means followed by the same letter are not significantly different
from those of other species within a stress treatment; Duncan’s
multiple range test, 5% level.
Significance of the comparison of means between stress treatments
within a species.
1
Treatment
Ψπ,o (MPa)
Significance1
Unstressed
Stressed
Unstressed
Stressed
−2.95
−2.86
−2.72
−2.33
0.6399
Unstressed
Stressed
Unstressed
Stressed
−1.50
−1.84
−1.95
−2.11
Unstressed
Stressed
Unstressed
Stressed
−3.46
-−2.82
−4.25
--
Unstressed
Stressed
Unstressed
Stressed
−2.71
−2.41
−2.78
−3.02
0.3126
0.0639
0.0034
0.3972
0.0067
0.1826
Probability of a greater F value for the comparison of means between drought-stressed and nonstressed plants within the same species and leaf type classes.
MODELING ROOT HYDRAULIC CONDUCTANCE AND OSMOTIC POTENTIAL
change in Ψπ,o reported by Duhme and Hinckley (1992).
A relative ranking of sensitivity to drought stress among the
three parameters measured in this study arises from the data.
In all species, Lp was reduced, yet Ψπ,o was reduced in only two
of the four species, and g (post-stress) was not significantly
reduced for any species. If the changes in g were significant,
the percent reductions would rank 60--76% for Lp, 23--50% for
Ψπ,o, and 11--44% for g. This is important in the subsequent
analysis because a decrease in Lp would be expected if osmotic
adjustment occurred in response to drought.
Analysis of offsetting effects of reduced Lp and osmotic
adjustment
Turgor pressures calculated by the model were sensitive to εmax
(data not shown). For example, a 50% reduction in εmax yielded
a 97% reduction in Ψ at the turgor loss point. In contrast, the
model was relatively insensitive to changes in β and apoplastic
water content (50% change in these parameters produced < 2%
change in Ψ at the turgor loss point). As εmax was not measured
in this study, the quantities presented here are realistic only if
there is close agreement between the assumed and actual εmax
values; however, the qualitative nature of the relationships
described below was conserved at all values of εmax.
The output from the PV curve model compared favorably to
published pressure--volume data. Values of Ψπ,o and Ψπ at the
turgor loss point for olive growing in Beskonak, Turkey, were
Figure 1. The difference in turgor pressure (∆Ψp) between previously
drought-stressed and nonstressed leaves of citrumelo plotted as a
function of water potential of previously drought-stressed leaves (Ψs).
The line labeled ‘‘OA only’’ (osmotic adjustment only) shows the
relationship when Ψ of drought-stressed and nonstressed leaves is the
same, and Lp and intercept are not reduced in stressed plants, i.e., the
effect of osmotic adjustment alone. Line labels 1.0 through 0.2 indicate the relative flow rate of water in drought-stressed plants versus
nonstressed plants (Jv,s /Jv,n); this simulates the effect of stomatal
closure. The ‘‘intercept’’ (indicated by the dotted vertical line) is the
maximum water potential that previously stressed citrumelo plants
achieved when flow was zero and the soil was saturated with water.
383
− 2.98 and −3.57 MPa, respectively (Hinckley et al. 1980); the
corresponding values from the model were −2.8 and −3.66
MPa, respectively. Also, data of Hinckley et al. (1980) show
the turgor loss point at a RWC of about 77% for olive; the RWC
at turgor loss from the model was 80%. Andersen and Brodbeck (1988) published Ψπ,o and Ψπ values at the turgor loss
point of −2.1 and −2.7 MPa, respectively, for expanded peach
leaves, and −1.7 and − 2.0 MPa, respectively, for expanding
peach leaves. Using their Ψπ,o data, the model predicted a Ψπ
value at turgor loss of −2.74 MPa (1.5% error) for expanded
peach leaves, and − 2.14 MPa (7.0% error) for expanding peach
leaves. Abrams (1988) compiled Ψπ,o and Ψπ values at the
turgor loss point from 37 North American tree species. Using
his values of Ψπ,o for seven broad-leaved trees as input, the
model predicted the corresponding Ψπ at the turgor loss point
with an average error of 11%.
The offsetting effects of decreased Lp and osmotic adjustment are illustrated using data for citrumelo and olive (Figures 1 and 2). The relationships in Figures 1 and 2 do not
extend to 0 MPa along the x-axis because both species have
nonzero intercepts (Table 1), i.e., zero flow occurred at
nonzero water potentials. For citrumelo, when water flow is
the same for drought-stressed and nonstressed plants, droughtstressed plants maintained higher Ψp than nonstressed plants
at Ψs values from −0.65 to ≈ − 0.9 MPa (following line for
relative flow = 1.0 in Figure 1). At Ψs < − 0.9 MPa, droughtstressed plants would have lower Ψp than nonstressed plants,
Figure 2. Relationships between ∆Ψp and Ψs for olive. The line
labeled ‘‘OA only’’ (osmotic adjustment only) shows the relationship
when Ψ of drought-stressed and nonstressed leaves is the same, and
Lp and intercept are not reduced in stressed plants, i.e., the effect of
osmotic adjustment alone. Line labels 1.0 through 0.2 indicate the
relative flow rate of water in drought-stressed plants versus nonstressed plants (Jv,s/Jv,n ); this simulates the effect of stomatal closure.
The ‘‘intercept’’ (indicated by the dotted vertical line) is the maximum
water potential that previously stressed olive plants achieved when
flow was zero and the soil was saturated with water.
384
RIEGER
because the decrease in Lp would more than offset the decrease
in Ψπ,o in terms of turgor maintenance. As flow is reduced by
stomatal closure (relative flows of 0.8 to 0.2), the range of Ψs
over which a turgor advantage is maintained in droughtstressed plants increases, such that when ∆Ψp = 0, Ψs is moved
progressively toward the turgor loss point of Ψs = −2.3 MPa.
The line marked ‘‘OA only’’ in Figure 1 illustrates the effect
of osmotic adjustment on ∆Ψp without a change in Lp or
intercept. Along this line, the Ψ values of drought-stressed and
nonstressed plants are equal, and osmotic adjustment confers
a turgor advantage at all Ψs values down to the turgor loss
point. The difference between the ‘‘OA only’’ line and lines
representing relative flows of 1.0, 0.8, 0.6 or 0.4 at any given
Ψs therefore represents the offsetting effect of reduced Lp and
intercept on osmotic adjustment. When relative flow in
drought-stressed plants is reduced to 20% of that in nonstressed plants, the turgor advantage produced by osmotic
adjustment increases above the ‘‘OA only’’ line. This results
from the combined effects of two turgor-maintaining processes
(stomatal closure and osmotic adjustment) over-compensating
for the turgor-reducing effect of low Lp. Hence, ∆Ψp is greater
than would be predicted from inspection of the change in Ψπ,o
when the relative flow falls below about 0.4.
The analysis suggests that partial stomatal closure must
accompany osmotic adjustment if a turgor advantage is to be
maintained in drought-stressed citrumelo plants through their
reported diurnal range of Ψ (0 to −1.5 MPa, Syvertsen et al.
1981). Because flow would have to be reduced by 40 to 60%
in drought-stressed plants to allow Ψ to reach −1.5 MPa
(Figure 1), a reduction in CO2 assimilation may also be expected. The reduction in g of ≈ 40% due to drought stress,
although not statistically significant (P > 0.05) for citrumelo
(Table 1), would not have reduced flow to the extent necessary
to allow ∆Ψp to remain positive at all expected values of Ψs.
In olive, the response of ∆Ψp to Ψs was similar to that of
citrumelo (Figure 2). However, in the absence of stomatal
closure, the large decrease in Ψπ,o would offset the 2.5-fold
decline in Lp at all Ψs values above ≈ −3.0 MPa (see Figure 2
where relative flow = 1.0). Thus, unlike citrumelo, the turgor
advantage due to osmotic adjustment would likely be maintained in olive throughout the diurnal range of Ψ (−0.6 to−2.0
MPa, Larsen et al. 1989). However, this magnitude of osmotic
adjustment (1.4 MPa) is uncharacteristically high for tree species and serves to illustrate an extreme rather than a typical
case.
One factor not considered in this analysis is reduced axial
conductance in the xylem due to cavitation and embolism
during moderate drought stress (Tyree and Sperry 1988). The
assumption was made that whole-plant hydraulic conductivity,
L, was equal to Lp, when in reality, L also includes stem
conductivity. A reduction in stem conductivity would reduce
the turgor advantage due to osmotic adjustment even more than
predicted here. Therefore, the amount of stomatal closure
required to counter-balance the reduction in plant conductivity
would be greater than that shown in Figures 1 and 2.
I conclude that the turgor advantage conferred by osmotic
adjustment is reduced by decreased Lp following drought
stress. Because Lp is more sensitive to drought than Ψπ,o, the
effect of osmotic adjustment on turgor maintenance is less than
that estimated from pressure--volume analyses alone. The
adaptive value of osmotic adjustment has also been questioned
by others (see Munns 1988), because evidence suggests that
growth must decrease for osmotic adjustment to occur. Although Ψp drives cell expansion and growth, cell wall properties such as yield threshold and extensibility may change in
response to drought to negate an increase in Ψp (Van Volkenburgh and Cleland 1984). Thus, the translation of osmotic
adjustment into increased growth or physiological function is
at best limited by Lp reduction, and at worst unobtainable as a
result of reduced Lp combined with other negative impacts of
drought stress.
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