Annals of Botany 78 : 703–710, 1996
Differences in Rehydration of Three Desiccation-tolerant Angiosperm Species
H E A T H E R W . S H E R W I N * and J I L L M . F A R R A N T
Botany Department, UniŠersity of Cape Town, PriŠate Bag, Rondebosch, 7700, South Africa
Received : 20 February 1996
Accepted : 5 June 1996
The rehydration characteristics of the desiccation-tolerant plants Craterostigma wilmsii and Myrothamnus flabellifolia
(homoiochlorophyllous) and Xerophyta Šiscosa (poikilochlorophyllous) were studied to determine differences among
them. A desiccation-sensitive plant (Pisum satiŠum) was used as a control. Recovery of water content, quantum
efficiency (FV}FM), photosynthetic pigments and chloroplast ultrastructure as well as damage to the plasmamembrane
were studied.
P. satiŠum did not recover after desiccation and considerable damage occurred during rehydration. The
desiccation-tolerant plants appeared to differ in their responses to dehydration and rehydration. The small
herbaceous C. wilmsii generally showed little damage in the dry state and recovered faster than the other tolerant
species. M. flabellifolia took longer to recover than C. wilmsii probably due to the presence of a woody stem in which
dehydration-induced xylem embolisms slowed the rate of recovery. The poikilochlorophyllous species X. Šiscosa took
the longest to recover because it took longer to reconstitute the chloroplasts and the photosynthetic pigments.
Quantum efficiency recovered in all species before water content and chlorophyll content recovered to control levels.
The significance of these different responses to desiccation and recovery from desiccation is discussed.
# 1996 Annals of Botany Company
Key words : Desiccation-tolerant, FV}FM, homoiochlorophyllous, poikilochlorophyllous, chlorophyll, chloroplast,
ultrastructure, Craterostigma wilmsii, Myrothamnus flabellifolia, Xerophyta Šiscosa, Pisum satiŠum.
INTRODUCTION
While the vegetative tissues of most angiosperm species
cannot survive severe water stress there are a few species
which do tolerate desiccation. These plants are commonly
known as ‘ resurrection ’ plants, due to their unique ability
to revive from an air-dried state (Gaff, 1971, 1989). Two
types of desiccation-tolerant angiosperms have been recognized : those that lose chlorophyll on drying (poikilochlorophyllous) and those that retain chlorophyll (homoiochlorophyllous) (Gaff, 1977 ; Bewley, 1979 ; Tuba et al.,
1993). To date there have been no studies reported which
have compared the desiccation responses of these two types
of plant.
It has been suggested that there are several challenges
which have to be overcome if a plant tissue is to be truly
tolerant of desiccation (Vertucci and Farrant, 1995). These
include the ability to : (a) minimize mechanical damage
associated with turgor loss ; (b) maintain the integrity of
macromolecules and membranes by the accumulation of
water stress proteins (dehydrins) and compatible solutes ;
and (c) minimize toxin accumulation and free radical
damage generated as metabolism becomes impaired. Upon
rehydration, such plant tissues must be able to repair
desiccation-induced damage. It has been proposed that
different plants will rely on the processes of protection and
repair to differing extents (Bewley and Oliver, 1992). Most
of the studies on desiccation tolerance have focused on how
plants survive in the dry state, while less work has been done
* For correspondence.
0305-7364}96}120703­08 $25±00}0
on the processes occurring during rehydration. During
rehydration the passage to a metabolically active state poses
particular problems if metabolic ‘ mayhem ’ is to be avoided
(Stewart, 1990). Too rapid rehydration has been shown to
cause damage to dry seeds (Simon, 1974 ; Hoekstra and van
der Wal, 1988). While rehydration causes its own set of
challenges to the desiccation-tolerant plant, it is also the
period when repair of physical damage and the restoration
of metabolic activity must take place. Thus, in studying the
phenomenon of desiccation tolerance, the study of the
processes occurring on rehydration are important.
Studies on the rehydration of desiccation-tolerant mosses,
ferns and angiosperms (reviewed in Bewley, 1979 ; Bewley
and Krochko, 1982 ; Gaff, 1989) have shown that recovery
is rapid and that, in general, it is quicker in homoiochlorophyllous than in poikilochlorophyllous plants.
Ultrastructural studies on the former have shown that some
damage does occur on drying but this is repaired on
rehydration (Bewley, 1979 ; Schneider, et al., 1993 ; Sherwin,
1995). In Craterostigma nanum, chlorophyll fluorescence
parameters were almost fully recovered after 18 h of
rehydration (Sherwin, 1995). In the poikilochlorophyllous
types examined to date, there were extensive changes to
chloroplast structure which can take up to 3 d after
rehydration to return to normal (Hetherington, Hallam and
Smillie, 1982 ; Gaff, 1989 ; Tuba et al., 1993). At least 2 d are
required for normal fluorescence characteristics (Hetherington et al., 1982 ; Tuba et al., 1994). Studies on rehydration
of excised leaves of the poikilochlorophyllous Xerophyta
scabrida (Tuba et al., 1994) have shown that the leaves take
approximately 24 h to rehydrate, after which chlorophyll
# 1996 Annals of Botany Company
704
Sherwin and Farrant—Rehydration of Three Desiccation-tolerant Species
production increases. In all species examined, carbon
assimilation reached a maximum after chlorophyll production was complete and chloroplast ultrastructure regained a normal appearance.
Studies done to date have used either whole plants or
excised leaf parts, making comparisons difficult. Furthermore, the rehydration studies reported have generally only
used isolated leaves. Unpublished work from our laboratory
has indicated that rehydration of isolated leaves does not
result in the full recovery of photosynthetic activity.
The aim of this work was to compare the rehydration of
whole plants of three different desiccation-tolerant plant
species and compare those to the rehydration of a
desiccation-sensitive plant, examining specifically the
changes occurring to the photosynthetic apparatus. The
three tolerant species chosen differed in form and in their
physical and physiological response to desiccation. Craterostigma wilmsii Engl. (Scrophulariaceae) is a small herbaceous
plant that curls its leaves tightly on drying and is
homoiochlorophyllous. Myrothamnus flabellifolia Welw.
(Myrothamnaceae) is a woody shrub often reaching heights
of 1 m. On dehydration, the leaves fold against the stem and
chlorophyll is retained in the adaxial mesophyll layers. The
outer, abaxial surfaces become dark brownish-red. Xerophyta Šiscosa Baker (Velloziaceae), a monocotyledonous
plant, is poikilochlorophyllous ; the leaves yellow and fold
in half along the main rib on drying. The desiccationsensitive plant Pisum satiŠum L. (Fabaceae) was used as a
control to establish differences between the tolerant plants
and one sensitive to desiccation.
MATERIALS AND METHODS
Plants which had been dried to ! 5 % relative water
contents (RWC) were allowed to rehydrate and their
recovery was monitored. Measurements of electrolyte
leakage were performed to assess membrane integrity and
thus viability. Changes in pigment content were determined
and chloroplast status was assessed in terms of quantum
efficiency and subcellular organization.
Plant material
The desiccation-tolerant plants were collected from the
Buffelskloof Nature Reserve near Lydenberg (Mpumalanga
Province, South Africa). They were grown in a mixture of
peat, river sand and potting soil and were maintained in a
greenhouse under 30 % shadecloth with no supplementary
lighting. To maintain the hardiness of the plants, they were
subject to regular cycles of desiccation and rewatering.
Seeds of P. satiŠum (cv. Greenfeast) were sown in trays of
potting soil and the material was kept in a greenhouse under
the same conditions as the other plants. Plants were dried
after 3 weeks of growth.
Dehydration and rehydration
Whole plants of the four species were dried by withholding
water and allowing the plant to dry out naturally. Once no
more water was lost from the leaves (RWCs ! 5 %) the
plants were left in the dry state exposed to natural sunlight
for between 1 and 3 months. Rehydration was carried out
by watering the plants using a spray to simulate rainfall.
Plants were well watered on the first day and then the soil
was kept damp for the remainder of the experiment. P.
satiŠum leaves did not rehydrate upon soil watering.
Rehydration was achieved by placing excised leaves directly
into water.
At regular intervals during the rehydration process, the
procedures outlined below were performed on leaf tissues.
In the case of C. wilmsii only the middle leaves of the rosette
were used and for M. flabellifolia and X. Šiscosa mature,
fully expanded leaves were used. The two youngest fully
expanded leaves were used in the case of P. satiŠum. Several
separate rehydration experiments were conducted (four for
C. wilmsii ; three for M. flabellifolia ; two for X. Šiscosa ; and
five for P. satiŠum) and in each case five leaf samples were
taken for each of the experimental procedures.
Electrolyte leakage
Leakage measurements were performed on desiccated and
fully rehydrated leaves of each species. As a control, the
leakage of leaves which had not been desiccated and
rehydrated was also monitored. The leaves (M. flabellifolia)
or leaf pieces (C. wilmsii, X. Šiscosa and P. satiŠum) were
placed directly into pure (distilled, de-ionised and filtered)
water and electrolyte leakage was measured every minute
for 40 min using a conductivity meter (Jenway 4070). The
rate of leakage was calculated (the slope of line generated
from the time course of leakage) and was corrected by leaf
dry mass.
Chlorophyll fluorescence
A modulated portable fluorometer (OS-500 : OptiSciences, USA) was used to calculate the quantum efficiency
of leaves at various stages of hydration. The initial
fluorescence, FO, and maximum fluorescence, FM, using a
saturating light intensity of approximately 4 mmol photons
m−# s−") and a duration of 1 s, were measured. FV was
obtained by subtracting FO from FM and FV}FM was
calculated.
Chlorophyll and carotenoid content
Photosynthetic pigments were extracted in 100 % acetone
and the absorbances were measured using a Schimadzu UV2201 light}UV spectrophotometer (Schimadzu Scientific
Instruments Inc., USA). Chlorophyll and carotenoid contents were calculated using the adjusted extinction coefficients according to Lichtenthaler (1987).
Ultrastructure
Leaf segments (approximately 5 mm#) were excised
randomly from fully turgid leaves (which had not undergone
any dehydration) as well as leaves in the dry and partially
rehydrated state (approximately 50 % RWC). These were
fixed in 2±5 % glutaraldehyde in 0±1  phosphate buffer
Sherwin and Farrant—Rehydration of Three Desiccation-tolerant Species
(pH 7±2) containing 0±5 % caffeine. Post-fixation was in 1 %
osmium tetroxide in phosphate buffer. Following ethanol
dehydration, the material was infiltrated and embedded in
epoxy resin (Spurr, 1969). The tissue was sectioned at a gold
interference colour (approximately 75 nm thick) using a
Reichert Ultracut-S microtome. Sections were stained with
uranyl acetate and lead citrate (Reynolds, 1963) and viewed
with a Jeol 200CX transmission electron microscope.
Observations were made on at least three sections of three
different leaf samples.
RESULTS
Figure 1 shows the time course of rehydration of the four
species. The desiccation-sensitive P. satiŠum did not rehydrate at all while the three desiccation-tolerant plants
Water content (% of control)
110
88
66
44
22
0
20
80
40
60
Rehydration time (h)
Electrolyte conductivity (% of control)
F. 1. Increase in water content with time after rehydration. The water
content is represented as a percentage of the control value. The plotted
data points are means of at least ten measurements and the standard
deviations of these means are represented by the vertical lines. (+) C.
wilmsii, (*) M. flabellifolia, (_) X. Šiscosa and (E) P. satiŠum.
e
4100
3280
d
2460
1640
c
820
a a a
a b a
C. wilmsii
M. flabellifolia
a
a
a
0
X. viscosa
P. sativum
F. 2. Changes in electrolyte leakage (as a percentage of the control)
in the four species. Control (*) levels were taken from fully turgid
leaves which had not been dehydrated or rehydrated. These were
compared with levels of dehydrated (9) tissue and tissue that had been
rehydrated (+) to full water content. Differences between letters
indicate significant differences (Anova and Duncans Multiple Range
test, 95 % confidence level) in leakage between treatments within and
among species.
705
regained full turgor. Leaves of C. wilmsii were fully hydrated
by 48 h after rewatering while those of M. flabellifolia took
65 h and X. Šiscosa 92 h. Both C. wilmsii and X. Šiscosa
rehydrated at relatively constant rates. The more rapid
rehydration in C. wilmsii was presumably because it was
smaller and is herbaceous. In M. flabellifolia, water uptake
during the initial 12 h was slow, but thereafter the rate of
rehydration increased and was similar to that of C. wilmsii.
M. flabellifolia is a woody plant, which probably accounts
for this pattern of water uptake. Once the xylem system
became functional (presumably after 12 h) the rate of
uptake increased.
There was no significant difference in the electrolyte
leakage rate among the control, dry and rehydrated leaves
of C. wilmsii (Fig. 2), suggesting that the integrity of the
plasma membrane was maintained during both drying and
rehydration of this species. Leakage in the dry state was
greater in X. Šiscosa than in M. flabellifolia, but in both
species leakage returned to control levels on rehydration.
Thus drying appeared to cause some change in membrane
configuration, but this was reversed and}or repaired on
rehydration of those species. In contrast to the tolerant
species, dry leaves of P. satiŠum showed a significant
increase in electrolyte leakage compared to the control and
there was a further substantial increase in leakage upon
rehydration of these leaves (Fig. 2). Thus, the desiccationinduced membrane changes were not reversible on rehydration in this species.
The changes in quantum efficiency (FV}FM) with rehydration are shown in Fig. 3A. The desiccation-tolerant species
all showed complete recovery of this variable, indicating
that chloroplasts became fully functional upon rehydration.
C. wilmsii recovered most rapidly, reaching control levels by
32 h. In M. flabellifolia and X. Šiscosa the rate of recovery
was similar, but the latter took longer for the quantum
efficiency to return to control levels (76 h in X. Šiscosa cf.
55 h in M. flabellifolia). In each case, FV}FM recovered to
control levels before water content had reached maximum
levels. P. satiŠum did not recover photosynthetic capacity
(Fig. 3A).
Figure 3B shows the changes in chlorophyll content
during rehydration. X. Šiscosa lost almost all chlorophyll on
drying ; very little was reconstituted within the first 24 h but
thereafter chlorophyll content increased, reaching control
levels after 120 h. C. wilmsii and M. flabellifolia lost 50 and
70 % of leaf chlorophyll, respectively. The chlorophyll
content of M. flabellifolia recovered rapidly and reached
control levels after 24 h. The chlorophyll content of C.
wilmsii recovered almost to control levels after 45 h. Thus
M. flabellifolia recovered chlorophyll content to control
levels before FV}FM had recovered fully. On the contrary, C.
wilmsii and X. Šiscosa recovered FV}FM before their
chlorophyll contents had fully recovered. As with the other
variables P. satiŠum showed no recovery of the 75 % of
chlorophyll that it lost on drying.
The carotenoid content declined during dehydration of
M. flabellifolia, X. Šiscosa and P. satiŠum whereas C. wilmsii
retained its carotenoid levels (Fig. 3C). Carotenoid levels
declined by 60 % in X. Šiscosa and, as with chlorophyll
production, there was a 24 h delay before recovery of those
706
Sherwin and Farrant—Rehydration of Three Desiccation-tolerant Species
Fv /Fm (% of control)
110
88
66
44
22
Total chlorophyll (% of control)
0
110
B
88
66
44
22
0
110
Total carotenoids (% of control)
A
C
88
66
44
22
0
20
40
60
Rehydration time (h)
80
F. 3. Changes in the quantum efficiency (FV}FM) (A), chlorophyll (B)
and carotenoid contents (C) with time after rehydration. FV}FM,
chlorophyll and carotenoid contents are represented as a percentage of
the control value. The plotted data points are means of at least ten
measurements and the standard deviations of these means are
represented by the vertical lines. (+) C. wilmsii, (*) M. flabellifolia,
(_) X. Šiscosa and (E) P. satiŠum.
pigments commenced. Total recovery occurred after 96 h.
In M. flabellifolia, the recovery of carotenoid levels was
slower (72 h) than the recovery of chlorophyll (24 h). P.
satiŠum showed no recovery of carotenoids on rehydration.
Figures 4–7 show the chloroplast organization from
control plants and those from dry and partially rehydrated
leaves. The use of standard fixation techniques might have
allowed some rehydration of the desiccated leaves. However,
as all species were fixed in the same manner, comparisons
between species are valid. A study using vapour fixation of
dried leaves of M. flabellifolia (Goldsworthy and Drennan,
1991) gave very similar results to those observed in the
present study.
F. 4. Micrographs of the chloroplasts of C. wilmsii at full turgor
(control) (A) ¬20 000, in the dry state (B), ¬17 200 and after 12 h of
rehydration (C), ¬18 750. L, Lipophilic bodies ; S, starch.
Chloroplasts from control leaves of C. wilmsii were
typical of hydrated, photosynthetically active tissues. Thylakoid membranes were clearly defined and some starch was
present (Fig. 4A). In the dry state chloroplasts became
rounded, the internal membranes were located peripherally
and no starch was evident. The boundary membranes were
intact and thylakoid stacks were still clearly visible, although
Sherwin and Farrant—Rehydration of Three Desiccation-tolerant Species
707
F. 5. Micrographs of the chloroplasts of M. flabellifolia at full turgor (A,B), ¬20 000 and ¬59 000, respectively, in the dry state (C), ¬16 500,
after 12 h of hydration (D), ¬16 500 and after 24 h of rehydration (E) ¬17 700. The staircase arrangement of thylakoids is shown in the inset
(Fig. 5B). Note the swollen nature of the thylakoids in rehydrating tissue (Fig. 5D).
there was a small degree of ‘ blistering ’ or separation of the
appressed membranes (Fig. 4B). After 12 h of rehydration
(60 % RWC and 80 % recovery of FV}FM), the chloroplasts
resembled those in the dry state, although they were more
oval than rounded (Fig. 4C). Upon further hydration the
chloroplasts progressively assumed the shape and thylakoid
distribution typical of control tissue (not shown). Lipophilic
bodies were present at all stages of dehydration and
rehydration.
Chloroplasts from control plants of M. flabellifolia were
typically elongated with well defined thylakoid membranes
and starch was present (Fig. 5A). The thylakoid membranes
had a unique form of stacking (Fig. 5B) referred to as a
‘ staircase ’ arrangement (Wellburn and Wellburn, 1976).
They suggested that such an arrangement allows a more
effective presentation of photosynthetically active membranes to incoming radiation. This feature is not specific to
resurrection species in general, as it has not been found in
other resurrection species such as Craterostigma spp. or
Xerophyta spp. (Tuba et al., 1993 ; Sherwin, 1995). In the
dry state the chloroplasts appeared ovate, the stroma
stained darkly and, while the thylakoids retained their
staircase arrangement, they had a blistered appearance.
There was no starch present (Fig. 5C). After 12 h of
rehydration (20 % RWC and 40 % recovery of FV}FM) the
appearance of the chloroplasts was very unusual. They had
become rounded and the appressed membranes of the
thylakoids appeared to have pulled apart (Fig. 5D). This
‘ honeycomb ’ appearance of the thylakoids was lost between
18 and 24 h of rehydration. After 24 h (60 % RWC and
60 % recovery of FV}FM) the staircase arrangement of the
thylakoids was evident, although electron transparent
regions were still present within the stroma (Fig. 5E).
Like C. wilmsii and M. flabellifolia, chloroplasts from the
control plants of X. Šiscosa were elongated and contained
starch. There were few granal layers in this species (Fig. 6A).
In the dry state the chloroplasts were rounded and while the
outer membranes remained continuous, the internal membranes lost their original conformation and appeared
vesiculated (Fig. 6B). An unusual double-membraned
structure became evident in virtually all chloroplasts
examined (arrowed, Fig. 6B). The origin and function of
this structure is unknown, but may have resulted from
invagination and vesiculation of the outer boundary
membrane. At this stage, the plant had lost more than 90 %
of its chlorophyll. After 24 h of rehydration (60 % RWC)
the internal membranes were less vesiculated and the circular
membranous structure evident in the dry state was not
present (Fig. 6C). At this stage less than 10 % of the
chlorophyll had been recovered yet there was a 60 %
recovery of FV}FM. After 48 h of rehydration (80 % RWC,
50 % chlorophyll recovery and 90 % recovery of FV}FM) the
708
Sherwin and Farrant—Rehydration of Three Desiccation-tolerant Species
F. 6. Micrographs of the chloroplasts of X. Šiscosa at full turgor (A), ¬20 000 ; in the dry state (B), ¬19 000 ; after 24 h of rehydration (C),
¬27 000 ; and after 48 h of rehydration (D), ¬20 400. Note the circular membranous structure within chloroplasts in the dry state (arrows, Fig.
6B) and RER associated with outer membranes of the chloroplasts in rehydrating tissues (Fig. 6C and D). RER, rough endoplasmic reticulum.
thylakoid membranes had reassembled (Fig. 6D). Strands
of rough endoplasmic reticulum (RER) and}or polysomes
were present in close association with the boundary
membranes of the chloroplasts (Fig. 6A–D). As in C.
wilmsii, lipophilic bodies were present at all stages.
Figure 7 shows details of chloroplasts of P. satiŠum in
leaves at full turgor (Fig. 7A), in the dry state (Fig. 7B) and
after rehydration of individual leaves (Fig. 7C). In the dry
state the chloroplasts became rounded and the thylakoids,
while clearly visible and still arranged in stacks, were
blistered. After rehydration it was difficult to distinguish the
chloroplasts. Although in some instances thylakoid stacks
were apparent, there was a general disruption of chloroplast
membranes.
DISCUSSION
The results from this study show the unusual ability of three
different resurrection plants to survive desiccation. It is also
apparent that while these plants presumably undergo similar
stresses on dehydration, there are differences in the way in
which they cope with these stresses and in the nature of
recovery during rehydration.
The nature of the damage associated with desiccation is
typified in the response of P. satiŠum to dehydration and
rehydration. The pattern of electrolyte leakage suggests that
there is irreversible damage to the plasmalemma and, while
organelles such as chloroplasts appear to retain some degree
of integrity on drying, there is total dissolution on
rehydration. Photosynthetic pigments were lost and not
recovered. Thus there appears to be no mechanism of
subcellular protection operating in this species and, furthermore, there is an inability to repair the damage induced
by desiccation (presumably because the repair enzymes are
damaged). Thus, on drying, metabolism such as photosynthesis is disrupted (rather than interrupted) by desiccation and this cannot be restored on rehydration.
Among the desiccation-tolerant species there were differences in the rate of recovery of water content and in
photochemical activity. Recovery was generally more rapid
in the homoiochlorophyllous species than in the poikilochlorophyllous X. Šiscosa, but there was also a difference in
the rate of recovery between the homoiochlorophyllous
types. The rate of recovery appears to depend on plant
morphology and the extent of subcellular repair}reconstitution required for the resumption of metabolism.
C. wilmsii, being a small herbaceous plant, recovered
water content very rapidly and this facilitated a rapid
recovery of metabolism. Photochemical activity was restored
before the plant was fully hydrated and before chlorophyll
content reached control levels, suggesting that maximal
Sherwin and Farrant—Rehydration of Three Desiccation-tolerant Species
F. 7. Micrographs of the chloroplasts of P. satiŠum at full turgor (A),
¬16 500 ; in the dry state (B), ¬18 000 and after 12 h of rehydration
(C), ¬17 000.
levels of these parameters are not required for full
photosynthetic activity. Carotenoid levels were maintained,
however, and it is possible that these were sufficient for
maximal levels of photosynthesis. The rapid recovery is
presumably also facilitated by the apparent ability of this
plant to maintain integrity of the plasmalemma and
chloroplast organization during dehydration and rehydration. Thus metabolism can resume without the delays
caused by reconstituting these organelles. These results
suggest that a mechanism of subcellular protection may
operate during desiccation. Dehydrin proteins have been
reported to be induced by drying in Craterostigma plantagineum (Piatkowski et al., 1990) and Craterostigma nanum
709
(Sherwin, 1995). The presence of such proteins in C. wilmsii
may contribute towards subcellular stabilization during
dehydration.
The rehydration of leaves of M. flabellifolia was slower
than in C. wilmsii, possibly because of the time to recover
hydraulic conductance in the xylem vessels in the former.
Embolisms in the xylem vessels could initially have posed a
significant resistance to water uptake. Thus, photochemical
activity was recovered over a longer period although, like C.
wilmsii, this occured before the plant was fully rehydrated.
There was a delay in the resumption of photochemical
activity during initial rehydration despite recovery of
chlorophyll content. This is possibly due to the lack of
continuity between adjacent thylakoid membranes and their
reconstitution appears to be necessary for full recovery of
photosynthetic activity. Increased levels of electrolyte
leakage occurred upon desiccation, suggesting that some
reconstitution of plasma membranes is required during
rehydration. Thus repair}reconstitution of subcellular
organization appears to play a more significant role in the
recovery of this species compared to C. wilmsii. However,
considering the degree of subcellular integrity maintained
and the relatively rapid recovery of this plant on rehydration,
there must also be some mechanism of protection. Drennan
et al. (1993) reported an increase in the levels of trehalose
and Bianchi et al. (1993) increases in the levels of sucrose,
arbutin and glucopyranosyl-β-glycerol on desiccation of
this species, which may contribute to subcellular stabilization. There is to date no information on the presence of
dehydrins in M. flabellifolia.
Recovery of turgor and photochemical activity was
slowest in X. Šiscosa. While slow water uptake must delay
metabolic recovery, this species showed the greatest degree
of membrane leakage and almost total loss of photosynthetic
apparatus. The greater degree of subcellular reorganization
required on rehydration of this species could account for the
longer time taken for its recovery compared to the
homoiochlorophyllus types. There is no information on the
nature of subcellular protection in this species. In the
present study, X. Šiscosa recovered photochemical activity
before chlorophyll levels reached their pre-desiccation levels,
and before full water content was attained. Tuba et al.
(1994) showed that the opposite is true of X. scabrida. Those
authors rehydrated isolated leaf tissues in their study, which
may account for the discrepancy in results between the
studies.
We suggest that recovery rate is influenced by plant form
(which influences the rate of hydration) and also the extent
of reconstitution of subcellular organization that is required.
We further suggest that the degree of reconstitution required
for the photosynthetic apparatus depends on the strategies
adopted to prevent light-related desiccation stresses. Removal of water from plant tissues ultimately results in
interruption of metabolic pathways. One consequence of
this in chlorophyllous tissue is that the energy generated
from light absorbed by a chlorophyll molecule cannot be
dissipated via the normal metabolic pathways. The energized
electrons (which may in turn generate free radical species)
can cause considerable subcellular damage. Poikilochlorophyllous plants like X. Šiscosa avoid such stress by losing
710
Sherwin and Farrant—Rehydration of Three Desiccation-tolerant Species
chlorophyll and dismantling the thylakoid membranes
during desiccation. On rehydration the photosynthetic
apparatus has to be reconstituted and this delays recovery
of carbon metabolism. Homoiochlorophyllous plants retain
most of the photosynthetic apparatus, but prevent lightchlorophyll interactions, for example by leaf curling in C.
wilmsii and folding in M. flabellifolia. Recovery of photosynthesis can be more rapid in these species relative to
poikilochlorophyllous types.
A C K N O W L E D G E M E N TS
Thanks to John and Sandie Burrows of the Buffelskloof
Nature Reserve for help in collecting the plant material.
Heather Sherwin acknowledges the Foundation for Research Development (FRD) for a post-doctoral bursary.
The project was funded by an FRD grant awarded to Jill
Farrant.
LITERATURE CITED
Bewley JD. 1979. Physiological aspects of desiccation tolerance. Annual
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