Journal of Experimental Botany, Vol. 51, No. 343, pp. 159–165, February 2000
Photosynthetic carbohydrate metabolism in the
resurrection plant Craterostigma plantagineum
M. Norwood1, M.R. Truesdale1, A. Richter2 and P. Scott1,3
1 School of Biological Sciences, University of Sussex, Brighton BN1 9QG, UK
2 Chemical Physiology of Plants, Institute of Plant Physiology, University of Vienna, Althanstr. 14, A-1091 Wien,
Austria
Received 7 May 1999; Accepted 16 September 1999
Abstract
The resurrection plant Craterostigma plantagineum
(Hochst) is able to survive almost complete tissue
dehydration when water is withheld from it, and then
can rehydrate rapidly on rewatering. This ability is
believed to be the result of the accumulation of sucrose in aerial tissues as a result of metabolism of
2-octulose. In this work the metabolic activity of wellwatered Craterostigma plantagineum plants has been
investigated. It is shown that Craterostigma makes
raffinose series oligosaccharides as a product of
photosynthesis and translocates them in the phloem.
Evidence is also provided that 2-octulose is a product
of photosynthesis and accumulates in the leaves over
the light period and is mobilized at night. Thus
2-octulose acts as a temporary storage carbohydrate
in leaves during photosynthesis in a similar fashion to
starch in most C plants. Other potential roles of
3
2-octulose are discussed. Other than these observations Craterostigma plants are very similar to other C
3
plants under these conditions.
Key words: Craterostigma, resurrection plants, octulose,
carbohydrate metabolism.
Introduction
Desiccation tolerance is most frequently seen as a capability possessed by mature seeds of higher plants. It is rarely
seen in any other higher plant tissues. However, resurrection plants (or poikilohydric plants) have the unique
ability amongst higher plants to be able to survive almost
complete dehydration and then be rehydrated in a biologically functional state (Gaff, 1971). This capacity is not
restricted to the main meristems or cores of these plants.
Fully mature leaves can lose up to 95% of their water
content and enter a dormant state and then, upon rewatering, the leaves are reanimated and are fully photosynthetically active within 24 h (Schwall et al., 1995). Tissue
damage through this drying and rehydration process
appears to be minimal to non-existent.
In most instances where the phenomenon has been
researched the acquisition of the resurrection capability
appears to be associated with the accumulation of a
carbohydrate in the tissues as they dry. In a majority of
cases sucrose is the major carbohydrate which accumulates (Ingram and Bartels, 1996), however, trehalose has
been reported in certain resurrection species (Drennan
et al., 1993). The period of time required for accumulation
of this carbohydrate must be crucial during the drying
process. If it is to protect the plant through the dehydration process then it must be able to accumulate rapidly
and in sufficient quantity to be of benefit to the plant. In
some resurrection plant species sucrose accumulates as a
product of photosynthesis (Müller et al., 1997). However,
it would appear that Craterostigma species have evolved
a mechanism by which to aid the accumulation of sucrose
during dehydration. Craterostigma plantagineum and C.
wilmsii accumulate the eight carbon carbohydrate
2-octulose in leaves under well-watered conditions
(Bianchi et al., 1991). Upon drought stress there is a
massive conversion of 2-octulose into sucrose. Thus
Craterostigma has the capacity to accumulate sucrose
very rapidly from carbohydrate sources already present
in the leaf rather than relying upon photosynthate.
This report has focused on the well-watered state of
Craterostigma plantagineum in order to understand the
preparations the plant makes in order to survive dehydration stress. It is demonstrated here that Craterostigma
3 To whom correspondence should be addressed. Fax: +44 1273 678433. E-mail: [email protected]
© Oxford University Press 2000
160 Norwood et al.
translocates raffinose series oligosaccharides in the
phloem, 2-octulose is one of the major products of
photosynthesis in mature and immature leaves, and there
is a great deal of cycling in 2-octulose concentration in
leaves across a 24 h period. Thus it is concluded that
2-octulose may have further roles in Craterostigma plantagineum than simply providing a carbohydrate source for
sucrose accumulation during drought stress.
Materials and methods
Plant material
Craterostigma plantagineum (Hochst) plants were obtained from
Professor D Bartels, Max Planck, Cologne, Germany which
were from the wild in Namibia. Plants were clonally propagated
by side shoot cutting and grown on peat until 6 months old
and then were used in experiments. All plants for experimental
studies were grown in growth cabinets under a 12 h light/12 h
dark regime, at 24 °C and 19 °C, respectively, and a PPFD of
300 mmol m−2 s−1.
Measurement of carbohydrates and enzymes
For measurement of Glu 6-P, Fru 6-P and 3-PGA tissue was
harvested and immediately frozen in liquid N and ground to a
2
fine powder. Then 1.4 M perchloric acid was added to the leaf
material and the mixture was frozen again in liquid nitrogen,
and left on ice for 2 h. The extract was then neutralized with
5 M K CO , and the insoluble debris was removed by
2 3
centrifugation at 10 000 g. Glu 6-P, Fru 6-P and 3-PGA were
assayed in the extract as described previously (Michal, 1984a,
b). Starch, sucrose, glucose, and fructose were also extracted
and measured as described previously (Morrell and ap Rees,
1986). The raffinose series oligosaccharides of roots and leaves
was assayed spectrophotometrically in the same way as sucrose,
but the sample was previously digested with a-galactosidase to
hydrolyse the galactosyl residue (Bergmeyer, 1984b). The
reliability of these metabolite assays was confirmed by performing recovery assays. For these, an amount of each authentic
metabolite similar in concentration to that in the Craterostigma
tissue was added to the assay. The percentage of standard
recovered was calculated from the concentration measured in
the presence and absence of leaf extract. For all of the
metabolites quoted here the recovery of added substrate was
greater than 80%.
For the GC-MS analysis of low molecular weight carbohydrates leaf material was extracted with methanol5chloroform5water (125553, by vol.) for 30 min at 65 °C using
pentaerythritol as an internal standard. The phases were
separated by the addition of 1 ml distilled water. Aliquots of
the aqueous phase were dionized by ion-exchange and dried.
Carbohydrates were converted to trimethylsilyl derivatives and
separated by GC or GC-MS as described previously (Peterbauer
and Richter, 1998).
The extraction procedures used in this work have been
described previously: fructose 1,6-bisphosphatase (EC 3.1.3.11),
PFP (EC 2.7.1.90), 6-PF-1-K ( EC 2.7.1.11) (Hajirezaei and
Stitt, 1991); hexokinase (EC 2.7.1.1), aldolase (EC 4.1.2.13)
and glyceraldehyde phosphate dehydrogenase (EC 1.2.1.12)
(Bergmeyer, 1984a) and the activities of these enzymes were
determined spectrophotometrically (Hatzfeld et al., 1990).
14C-feeding experiments
The 14C-labelling of cell components of Craterostigma leaves
was performed by illuminating whole plants at a PPFD of
300 mmol m−2 s−1 at 24 °C for 30 min in a sealed vessel. The
radiolabelled carbon dioxide was supplied from 10 ml of 1 M
NaH14CO (specific activity, 3.7 GBq mmol−1) pH 9.0, placed
3
in a microfuge tube within the vessel. The distribution of
radioactivity between metabolites in the leaves was extracted
and analysed as detailed (Quick et al., 1988).
Photosynthetic rate and stomatal conductance
Measurements of photosynthetic rate and stomatal conductance
were made using an infrared gas analyser (Ciras-1, PP Systems,
Unit 2, Glovers Court, Bury Mead, Hitchin, Herts, Great
Britain) across the light and dark periods. The cuvette of the
IRGA was clipped over a known area of the leaves and the
measurements were taken once the leaves had acclimatized to
the conditions.
Phloem exudation experiments
Phloem exudation experiments were based on the techniques
used earlier ( King and Zeevaart, 1974). The region of the
leaves to be cut was lightly covered with a solution of 2 mM
EDTA and 5 mM sodium phosphate buffer (pH 7.0). Once cut
the leaf petiole was immediately placed in a microfuge tube
containing 1 ml of 2 mM EDTA and 5 mM sodium phosphate
buffer (pH 7.0). The leaves were then left and samples were
taken from the microfuge tube after 15 h light or dark and then
the carbohydrate content was assayed spectrophotometrically.
For GC determinations of phloem exudation content, samples
were taken between 2 h and 6 h after the start of incubation of
the leaves in the microfuge tubes.
Results
To determine the major synthetic pathways used during
photosynthesis in Craterostigma plantagineum plants
14CO was supplied to leaves at the beginning and at the
2
end of the light period ( Table 1). The measurements were
from both mature leaves and developing leaves. Mature
leaves were taken to be leaves that had attained greater
than 50% of their final size, whereas, young leaves were
growing leaves that were smaller than 50% of their final
size. The major products of photosynthesis in the leaves
were soluble and insoluble carbohydrates. There was a
clear change in partitioning of carbon fixed between the
start and end of the light period. The percentage of
carbon partitioned to soluble carbohydrates fell as the
photoperiod progressed, whereas that partitioned to
starch rose. A major proportion of the soluble carbohydrates was made up of the raffinose series oligosaccharides,
raffinose and stachyose. It was clear from these data that
2-octulose was made as a product of photosynthesis in
both young and mature leaves.
The concentration of sugars and starch within the
leaves of Craterostigma at a range of time points over a
24 h period was determined using GC and enzymatic
assays ( Fig. 1A, B). These data show that the concentration of all of the carbohydrates rose over the light period
Carbohydrate metabolism in Craterostigma plantagineum 161
Table 1. Fate of 14CO metabolized during photosynthesis in
2
young and mature Craterostigma leaves at the start and end of
the light period
Fraction
Starch
Soluble
Acidics
Basics
Neutrals
Stachyose
Raffinose
2-Octulose
Sucrose
Glucose
Fructose
Total 14CO
2
metabolized (kBq)
14C per fraction as % of metabolized
1 h into light period
11 h into light period
Young
leaves
Mature
leaves
Young
leaves
Mature
leaves
9.9±0.5
90.3±0.4
2.3±1.9
7.0±3.1
81.0±4.3
16.6±1.5
15.3±2.6
12.1±0.6
14.1±0.6
18.7±1.0
12.2±2.6
217±33
9.9±1.8
91.4±1.8
1.4±0.4
14.0±0.9
76.0±0.3
19.0±1.7
22.7±4.5
5.1±0.6
18.0±1.9
12.6±0.5
12.3±5.3
253±18
26.6±5.3
73.1±5.3
1.3±0.4
17.8±1.2
55.0±5.3
8.8±0.4
19.6±2.5
7.4±1.8
11.0±1.7
13.1±1.2
7.6±1.6
300±22
27.5±6.3
72.4±5.6
0.7±0.2
22.7±2.9
49.0±2.9
8.3±4.4
19.2±6.2
7.0±3.9
8.2±1.0
16.9±3.4
9.6±4.7
155±6
Craterostigma plants were supplied 14CO (for 30 min) in a sealed
2
vessel 1 h and 11 h into the light period. The young ( less than 50% of
mature size) and mature leaves were then harvested and the fate of the
14CO was determined. The results are shown ±SE from three replicate
2
measurements from three different plants.
and fell over the dark period. The largest fluctuations
were apparent in 2-octulose and starch amounts. Similar
measurements for root tissue, but at two time points, are
shown in Table 2. In the roots there were large quantities
of raffinose series oligosaccharides. GC analysis identified
this as being solely stachyose (data not shown). The
concentration of stachyose did not vary appreciably
across the day.
Since, in Table 1, raffinose series oligosaccharides were
a major product of metabolized 14CO in both young and
2
mature Craterostigma leaves, measurements were performed to investigate whether there was evidence that
raffinose series oligosaccharides were translocated in
Craterostigma plants. Therefore, phloem exudation
experiments were performed ( Table 3). These data reveal
that there are substantial concentrations of raffinose series
oligosaccharides in the phloem exudates. Fructose and
sucrose were also detected. A major percentage of the
exudates were identified as 2-octulose on the chromatograms and by GC analysis of the components of the
exudates. The raffinose series oligosaccharides were identified to be either stachyose or raffinose—78% and 22% of
the fraction, respectively.
To investigate the photosynthetic capacity of
Table 2. Carbohydrate content of roots of Craterostigma plantagineum at the start of the light and dark periods
Time of
day
Concentration of carbohydrate in root extract
(mmol hexose g−1 FW )
Glucose
Day
Night
Fructose
2.9±1.2 0.7±0.1
1.3±0.4 0.6±0.1
Sucrose
Starch
0.6±0.1 17.7±3.6
1.9±0.6 15.3±5.6
Raffinose series
oligosaccharides
179.0±12.7
164.9±10.4
Carbohydrates were extracted from boiled root samples and then
assayed spectrophotometrically. The measurements are the mean of
assays of four separate root samples from different plants ±SE.
Table 3. Percentage of sugars present in exudates from phloem
tissue in cut leaves of Craterostigma
Time of day
Percentage of carbohydrate in phloem exudate
Glucose Fructose
End of day
End of night
End of daya
Fig. 1. Variation in carbohydrate content in leaves of Craterostigma
over a 24 h period. In (A) measurements of myo-inositol (%), sucrose
(#), raffinose ($), and stachyose (2) are shown, and in (B)
measurements of 2-octulose (&) and starch (+) are shown. The values
are the means of three replicate values from different plants ±SE. All
measurements were performed using GC for this figure except for
starch which was measured enzymatically.
Sucrose
Raffinose
series
oligosaccharides
3.3±0.8 25.6±7.1 16.5±3.8 54.6±6.6
5.4±1.0 33.0±8.6 12.1±4.7 49.5±6.3
7.0±1.3 19.9±4.7 20.0±5.9 19.0±3.0
Octulose
NM
NM
27.3±3.5
Leaves were harvested at the end of the day or end of the night from
separate Craterostigma plants and then dipped in a solution of 2 mM
EDTA and 5 mM sodium phosphate for 15 h in the dark. After this
period the percentage of the carbohydrate present in different carbohydrates was determined spectrophotometrically.
aMeasurements were performed using GC in order to quantify
2-octulose content in the phloem. The measurements are the mean from
three separate plants shown±SE. NM not measured.
162 Norwood et al.
Craterostigma plants and the leaf water loss, the photosynthetic rate and stomatal conductance in leaves were
measured over the light period (Fig. 2). Photosynthetic
rates rose and then fell at the middle of the day, but
showed a second sharp rise just before night. The stomatal
conductance measurements correlated well with the
photosynthetic rates. The conductance was greatest when
photosynthetic rates peaked.
Since the Craterostigma plants accumulated large
amounts of 2-octulose in their leaves, the metabolic
pathways used for its metabolism were investigated. To
do this a range of enzymes and metabolites associated
with the glycolytic and gluconeogenic pathways was measured. Activity of the following enzymes was measured;
aldolase, glyceraldehyde phosphate dehydrogenase,
hexokinase, fructose 1,6-bisphosphatase, pyrophosphate5fructose 6-phosphate 1-phosphotransferase, and phosphofructokinase (Fig. 3). These enzymes were chosen
since it is known that aldolase can metabolize octulose
1,8-bisphosphate. Thus during photosynthetic synthesis
of 2-octulose, if octulose 1,8-bisphosphate was an intermediate of metabolism then there may be obvious changes
in enzyme activity associated in fluxes between CO
2
fixation and 2-octulose synthesis (in the light), and conversion of 2-octulose to sucrose and raffinose (in the
dark). With the exception of hexokinase, the changes in
enzyme activities across the day were almost identical.
Activity remained high during the light period and fell
on the onset of darkness. Thus the activity of these
enzymes fell as carbohydrate in the leaves (starch, sucrose
and 2-octulose) was mobilized.
Measurements of Glc 6-P, Fru 6-P and 3-PGA over a
24 h period are shown in Fig. 4. The concentration of
3-PGA rose during the light period and fell at night. Glc
6-P acted similarly to 3-PGA but concentrations fell more
Fig. 3. Activity of a range of enzymes thought to be involved in
carbohydrate metabolism in Craterostigma leaves over a 24 h period.
Enzyme measurements were taken every 4 h over a 24 h period using a
spectrophotometer. The points are aldolase (+), glyceraldehyde phosphate dehydrogenase (2), fructose 1,6-bisphosphatase (#), hexokinase
(&), phosphofructokinase (%), and pyrophosphate: fructose
6-phosphate 1-phosphotransferase ($).The results are the mean±SE
from three replicate measurements from different plants.
slowly during the dark period. Fru 6-P concentrations
showed greater variability than the other two metabolites.
Fru 6-P concentrations were steady during the day but
peaked at night.
Discussion
Fig. 2. Photosynthetic rates and stomatal conductance of leaves of
Craterostigma over the light period. Measurements of photosynthetic
rate (&) and stomatal conductance (#) were made with an IRGA
every 2 h across the light period. The results are the mean±SE from
four replicate measurements from different plants.
Although this investigation has not focused upon the
metabolic events of dehydration and rehydration of the
resurrection plant Craterostigma plantagineum, it is
important to understand how this plant prepares itself
for this unusual capability. From these measurements the
plant appears much like any other C species. With the
3
exception of fructose 6-phosphate the phosphorylated
Carbohydrate metabolism in Craterostigma plantagineum 163
Fig. 4. Concentrations of sugar phosphates in leaves of Craterostigma
over a 24 h period. Metabolite measurements were taken every 4 h over
a 24 h period using a spectrophotometer. The points are glucose
6-phosphate (&), fructose 6-phosphate (#), and 3PGA (%). The
results are the mean±SE from four replicate measurements from
different plants.
metabolic intermediates and enzyme activities were not
greatly different from those seen in plants such as spinach
(Gerhardt et al., 1987). Generally, in C plants the
3
concentrations of metabolic intermediates and activity of
enzymes associated with gluconeogenic fluxes are high
during the day, fall at the start of the night and then rise
again throughout the night. This can be seen for the
enzyme activities (except hexokinase) and two of the
phosphorylated metabolic intermediates measured. At
night the Craterostigma plants contain very high concentrations of fructose 6-phosphate. Why this should be so
requires further analysis. Three significant observations
stand out from the measurements presented in this report.
(1) Craterostigma plantagineum transports raffinose
series oligosaccharides in the phloem. This is a mode of
translocation of carbohydrate around the plant which is
less frequently adopted than the transport of sucrose, but
it is not uncommon ( Turgeon, 1995). In addition, raffinose series oligosaccharides are very frequently translocated in members of the Scrophulariaceae family of which
Craterostigma is a member ( Turgeon et al., 1993). There
was evidence for a very large accumulation of the raffinose
series oligosaccharide, stachyose, in the roots of the plant.
This has been shown before by other workers using
HPLC (Schwall et al., 1995). Thus, not only are the
raffinose series oligosaccharides used for translocation of
carbohydrate in Craterostigma but also as a carbohydrate
store in roots. Storage of raffinose series oligosaccharides
in plant tissues has been identified in a number of plants
such as stachyose in the Japanese artichoke (Stachys
sieboldii ) and ajugose in common bugle (Ajuga reptans)
( Keller, 1995).
(2) In agreement with other research, the dominant
carbohydrate in leaves of Craterostigma was found to be
2-octulose (Bianchi et al., 1991). However, these observations were taken further and ways in which the concentrations of 2-octulose vary throughout the light and dark
periods was studied. 2-octulose concentrations cycle over
the 24 h period. In fact they appear to act as a storage
carbohydrate like starch in most C plants (Gerhardt
3
et al., 1987). The Craterostigma plants do make starch,
but the amount of carbon entering starch for storage
compared to 2-octulose is small. The difference between
the high and low points for concentration of hexose in
starch compared with similar measurements for 2-octulose
were 11.1 mmol g−1 FW and 20.5 mmol g−1 FW, respectively. Thus 2-octulose appears to be used as a soluble
storage carbohydrate in the leaves, which is mobilized at
night. The accumulation of 2-octulose and its mobilization
appeared to anticipate the change of the light state rather
than respond to it. The significance of this observation
may be that 2-octulose concentrations are controlled via
circadian rhythms.
The observation that 2-octulose concentrations exhibit
a diurnal variation is very important if the metabolism
of this carbohydrate is ever to be understood. These data
suggest that any programme to analyse the pathways for
2-octulose metabolism need not necessarily focus solely
on the dehydration and rehydration phases of the plant’s
life cycle. The enzymes required for 2-octulose metabolism
must be present in young and mature leaves even in the
well-watered state. Certainly no new enzymes need to be
up-regulated in order to allow the interconversion of
2-octulose and sucrose during dehydration or rehydration.
However, it is clear from earlier data that a large number
of different proteins are up-regulated in Craterostigma
during drought stress (Alamillo and Bartels, 1996). The
enzymes measured here were chosen since they are
enzymes potentially involved in the metabolism of octulose 1,8-bisphosphate that may be an intermediate of
2-octulose metabolism (Bergmeyer, 1984c). During
dehydration and rehydration in Craterostigma, mRNA
concentrations of glyceraldehyde phosphate dehydrogenase (a glycolytic enzyme) and transketolase (oxidative
pentose phosphate pathway enzyme) have been shown to
increase ( Velasco et al., 1994; Bernacchia et al., 1995).
Measurements across the 24 h period show that most of
164 Norwood et al.
the enzymes measured had their highest activity in the
day and lowest at night. Thus enzyme activity peaked
when sucrose, starch and 2-octulose were accumulating
in leaves. Across the 24 h period these data show that
despite large changes in the concentration of 2-octulose
in the tissue there was little diurnal fluctuation in the
extractable activities of any of the enzymes measured.
Further analysis is necessary to understand the pathways
for metabolism of 2-octulose in Craterostigma and it is
possible that the cycling in 2-octulose that was observed
is very different from the mobilization of 2-octulose
observed during dehydration and rehydration of the plant.
(3) 2-Octulose was found to be a major component of
the phloem exudates. Since plant species that translocate
raffinose series oligosaccharides use symplastic loading of
the phloem there is no requirement for a specific
2-octulose transporter to gain entry into the seive tubes
( Turgeon 1995). These data indicate that 2-octulose is
one of the major components of the phloem in the leaf
petioles. However, whole root measurements suggest that
2-octulose makes up only a trace component of the roots.
Thus at some point during translocation to the root cell
the 2-octulose must be metabolized to other
carbohydrates.
Other measurements made from the Craterostigma
plants were unremarkable. The photosynthetic rate that
was measured from the leaves was low compared with
other C plants. However, the measurements from this
3
study are similar to those reported in Craterostigma by
other authors (Schwab et al., 1989), when they studied
the response of photosynthesis with respect to dehydration stress. Accumulation of sucrose and raffinose series
oligosaccharides in the leaves during the light period was
minimal which is typical of plant species which translocate
raffinose series oligosaccharides ( Keller, 1995). The root
tissues showed no accumulation of 2-octulose, but accumulated very large concentrations of stachyose. From
these observations, the primary roots of Craterostigma
are able to resurrect, but no detailed studies of the
physiology of roots during dehydration and rehydration
have been performed, so it is not possible at this time to
comment on the extent of desiccation tolerance exhibited
by roots. If roots accumulate sucrose in order to become
desiccation tolerant, then since 2-octulose is absent from
roots an alternative carbohydrate source must be used to
fuel this accumulation. However, the presence of raffinose
series oligosaccharides may be involved in the resistance
of the roots to drought stress, as has been suggested in
other plant tissues ( Keller, 1995). What these indicate is
that, other than the synthesis of 2-octulose in leaves,
Craterostigma appears to be little different from other
plants that are unable to undergo the resurrection process.
This work has provided the basis for a programme of
research investigating the metabolic abilities of
Craterostigma plantagineum that allow it to be able to
survive almost complete desiccation. Further research is
in progress to investigate the metabolic processes that
Craterostigma uses in order to allow tissues to dehydrate
and then resurrect.
Acknowledgements
Ms M Norwood thanks the University of Sussex for funding
her PhD post. Dr M Truesdale thanks the BBSRC for
supporting his role in this research.
References
Alamillo JM, Bartels D. 1996. Light and stage of development
influence the expression of desiccation-induced genes in the
resurrection plant Craterostigma plantagineum. Plant, Cell
and Environment 19, 300–310.
Bergmeyer HU. 1984a. Methods of enzymatic analysis, Vol. 4.
Weinheim, Germany: Verlag Chemie, 212–223.
Bergmeyer HU. 1984b. Methods of enzymatic analysis, Vol. 6.
Weinheim, Germany: Verlag Chemie, 90–96.
Bergmeyer HU. 1984c. Methods of enzymatic analysis, Vol. 6.
Weinheim, Germany: Verlag Chemie, 142–148.
Bernacchia G, Schwall G, Lottspeich F, Salamini F, Bartels D.
1995. The transketolase gene family of the resurrection plant
Craterostigma plantagineum: differential expression during the
rehydration phase. EMBO Journal 14, 610–618.
Bianchi G, Gamba A, Murelli C, Salamini F, Bartels D. 1991.
Novel carbohydrate metabolism in the resurrection plant
Craterostigma plantagineum. The Plant Journal 1, 355–359.
Drennan PM, Smith MT, Goldsworth D, Van Staden J. 1993.
The occurrence of trehalose in the leaves of the desiccation
tolerant angiosperm Myrothamnus flabellifolius Welw. Journal
of Plant Physiology 142, 493–496.
Gaff DF. 1971. Desiccation tolerant plants in Southern Africa.
Science 174, 1033–1034.
Gerhardt R, Stitt M, Heldt HW. 1987. Subcellular metabolite
levels in spinach leaves. Plant Physiology 83, 399–407.
Hajirezaei M, Stitt M. 1991. Contrasting roles for pyrophosphate:fructose 6-phosphate phosphotransferase during aging of
tissues from potato tubers and carrot storage tissues. Plant
Science 77, 177–183.
Hatzfeld W-D, Dancer J, Stitt M. 1990. Fructose-2,6-bisphosphate: metabolism and control of pyrophosphate5fructose
6-phosphate phosphotransferase during triose phosphate
cycling in heterotrophic cell-suspension cultures of
Chenopodium rubrum. Planta 180, 205–211.
Ingram J, Bartels D. 1996. The molecular basis of dehydration
tolerance in plants. Annual Review in Plant Physiology and
Plant Molecular Biology 47, 377–403.
Keller F. 1985. Role of the vacuole in raffinose oligosaccharide
storage. In: Pontis H, Salerno G, Echeverria E, eds. Sucrose
metabolism, biochemistry, physiology, and molecular biology.
Current topics in plant physiology, Vol. 14. American Society
of Plant Physiologists, 156–166.
King R, Zeevaart J. 1974. Enhancement of phloem exudation
from cut petioles by chelating agents. Plant Physiology
53, 96–103.
Michal G. 1984a. -glucose 6-phosphate and -fructose
6-phosphate. In: Bergmeyer HU, ed. Methods of enzymatic
analysis, Vol. 6. Weinheim, Germany: Verlag Chemie,
191–198.
Michal G. 1984b. -fructose 1,6-bisphosphate, dihydroxyacetone
Carbohydrate metabolism in Craterostigma plantagineum 165
phosphate and -glycerate 3-phosphate. In: Bergmeyer HU,
ed. Methods of enzymatic analysis, Vol. 6. Weinheim,
Germany: Verlag Chemie, 342–350.
Morell S, ap Rees T. 1986. Control of hexose content of potato
tubers. Phytochemistry 25, 1073–1076.
Müller J, Sprenger N, Bortlik K, Boller T, Wiemken A. 1997.
Desiccation increases sucrose levels in Ramonda and Haberlea,
two genera of resurrection plants in the Gesneriaceae.
Physiologia Plantarum 100, 153–158.
Peterbauer T, Richter A. 1998. Metabolism of galactosylononitol
in seeds if Vigna umbellata. Plant Cell Physiology 39, 334–341.
Quick WP, Neuhaus HE, Stitt M. 1989. Increased pyrophosphate is responsible for a restriction of sucrose synthesis after
supplying fluoride to spinach leaf discs. Biochimica et
Biophysica Acta 973, 263–271.
Schwab KB, Schreiber U, Heber U. 1989. Response of
photosynthesis and respiration of resurrection plants to
desiccation and rehydration. Planta 177, 217–227.
Schwall G, Elster R, Ingram J, Bernacchia G, Bianchi G,
Gallagher L, Salamini F, Bartels D. 1995. Carbohydrate
metabolism in the desiccation tolerant plant Craterostigma
plantagineum Hochst. In: Pontis H, Salerno G, Echeverria E,
eds. Sucrose metabolism, biochemistry, physiology, and molecular biology. Current topics in plant physiology, Vol. 14.
American Society of Plant Physiologists, 245–253.
Turgeon R. 1995. The selection of raffinose family oligosaccharides as translocates in higher plants. In: Madore, MA, Lucas
WJ, eds. Carbon partitioning and source sink interactions in
plants. Current topics in plant physiology, Vol. 13. American
Society of Plant Physiologists, 195–203.
Turgeon R, Beebe DU, Gowan E. 1993. The intermediary cell;
minor vein anatomy and raffinose oligosaccharide synthesis
in the Scrophulariaceae. Planta 191, 446–456.
Velasco R, Salamini F, Bartels D. 1994. Dehydration and ABA
increase mRNA levels and enzyme activity of cytosolic
GAPDH in the resurrection plant Craterostigma plantagineum. Plant Molecular Biology 26, 541–546.