Plant Physiol, December 2001, Vol. 127, pp. 1346-1353
SCIENTIFIC CORRESPONDENCE
Desiccation Tolerance in the Resurrection Plant
Craterostigma plantagineum. A Contribution to the Study of
Drought Tolerance at the Molecular Level1
Dorothea
Bartels* and
Francesco
Salamini
Institute of Botany, University of Bonn, Kirschallee 1, D-53115
Bonn, Germany (D.B.); and Max-Planck-Institut für
Züchtungsforschung, Carl-von-Linné-Weg 10, D-50829
Köln, Germany (F.S.)
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INTRODUCTION |
Adverse environmental
conditions restrict the productivity and the range of habitats
available to plants. This represents a severe economic constraint on
agricultural production. Plants as sessile organisms have evolved a
wide spectrum of adaptations to cope with the challenges of
environmental stress. Quite often, however, adaptation mechanisms
themselves adversely affect yield parameters, and a compromise between
biomass production and environmental fitness has to be accepted. One
major factor that limits the productive potential of higher plants is
the availability of water. The International Water Management Institute
predicts that by the year 2025, one-third of the world's population
will live in regions that will experience severe water scarcity
(www.iwmi.org). Therefore, it has become imperative for plant
biologists to understand the mechanisms by which plants can adapt to
water deficit while retaining their capacity to serve as sources of
food and other raw materials.
Water deficit can affect plants in different ways. A mild water deficit
leads to small changes in the water status of plants, and plants cope
with such a situation by reducing water loss and/or by increasing water
uptake (Bray, 1997
). The most severe form of water deficit is
desiccation
when most of the protoplasmic water is lost and only a
very small amount of tightly bound water remains in the cell.
Both forms of water deficit have been studied at the molecular level
using a variety of experimental systems. Arabidopsis has been
extensively studied as a model plant that tolerates moderate water
deficit. Genes involved in many different pathways are expressed in
response to water stress in Arabidopsis, and the molecular complexity
of the process is best illustrated by recent microarray experiments
(Seki et al., 2001). Mutant analysis has greatly contributed to our
knowledge of the mode of gene regulation under stress, and it has
become obvious that a network of signal transduction pathways allows
the plant to adjust its metabolism to the demands imposed by water
deficit (Shinozaki and Yamaguchi-Shinozaki, 2000; for review, see Kirch
et al., 2001b). These studies raise two major questions: (a) Do diverse
plants use different pathways to respond to the stress?, and (b) Do
variable degrees of water stress activate different metabolites?
Most flowering plants cannot survive exposure to a water deficit
equivalent to less than 85% to 98% (v/v) relative humidity during their vegetative growth period, although desiccation is an
integral part of the normal developmental program of most higher plants
in the context of seed formation. Only a few plants possess desiccation-tolerant vegetative tissues; these include a small group of
angiosperms, termed resurrection plants (Gaff 1971), some ferns, algae,
lichens, and bryophytes.
Some of these species can equilibrate the leaves with air of 0%
(v/v) relative humidity. Resurrection plants can be revived from
an air-dried state and are often poikilohydrous, i.e. their water
content varies with the relative humidity in the environment. Resurrection plants are found in ecological niches with limited seasonal water availability, preferentially on rocky outcrops at low to
moderate elevations in tropical and subtropical zones (Porembski and
Barthlott, 2001). It has been estimated that around 200 species of
resurrection plants may exist, mainly in Southern Africa, Australia,
India, and South America (W. Barthlott, personal communication). The
physiological basis of desiccation tolerance in resurrection plants is
complex. Some mechanisms may vary between different species; for
example, some species retain chlorophyll during dehydration, whereas
others lose their chlorophyll.
Studies aimed at understanding the molecular basis of desiccation
tolerance have focused on a few species representing different groups:
the dicotyledonous South African Craterostigma plantagineum (Bartels et al., 1990), the monocotyldonous species Sporobulus stapfianus (Neale et al., 2000), and the moss Tortula
ruralis (Oliver and Bewley, 1997). Most information is available
on C. plantagineum, which will be the main focus of this
review. For this plant, the phenomenon of desiccation tolerance is
shown in Figure 1.
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Figure 1.
The desiccation-tolerant resurrection plant
Crateostigma. A, C. pumilum
plants in their native habitat in Kenya (photograph courtesy of
Dr. W. Barthlott, University of Bonn). B, Effect of desiccation
on a C. plantagineum fully turgid plant, a desiccated plant,
and a plant rehydrated for 12 h. C, Callus from left to right:
untreated, 0 to 7 d. Abscisic acid (ABA)-treated callus, dried and
regrown.
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C. PLANTAGINEUM AS AN EXPERIMENTAL SYSTEM |
The attraction of C. plantagineum as an experimental
system is due to the fact that desiccation tolerance is expressed in vegetative tissues and in undifferentiated callus cultures. This allows
one to compare gene expression in two systems with the same genetic
backgroundin the absence of developmental complications, such as
those that may arise when acquisition of desiccation tolerance during
seed development is investigated. Callus from C. plantagineum is not intrinsically desiccation tolerant, but it
acquires tolerance after it has been cultured on medium containing the
plant hormone ABA (Bartels et al., 1990). Treatment of callus with ABA
induces the expression of a set of mRNAs comparable with that activated upon drying in the whole plant. C. plantagineum is suited
for molecular studies because it can be genetically transformed by Agrobacterium tumefaciens (Furini et al., 1994) and it is
suited for transient expression analysis using protoplasts or a
ballistic approach.
Studies with C. plantagineum have shown that the
physiological state of the plant before the onset of drying appears to
be critical for survival. The plants only develop the ability to survive desiccation, if water loss occurs slowly enough to allow their
metabolism to adapt by activating a specific program of gene
expression. If dehydration occurs too rapidly, plants do not acquire
tolerance to desiccation. Most changes in gene expression occur during
dehydration and relatively few are observed during the rehydration
phase. Thus, many dehydration-specific gene products have been isolated
but very few rehydration-specific proteins are known (Bernacchia et
al., 1996). This is in contrast to observations made on T. ruralis, a representative of the desiccation-tolerant bryophytes,
which survives rapid desiccation. Here, the major changes in gene
expression occur during the first hours of rehydration (Wood and
Oliver, 1999). In this case, changes in gene expression in response to
dehydration and rehydration are regulated at the translational level,
resulting in a change in the complement of mRNAs selected for protein
synthesis from a relatively constant mRNA pool (Wood and Oliver, 1999).
These findings support the suggestion that desiccation tolerance in
bryophytes differs from that in C. plantagineum in being
mainly a rehydration-induced cellular repair response (Oliver and
Bewley, 1997).
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MOLECULAR AND METABOLIC CHANGES IN C. PLANTAGINEUM
DURING THE DEHYDRATION/REHYDRATION CYCLE |
In C. plantagineum, dehydration leads to
drastic changes in gene expression and carbohydrate metabolism,
increases in ABA levels and photosynthesis-related processes, and
changes in cell ultrastructure. This plant reacts within the first
2 h to dehydration, and the metabolic changes are initiated before
any signs of wilting are apparent. All of the dehydration-induced
processes are reversed during rehydration. In this review, we will
mainly focus on the processes that occur during dehydration because
these appear to be important for cellular protection and probably also
for recovery during rehydration.
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PHOTOSYNTHESIS AND ENERGY METABOLISM |
Water relations in plants are regulated to a large extent via the
opening and closure of stomata. Water deficit leads to closure of
stomata and at the same time to a decrease in intercellular CO2 concentration. As a consequence of the lower
CO2 availability, carbon assimilation is
inhibited and ultimately photosynthetic capacity is lost. This
observation is common to dehydration-sensitive and drought-tolerant
species (Schwab et al., 1989). These physiological changes are reflected at the molecular level: The steady-state levels
of transcripts related to photosynthesis are down-regulated in response
to water stress, e.g. the transcript for the small subunit of
the Rubisco enzyme in C. plantagineum (Bernacchia et al.,
1996). However, a particular feature of resurrection plants is that
they recover full photosynthetic activity following rewatering. Respiration is quickly restored in C. plantagineum on
rewatering when the water content reaches about 20% of its initial
value. This allows us to conclude that protective mechanisms must be in
place that maintain the integrity of the photosynthetic machinery in
the dried plant tissue. This inference correlates well with observations that several putative protective proteins accumulate in
plastids of C. plantagineum, which are targeted to the
stroma and to thylakoid membranes (Schneider et al., 1993).
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CARBOHYDRATE METABOLISM |
In many organisms, bacteria and yeasts in particular, high
concentrations of carbohydrates are observed in dry tissues, and a
contribution of carbohydrates to desiccation tolerance has been proposed. This is supported by in vitro studies showing that a wide
range of biomolecules is less susceptible to denaturation when
dehydrated in the presence of sugars (Crowe et al., 1992). In seeds of
higher plants, a correlation has been observed between the accumulation
of soluble sugars and the acquisition of desiccation tolerance
(Leprince et al., 1993). In C. plantagineum, a remarkable change in carbohydrate metabolism occurs on dehydration (Fig. 2). The unusual C8 sugar octulose is
present in large quantities (up to 90% of the soluble sugars,
corresponding to up to 400 mg g
1 of lyophilized
leaf material) in photosynthetically active leaves. Upon dehydration,
the octulose level declines and conversely Suc accumulates; the reverse
is observed during rehydration (Bianchi et al., 1991). Despite the
qualitative change in sugar composition, the overall sugar content is
similar in hydrated and dried leaves. The accumulation of Suc in
dehydrated tissues seems to be a common theme in different resurrection
plants, although different metabolic routes may be used for the
synthesis of Suc. It is interesting that the sugar composition in roots
of C. plantagineum does not change drastically with water
availability. The tetrasaccharide stachyose is the dominant sugar,
comprising more than 50% of the total sugar content, and octulose is
only found in small amounts in untreated and in dehydrated roots.
Octulose is probably a product of photosynthesis that accumulates in
leaves during the light period, but is partially metabolized at night.
Because octulose has been found in the phloem sap, it is likely that it
is transported from leaves to roots (Norwood et al., 2000).
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Figure 2.
The most prominent sugars found in C. plantagineum. 2-Octulose is predominant in untreated leaves and is
converted to Suc upon dehydration. Stachyose is the major sugar in both
untreated and dried roots.
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To understand the biochemical basis for this switch in sugar
metabolism, the expression of genes encoding sugar-metabolizing enzymes
was investigated. C. plantagineum possesses a set of genes encoding isoenzymes of Suc synthase and Suc phosphate synthase (Ingram
et al., 1997; Kleines et al., 1999), which are differentially expressed. Besides these enzymes and the dehydration-induced expression of cytosolic glyceraldehyde dehydrogenase, it has been proposed that
transketolase contributes to the conversion of octulose to Suc. In
addition to a constitutively expressed, plastid-localized transketolase, induction of two genes for transketolases during rehydration has been reported (Bernacchia et al., 1995). In C. plantagineum, two main questions concerning the carbohydrate
metabolism are still open: (a) What enzymes are involved in the
biosynthetic pathway leading to octulose?, and (b) Does Suc act as a
protectant in the dehydrated leaves?
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THE TRANSCRIPTIONAL RESPONSE TO DEHYDRATION |
The basic pattern of changes in gene expression that occur in
response to dehydration can be summarized for C. plantagineum as follows: (a) Transcripts accumulate to high levels
during dehydration and disappear early during rehydration, (b)
transcripts accumulate transiently during the initial dehydration
phase, (c) transcripts decline during dehydration, and (d) transcripts
remain unchanged in response to dehydration.
It is estimated from transcript profiling that several hundred genes
probably are differentially expressed in response to dehydration
(Bockel et al., 1998). The identified genes encode compounds that can
be assigned to diverse metabolic pathways, although their precise
function has not yet been demonstrated. The following main groups can
be distinguished: (a) genes encoding proteins with protective
properties, (b) genes encoding membrane proteins involved in transport
processes, (c) genes encoding enzymes related to carbohydrate
metabolism, (d) genes encoding regulatory molecules, such as
transcription factors, kinases, or other putative signaling molecules,
and (e) genes that show no homologies to known sequences. Studies on
tissue-specific expression patterns and subcellular localizations have
revealed specific cellular distributions of RNAs and proteins that
appear to correlate with their predicted functions (Phillips et al.,
2001).
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PROTEINS WITH PROTECTIVE PROPERTIES |
This group includes the proteins that accumulate most abundantly
in different tissues of C. plantagineum during dehydration. Its major representatives include late embryogenesis-abundant (LEA)
proteins (Schneider et al., 1993), some proteins with enzymatic function, e.g. an aldehyde dehydrogenase (Kirch et al., 2001a), and
also some small heat shock proteins (Alamillo et al., 1995). LEA
proteins are a heterogenous group of proteins found universally in
plants, which were first discovered because they accumulate to high
levels during late stages of embryo development. Synthesis of LEA
proteins is associated with dehydration in seeds and with water deficit
in vegetative tissues (Cuming, 1999). Dehydration-elicited expression of LEA genes is not restricted to resurrection plants but
has been extensively reported also for non-tolerant plants.
LEA proteins are divided into different classes based on conserved
sequence motifs. In general, LEA proteins are hydrophilic and have a
biased amino acid composition, mostly lacking Cys and Trp. They are
typically highly water soluble, and they often remain soluble after
boiling. Despite extensive studies, our knowledge of the biochemical
function of LEA proteins is still rudimentary, but molecular and
biochemical features strongly suggest a protective role for them. A
protective function correlates with their cellular distribution: LEA
polypeptides are found in all cell types, accumulating abundantly in
cytoplasm or plastids (Schneider et al., 1993). This protective role is
further corroborated by Wolkers et al. (1998), who showed that LEA
proteins may be anchors in a structural network stabilizing cytoplasmic
components during pollen drying. Two approaches have been used to
demonstrate that LEA proteins function as cellular protectants: in
vitro protection assays with purified proteins and in planta studies in
which LEA proteins were overexpressed. The results generally support a
protective role (Xu et al., 1996), although contradictory observations
have also been reported (Iturriaga et al., 1992). One conclusion
that can be drawn from functional analysis indicates that individual LEA proteins make only a small contribution to dehydration tolerance, whereas the coordinated synthesis of the complete set of proteins probably plays a central role. Biochemical experiments, including structural analysis of native proteins, are needed to understand the
role of each specific LEA protein. It is remarkable that LEA genes contain sequence motifs that are conserved in all higher plants.
This strict conservation during evolution indicates that these motifs
define functional units within these proteins.
Thus, our studies suggest that desiccation tolerance in vegetative
tissues in C. plantagineum is probably not due to structural genes that are unique to resurrection plants, but that relevant genes
are also present in the genome of non-tolerant plants. The difference
between tolerant and non-tolerant plants is likely to reside in the
expression patterns and is likely to be at least in part a quantitative
characteristic with respect to LEA genes. A comparison of
dehydration-induced gene expression in the tolerant C. plantagineum with a non-tolerant close relative may provide further evidence for this hypothesis.
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REGULATION OF GENE EXPRESSION DURING DEHYDRATION |
An understanding of gene regulation is particularly important in
the case of a multigenic trait like desiccation tolerance because
different regulatory pathways determine the expression of a whole set
of genes. Knowledge of regulatory circuits is scarce; individual
factors have been characterized, but their interaction with other
molecules within the network is for the most part unknown. Several
experimental approaches have been followed to identify molecules
involved in the activation of gene expression in response to stress.
Most information is derived from promoter analyses and from
differential screening procedures. Mutants have contributed to
understanding gene regulation in Arabidopsis (Shinozaki and Yamaguchi-Shinozaki, 2000). A mutational approach to desiccation tolerance in C. plantagineum is quite difficult because of
the polyploid nature of its genome.
One molecule that is central to dehydration-regulated gene expression
is the plant hormone ABA. Exposure of C. plantagineum plants
and callus to exogenous ABA induces genes that are otherwise activated
by dehydration. Specifically in callus tissue, ABA is required to
induce the genes needed for the expression of tolerance. The regulation
of gene expression by dehydration and ABA involves several signaling
pathways and different cis-acting elements in the stress-responsive genes.
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PROMOTER ANALYSIS |
Promoters of LEA-type genes and of genes encoding
dehydration-inducible enzymes have been analyzed and compared.
Comparisons of the promoter sequences did not reveal obvious common
motifs. Therefore, several promoters were analyzed in transgenic
tobacco (Nicotiana tabacum) and Arabidopsis plants to
define functional cis-elements. The promoters tested were found to be
highly active in seeds and pollen, but two out of three promoters were
not active in vegetative tissues of Arabidopsis or tobacco (Furini et
al., 1996; Velasco et al., 1998). Only the promoter of the gene
CDeT6-19 was inducible by dehydration or ABA in vegetative
tissues of a heterologous plant. However, ectopic expression of the
Arabidopsis ABI-3 gene product leads to activation of the other two
promoters in Arabidopsis leaves upon ABA treatment (Furini et al.,
1996; Velasco et al., 1998). ABI-3 encodes a transcription
factor that is active during seed development in Arabidopsis. In view
of the fact that C. plantagineum synthesizes in vegetative
tissues many LEA-type transcripts that are closely related to those of
LEA genes expressed during seed maturation, an
ABI-3 homolog was isolated from C. plantagineum
to test the possibility that such a gene might be responsible for
transcriptional activation of LEA-type genes in vegetative tissues of
C. plantagineum. A gene closely related to the Arabidopsis
ABI-3 gene was isolated, and its product was indeed able to
transactivate LEA genes in transient expression assays
(Chandler and Bartels, 1997). However, expression of the ABI-3
homolog was not detected in fully developed leaves of C. plantagineum. Therefore, other transcription factors must be
involved in the activation of LEA genes.
In many genes regulated by ABA and osmotic stress, one or more ABA
response elements (ABREs) play a key role in promoter activity. The
ABREs have a core ACGT-containing G-box motif. It is assumed that
transcription factors of the basic Leu zipper type bind as dimers to the ABREs. Modified core ABRE elements are present in LEA
gene promoters in C. plantagineum, but they do not seem to be the major determinant of ABA responsiveness. Instead, e.g. in the
CDeT27-45 promoter, other elements have been identified that bind
nuclear proteins in an ABA-dependent fashion and are essential for
activation of a reporter gene in response to ABA (Kirch et al.,
2001b).
Molecules with putative transcriptional activities or with a putative
signaling role have been defined in our laboratory in the course of
various differential screening experiments. Their identification is
based on sequence homology to known molecules. Transcripts encoding
these molecules are induced during the early phase of dehydration
and/or by ABA treatment, thus suggesting an involvement in the
dehydration response. In this way, genes for several potential
transcription factors were isolated, and it was shown that members of
diverse gene families participate in the response of C. plantagineum to dehydration. These include genes for Myb and a
heat shock transcription factor, members of the homeodomain Leu zipper
(HDZIP) family, a phospholipase D (PLD), a kinase, and the gene
CDT-1. These genes represent single building blocks in a
complex regulatory network, but in most cases their target genes are
still elusive and it is not known whether and, if so, how individual
regulatory pathways interact with each other. In the following section,
three examples of studies on such C. plantagineum factors
will be described.
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HDZIP GENES |
HDZIP genes are specific for plants and are thought to regulate
developmental processes, and responses to environmental cues ranging
from light perception to pathogen-induced and abiotic stress. HDZIP
proteins are characterized by the presence of a DNA-binding homeodomain
adjacent to a Leu zipper motif that mediates protein-protein
interactions (Ruberti et al., 1991). The activity of HDZIP proteins
resides primarily in binding of the homeodomain to specific HDE
recognition sequences present in promoters of target genes. Several
HDZIP genes that are regulated by dehydration have been isolated from
C. plantagineum, indicating that this family of
transcription factors is likely to play a major role in modulating gene
expression during dehydration. Research in Arabidopsis supports this
idea. Two HDZIP genes from C. plantagineum, CPHB-1 and CPHB-2, are of particular interest
because their products were shown to interact in a yeast
(Saccharomyces cerevisiae) two-hybrid system (Frank
et al., 1998). Both transcripts were inducible by dehydration, but only
CPHB-2 was responsive to ABA. This suggests that the two
genes act in different pathways of the regulatory network, an
ABA-mediated pathway and an ABA-independent pathway. Cross talk between
these two pathways should be possible through the interaction of the
two HDZIP proteins. Although no target genes for the HDZIP proteins
have been definitively identified, active binding sites for HDZIP
proteins were found in the promoters of at least two
desiccation-regulated genes.
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THE NOVEL CDT-1 GENE |
Because of its ploidy level, the best way to obtain mutants in
C. plantagineum is to induce dominant mutations. The
ABA-dependent induction of desiccation tolerance in the callus system
offers the opportunity to screen for such dominant mutants. The
C. plantagineum leaf discs are transformed by infection with
A. tumefaciens cells bearing a T-DNA vector
containing enhancer fragments of the 35S-cauliflower mosaic
virus promoter. The enhancers are inserted randomly into the
genome and, if present in appropriate positions, should lead to gene
activation. Among thousands of regenerated calli, a transgenic callus
was selected that was capable of surviving desiccation without prior
addition of ABA to the medium. Analysis of RNA transcripts showed that
genes were constitutively expressed in the mutant callus, which in
non-transformed calli can only be induced by ABA treatment. The gene
targeted by the T-DNA, which led to the constitutive activation of
desiccation-related genes, was isolated and named CDT-1
(Furini et al., 1997). CDT-1 is present in multiple copies
in the genome of C. plantagineum and its expression can be
induced by ABA in non-transformed callus and plants. The most surprising feature of the gene is that it has only a very short open
reading frame encoding a putative polypeptide of 22 amino acids. To
date, it has not been possible to demonstrate the presence of a
polypeptide encoded by cDT-1, and further experiments
support the hypothesis that CDT-1 may act as a regulatory RNA. Besides CDT-1, another example for a gene with such properties is
the ENOD40 gene from Medicago sativa,
which controls the organogenesis of Rhizobium
meliloti-induced N2-fixing
nodules (Crespi et al., 1994). No sequence homolog to cDT-1
was identified in the Arabidopsis genome, but this does not exclude the
possibility that Arabidopsis encodes transcripts that may function at
the RNA level. On the other hand, the function of cDT-1 may
be specifically related to the highly sensitive and effective set of
reactions that protect C. plantagineum from the effects of
severe desiccation.
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ACTIVATION OF PLD: AN EARLY EVENT IN THE DEHYDRATION RESPONSE |
Recently, phospholipid metabolism has been suggested to be
involved in plant responses to various forms of osmotic stress (Munnik
and Meijer, 2001). The formation of phospholipid-based signaling
molecules may well be among the primary events in the signaling cascade
that leads from the perception of water stress to stress-adapted
metabolism. In the context of the desiccation response in C. plantagineum, PLD is of particular interest. PLD catalyzes the
hydrolysis of a structural phospholipid, phosphatidylcholine, and other
phospholipids, to form phosphatidic acid (PA). PA in turn regulates
protein kinases or small GTP-binding proteins. In C. plantagineum, PLD activity is induced within minutes by dehydration (Frank et al., 2000). The PLD activity is specific for
dehydration and is not induced by ABA. Two cDNA clones
(CpPLD-1 and CpPLD-2) encoding PLDs have been
isolated. The CpPLD-1 transcript is constitutively
expressed, whereas CpPLD-2 is responsive to dehydration
(Frank et al., 2000). Analysis of PLD proteins indicates a complex
regulation at the level of expression and cellular distribution depending on the physiological status of the plant. The constitutively expressed CpPLD-1 is likely to be involved in early
responses to dehydration, producing PA as a second messenger that
transmits the stress signal. CpPLD-2 may be involved in
phospholipid metabolism and the membrane rearrangements that are
observed as a consequence of cellular desiccation.
Multiple forms of PLD exist in Arabidopsis, and a
dehydration-responsive PLD was also recently reported from this plant
(Katagiri et al., 2001). This PLD shows low sequence similarity with
the PLDs from C. plantagineum. The Arabidopsis PLD that is
structurally most closely related to the products of the C. plantagineum genes is not responsive to water deficit in
vegetative tissues. Instead, it is associated with senescence, and is
reported to be present in guard cells, regulating the closure of
stomata, and is thus involved in controlling water relations (Sang et
al., 2001). The comparison of the PLDs in two plant species, C. plantagineum and Arabidosis, demonstrates that despite close
sequence homologies, expression patterns and gene functions have
diverged during evolution. The adaptation of C. plantagineum
to cope with extreme desiccation may have resulted from the recruitment
of more genes to dehydration-responsive regulons than are devoted to
this task in a plant that only tolerates a moderate degree of water stress.
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CONCLUSIONS |
Although more work is necessary to define gene functions and
dissect the complex regulation of gene expression, the genes isolated
and characterized from C. plantagineum to date give us many
intriguing insights into the protective mechanisms that determine desiccation tolerance. The studies on C. plantagineum extend
our knowledge of the responses of plants to dehydration, providing a
wider perspective on significance of the information gained from the
extensive studies of Arabidopsis. A comparison of the information
obtained from C. plantagineum and Arabidopsis can help to answer the following question: Is the mechanism of desiccation tolerance in resurrection plants comparable with the mechanism used in
the seeds of most higher plants or has C. plantagineum recruited unique genes to protect its vegetative tissues?
In view of technological advantages, it is a safe bet that most
advances in general understanding of basic patterns of growth and
performance of plants will be obtained from studies on Arabidopsis. However, these studies will not be sufficient to explain the adaptation of C. plantagineum to extreme drought. The information
available from Arabidopsis research is often useful in identifying
genes isolated from C. plantagineum. Nevertheless, careful
comparative studies have to be performed because several cases (e.g.
see the section on PLD above) have taught us that sequence homology
does not always imply functional identity.
Research on C. plantagineum has uncovered novel features.
This is the case for the unusual and biotechnologically very
interesting accumulation in leaves of the C8 sugar octulose, which
seems to be restricted to a small group of plants. An understanding of the underlying mechanism may teach us new lessons in carbohydrate technology.
A discovery that would not have been possible without the research on
C. plantagineum was the isolation of the CDT-1
gene. Although the function of the CDT-1 gene is not
understood, it is likely that it acts as a regulatory RNA. This points
to novel molecular mechanisms that may have played a particularly
important role in the evolution of adaptation to extreme environmental stress.
The analysis of desiccation tolerance in C. plantagineum
suggests that, at least to a large extent, the same molecules are involved in the tolerance mechanism in seeds and in vegetative tissues
of C. plantagineum. This is important because it means that
the genetic information for desiccation tolerance is present in the
genome of most, if not all, higher plants. Differences in the control
of gene expression probably account for the restriction of desiccation
tolerance to specific stages of seed development. Identification of the
molecular switches that determine the spatial and temporal patterns of
gene expression induced during the acquisition of desiccation tolerance
in seeds may, in the future, lead to the programmed control of the
desiccation response also in vegetative organs.
Research on C. plantagineum has allowed us to answer several
questions that are important in understanding biodiversity and plant
adaptation to ecological niches. The combination of data from studies
on the genetic model plant Arabidopsis and on diverse plant species
should help us to understand one of the most amazing inventions in
plant biologythe ability to survive without water.
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ACKNOWLEDGMENTS |
We thank Elinor Hertweck for help with the preparation of
the manuscript and Michael Kutzer for help with the figures.
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FOOTNOTES |
Received August 14, 2001; returned for revision September 11, 2001; accepted September 13, 2001.
1
The work was supported by the DFG
Schwerpunkt "Molekulare Analyse der Phytohormonwirkung" and by the
European Union project "Transcription Factors Controlling Plant
Responses to Environmental Stress Conditions" (grant no.
QLK3-2000-00328).
*
Corresponding author; e-mail dbartels{at}uni-bonn.de; fax
49-228-73-2689.
www.plantphysiol.org/cgi/doi/10.1104/pp.010765.
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Bockel C, Salamini F, Bartels D
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J Plant Physiol
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Trends Plant Sci
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© 2001 American Society of Plant Physiologists
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INTRODUCTION
C. PLANTAGINEUM AS AN...
