PHYSIOLOGIA PLANTARUM 121: 175–181. 2004
Printed in Denmark – all rights reserved
DOI: 10.1111/j.1399-3054.2004.00321.x
Copyright # Physiologia Plantarum 2004
Minireview
Biochemical and molecular responses to water stress in
resurrection plants
Giovanni Bernacchiaa,* and Antonella Furinib
a
Università di Ferrara, Dip. Biologia, Via Borsari 46, 44100 Ferrara, Italy
Università di Verona, Dip. Scientifico e Tecnologico, Strada Le Grazie 15, 37134 Verona, Italy
*Corresponding author, e-mail: [email protected]
b
Received 13 October 2003; revised 19 November 2003
A small group of angiosperms, known as resurrection plants,
can tolerate extreme dehydration. They survive in arid environments because they are able to dehydrate, remain quiescent
during long periods of drought, and then resurrect upon rehydration. Dehydration induces the expression of a large number
of transcripts in resurrection plants. Gene products with a
putative protective function such as LEA proteins have been
identified; they are expressed at high levels in the cytoplasm or
in chloroplasts upon dehydration and/or ABA treatment of
vegetative tissue. An increase in sugar concentration is usually
observed at the onset of desiccation in vegetative tissue of
resurrection plants. These sugars may be effective in osmotic
adjustment or they may stabilize membrane structures and
proteins. Regulatory genes such as a protein translation initiation factor, homeodomain-leucine zipper genes and a gene
probably working as a regulatory RNA have been isolated
and characterized. The knowledge of the biochemical and
molecular responses that occur during the onset of drought
may help to improve water stress tolerance in plants of agronomic importance.
Introduction
Since agriculture began, drought, or more generally
inadequate water availability, has been one of the
major crop production-limiting factor, causing famine
and death. It continues to be a permanent constraint to
agricultural production in many developing countries
and causes yield reduction in developed ones (Ceccarelli
and Grando 1996). Thus, in environments where water
deficit occurs, understanding the mechanisms that allow
plants to tolerate drought is an urgent need for agriculture.
Some angiosperms are able to cope with arid environments by mechanisms that mitigate drought stress, such as
stomatal closure, partial senescence of tissues, reduction
of leaf growth, development of water storage organs, and
increased root length and density, in order to use water
more efficiently. Water flux through the plant can be
reduced or water uptake can be increased by several physiological adaptations. These mechanisms allow plants to
survive in arid environments by lessening the severity of
drought stress, but they do not make these plants tolerant
to desiccation. In fact, with long periods of drought these
plants will dehydrate and die (Scott 2000).
Physiol. Plant. 121, 2004
The modern scientific study of drought tolerance began
in 1702 when Anthony von Leeuwenhoek discovered that
rotifers could survive without water for months. Now it is
known that a few groups of animals and a wide variety of
plants can tolerate desiccation in the adult stages of their
life cycle. Many lichens, bryophytes, and a few ferns can
survive in a dried state. Among vascular plants a small
group of angiosperms known as poikilohydric or resurrection plants (Gaff 1987) can tolerate extreme dehydration.
Desiccation tolerance allows a plant to survive equilibrium
with 0% air humidity and it is preserved until water
becomes available. Upon watering, dried resurrection
plants rapidly revive and become fully photosynthetically
active within 24 h (Bernacchia et al. 1996). In addition, the
processes of drying and rehydration cause only limited
damage to plant tissues. Thus, resurrection plants have
the advantage over other species in arid environments in
that they can remain quiescent during long periods of
drought. They can resurrect upon rehydration, grow and
reproduce long before non-resurrecting plants have the
opportunity to do so (Scott 2000).
175
Desiccation tolerance is common in non-vascular
plants, but is rare in vascular plants, even though dried
structures (i.e. seeds and pollen grains) are frequently
present in most plant species. This would suggest that
the genetic properties required for tolerance are present
in flowering plants and that only some tightly regulated
programmes of gene expression in plant development are
required to induce the revival of a dried plant body
(Hartung et al. 1998). The study of desiccation-tolerant
plants started at the beginning of the last century
(Irmscher 1912) with the botanical description of several
species, and has continued until the present day, focusing
on the physiological, biochemical and molecular aspects
of this phenomenon.
The importance of drought resistance in determining
crop productivity is well known. In arid lands or environments where drought occurs, the mechanisms of desiccation tolerance can play a role in plant survival until
water becomes available. It is justifiable that a large
number of scientists are interested in plant responses to
water deficit at physiological, biochemical and molecular
levels because this knowledge may be applied in the
development of drought-tolerant agricultural species.
The purpose of this minireview is to show what is currently known about resurrection plants with a special
focus on the biochemical and molecular events that
lead to desiccation tolerance.
Resurrection plants: definition and distribution
Angiosperms that possess the unique ability to withstand
desiccation of their vegetative tissues and to revive from
an air-dried state are called resurrection plants (Gaff
1987, Fig. 1). These poikilohydrous plants can experience
different rates of desiccation, depending upon the water
status of the environment, and they can recover uninjured from complete dryness within 24 h of contact with
water. Some resurrection plants lose chlorophyll and
dismantle their photosynthetic apparatus during the
onset of drought and they are then defined as poikilochlorophyllous. Others retain chlorophyll and the photosynthetic machinery during dehydration and are
therefore called homoiochlorophyllous (Tuba et al.
1998). In earlier studies, Bewley (1979) suggested that
to survive in a dehydrated state, plants must be able to
limit the damage, they must maintain the physiological
integrity in the desiccated state, and they must possess
repair mechanisms to recover from the damage upon
rehydration. More recent studies (Bewley and Oliver
1992) confirmed that interpretation and suggested that
desiccation-tolerant plants can also be classified into two
groups based on their resistance mechanism: protection
of cellular integrity or cellular repair of desiccationinduced damage.
Resurrection plants are widely distributed, they are
found in all continents except Antarctica. According to
Gaff (1987), they are mainly concentrated in arid climates such as southern Africa, eastern South America
and western Australia, while only a few species have been
found in Europe in the Balkan mountains (Stefanov et al.
1992). About 330 species of angiosperms have been
found to survive desiccation (Gaff 1987; Porembski
and Barthlott 2000), but no resurrection gymnosperms
are known (Hartung et al. 1998). There are both
monocotyledonous plants such as Xerophyta viscosa and
Sporobolus stapfianus and dicotyledonous species such as
Myrothamnus flabellifolia, Craterostigma plantagineum
and Chamaegigas intrepidus. The latter is the unique
example known of aquatic resurrection plants (Hartung
et al. 1998). Despite their broad geographical distribution, the ecological range for resurrection plants is narrow. Usually they are found in habitats subjected to
lengthy periods of drought, where rainfall is extremely
sporadic, particularly on rock outcrops below 2000 m in
tropical and subtropical areas, and to a lesser extent in
temperate zones (Porembski and Barthlott 2000).
Resurrection plants have evolved structures and
mechanisms to allow survival under extreme conditions.
For instance, a recently described and very interesting
aspect of the physiology of resurrection plants is the
response of the xylem to desiccation. In fact, when the
plant is in the air-dried state the xylem vessels are completely embolized. During rehydration, the xylem must
be able to refill, avoiding the formation of air bubbles, in
order to provide a supply of water to the leaves. Vulnerability of xylem to the formation of air bubbles depends
on wood anatomy, particularly the size of pores in intervessel pits. Larger pores are more susceptible to air entry
than small pores. In M. flabellifolia narrow reticulate
xylem vessels have been observed, which cavitate upon
desiccation but refill from root pressure and capillarity
when water becomes available (Sherwin et al. 1998).
Fig. 1. An example of resurrection plant: Craterostigma plantagineum.
176
Physiol. Plant. 121, 2004
Although the mechanisms that allow these plants to
survive a severe water stress have potential applications
in agriculture, molecular and biochemical studies are
to date restricted to a few species: C. plantagineum
(reviewed in Ingram and Bartels 1996; Bartels and
Salamini 2001), S. stapfianus (Neale et al. 2000),
X. viscosa (Mundree et al. 2000) and the moss Tortula
ruralis (Bewley and Oliver 1992; Oliver and Bewley 1997;
Oliver et al. 2000).
Molecular and biochemical studies
LEA proteins
Many transcripts and proteins accumulate during drying
in resurrection plants and some of them have been
cloned and/or sequenced. They include, for instance,
gene products that may play a role in protecting cytoplasmic structures during dehydration such as Late
Embryogenesis Abundant (LEA) proteins. LEA proteins
include a large group of proteins that accumulate in
mature embryos during the onset of desiccation (Galau
et al. 1986), and they can be induced in immature
embryos by ABA treatment. Generally their expression
is found in osmotically stressed or ABA-treated tissue
(Mundy and Chua 1988) in desiccation-tolerant as well
as in desiccation-sensitive plants (Skriver and Mundy
1990; Campbell and Close 1997; Svensson et al. 2002).
LEA proteins, even if quite heterogeneous, are usually
rich in hydrophilic amino acids, are water soluble and
can be divided into different groups based on sequence
similarities and properties. For example group 1 LEA
proteins are characterized by a 20-amino-acid-motif that
was first found in the wheat Em protein (Litts et al.
1987). The most widely distributed and best-studied
LEA genes belong to group 2, which includes a set of
genes rapidly induced by ABA (RAB, King et al. 1992)
or by water stress (dehydrins in barley and maize, Close
1997) in embryos and vegetative tissues of different plant
species. LEA2 proteins are hydrophilic; they share a
conserved serine and lysine-rich motif and remain soluble after boiling. Group 3 LEA proteins are characterized by a motif of 11 amino acids, which is predicted to
form an amphipathic a-helix probably involved in structural interactions (Dure et al. 1989). Group 4 and 5 show
relatively less conserved structures and are probably
involved in protecting membranes and binding water,
respectively (Ingram and Bartels 1996). Sequence homologies to LEA genes from all five groups have been
isolated and characterized in the resurrection plant
C. plantagineum (Bartels and Salamini 2001). They are
expressed at high levels in the cytoplasm or in the chloroplast upon dehydration and/or ABA treatment of vegetative or callus tissue. The accumulation of LEA proteins
in desiccated vegetative tissues of C. plantagineum
pointed out the similarity between seeds and resurrection
plants: both systems survive in an air-dried state and
revive during rehydration. In addition, the high cellular
concentration of different LEA proteins in desiccated
Physiol. Plant. 121, 2004
C. plantagineum tissues and their high hydrophilic structure suggest that they may play a role in protecting
cellular structures during drought stress.
A cellular protection mechanism is also present in
the moss T. ruralis, whose cellular integrity is maintained
during drying, allowing a rapid recovery of the photosynthetic activity upon rehydration (Proctor and
Smirnoff 2000). Interestingly, it has been reported that
dehydrin-type LEA proteins accumulate constitutively
also in the hydrated state of vegetative tissue of T. ruralis
(Bewley et al. 1993). By using purified antibodies raised
against corn seedling dehydrin, it was shown that
T. ruralis produces two dehydrins of 90 and 35 kDa.
They are present constitutively and do not appear to
increase during rapid or slow drying (Bewley et al.
1993). This fact may indicate that different mechanisms
of drought tolerance are present in Bryophytes and in
vascular plants. Nevertheless, T. ruralis gametophytes
recover at a much slower rate if the water loss occurs
rapidly and this suggests that this moss can activate
system(s) during the desiccation phase that can decrease
the time necessary to recover upon rehydration.
Carbohydrate metabolism
In addition to the synthesis of proteins, an increased
concentration of sugars is usually observed in seeds of
many species at the onset of desiccation (Leprince et al.
1993) and also in vegetative tissues of resurrection plants
such as C. plantagineum (Bianchi et al. 1991), Ramonda
myconi, Haberlea rhodopensis (Müller et al. 1997),
S. stapfianus (Albini et al. 1994) and others. Studying
the mechanisms by which diverse organisms such as
bacteria, fungi and yeast can withstand desiccation,
Crowe and Crowe (1986) reported that in Saccharomyces
cerevisiae trehalose was effective in preserving the integrity of membranes during desiccation and rehydration.
This sugar is extremely rare in plants where sucrose and
other sugars may play a similar role. Sugars may be
effective in osmotic adjustment during water loss, but
they may protect the cells by causing, during severe
desiccation, glass formation with the mechanical properties of a solid. This phenomenon has been observed, for
instance, in maize seeds and has been correlated with
their viability (Williams and Leopold 1989). In addition,
sucrose may preserve the integrity of the lipid bilayer
during dehydration (Crowe and Crowe 1986).
It has been observed that in many desiccation-tolerant
plants, independently of the species of soluble sugar
accumulated in fully hydrated tissues, sucrose is invariably present at high levels in the dried state (Leprince
et al. 1993). A particular case is represented by the leaves
of C. plantagineum. During desiccation, the unusual
eight-carbon sugar 2-octulose, representing approximately 90% of the total sugar in fully hydrated leaves,
is converted in sucrose, which then represents about 40%
of the DW (Bianchi et al. 1991).
2-Octulose is the main photosynthetic storage sugar
that C. plantagineum leaves build up during the day.
177
During dehydration, 2-octulose is rapidly converted into
sucrose without any significant alteration in the overall
sugar content. Little is known about the mechanism of
this conversion. Nevertheless, it has been shown to correlate with an increased synthesis of sucrose-metabolizing
enzymes. Specific isoenzymes of sucrose synthase and
sucrose phosphate synthase are in fact differentially
expressed during this phase, along with an upregulation
of glyceraldehyde dehydrogenase (reviewed in Ingram and
Bartels 1996; Bartels and Salamini 2001). Interestingly,
fully hydrated roots of C. plantagineum accumulate the
oligosaccharide stachyose and its level does not appear
to change significantly during dehydration. Because there
is no additional information on the sugar composition of
C. plantagineum dehydrated roots, it is not known if these
also accumulate sucrose during dehydration or rely on the
presence of this oligosaccharide for their desiccation
tolerance.
Sucrose is also the only available sugar for cellular
protection in T. ruralis. The amount of this sugar in
gametophytic cells is usually 10% of the DW. Wet-dry
episodes do not induce changes in sucrose concentration,
thus indicating that this moss needs to maintain sufficient amount of this sugar in the event of desiccation
(Oliver and Bewley 1997). Other resurrection plants rely
on different carbohydrate sources for their survival: in
X. viscosa for instance, glucose and fructose accumulate
as leaves dry, while in Ramonda it was reported that
starch content declines as sucrose accumulates during
drying (Müller et al. 1997).
In C. plantagineum plants, the rehydration process has
been studied in terms of metabolic activity and gene
expression profiles (Bernacchia et al. 1995, 1996). A
fast recovery of full photosynthetic activity and of
respiration was observed upon rewatering, along with a
restart of the synthesis of related proteins (Bartels and
Salamini 2001). Differential screenings also revealed a
particular behaviour of transketolase-encoding genes in
rehydrating C. plantagineum leaves. In fact, two genes
coding for putatively cytosolic transketolases are upregulated during recovery, while the plastid-localized one
appears to be expressed independently of the water content of the plant (Bernacchia et al. 1995). These results
suggest a possible role of transketolases in the sugar
conversions taking place during the dehydrationrehydration cycle, even if questions about the nature of
the metabolic pathway are still open.
Role of ABA
The involvement of ABA in the desiccation tolerance of
resurrection plants is well known. The ABA content has
been measured in fully hydrated and dehydrated leaves
of several resurrection plants (Gaff and Loveys 1984;
Schiller et al. 1997; Bartels and Salamini 2001). In general a 3- to 7-fold increase of leaf ABA content was
observed upon desiccation; moreover, when leaves of
M. flabellifolia and Borya nitida were too rapidly dehydrated, the increase in ABA was not observed and leaves
178
did not survive after rehydration (Gaff and Loveys
1984). As reported, leaves of C. plantagineum do not
require ABA treatment to establish or to increase
drought tolerance (Bartels and Salamini 2001); however,
a feature of this species is that a pretreatment with ABA
prior to dehydration is essential to induce desiccation
tolerance in dediferrentiated callus tissue.
Most of the proteins studied so far showing an
increased accumulation during drought in resurrection
plants are also induced by an exogenous ABA treatment.
Genetic studies with Arabidopsis thaliana mutants (Parcy
et al. 1994) defective in their sensitivity to ABA or with
an altered ABA biosynthetic pathway also confirmed the
role of ABA in inducing gene expression in response to
water stress. Furthermore, different types of cis-acting
elements relevant to ABA and/or drought have been
extensively analysed (Skriver et al. 1991; YamaguchiShinozaki and Shinozaki 1994). In the resurrection
plant C. plantagineum, the promoters studied are derived
from LEA-like genes induced by dehydration and ABA
(Furini et al. 1996; Ingram and Bartels 1996). These
promoters were analysed in transgenic Arabidopsis and
tobacco plants and resulted expressed in seeds and pollen
in the dry state. This observation suggests that in vegetative tissues of C. plantagineum the signal transduction
pathway from water stress to gene expression requires
the activation of specific genes, which in angiosperms are
expressed only in dried organs.
Arabidopsis abscisic acid-insensitive abi3 mutant seeds
do not acquire desiccation tolerance and remain nondormant (Ooms et al. 1993). Further studies (Parcy
et al. 1994) indicated that the ABI3 encodes a transcriptional factor that regulates the expression of several
genes during seed development. The ABI3 gene is specifically expressed in seeds but its ectopic expression leads
to the accumulation of seed-specific transcripts in transgenic Arabidopsis plantlets in response to ABA. In addition, it has been observed (Furini et al. 1996) that the
ectopic expression of ABI3 also conferred the ability to
induce C. plantagineum promoter activity of LEA-like
genes in vegetative tissues of transgenic Arabidopsis
after ABA treatment. These results led to the hypothesis that a gene product necessary for the induction of
ABA-and/or desiccation-inducible genes accumulates in
vegetative tissue of C. plantagineum while its analogous
counterpart accumulates in seeds of angiosperms. An
ABI3 homologue was isolated from C. plantagineum to
verify if this gene may be responsible for the activation of
dehydration- and/or ABA-inducible genes. The encoded
product was, indeed, able to induce LEA-like genes in
transient expression assays, but its expression was not
detected in vegetative tissue of C. plantagineum (Bartels
and Salamini 2001), indicating that another factor may
be involved in the induction of drought-tolerance genes.
Genes induced at very low levels during the early
stages of desiccation have been isolated from the resurrection grass Sporobolus stapfianus. The SDG134c gene,
encoding an eIF1 protein translation initiation factor,
was detected at very low levels in hydrated leaves and
Physiol. Plant. 121, 2004
LEA, structural,
hydrophilic.
Sucrose:
osmoprotection,
glass formation.
process of desiccation tolerance: CDT-1 is a member of a
repeated gene family that, when transcribed at high level
in callus tissue, leads to the constitutive activation of
desiccation-related genes. This gene upregulation enables
callus cells to survive desiccation without an ABA pretreatment (Furini et al. 1997). CDT-1 mRNA does not
carry a long ORF starting with ATG and no protein
product was detected by in vitro translation. Therefore,
further experiments were designed to verify whether
CDT-1 might be involved in the activation of the signal
pathway that leads to desiccation tolerance via regulatory RNA or via a small polypeptide. Preliminary results
suggest (Furini et al., unpublished data) that a putative
peptide encoded by CDT-1 is not required for conferring
desiccation tolerance in C. plantagineum callus tissue,
therefore strengthening the hypothesis that the CDT-1
transcript may be responsible for the observed phenotype.
Sugars conversions:
Sucrose synthase
Sucrose-P-synthase
Transketolases (?)
Conclusions
Table 1. The different responses observed in resurrection plants
upon water stress.
Resurrection plants
can exploit
j
damage repair mechanism
cell protection mechanism
t
Molecular
responses
j
t
Morphological
responses
Protective molecules
Metabolic enzymes
j
t
Protective proteins
j
j
t
t
Regulatory factors
involved
ABI3
CDT1
CPHB-1 and CPHB-2 (HD-ZIPs)
Myb factors
Translation factor eIF1
...
j
j
t
ABA-dependent
ABA-independent
t
Signal transduction
pathways can be
chlorophyll loss, poikilochlorophyllous
no chlorophyll loss, homoiochlorophyllous
the transcript level increased and persisted during
drought (Neale et al. 2000). In desiccation-tolerant
plants, many components essential for re-initiation of
metabolic activity are present in the dried tissue. It was
suggested (Neale et al. 2000) that SDG134c is required
during the rehydration process that leads to full metabolic activity within several hours.
Homeodomain-leucine zipper (HD-ZIP) genes are
specific for plants and are involved in the regulation of
developmental processes and induced by biotic and abiotic stresses. From C. plantagineum two HD-ZIP family II
genes were isolated and their products were shown to
interact in a yeast (S. cerevisiae) two-hybrid system
(Frank et al. 1998). These genes, CPHB-1 andCPHB-2,
are of particular interest because both are induced by
dehydration but show different responses to ABA:
CPHB-1 was not induced by the phytohormone, while
the transcript level of CPHB-2 increased upon ABA
treatment. This suggests that ABA-dependent and
ABA-independent pathways are responsible for adaptation to dehydration in C. plantagineum (Table 1). In fact,
previous studies on Arabidopsis ABA mutants have
revealed the existence of different water-stress signaltransduction pathways. ABA regulates one mechanism,
while the other works independently of the phytohormone (Shinozaki and Yamaguchi-Shinozaki 2000).
These observations strengthen the hypothesis that similar
mechanisms underlying water-stress responses exist in
resurrection and in non-resurrection plants.
Other genes that act as putative regulators during the
dehydration stress have been isolated from C. plantagineum. For example, Myb-related genes and a heat-shock
transcriptional factor (for a review see Phillips et al.
2002) are induced by dehydration. A further gene isolated via T-DNA activation tagging is implicated in the
Physiol. Plant. 121, 2004
The importance of drought resistance in determining
crop productivity is well known. In arid lands or environments where drought occurs, the mechanisms of desiccation tolerance may promote plant survival until soil
moisture levels improve. Thus, studies of these mechanisms have potential applications in the development of
desiccation-tolerant crops. Although more work is still
necessary, many genes that play a possible role in desiccation tolerance have been isolated from resurrection
plants and the function of the encoded proteins have
been established for several of them. Molecular
responses to dehydration such as the expression of LEA
genes and changes in sugar metabolism and regulatory
pathways have been extensively studied.
It is known from molecular marker analysis (Quarrie
1996) that tolerance to water stress is a quantitative trait;
nevertheless all the knowledge so far achieved with the
available gene technology opens up new opportunities
for improving stress tolerance in crop plants. For
instance, in transgenic Arabidopsis plants carrying the
transcriptional activator DREB1a driven by an abiotic
stress-inducible promoter, induction of LEA genes was
observed and these plants were more tolerant to water
stress (Kasuga et al. 1999).
The use of cDNA microarrays to identify droughtand cold-inducible genes in Arabidopsis allowed the isolation of stress-induced genes that were not previously
identified (Seki et al. 2001). This technology may be
applied for the isolation of new genes involved in the
signal transduction pathway that leads resurrection
plants to survive extreme water stress.
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