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Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 2000.51:463-499. Downloaded from www.annualreviews.org
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CONTENTS
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 464
SALINE STRESS AND PLANT RESPONSE . . . . . . . . . . . . . . . . . . . . . . . . . . . . 465
Salt Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 465
Salt Movement through Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 466
Lessons from Halophyte and Glycophyte Comparisons . . . . . . . . . . . . . . . . . . . . 466
SALT STRESS TOLERANCE DETERMINANTS: Effectors
and Signaling Components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 467
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Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 2000.51:463-499. Downloaded from www.annualreviews.org
INTRODUCTION
It has been two decades since salinity stress biology and plant responses to high
salinity have been discussed in this series (65, 80) and one decade since salinity
tolerance in marine algae has been covered (129). Together with a monograph, still
unsurpassed in its comprehensive discussion of the biophysical aspects of plant
abiotic stresses (141), these reviews covered organismal, physiological, and the
then-known biochemical hallmarks of stress and the bewildering complexity of
plant stress responses. Much research information has subsequently been gathered
about cellular, metabolic, molecular, and genetic processes associated with the
response to salt stress, some of which presumably function to mediate tolerance
(28–30, 36, 67, 78, 96, 105, 154, 189, 229, 240, 241, 285, 249). Our knowledge of
how plants re-establish osmotic and ionic homeostasis after salt stress imposi-
tion, and then maintain physiological and biochemical steady states necessary for
growth and completion of the life cycle in the new environment is fundamental to
our understanding of tolerance (29, 78, 160, 182, 189, 285).
During the past decade, concerted experimental focus targeted the identification
of cell-based mechanisms of ion and osmotic homeostasis as essential determinants
of tolerance (37, 96, 255). Plant scientists now recognize that underlying cellular
mechanisms of salt tolerance are evolutionarily more deeply rooted than previously
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perceived. Consequently, research that has exploited the molecular genetic advan-
tages of model unicellular organisms (e.g. bacteria, yeast, and algae) has been
highly applicable to, and will continue to provide, greater understanding of higher
plant salt tolerance (36, 48, 87, 181, 203, 230). However, it is obvious that plant
cells become specialized during ontogeny. Cell differentiation and spatial location
within plant tissues affect what adaptive mechanisms are most important to proper
functioning of specific cells within the organism. In fact, integrative hierarchical
functioning among cells, tissues, and organs, in a developmental context, certainly
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is an essential requisite for salt tolerance of the organism (29, 78, 96, 173, 230, 285).
It is acknowledged that whole plant studies are as necessary as always, but will be
more insightful, because the prevailing reductionist approaches of the past have
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provided mechanistic understanding that can be appreciated as the basis for inte-
gration of cellular level tolerance to the whole plant.
Algal genera such as Dunaliella, which includes many extreme halophytes (flora
of saline environments), and higher plants in the halophyte category, for example,
species of Atriplex and Mesembryanthemum crystallinum (2, 18, 19, 59, 89, 184,
263), have provided substantial insight into the response of halophytes to stress,
which by comparison with that of non-halophytes (glycophytes) has led to greater
comprehension of adaptive mechanisms. More recently, plant molecular genetic
models, in particular Arabidopsis thaliana, have provided inroads through the in-
vestigative power and causal demonstration of gain- and loss-of-function molecular
genetic experimentation to elucidate both cellular and organismal mechanisms of
salt tolerance (145, 146, 279, 293, 295). We feel that the preceding 20 years of re-
search, coupled with powerful new genetic tools, have brought the field to the brink
of understanding the genetic mechanisms underlying the physiological and eco-
logical complexity of salt tolerance. We summarize in this review salient research
advances in the topic area since the previous reports in this series (65, 80, 129).
We discuss briefly basic physiological stress responses and then outline how new
molecular and genetic tools have begun to link and integrate the stress-responsive
signaling cascades with the effectors (identified as physiological, biochemical and
eventually genetic components) that mediate adaptive processes, indicating that
signaling controls and mediates salt adaptation.
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spiration can result in toxic levels of ion accumulation in the aerial parts of the
plant. An immediate response to salinity, which mitigates ion flux to the shoot, is
stomatal closure. However, because of the water potential difference between the
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atmosphere and leaf cells, and the need for carbon fixation, this is an untenable
long-term strategy of tolerance (173, 285).
To protect actively growing and metabolizing cells, plants regulate ion move-
ment into tissues (66, 174). One mode by which plants control salt flux to the
shoot is the entry of ions into the xylem stream. Still debated is the extent to which
symplastic ion transport through the epidermal and cortical cells contributes to
a reduction in Na+ that is delivered to the xylem (44, 66). However, at the en-
dodermis, radial movement of solutes must be via a symplastic pathway, as the
Casparian strip constitutes a physical barrier to apoplastic transport (44, 66).
The accumulation of large quantities of ions in mature and old leaves, which
then dehisce, has often been observed under salt stress (66, 174). In a function as ion
sinks, old leaves may restrict ion deposition into meristematic and actively growing
and photosynthesizing cells. An alternative possibility is that cellular ion discrim-
ination is a natural consequence of transpirational and expansive growth fluxes,
cell morphology, and degree of intercellular connection. Meristematic cells, which
are not directly connected to the vasculature, are less exposed to ions delivered
through the transpiration stream, and their small vacuolar space is not conducive
to ion storage. De facto, the solute content of tissues containing cells with little
vacuolation (e.g. meristematic regions) is predominated by organic osmolytes and
in tissues with highly vacuolated cells by ions (22, 280).
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as both glycophyte cells and plants exhibit substantial capacity for salt tolerance
provided that stress imposition is gradual (8, 37, 96). The question then remains as
to whether particular biochemical mechanisms of halophytes are better activated
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or are preactivated, allowing a more rapid and successful overall response to saline
stress. Because of the diversity of halophyte species, there is no simple answer to
this question, but unique adaptive responses to NaCl stress are not apparent in the
overwhelming majority of halophytes (65, 78, 285).
Whereas glycophytes restrict ion movement to the shoot by attempting control
of ion influx into root xylem, halophytes tend more readily to take up Na+ such
that the roots typically have much lower NaCl concentrations than the rest of the
plant (3, 37). It seems that a major advantage that halophytes have over glyco-
phytes is not only more responsive Na+ partitioning but more effective capacity to
coordinate this partitioning with processes controlling growth, and ion flux across
the plasma membrane, in both cellular and organismal contexts. This may explain
why halophytes can use, and perhaps rely on, Na+ and Cl− for osmotic adjustment
that then supports cell expansion in growing tissues and turgor in differentiated
organs (3, 78, 80, 285). In a saline environment, the ability to take up and confine
Na+ to leaves lowers the osmotic potential of aerial plant parts; this then facilitates
water uptake and transport and lowers the metabolic cost for the production of os-
molytes. Contrarily, the necessity for efficient vacuolar deposition of Na+ exacts a
higher cost for H+ pumping, and possibly requires additional mechanisms for the
acquisition of ion nutrients (principally K+). Also, the osmotic benefits of storing
Na+ and Cl− as abundant, cheap osmolytes are limited by the available vacuolar
space. Therefore, continued growth, i.e. the production of new vacuoles, may be
a factor limiting tolerance (139).
Figure 1 Cellular homeostasis established after salt (NaCl) adaptation. Indicated are the
osmolytes and ions compartmentalized in the cytoplasm and vacuole, transport proteins
responsible for Na and Cl- homeostasis, water channels, and electrochemical potentials
across the plasma membrane and tonoplast. Included are organelles (chloroplast (cp), mito-
chondrion (mt), and peroxisome (perox)) for which the importance of ROS-scavenging is
implicated.
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TABLE 1 Osmotic regulated genes that encode proteins with function in stress tolerance downstream of signaling cascades
14:55
Polyols Inhibiting OH∗ -production from Fenton-reaction Mtld, Imt1, Stldh 257, 258, 272
osmotic adjustment; redox control 232, 233, 234, 236, 237, 238
Fructan (levansucrase) Osmoprotection SacB 200
Trehalose Osmoprotection; (signaling?) Tps; Tpp, trehalase 79, 106
Quaternary N-compounds Osmoprotection
Glycine betaine Protein protection, one-carbon sink codA 98, 161
BADH 194, 209
?Dimethyl sulfonium
compounds
Protein protection; pathogen defense
CMO 4, 109, 219
73, 212, 216
189
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K+-channels Low affinity or dual affinity K+ uptake; minimal Akt1, Akt2 9, 228
contribution to sodium uptake
Sodium stimulation of potassium uptake 247
Sodium partitioning Tissue/cell-specific deposition of sodium
Na+/H+ transport Vacuolar storage of Na+ as an osmoticum Na+/H+ antiporters 3, 76
or antiport and/or plasma membrane Na+ exclusion/export 10, 72
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Ion Homeostasis
A hypersaline environment, most commonly mediated by high NaCl, results in per-
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turbation of ionic steady state not only for Na+ and Cl− but also for K+ and Ca2+
(182). External Na+ negatively impacts intracellular K+ influx, attenuating acquisi-
tion of this essential nutrient by cells. High NaCl causes cytosolic accumulation of
Ca2+ and this, apparently, signals stress responses that are either adaptive or patho-
logical. Ion homeostasis in saline environments is dependent on transmembrane
transport proteins (Figure 1) that mediate ion fluxes, including H+ translocating
ATPases and pyrophosphatases, Ca2+-ATPases, secondary active transporters, and
channels (23, 26, 182, 254). A role for ATP-binding cassette (ABC) transporters
(210) in plant salt tolerance has not been elucidated, but ABC transporters regulate
cation homeostasis in yeast (166).
The molecular identity of many transport proteins that putatively mediate Na+,
K , Ca2+, and Cl− transport has been determined. Most of these transport proteins
+
Figure 3 Osmotic stress regulatory molecules in plants compared to categories of yeast signal compo-
nents. Vertical columns indicate type of evidence for participation of gene in plant stress signaling.
HASAGAWA ET AL C-3
Horizontal rows indicate category of signal component organized according to the yeast model hierarchy.
Superscripts indicate component subtypes and appropriate references. * denotes yeast gene. For all yeast
signal genes see Reference (87).
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Na+ and Cl – Transport Across the Plasma Membrane Na+ and Cl− transport
across the plasma membrane in a hypersaline environment must be considered in
two cellular contexts, after salt stress shock and after re-establishment of ionic
homeostasis. Immediately after salt stress, the H+ electrochemical gradient is
altered. Influx of Na+ dissipates the membrane potential, thereby facilitating up-
take of Cl− down the chemical gradient. An anion channel has been implicated
in this passive flux (50, 100, 242). However, after steady-state conditions are re-
established, including establishment of an inside negative plasma membrane po-
tential of −120 to −200 mV, Cl− influx likely requires coupling to downhill
H+ translocation, presumably via a Cl−-H+ symporter of unknown stoichiometry
(201).
The precise transport system responsible for Na+ uptake into the cell is still
unknown. Physiological data indicate that Na+ competes with K+ for intracellu-
lar influx because these cations are transported by common proteins (Figure 1)
(7, 26, 182). Whereas K+ is an essential co-factor for many enzymes, Na+ is not.
The need for Na+ as a vacuolar osmolyte in saline environments may be the
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472 HASEGAWA ET AL
reason why plants have not evolved transport systems that completely exclude
Na+ relative to K+. K+ and Na+ influx can be differentiated physiologically into
two principal categories, one with high affinity for K+ over Na+ and the other
for which there is lower K+/Na+ selectivity. Many K+ transport systems have
some affinity for Na+ (26, 43, 223). These include inward rectifying K+ chan-
nels (9, 288); Na+-K+ symporter (224); K+ transporters (71, 128, 222); voltage-
dependent, nonselective, outward-rectifying cation channel that mediates Na+ in-
flux upon plasma membrane depolarization (26, 225); and voltage-independent
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cation channels (7, 26, 275). The size of the Na+ electrochemical potential gradient
across the plasma membrane, resulting from the large inside negative membrane
potential and the Na+ chemical potential, implicates electrophoretic flux as the
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tation. Externally supplied Ca2+ reduces the toxic effects of NaCl, presumably by
facilitating higher K+/Na+ selectivity (46, 137, 145). High salinity also results in
increased cytosolic Ca2+ that is transported from the apoplast and intracellular
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compartments (132, 151). The resultant transient Ca2+ increase potentiates stress
signal transduction and leads to salt adaptation (132, 163, 197, 221, 277). A pro-
longed elevated Ca2+ level may, however, also pose a stress; if so, re-establishment
of Ca2+ homeostasis is a requisite. Ca2+ transport systems have been summarized
in recent reviews (192, 218).
Osmolyte Biosynthesis
One response, which is probably universal, to changes in the external osmotic
potential is the accumulation of metabolites that act as “compatible” solutes,
i.e. they do not inhibit normal metabolic reactions (38, 68, 284). With accumu-
lation proportional to the change of external osmolarity within species-specific
limits, protection of structures and osmotic balance supporting continued water
influx (or reduced efflux) are accepted functions of osmolytes. Frequently observed
metabolites with an osmolyte function are sugars (mainly sucrose and fructose),
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474 HASEGAWA ET AL
sugar alcohols (glycerol, methylated inositols), and complex sugars (trehalose, raf-
finose, fructans). In addition, ions (K+) or charged metabolites [glycine betaine,
dimethyl sulfonium propionate (DMSP), proline and ectoine (1,4,5,6-tetrahydro-
2-methyl-4-carboxyl pyrimidine)] are encountered (Figure 2). The accumulation of
these osmolytes is believed to facilitate “osmotic adjustment,” by which the internal
osmotic potential is lowered and may then contribute to tolerance (52, 149, 160).
Compatible solutes are typically hydrophilic, which suggests they could replace
water at the surface of proteins, protein complexes, or membranes, thus acting as
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can reduce inhibitory effects of ions on enzyme activity (39, 245) to increase ther-
mal stability of enzymes (74), and to prevent dissociation of enzyme complexes,
for example, the oxygen-evolving complex of photosystem II (194). One argu-
ment raised against such studies is the high effective concentration necessary for
protection in vitro, which is usually not matched in vivo. Considering the cellular
concentration of proteins, protection may be achieved at lower solute concentra-
tions found in vivo. It may not be the concentration in solution that is important.
Glycine betaine, for example, protects thylakoids and plasma membranes against
freezing damage or heat destabilization even at low concentration (118, 290). This
indicates that the local concentration at a surface may be more important than the
absolute amount.
The terms osmoprotection and osmotic adjustment focus on biophysical and physi-
ological characters. Following this view, the multiplicity of accumulating metabo-
lites may be interpreted to reflect the relative enzymatic capacities of various
biochemical pathways in different species. In reviewing physiological studies,
Greenway & Munns (80) come down on the side of pathology, or favor a view
of osmolytes as sinks of reducing power following metabolic disturbance that
might be mobilized as a source of carbon and nitrogen once stress is relieved.
More recently, new arguments interpreting biochemical and molecular analyses,
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based on mutant analysis and transgenic approaches, have been introduced into the
discussion (29, 30, 95, 189, 294). Plants engineered to synthesize and moderately
accumulate a number of osmolytes showed marginally improved performance un-
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der abiotic stress conditions. The effects seen with modest increases in mannitol,
fructans, trehalose, ononitol, glycine betaine, or ectoine, and with strong increases
in proline amount indicate that the purely osmotic contribution of these metabolites
to stress tolerance may not describe their function completely, i.e. that the pathway
leading to a particular osmolyte may be more important than accumulation per se
(30, 95, 112, 181).
Proline accumulation provides an example. Under stress, the imbalance be-
tween photosynthetic light capture and NADPH utilization in carbon fixation may
alter the redox state and lead to photoinhibition. Proline synthesis, following tran-
scriptional activation of the NAD P H-dependent P5C-synthetase (P5CS), could
provide a protective valve whereby the regeneration of NADP+ could provide the
observed protective effect (52, 95, 125, 271, 286). An argument against accumu-
lation per se can be seen from the analysis of the sos1 mutant of Arabidopsis,
defective in K+ uptake in which proline accumulated to levels twofold higher than
in wild type under moderate salt stress but the plants were not tolerant (53, 145).
The regulated synthesis of both proline synthesis and degradation enzymes indicate
that cycling between precursor and product may be important (130, 175, 270). Sup-
portive evidence for a nonosmotic function of at least some osmolytes comes from
transgenic overexertion of osmolyte-producing enzymes (233, 234) with moder-
ate accumulation of osmolytes leading to the protection of the carbon reduction
cycle by reducing the production of hydroxyl radicals generated by a Fenton re-
action. There may be more than one function for a particular osmolyte and, based
on results from in vitro experiments (92, 192), different compatible solutes could
have different functions. Among these functions a role in prevention of oxygen
radical production or in the scavenging of reactive oxygen species (ROS) may be
paramount (12, 185, 187).
Transgenic plants bave been generated to probe the effect of ROS scavenging
on salinity stress tolerance, based on observations of gene expression changes in
stressed plants. A putative phospholipid hydroperoxide glutathione peroxidase,
PHGPX, transcript increased during salt stress in Arabidopsis and citrus (83, 252)
and, also in citrus, transcripts and enzyme activities of Cu/Zn-SOD, glutathione
peroxidase, and a cytosolic APX (83, 104). Catalase-deficient (antisense) tobacco
showed enhanced sensitivity to oxidative stress under conditions of high light and
salinity (276).
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idase can increase the performance of plants under stress (31, 84, 85, 217, 239,
268).
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478 HASEGAWA ET AL
REGULATORY MOLECULES
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We have conceptually divided genetic determinants of salt tolerance into two
Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 2000.51:463-499. Downloaded from www.annualreviews.org
classes: encoding effectors responsible for remodeling the plant during adaptation,
and regulatory genes that control the expression and activity of the effectors. Rapid
technical developments and insightful use of yeast as a model organism have greatly
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facilitated our discovery of these regulator genes (155, 230, 246). Plant growth reg-
ulator/hormone physiological function(s) in plant stress responses is not surveyed
in this report, as relevant and recent treatises are available (51, 127, 169, 170). In-
stead, plant growth regulator function is described in the context of stress regulatory
determinants that have been linked to osmotic tolerance. We now summarize and
provide a framework for the organization of these plant regulatory genes, compar-
ing them to the yeast model (Figure 3).
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480 HASEGAWA ET AL
stress-responsive genes include regulatory elements that interact with basic leucine-
zipper motif (bZIP), MYB, or MYC domains in DNA binding proteins (1, 235,
241). The bZIP transcription factors interact with the ABA-responsive element
(ABRE) (241). The promoter of the osmotic/salt stress-responsive rd22 gene con-
tains signature recognition motifs for MYC and MYB transcription factors. DNA
binding proteins, rd22BP1 (MYC) and Atmyb2 (MYB), interact with their corre-
sponding cis-elements and trans-activate rd22. However, the rd22 promoter does
not contain ABRE motifs, which indicates that ABA dependency is mediated
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ABA, include dehydration response element (DRE) binding proteins (147, 248).
Two gene families have been characterized, DREB1 (which includes the previously
identified CBF1), and DREB2 (which trans-activates the osmotic/salt-responsive
rd29A). Both DREB1 and DREB2 family members also have domains that bind
ethylene-responsive elements (147, 248).
DREB1A overexpressing transgenic plants exhibited constitutive activation of
stress-responsive genes and enhanced freezing, dehydration, and salt tolerance
(123, 147). Driving DREB1A with the stress-inducible rd29A promoter substan-
tially increases salt tolerance, with minimal adverse growth effects in the ab-
sence of stress (123). Ectopic overexpression of CBF1/DREB1B in transgenic
plants induces cold-responsive genes and enhances freezing tolerance (111, 261).
Overexpression of the zinc finger transcription factor ALFIN1 activates MsPRP2
(NaCl-responsive gene) expression and increases salt tolerance of alfalfa (278).
In addition to transcription factors, some other signaling components affect a
salt-tolerance phenotype in plants (Figure 3). Notable among these is the SOS3
gene that encodes a Ca2+ binding CNB-like protein. Mutation of SOS3 produces
salt-sensitive plants with altered K+ transport characteristics (145, 146). Another
CNB-like protein AtCLB1 is able to suppress salt sensitivity in CNB yeast mutants,
but only in the presence of a mammalian CNA subunit (134). The yeast CNA/CNB
genes are also able to confer salinity tolerance when overexpressed in transgenic
plants (195), further implicating these regulatory molecules in plant stress signal-
ing. It seems clear that a Ca2+ binding, CNB-like molecule plays an important role
in osmotic stress responses in plants. Mutation of the ABI1 gene that renders plants
insensitive to ABA also causes an osmotic stress-sensitive phenotype (11, 63, 133),
confirming the important role of ABA in stress signaling.
and although CNB-like proteins were eventually identified, none can interact
with yeast CNA1/2 (134), which indicates that their function is apparently not
the same as in yeast. The use of sequence comparisons to identify potential sig-
nal genes will undoubtedly increase rapidly and dramatically. As gene knockout
technology in Arabidopsis becomes increasingly facile, a quick and easy test of
fidelity will also be available for bioinformatic mining (15, 126, 246). Eventually
this will become the dominant approach to gene discovery. Phenotypic changes
such as increases in salt tolerance caused by ectopic overexpression of regula-
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tory genes in plants are also important for crop improvement, but in many cases
may not be able to address the question of necessity, i.e. whether a regulatory
protein is necessary for salt tolerance in plants. In one scenario, a gene of a
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482 HASEGAWA ET AL
This kind of information is needed for many other signal components. In a compre-
hensive genetic screen, Ishitani et al (110) isolated a large number of Arabidopsis
mutations that either reduce or enhance salt stress induced gene expression. The
authors used the salt-, drought-, cold-, and ABA-responsive rd29A promoter fused
to the firefly luciferase gene to report plant responses to salt treatments. The fire-
fly luciferase reporter allows large-scale, nondestructive screening of mutants by
real-time, high throughout low light imaging technology (110). The recessive los
(low expression of osmotic stress-responsive genes) mutants define positive reg-
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ulators of salt stress gene expression, while the recessive hos (high expression
of osmotic stress-responsive genes) and cos (constitutive expression of osmotic
stress-responsive genes) mutations are presumed to be in genes that negatively
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regulate stress responses. Some los, hos, and cos mutations also alter plant re-
sponses to ABA or low temperature, thus revealing points of crosstalk between
salt, cold, and ABA signaling pathways. Molecular cloning of these mutations as
well as their interactors, enhancers, and suppressors (Figure 4, see color plates)
will eventually allow plant regulatory pathways to be built, like the ones in yeast
(Figure 3).
Direct physical interaction information by yeast two-hybrid or by in vitro as-
says also is lacking for most plant gene products so far. Yeast two-hybrid as-
says have been used to demonstrate that the AtMEKK1 protein interacts with
AtMEKK2/MEK and AtMPK4 (167, 168). Both genetic and biochemical evi-
dence for interactions between many more of these plant genes and their products
is now needed. On the genetic side, allelism, additivity and epistasis data must
be obtained now for the plant genes where function is evident (see Figure 4).
Conducting biochemical interaction studies in both yeast two-hybrid and in vitro
assays as well as ability to modify through phosphorylation, dephosphorylation,
etc, are logical next steps for these genes. Additional signal pathway participants
can also be identified by activation or suppression screens with known mutants.
Such information is now needed to establish the exact roles of signal components
in stress-signaling to allow ordered signaling pathways to be revealed.
One potential pathway that is increasingly meeting these criteria involves the
genes mutated at the SOS1, 2, and 3 loci. Genetic experiments determined that
these loci are not additive (same pathway) and that the sos1 phenotype is epistatic
to the other two, placing it furthest downstream. Recent cloning and interaction
studies of SOS2 and 3 indicate that SOS3 is a CNB-like Ca2+ binding protein that
physically interacts with and activates the SOS2 protein, which is similar to the
SNF1/AMPK family of kinases (91).
As new genes enter the camp of potential mediators of stress-adaptation through
bioinformatic or expression studies, evidence for their function in mediating adap-
tation through overexpression and gene knock-out studies must follow (Figure 4).
Armed with this evidence for function, further genetic studies and interaction de-
terminations will finally allow us to draw complete signaling pathways for plant
osmotic stress responses.
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C-4 HASAGAWA ET AL
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responses, this is most likely a mechanism that functions to amplify the signal
Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 2000.51:463-499. Downloaded from www.annualreviews.org
response (87). It is now obvious that besides genes involved in signaling, a very
large number of plant genes are transcriptionally controlled by osmotic stress, and
several previous reviews have summarized these genes (35, 294). These transcripts
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484 HASEGAWA ET AL
ACKNOWLEDGMENTS
Our work has been or is supported by the US Department of Agriculture (NRI)
Plant Responses to the Environment Program; by the National Science Foundation
Metabolic Biochemistry and International Programs; by the US Department of En-
ergy Biological Energy Research program; Binational Agricultural Research and
Development Program, and by Arizona and Purdue Agricultural Experiment Sta-
tions. Generous support has recently been provided by the NSF Plant Genome
?
Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 2000.51:463-499. Downloaded from www.annualreviews.org
zation (Japan), and the Rockefeller Foundation (USA). We wish to thank many
colleagues for making available unpublished data and for discussions.
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Annual Review of Plant Physiology and Plant Molecular Biology
Volume 51, 2000
CONTENTS
FIFTY YEARS OF PLANT SCIENCE: Was There Really No Place for A
Woman, Ann Oaks 1
BIOTIN METABOLISM IN PLANTS, Claude Alban, Dominique Job,
Roland Douce 17
SUGAR-INDUCED SIGNAL TRANSDUCTION IN PLANTS, Sjef
Smeekens 49
THE CHLOROPLAST ATP SYNTHASE: A Rotary Enzeme?, R. E.
McCarty, Y. Evron, E. A. Johnson 83
NONPHOTOSYNTHETIC METABOLISM IN PLASTIDS, H. E.
Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 2000.51:463-499. Downloaded from www.annualreviews.org