Download Although ABA is mainly made in the leaves and the root cap, all

ABA signaling
Byeong-ha Lee
ABA can be made in all parts of plant with higher production in the leaves and the
root cap (Zeevaart and Creelman, 1988). ABA is structurally carotenoid-derived. Thus, it
is believed to be produced mainly in plastid with the final conversion of xanthoxin into
ABA in the cytosol (Seo and Koshiba, 2002). Movement of ABA occurs in both the
phloem and xylem as well as by diffusion between cells (Zeevaart and Creelman, 1988).
Upon drought stress, ABA produced in roots is thought to move into leaves resulting in
reduced transpiration. Unlike other plant hormones, ABA content in plants fluctuates
dramatically with environmental conditions. What triggers ABA biosynthesis is not clear.
It is believed that plasma membrane loosening from cell wall due to desiccation and other
stresses is the signal for ABA biosynthesis, and consequently the ABA signaling.
ABA signaling would be mediated by the receptor(s). Despite the intensive effort
to identify ABA receptors, no such components have been reported. ABA is a weak acid
and its protonated form can be easily diffusible through lipid bilayer (Kaiser and Hartung,
1981). Therefore, theoretically ABA receptor can be intracellular and/or extracellular.
Nevertheless, there is some information about the cellular localization about ABA
receptor.
At first, it was believed that ABA perception takes place at the plasma membrane
based on the two experiments; (1) In epidermal peels of Valerianella locusta, stomatal
closure occurred in medium of not only pH5 but also pH8 where no ABA uptake was
recorded (Hartung, 1983) and (2) Binding of ABA by intact Vicia faba guard cell
protoplast is trypsin-sensitive (Hornberg and Weiler, 1984). However, the idea of
extracellular ABA perception was challenged by the observations that the ABA-induced
stomatal closure was achieved by microinjection of ABA into guard cell cytosol,
indicating the existence of internal ABA receptors (Allan et al., 1994; Schwartz et al.,
1994). Interestingly, it was also reported that injected ABA into cytosol does not inhibit
the stomatal opening, whereas external ABA does inhibit the stomatal opening,
suggesting the extracellular ABA receptor (Anderson et al., 1994). In addition, in
suspension cell culture systems, ABA-protein conjugates that cannot enter the cells
induced ion channel activity (Jeannette et al., 1999) and gene expression (Schultz and
Quatrano, 1997; Jeannette et al., 1999), suggesting the existence of extracellular ABA
receptor. Changes in ABA-induced ion efflux efficiency depending on external pH
suggested both internal and external ABA perceptions are required for the full stomatal
response (Macrobbie, 1995a). These results suggest the presence of both extracellular and
intracellular ABA receptors.
There is no simple defined ABA signaling and most ABA signaling is done in
guard cell or aleurone cell. It is not certain that the signaling pathway in guard cells or
aleurone cells can be applied to other cells in plants. Indeed, Ca2+ increase by ABA in
guard cells is not observed in barley aleurone cells (Wang et al., 1996) although some
common signaling modules appear to be present in both systems. Also, heterogeneous
expression system study with Xenopus oocytes, reveled the different response to ABA in
guard cells and mesophyll cells (Sutton et al., 2000). Thus, it is very primitive to draw
conclusive ABA signaling that works for all cells. Discussion below is very idealized
signaling mainly based on the guard cell signaling with some signaling components from
other systems.
Cytosolic Ca2+ has been implicated as a second messenger in ABA responses in a
variety of plant cells. In guard cells, plasma membrane proton pumps and inwardrectifying K+ (K+in) channels are inhibited by this Ca2+ increase, whereas anion efflux
channels are activated by Ca2+ elevation. Anion efflux from guard cells causes plasma
membrane depolarization that in turn suppresses K+in channel activities and activates
outward-rectifying K+(K+out) channels. Both K+ and anion efflux from guard cells cause
stomatal closure.
The abi1-1 and abi2-1 mutants show reduced ABA-induced cytosolic Ca2+
elevation in guard cells (Allen et al., 1999), which may be the cause of abolished ABAinduced stomatal closure in the abi1 and abi2 mutants. Extracellular Ca2+ addition (which
in turn causes increase Ca2+ in cytosol in guard cells) bypasses abi1-1 and abi2-1
mutation and brings about the normal anion channel activity and stomatal closure in abi11 and abi2-1. This result suggests that the dominant abi1 and abi2 mutations are located
upstream of or close to cytosolic Ca2+ increases in ABA signaling in guard cells.
In Arabidopsis guard cells, hydrolysable ATP treatment bring about more
efficient activation of slow-type anion channel by Ca2+ increase. Also preincubation of
guard cells with kinase inhibitors 2 M K-252a and 50 M staurosporine inhibited Ca2+
activation of anion channels. This suggests that the kinase activity is involved
downstream of abi1 and abi2 phosphatases in connecting between Ca2+ and slow-type
anion channels as positive regulator. The final step in activation of slow-type anion
channels was shown to be achieved by high ATP concentration and suboptimal
nanomolar cytosolic Ca2+ concentration (Schwartz et al., 1994), suggesting that final step
for anion channel activation involves Ca2+ independent kinase activity. In aleurone cells,
calcium-independent MAP kinase activity is also activated by ABA (Knetsch et al.,
1996). Thus, in summary, abi1 and abi2 phosphatases are located upstream of or close to
Ca2+ increase that is followed by phosphorylation events by kinase(s) with Ca2+
independent kinase activity at the final step for anion channel activation in guard cells.
Although it has been studied in the guard cells, it may be, if not all, applied to other cell
types as similar responses were observed in aleurone cells for example. However, it
should be noted that in abi1 mutants, guard cell response to ABA was restored by
simultaneous application of protein kinase inhibitors along with ABA (Pei et al., 1997)
and in some cases, timing difference, concentration difference, cotreatment with ABA in
the treatment of kinase inhibitor result in non-inhibition in ABA-induced anion channel
activation in guard cells. These results suggest that different protein kinases are involved
positively or negatively in ABA signaling.
Overexpression of a constitutively activated Ca2+ dependent protein kinase in
maize mesophyll protoplasts leads to the activation of ABA signaling, which can be
partially reversed by expression of mutant abi1 phosphatase (Sheen, 1996; Sheen, 1998).
This suggests that additional phosphorylation event upstream of abi1 might be present.
Alternatively, different system has different ABA signaling pathway. Indeed, recent
studies with heterogeneous expression of total mRNA from guard cells and mesophyll
cells from Vicia faba revealed distinct ABA signaling pathway between two cell types
(Sutton et al., 2000).
ABA-induced Ca2+ increase is mediated by second messengers, IP3 and cADPR.
cADPR has been shown to induce cytosolic Ca2+ increase and stomatal closure in
Commelina guard cells (Leckie et al., 1998). Also in tomato hypocotyls cells,
microinjected cADPR induced ABA-inducible gene expression that can be abolished by
EGTA treatment (Wu et al., 1997). IP3 involvement was also implicated by the
observation that AtPLC1 (phospholipase C) gene is ABA-inducible (Hirayama et al.,
1995). IP3 was shown to cause cytosolic Ca2+ increase and stomatal closure (Gilroy et
al., 1990). Consistent with this, ABA elevates IP3 levels and the PLC inhibitor, U-73122
suppresses ABA-induced stomatal closure suggesting IP3 involvement in ABA signaling
by triggering Ca2+ increase in cytosol. However, inhibition of either cADPR or IP3 action
by inhibitors cannot completely suppress ABA-induced stomatal closure (Leckie et al.,
1998; Jacob et al., 1999; Staxen et al., 1999). Instead, treatment with both U-73122 and
nicotinamide, an inhibitor of cADPR production completely inhibits ABA-induced
stomatal closure (Jacob et al., 1999; MacRobbie, 2000), suggesting both IP3 and cADPR
are required for ABA signaling in guard cells inducing cytosolic Ca2+ increase.
Nevertheless, ABA-responsive promoters (RD29A promoter or KIN2 promoter hooked
up to the GUS reporter gene) are activated in tomato hypocotyls by application of ABA,
cADPR, or IP3 of which only IP3 effect is abolished with treatment of heparin, an
inhibitor of IP3 receptor, suggesting that IP3 may not play a primary role in ABA
signaling. Genetic evidence IP3 involvement in ABA signaling (gene induction and
germination) can be found in the Arabidopsis fry1 mutant (Xiong et al., 2001a).
Phospholipase D (PLD) has been implicated in ABA signaling in both guard cells
(Jacob et al., 1999) and aleurone cells (Ritchie and Gilroy, 1998). The level of
phosphatidic acid, product of PLD enzyme reaction transiently increases upon ABA
treatment in Vicia guard cells (Jacob et al., 1999), leading to stomatal closure.
Phosphatidic acid treatment does not bring about cytosolic Ca2+ increase and 1-butanol,
an inhibitor of PLD activity cannot completely inhibit ABA-induced stomatal closure.
Instead, near complete inhibition is achieved by 1-butanol and nicotinamide, an inhibitor
of cADPR production. These results indicate that PLD-mediated ABA signaling is a
parallel pathway of cADPR-mediated ABA signaling. Also in aleurone cells,
phosphatidic acid induced the ABA response in the absence of ABA and ABA response
was inhibited by 1-butanol (Ritchie and Gilroy, 1998).
In microsomal membranes prepared from aleurone protoplasts that have ABAinduced PLD activity, the activation of PLD by ABA is associated with a plasma
membrane-enriched fraction and is GTP-dependent. G protein agonist, GTPS is capable
of stimulating PLD independently of ABA, while G protein antagonist, GDPS or
pertussis toxin inhibits the PDL activation by ABA (Ritchie and Gilroy, 2000).
These results suggest that in aleurone cells ABA signaling through PDL takes
place at the plasma membrane and is mediated by G-protein activity although the identity
of G protein remains to be solved. Similarly, G-protein involvement in stomatal opening
inhibition by ABA was demonstrated with the Arabidopsis gpa1 mutants (Wang 2001
Science). Although GCR1, a heptahelical G protein-coupled receptor was proposed to be
coupled with GPA1 (Gα protein) (Ellis and Miles, 2001), no linked signaling components
have been experimentally determined.
The ERA1 gene encodes the β-subunit of farnesyl transferase, an enzyme that
catalyses the attachment of a 15-carbon farnesyl lipid to specific proteins for membrane
localization (Cutler et al., 1996). Due to its nature, it may not function directly as a
signaling component. Instead, it will play a role as a partner of signaling components.
The era1 mutant is hypersensitive to ABA in germination, suggesting its negative role in
ABA signaling. In both abi1 era1 and abi2 era1 double mutants, era1 suppresses the abi
phenotype indicating that ERA1 may act on signaling components at or downstream of
the ABI1 and ABI2 phosphatases. The ABI1 and ABI2 gene are expressed in all tissues
examined so far (Leung et al., 1997). The ERA1 gene is expressed ubiquitously in all
actively growing tissue (Pei et al., 1998; Ziegelhoffer et al., 2000). The cellular
localizations of ERA1 have not been experimentally determined.
ABA signal, mediated by receptor(s), Ca2+ increase by IP3 and cADPR,
phosphatidic acid by PLD, G protein, and/or phosphorylation/dephosphorylation, should
reach effector molecules such as ion channels in guard cells and/or nucleus for ABAinduced gene expression.
Mutations in ABI3, ABI4, and ABI5 genes caused reduced seed dormancy and
reduced sensitivity to ABA in germination but no obvious defects were observed in
vegetative tissue, suggesting that their functions might be confined in seeds development.
However, gene expression analysis revealed that these three genes are expressed not only
during seed development but also in vegetative tissue to a limited degree though. Also,
ectopic expression of ABI3 or ABI4 led the transgenic Arabidopsis plants to ABA
hypersensitivity in vegetative tissue. These results indicate that they may play a role in
vegetative ABA response as well. In consistence with this, another abi4 alleles was
isolated from screening designed sugar-insensitive seedling growth mutants, which
suggests, in a different point of view, the cross-talk between ABA signaling and sugar
signaling.
ABI3, ABI4, and ABI5 genes encode transcription factors with the B3 domain, the
AP2 domain, and the bZIP domain, respectively. In contrast to the fact that the AP2
domain in ABI4 and bZIP domain in ABI5 have DNA binding and dimerization activity,
ABI3 cannot specifically bind to DNA in vitro, although ABI3 can activate the
transcription in vivo. This suggests ABI3 may interact with other proteins to gain DNA
binding activity. These ABI3, ABI4, and ABI5 genes function in a combinatorial network,
rather than a regulatory hierarchy, controlling seed development and ABA responses.
Evidences are (1) physiologically, mutations in the genes show similar defect in seed
development, (2) abi3/abi4 or abi3/abi5 double mutants display only slightly more ABAresistant phenotype than the single mutant, and (3) ectopic expression of ABI3 or ABI4
resulted in ABA hypersensitivity in vegetative tissue. In fact, in yeast two hybrid system,
rice OSVP1 (ABI3 homolog) and TRAB1 (ABI5 homolog) interact with each other.
Similarly, it was shown that ABI3 interact directly with ABI5 and ABI5 can also bind to
itself.
Using transient gene expression in rice protoplasts, the functional interactions of
ABI5 with ABA signaling effectors such as VP1 and ABI1 have been shown (Gampala et
al., 2002). Co-transformation with ABI5 results in specific transactivation of the ABAinducible promoters. This ABI5-mediated transactivation is inhibited by overexpression
of abi1-1 protein phosphatase and by 1-butanol suggesting ABI1 interacts with ABI1mediated and PLD-mediated early ABA signaling modules. Furthermore, ABI5 interacts
synergistically with ABA and co-expressed VP1, indicating that ABI5 is involved in
ABA-regulated transcription mediated by VP1. These results provide the links between
early ABA signaling and transcriptional activities through ABI5 and VP1 transcription
factors.
Many proteins with bZIP domain have been reported for their capacity of binding
to ABA-responsive element (ABRE) found in the promoters of ABA-responsive genes,
which contain (C/T)ACGTGGC consensus sequence. Using this consensus sequence in
yeast one hybrid system, several bZIP factors (ABRE-binding factors; ABF) were
isolated. ABF genes are induced by ABA and their activity to induce an ABA-responsible
gene is inhibited in abi1-1 mutant. However, no functional evidence for the bZIP factors
in ABA signaling has been revealed until very recent. Transgenic Arabidopsis plants
overexpressing ABF3 and ABF4 display ABA hypersensitivity in germination, root
growth, and stomatal opening. Some ABA-inducible genes are more upregulated in
ABF3/4 overexpression lines than in the wild type, while the expression of some ABArepressible gene were reduced more in the ABF3/4 overexpression lines. The expression
of ABI1 and ABI2 genes were also enhanced in the ABF3/4 overexpression lines,
especially in the ABF3 lines, suggesting that ABI1 (and ABI2) might be regulated by
ABF3 (and ABF4). Similarly, overexpression of ABI5 brings about hypersensitivity to
ABA in germination inhibition and better water-retention capacity in vegetative tissue.
Many signaling components in ABA signaling pathway need to be identified.
Genomics approach will be helpful for this ABA signaling components hunting. Global
gene expression profile by microarray will provide a map to develop the strategy. If
possible, protein profile would be of a great help. ABA perception by receptor(s) is an
most early event in ABA signaling. Therefore, if we can get gene and protein expression
changes in this early event, then probability for cloning receptors will be much higher. In
addition, as ABA induces a pleiotropic response in plant, focusing on the most upstream
signaling event may be necessary. For this, abi1 mutant will provide very good tool. abi1
mutant is defective in cytosol Ca2+ increase and consequently displays abolished ABAinduced stomatal closure. In addition, ABF ability to induce ABA-responsible gene is
inhibited in abi1 mutant. As abi1 acts on upstream or at Ca+ increase in ABA signaling,
aib1 can only provide the narrow window of ABA early signaling which we want to
focus on.
ABA receptors are believed to exist both inside and outside of the cells and
mesophyll cells and guard cells may have distinct ABA signaling pathways as shown in
Vicia faba (Sutton et al., 2000). Therefore, ABA perception location (extracellular and
intercellur) and tissue type (guard cells and mesophyll cells) should be considered for
ABA receptor(s) cloning. Guard cells from abi1 should be the best tissue for ABA
receptor (or ABA signaling components) cloning. To distinguish the extracellular and
intercellular receptors, ABA-protein conjugates treatment or ABA microinjection may be
required although for the genomics approach ABA microinjection of tons of guard cells
seems impossible.
Global gene and protein expression profile obtained with abi1 after ABA
treatment (control = abi1 without ABA treatment) will show smaller number (that we can
handle) of very specific genes with high probability of them being ABA most upstream
signaling components including ABA receptor(s). This is based on the assumption that
ABA signaling components are most likely ABA-inducible. In fact, ABA receptors might
not be ABA-inducible or at least they should be constitutively present to some extent, so
they can perceive ABA signaling. Even in the case ABA receptor is not inducible, we
might get some signaling molecules. As receptor should interact with these signaling
molecules, yeast two hybrid experiment can be applied to fish out the receptor
candidates. ABA receptor candidates can be tested their ABA binding ability to facilitate
the cloning. Once the candidate genes are selected, one should find the receptor gene
knock-out Arabidopsis mutants. Then, ABA response such as stomatal closure or ABAinducible gene expression in the knock-outs should be tested accordingly. Recently,
expression studies in Xenopus oocytes showed a successful ABA response (Sutton et al.,
2000). In there mesophyll mRNA-injected oocytes responded to ABA in a similar way as
mesophyll cells. Further, induced knock-out by introducing a specific complementary
RNA (cRNA) resulted in specific defect. This system can be employed for ABA
signaling component cloning or functional test of the candidate gene. ABA-responsible
oocytes with a cRNA of candidate gene may present more functional information. When
this system is utilized with genomics, the outcome should be synergistically informative.
References
Allan, A.C., Fricker, M.D., Ward, J.L., Beale, M.H., and Trewavas, A.J.
(1994). Two transduction pathways mediate rapid effects of abscisic acid in Commelina
guard cells. Plant Cell 6, 1319-1328.
Allen, G.J., Kuchitsu, K., Chu, S.P., Murata, Y., and Schroeder, J.I. (1999).
Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced
cytoplasmic calcium rises in guard cells. Plant Cell 11, 1785-1798.
Anderson, B.E., Ward, J.M., and Schroeder, J.I. (1994). Evidence for an
Extracellular Reception Site for Abscisic-Acid in Commelina Guard-Cells. Plant
Physiology 104, 1177-1183.
Cutler, S., Ghassemian, M., Bonetta, D., Cooney, S., and McCourt, P. (1996).
A protein farnesyl transferase involved in abscisic acid signal transduction in
Arabidopsis. Science 273, 1239-1241.
Ellis, B.E., and Miles, G.P. (2001). One for all? Science 292, 2022-2023.
Gampala, S.S.L., Finkelstein, R.R., Sun, S.S.M., and Rock, C.D. (2002). ABI5
interacts with abscisic acid signaling effectors in rice protoplasts. J. Biol. Chem. 277,
1689-1694.
Gilroy, S., Read, N.D., and Trewavas, A.J. (1990). Elevation of Cytoplasmic
Calcium by Caged Calcium or Caged Inositol Trisphosphate Initiates Stomatal Closure.
Nature 346, 769-771.
Hartung, W. (1983). The Site of Action of Abscisic-Acid at the Guard-Cell
Plasmalemma of Valerianella-Locusta. Plant Cell Environ. 6, 427-428.
Hirayama, T., Ohto, C., Mizoguchi, T., and Shinozaki, K. (1995). A Gene
Encoding a Phosphatidylinositol-Specific Phospholipase-C Is Induced by Dehydration
and Salt Stress in Arabidopsis- Thaliana. Proc. Natl. Acad. Sci. U. S. A. 92, 3903-3907.
Hornberg, C., and Weiler, E.W. (1984). High-Affinity Binding-Sites for
Abscisic-Acid on the Plasmalemma of Vicia-Faba Guard-Cells. Nature 310, 321-324.
Jacob, T., Ritchie, S., Assmann, S.M., and Gilroy, S. (1999). Abscisic acid
signal transduction in guard cells is mediated by phospholipase D activity. Proc. Natl.
Acad. Sci. U. S. A. 96, 12192-12197.
Jeannette, E., Rona, J.P., Bardat, F., Cornel, D., Sotta, B., and Miginiac, E.
(1999). Induction of RAB18 gene expression and activation of K+ outward rectifying
channels depend on an extracellular perception of ABA in Arabidopsis thaliana
suspension cells. Plant Journal 18, 13-22.
Kaiser, W.M., and Hartung, W. (1981). Uptake and Release of Abscisic-Acid
by Isolated Photoautotrophic Mesophyll-Cells, Depending on Ph Gradients. Plant
Physiology 68, 202-206.
Knetsch, M.L.W., Wang, M., SnaarJagalska, B.E., and HeimovaaraDijkstra,
S. (1996). Abscisic acid induces mitogen-activated protein kinase activation in barley
aleurone protoplasts. Plant Cell 8, 1061-1067.
Leckie, C.P., McAinsh, M.R., Allen, G.J., Sanders, D., and Hetherington,
A.M. (1998). Abscisic acid-induced stomatal closure mediated by cyclic ADP- ribose.
Proc. Natl. Acad. Sci. U. S. A. 95, 15837-15842.
Leung, J., Merlot, S., and Giraudat, J. (1997). The Arabidopsis ABSCISIC
ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein
phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9, 759-771.
Macrobbie, E.A.C. (1995a). Aba-Induced Ion Efflux in Stomatal Guard-Cells Multiple Actions of Aba inside and Outside the Cell. Plant Journal 7, 565-576.
MacRobbie, E.A.C. (2000). ABA activates multiple Ca2+ fluxes in stomatal
guard cells, triggering vacuolar K+(Rb+) release. Proc. Natl. Acad. Sci. U. S. A. 97,
12361-12368.
Pei, Z.M., Ghassemian, M., Kwak, C.M., McCourt, P., and Schroeder, J.I.
(1998). Role of farnesyltransferase in ABA regulation of guard cell anion channels and
plant water loss. Science 282, 287-290.
Pei, Z.M., Kuchitsu, K., Ward, J.M., Schwarz, M., and Schroeder, J.I. (1997).
Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis
wild-type and abi1 and abi2 mutants. Plant Cell 9, 409-423.
Ritchie, S., and Gilroy, S. (1998). Abscisic acid signal transduction in the barley
aleurone is mediated by phospholipase D activity. Proc. Natl. Acad. Sci. U. S. A. 95,
2697-2702.
Ritchie, S., and Gilroy, S. (2000). Abscisic acid stimulation of phospholipase D
in the barley aleurone is G-protein-mediated and localized to the plasma membrane. Plant
Physiology 124, 693-702.
Schultz, T.F., and Quatrano, R.S. (1997). Evidence for surface perception of
abscisic acid by rice suspension cells as assayed by Em gene expression. Plant Sci. 130,
63-71.
Schwartz, A., Wu, W.H., Tucker, E.B., and Assmann, S.M. (1994). Inhibition
of Inward K+ Channels and Stomatal Response by Abscisic-Acid - an Intracellular Locus
of Phytohormone Action. Proc. Natl. Acad. Sci. U. S. A. 91, 4019-4023.
Seo, M., and Koshiba, T. (2002). Complex regulation of ABA biosynthesis in
plants. Trends Plant Sci. 7, 41-48.
Sheen, J. (1996). Ca2+-dependent protein kinases and stress signal transduction
in plants. Science 274, 1900-1902.
Sheen, J. (1998). Mutational analysis of protein phosphatase 2C involved in
abscisic acid signal transduction in higher plants. Proc. Natl. Acad. Sci. U. S. A. 95, 975980.
Staxen, I., Pical, C., Montgomery, L.T., Gray, J.E., Hetherington, A.M., and
McAinsh, M.R. (1999). Abscisic acid induces oscillations in guard-cell cytosolic free
calcium that involve phosphoinositide-specific phospholipase C. Proc. Natl. Acad. Sci. U.
S. A. 96, 1779-1784.
Sutton, F., Paul, S.S., Wang, X.Q., and Assmann, S.M. (2000). Distinct
abscisic acid signaling pathways for modulation of guard cell versus mesophyll cell
potassium channels revealed by expression studies in Xenopus laevis oocytes. Plant
Physiology 124, 223-230.
Wang, M., Oppedijk, B.J., Lu, X., VanDuijn, B., and Schilperoort, R.A.
(1996). Apoptosis in barley aleurone during germination and its inhibition by abscisic
acid. Plant Mol.Biol. 32, 1125-1134.
Wu, Y., Kuzma, J., Marechal, E., Graeff, R., Lee, H.C., Foster, R., and Chua,
N.H. (1997). Abscisic acid signaling through cyclic ADP-Ribose in plants. Science 278,
2126-2130.
Xiong, L., Lee, B.-h., Ishitani, M., Lee, H., Zhang, C.Q., and Zhu, J.K.
(2001a). FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative
regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev. 15, 1971-1984.
Zeevaart, J.A.D., and Creelman, R.A. (1988). Metabolism and Physiology of
Abscisic-Acid. Annu. Rev. Plant Physiol. Plant Molec. Biol. 39, 439-473.
Ziegelhoffer, E.C., Medrano, L.J., and Meyerowitz, E.M. (2000). Cloning of
the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem
development. Proc. Natl. Acad. Sci. U. S. A. 97, 7633-+.