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Genetic analysis of ABA signal
transduction pathways Dario Bonetta and Peter McCourt
The plant hormone abscisic acid (ABA) has been demonstrated to modulate a variety of
physiological processes, including seed dormancy, leaf water relations and adaptation to
environmental stresses such as cold, drought and salinity. Recent analysis of Arabidopsis
mutants with altered responses to ABA is now beginning to indicate the molecular mechanisms of ABA action. The signaling components so far studied show some genetic
redundancy, defining a signaling pathway with multiple inputs and outputs. The complexity
of these pathways must be taken into account when modeling ABA signal transduction or
designing new genetic screens for identifying other signaling components.

T

he sesquiterpene abscisic acid (ABA) was first described in
the mid-1960s and, like other phytohormones, appears to
influence an array of both physiological and developmental
events1,2. However, in contrast to other plant hormones, endogenous concentrations of ABA can rise and fall dramatically in
response to either environmental or developmental cues. For example, leaf ABA concentrations can increase 10- to 50-fold
within a few hours of the onset of a water deficit1. Subsequent

rewatering will return the concentrations to normal over the same
time period. In seeds, after embryonic pattern formation is complete, ABA concentrations rise while the embryo establishes dormancy and acquires storage reserves3. This spectrum of changes
in ABA concentrations led to attempts to understand ABA action
by either applying the compound onto tissues and evaluating its
effects or measuring its endogenous level in specific tissues and
correlating this with physiological responses4. These approaches
have shown a correlation between ABA and particular processes,
but they have not provided any clear mechanistic evidence for the
role of ABA. In addition, the interpretation of application experiments is influenced by questions of uptake, sequestration and
metabolism of the substance applied, and studies aimed at correlating hormone levels with function often make assumptions
about tissue or cell types based solely on gross anatomical observations that may not reflect subcellular organization4.
The power of the genetic approach
ABA synthesis

Clues are now starting to emerge as to how the ABA signal is
transduced in higher plants, mainly through approaches using
molecular genetics. ABA is dispensable to plants, and therefore
endogenous levels can be genetically altered without causing serious deleterious effects under lab conditions. Mutants deficient in
ABA biosynthesis in a variety of plant species also lose control of
stomatal aperture in leaves and whole plant acclimation to environmental stresses such as drought, salt and cold5. An allelic series

of ABA auxotrophic mutations in Arabidopsis has demonstrated
that seed dormancy correlates directly with the amount of ABA
synthesized by the embryo6. Because many of the signaling pathways that have been studied are dosage dependent, the concentration-dependent effect of ABA on embryo dormancy suggests that
the ABA specifies dormancy through some form of intracellular
signaling.
ABA signal transduction

A working hypothesis is that ABA acts through a standard signal
transduction pathway in which the binding of the hormone to a
receptor elicits a transduction cascade. According to this hypothesis, the identification of specific genes or gene families that are

expressed in response to ABA would probably represent the end
point of the signaling pathway. Experiments that focus on ABAdependent gene expression are mostly designed to identify proteins
that respond to the ABA after the signal has been transduced7. By
contrast, genetic analysis has been an invaluable tool in the identification of early ABA signaling components, because genetic
screens can be based on the phenotypes of well characterized ABAbiosynthesis mutants. Ideally, one can reasonably expect that mutations in genes that disrupt any one of the positively acting
components of a signal transduction pathway should have similar
phenotypes to those of the biosynthetic auxotroph. In turn, it is
possible to distinguish between response and auxotrophic mutants
because the former is not rescued by exogenous application of the

hormone.
Phenotypic analysis of mutations that alter ABA signal transduction should provide some indication as to what part of the
pathway has been affected. For example, mutations in an ABA
receptor or in a transduction component should result in pleiotropic phenotypes, whereas mutations in a downstream component
might be limited to more specific responses. However, a possible
caveat to this logic can be made from work on signaling in fungal
and animal systems. In these systems, signaling pathways are
highly intersected so that there are as many inputs as there are outputs8. Recent genetic screens using transgenic Arabidopsis plants
containing reporter gene constructs that respond to ABA, drought
and cold suggest that ABA-dependent and ABA-independent pathways interact and converge to activate genes involved in stress
responses9. Therefore, although traditional ABA-response mutant
screens were designed to isolate defects in specific ABA processes, the degree of pleiotropy of phenotypes seen in some of
these mutants might reflect communication between signaling
pathways. If this is true, the lack of pathway specificity puts a
greater burden on geneticists to establish whether an ABA-response
mutant will provide insights into the process being investigated.
The specificity of ABA signal transduction

Mutational analysis of ABA signaling has been confined to a few
species in which mutants can be easily identified10. In Arabidopsis,

genetic screens to distinguish genes involved in ABA responses
usually entail identifying seeds that germinate on exogenous concentrations of ABA that normally inhibit wild-type germination.
The popularity of screening for defective ABA responses at the
level of seed germination reflects the relative ease with which
screens and selections can be performed on sufficient numbers of
mutagenized individuals. To date, five distinct mutations, designated abi (‘ABA insensitive’), have been identified11,12. The abi1
and abi2 mutations are semi-dominant and appear to alter many
vegetative and seed ABA-regulated functions. Seeds defective at

Copyright © 1998 Elsevier Science Ltd. All rights reserved. 1360 - 1385/98/$19.00 PII: S1360-1385(98)01241-2

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ABA

Developmental or environmental signal

(a)

(b)
ABA reception

FUS3 and LEC1

ABI1

ABI3

Physiological responses

Seed maturation

Fig. 1. Genetic model of interactions of ABI3 with ABI1, FUS3
and LEC1. ABI3 might be a shared component of developmental
and ABA signaling pathways. FUS3 and LEC1 regulate ABI3

protein accumulation, suggesting that a developmental or environmental signal is tranduced via LEC1 and FUS3 to mediate ABI3regulated seed maturation. At the same time, a developmental or
environmental signal can also influence ABI3 indirectly by affecting endogenous ABA concentration. Because ABI3 ectopic
expression can suppress abi1 mutant phenotypes, the transduction
of this ABA signal would be through an ABI1-mediated pathway.
It is also possible that ABI3 can directly regulate physiological
responses (broken arrow), because ABI3 can suppress ABI1mediated stomatal closure.

these loci show reduced dormancy and mature plants wilt excessively under mild water stress because of a loss of stomatal regulation. The other abi mutations are recessive and their phenotypes
appear to be restricted to late seed development. Recently, a second class of mutations that causes seeds to show an enhanced
response to ABA (era) at the level of seed germination has also
been identified13. The era mutations are recessive, indicating that
the genes involved might encode negative regulators of ABA
action. Although molecular analysis of many of these ABA mutants is incomplete, their phenotypes imply that there are at least
two partially redundant pathways for ABA signaling: one specific
for seed development and the other for both seed and vegetative
responses.
Is ABI3 insensitive or just indifferent?

The genetic studies with abi and era mutations are compelling
because some of the response-mutant phenotypes overlap those of

an ABA-auxotrophic mutant. As expected, the majority of abi
mutants have varying degrees of diminished dormancy, whereas
era1 mutants have extended dormancy. However, full understanding of a complex process such as seed development requires
analysis of many mutant alleles at a given locus, so that relationships between gene activity and the resulting phenotypes can be
established. Developmental phenotypes resulting from different
alleles of the same locus often vary widely depending on the
severity of the allele in question. For example, aside from reduced
dormancy and seed ABA sensitivity, early phenotypic comparison
showed little difference between a weak allele of abi3 (abi3-1)
and a wild-type allele at the level of seed development11. The limited phenotypes of abi3-1 mutants suggest that the ABI3 gene
product is restricted to seed ABA signaling. However, null alleles
of abi3 result in highly non-dormant, underdeveloped seeds that
are desiccation intolerant14,15. Processes such as the breakdown of
chlorophyll, accumulation of storage reserves and premature activation of the germination program, all processes not normally
observed in ABA auxotrophs or Abi1 and abi2 mutants, suggest
that ABI3 might have functions broader than just ABA signal
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ABI1

ABI1

Kinase inactive

Kinase active

P
Activation of
anion channel

Stomata
closed

Stomata
open

Fig. 2. Speculative model of the involvement of ABI1 in slow
anion channel regulation in guard cells. By performing patchclamp experiments on Arabidopsis guard cells, it is possible to

show that ABA is involved in the control of slow anion channels
and that this regulation is mediated by the ABI1 protein phosphatase. The inability of Abi1 mutants to close their stomata in the
presence of ABA is partially rescued by a kinase inhibitor, which
suggests that a protein kinase works downstream of the ABI1
phosphatase. (a) In the presence of ABA, the ABI1 wild-type protein either directly or indirectly inactivates the kinase so that it
cannot catalyze the phosphorylation of a downstream element that
could be the channel itself or some protein needed for channel
inactivation. Alternatively, the ABI1 phosphatase could directly
dephosphorylate the kinase substrate. Either of these scenarios
will result in anion-channel activation and stomatal closure. (b) In
the absence of ABA, ABI1 is inactive and can no longer inhibit
the kinase. The kinase phosphorylates the downstream component, which results in inactivation of the channel.

transduction. It is interesting that severe alleles of abi3 share
many phenotypic similarities with the viviparous (vp1) mutation
of maize and that molecular characterization of these two genes
has shown that they encode evolutionarily conserved seed-specific
transcriptional activators16. Thus, the role of ABI3 and VP1 in
seed development appears to be conserved between monocot and
dicot species.

Evidence that ABI3 specifies seed developmental programs is
that its ectopic expression causes seed-specific mRNA transcript
accumulation in leaves in response to ABA (Ref. 17). However,
these ABI3-dependent expression patterns require a functional
ABI1 protein, because they are lost in an abi1 mutant background18. These results indicate that ABI3 is sufficient to change
ABA responsiveness in vegetative tissues and that ABI1 is required for these ABI3-regulated processes. However, clear assignment of genetic relationships based on ectopic expression
studies can be difficult because the situation is artificial. For example, loss of stomatal control in abi1 mutants is suppressed by

trends in plant science
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ectopic expression of ABI3 (Ref. 18).
(a)
(b)
If ABI3 is a transcription factor, this result
ABA signal
ABA signal
is surprising because guard cell closure
in response to the application of ABA is
too rapid to involve gene expression. Possibly, these studies and the expansive role
Receptor

Effector
Receptor
Effector
of ABI3 beyond ABA-established seed
dormancy might mean that this gene is
F
actually a global regulator of cell fate
X
X
rather than an ABA signaling molecule.
If ABI3 has an ‘instructive’ role, the reERA1
era1
sponding cells should develop along one
(embryonic) pathway in the presence of
the ABI3 signal, and along another (vegReceptor
Effector
Receptor
Effector
F
etative) pathway in its absence. AlternaX
tively, if ABI3 is merely ‘permissive’,
then the cells would be dependent on
X
an ABI3 signal to complete their maturAttenuation of
No attenuation of
ation. For example, if embryonic cells
ABA response
ABA response
were more sensitive to ABA than other
cells in the plant, conversion of cells toFig. 3. Possible role for farnesylation in ABA-mediated signaling. Mutations in the ERA1
wards a more embryonic fate might make
gene of Arabidopsis result in loss of farnesylation activity and increased ABA sensitivity in
them more sensitive to ABA. Ectopic
the seed. Loss-of-function mutations result in increased sensitivity, suggesting that a negative
expression of ABI3 suggests that it has an
regulator of ABA signal transduction needs to be farnesylated to function. (a) In the wildinstructive role, because the domain of
type, after perception of the ABA signal by a hypothetical receptor, the signal is transduced
via a membrane-bound effector down the response pathway. At some point after perception
embryo-specific gene expression is exof the ABA signal, a farnesylated protein (X) inserts itself into the membrane, interfering
panded. If ABI3 is instructive then it
with effector function. This results in an attenuation of the ABA response. (b) In the era1
would not be directly involved in ABA sigmutant, X is not farnesylated and therefore does not localize to the membrane. The lack of
nal transduction but would ‘select’ cells to
interference of effector function prevents attenuation of the ABA response.
become sensitive to the hormone. Thus,
loss of ABI3 function results in cells that
are unable to respond to ABA appropriately.
Another possibility is that ABI3 is a shared component in both FUS3 and LEC1 are essential components of cotyledon identity,
ABA signal transduction and seed maturation, thereby allowing their interaction with ABI3, an ABA-associated late-embryogenesis
coordinate regulation of ABA-dependent and ABA-independent regulator, may allow the coordinate control of ABA-related seed
processes (Fig. 1). A coordinate model of ABI3 action is sup- functions with morphological development.
ported by the demonstration that maize VP1 participates in both
the activation of seed maturation-specific programs and the re- To phosphorylate or not to phosphorylate?
pression of germinative programs19. Thus, mutually exclusive de- Although interpretation of the role of ABI3 in ABA signaling is
velopmental programs in maize seed development would be unclear, the molecular characterization of ABI1 and ABI2 sugregulated by the ABI3 homolog. Alternatively, if ABI3 is directly gests that protein phosphorylation and dephosphorylation are
involved in ABA signaling, its molecular identity and seed speci- involved in ABA action26–28. Both genes encode homologous proficity imply that it is just one of the possible outputs of a branched tein type 2C phosphatases, suggesting that their functions are parpathway. Support for this latter possibility comes from recent tially redundant. This overlapping functionality has been suggested
experiments in which tobacco seed ABA concentrations were to explain why only dominant mutations in these two genes can be
dramatically reduced by the transgenic expression of an ABA- identified in ABA-insensitive genetic screens. Moreover, dephosspecific antibody that sequesters free ABA (Ref. 20). These seeds phorylation assays of abi1 mutant protein show decreased enzyme
were phenotypically similar to severe abi3 null mutants, suggest- activity, suggesting that this mutation might act in a dominant
ing that the available ABA auxotrophic mutations in Arabidopsis negative manner29. In this case, the abi1 mutant protein would
are still leaky enough to allow seed maturation to proceed un- interfere with a signaling complex of proteins that might include
hindered. However, ultrastructural analysis of immunomodulated the ABI2 protein. However, loss-of-function alleles do not exist
transgenic seed showed alteration in cotyledon development that for ABI1 and ABI2, making modeling the function of these prowas more reminiscent of fus3 and lec1 mutants of Arabidopsis21–24. teins in ABA signaling difficult.
The FUS3 and LEC1 genes encode proteins that are important in
Nevertheless, the recent achievements of patch clamping Arabidspecifying cotyledon identity, since loss of these functions re- opsis guard cells have opened up the possibility of applying the
sults in ‘leaf-like’ development of the cotyledons. Originally, these technology of electrophysiology directly to mutant cells altered in
genes were not considered to have a direct role in ABA signal their ABA response30. These studies indicate that both ABI1 and
transduction, because the fus3 and lec1 mutant seeds retained nor- ABI2 function in stomata by facilitating the ABA-induced actimal sensitivity to exogenously applied ABA (Refs 21 and 22). vation of both slow anion channels and stomatal closing. FurtherRecent molecular studies, however, indicate that different combi- more, protein kinase inhibitors can partially rescue the defects in
nations of abi3, fus3 and lec1 alleles can impact on seed ABA sen- ABA signaling of abi1 but not of abi2. The simplest interpretation
sitivity, with FUS3 and LEC1 regulating the abundance of ABI3 of these results is that a protein kinase acts as a negative regulator
protein25. The action of ABI3 might be modulated by both ABA of stomatal closing and that ABI1 down-regulates this kinase by
and developmental regulators such as FUS3 and LEC1. Because acting either on the kinase itself or on the kinase substrate (Fig. 2).
June 1998, Vol. 3, No. 6

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The abi2-mutant guard cells are not rescued by kinase inhibitors;
and inhibitors alone are insufficient to produce anion-channel
activation and stomatal closure. These two results suggest that a
second pathway might be involved in ABA-mediated stomatal
closure in Arabidopsis. However, the substrates for neither ABI1
nor ABI2 are known and consequently they could have very different roles in ABA signaling.
Putting on the brakes

Aside from the phosphorylation status of the cell, the recent molecular characterization of one of the era loci (era1) indicates that
protein farnesylation could be another modulator of ABA signaling in higher plants13. The ERA1 gene encodes the b-subunit of a
heterodimeric farnesyl transferase, an enzyme that catalyzes the
attachment of a 15-carbon farnesyl lipid to specific proteins. Although little is known about the biological function of this activity in plants, this covalent lipid modification plays a critical role in
the subcellular localization and function of eukaryotic signaling
molecules such as trimeric G-proteins and small GTP-binding
proteins of the RAS superfamily in yeast and mammalian cells31.
If the molecular function of farnesylation is analogous in plants,
then the increased sensitivity to ABA observed in the era1 farnesylation-deficient mutants suggests that a negative regulator of
ABA signaling might have to be membrane-localized to function
(Fig. 3). However, as with the interpretation of ABI3 function,
ERA1 might modify proteins that are only peripherally associated
with ABA signaling. The ABA and dormancy defects of era1 mutants could be a reflection of a developmental program that only
loosely cross-connects with ABA-induced responses that reinforce the same processes. Hopefully, once the targets of ERA1 are
identified, differentiation of these models can be resolved.
It is possible that a greater number of checks and balances exist
in the seed because the commitment to germinate, unlike many
developmental decisions in higher plants, cannot be reversed or
reiterated. Thus, the role of ABA in the establishment of seed dormancy might be buffered by other developmental pathways.
Ostensibly, all the proteins identified by ABA sensitivity mutant
screens are potential candidates as signaling components. Based
on the molecular identity of these proteins it is likely that either a
phosphatase or a farnesyltransferase would be located further
upstream in a signaling pathway than would a transcription factor.
Back to the future: more genetic screens

Many genes in signaling pathways can function as components of
a binary switch. The state of this switch is defined mutationally by
either the dominant, gain-of-function allele, which fixes the
switch to a high level or constitutively active state, or alternatively
by the null, loss-of-function allele, which fixes the switch to a low
level or inactive state32. In perceiving a signal, a gene could either
positively or negatively regulate another; thus, by defining the
alternative states of the whole pathway, it is possible to divide
genes into either positive or negative regulators of that pathway.
Because of the lack of appropriate mutations, we do not yet have
a clear understanding of how the ABA signal is transmitted or
perceived. Although traditional genetic techniques identify the
loss-of-function mutation of a gene with relative ease, the gain-offunction mutation can be more difficult to obtain. The value of
gain-of-function mutations is that they can uncover the function
of non-essential or functionally redundant genes that would be
missed because they have no loss-of-function phenotype. Molecular techniques have made it possible to simulate these mutations
by overexpression of cloned genes, creating gain-of-function scenarios to juxtapose the loss-of-function situations. However, as
with ectopic ABI3 expression, the interpretation of misexpression
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June 1998, Vol. 3, No. 6

mutant phenotypes requires careful consideration, because tissue
specificity is lost and misexpression is normally constitutive over
the life of the plant.
Expanding the current collection of mutants by traditional genetic screens will definitely help to increase our knowledge of ABA
signaling. Moreover, since mutants already exist, it should be possible to design genetic screens to address the problems of pleiotropy.
One method that is widely used to identify new loci in a signaling
pathway is a suppressor or enhancer screen33. Either suppressor or
enhancer mutations can identify genes located downstream of a
known gene. This approach is based on the premise that such second-site mutations can cause imbalances in the flux of a pathway,
either by reducing it or by exaggerating it, and as a consequence
have a detectable phenotype. In the case of a phenotypically complex mutation such as abi3, specific phenotypes can be targeted
for suppression or enhancement: for example, dormancy versus
desiccation intolerance or ABA insensitivity. The success of such
screens is, however, largely dependent on the initial mutant allele.
There is no guarantee that mutations will be limited to the same
signaling pathway or to parallel redundant pathways.
Apart from for the isolation of mutations that affect gene interactions, mutations identified by screens that do not utilize ABA
directly have been mostly set aside. This is because of the likelihood that these screens do not identify mutations that directly
affect ABA signaling. However, this standard is based on the assumption that ABA is an instructive signal. In many physiological
experiments, ABA seems to act as a relay between the environment and the plant2. If this is true, then there would be no need to invent specific pathways for ABA signaling. The alternative is that
ABA acts in a more permissive way to modulate multiple pathways,
thereby either amplifying or dampening the strength of the signal
in some essential developmental or physiological pathway. This
may explain why ABA and perhaps other plant hormones seem to
have a role in apparently distinct processes. Based on what is currently known about ABA signaling, however, it is difficult to distinguish between the two possibilities. For instance, the genes that
have so far been cloned through ABA screens all encode proteins
that are modulators of signal transduction pathways rather than the
core components of a typical signaling pathway (e.g. a receptor).
Conclusions

Genetic analysis has limitations: some genes can act at more than
one stage in development and growth, or can function in more
than one cell or tissue type, making phenotypic analysis difficult.
For example, the recent identification of a cyclic ADP-ribose in
ABA signaling through microinjection experiments might not
have been found through a traditional genetic screen34. It is also
possible that certain steps in the ABA pathway are genetically
redundant, as with the ethylene receptor in Arabidopsis35. Recessive, loss-of-function mutations in such genes will have no obvious phenotype. However, as hormone screens become more
sophisticated, these problems will become surmountable. For
example, suppression of era mutants that are already sensitized to
ABA might uncover mutations that would normally only give
weak insensitivity phenotypes. Although our understanding of
ABA signaling in higher plants is still rudimentary, the collection
of abi and era mutations that presently exist in Arabidopsis can
now serve as a foundation for many new genetic screens. Deciphering the ABA signal transduction map is still a formidable
challenge, but for plant geneticists the route is clear.
Acknowledgements

We wish to thank Sara Sarkar and Majid Ghassemian for critically
reading the manuscript and for helpful discussions.

trends in plant science
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Dario Bonetta and Peter McCourt* are at the Dept of Botany,
University of Toronto, 25 Willcocks St,
Toronto, Canada M5S 3B2
*Author for correspondence
(tel +1 416 978 0523; fax +1 416 978 5878;
e-mail mccourt@botany.utoronto.ca).

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