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Genetic interactions between ABA, ethylene and sugar
signaling pathways
Sonia Gazzarrini and Peter McCourt*
The identification of genes through mutant screens is beginning
to reveal the structure of a number of signaling pathways in
plants. In the past year, genes that determine the plant’s
response to the hormones ethylene and abscisic acid have also
been shown to be involved in sugar sensing in early seedlings.
These results suggest that hormone signaling and carbon
homeostasis are tightly coupled but that the architecture of
these interactions is complex. Part of this complexity may be
because some genetic screens on exogenous compounds
produce signaling linkages that are not necessarily pertinent
under normal growth conditions. Because many of the genes
identified in these screens are cloned, the relevance of these
interactions can now be unraveled at the molecular level.
Addresses
Department of Botany, 25 Willcocks Street, University of Toronto,
Toronto, Ontario M5S 3B2, Canada
*e-mail: [email protected]
Current Opinion in Plant Biology 2001, 4:387–391
1369-5266/01/$ — see front matter
© 2001 Elsevier Science Ltd. All rights reserved.
Abbreviations
ABA
abscisic acid
ABI
ABA INSENSITIVE
ctr
constitutive triple response
ein
ethylene insensitive
era
enhanced response to ABA
ETR1
ETHYLENE RECEPTOR1
Introduction
Most of our current notions on how plant hormones transduce a signal into a cellular response come from studies of
hormone response mutants identified in Arabidopsis thaliana
[1]. In certain respects, the story has been plain and simple,
single mutations that alter a hormonal response are identified
and placed into a signaling pathway using a combination of
phenotypic analysis, genetic epistasis and gene expression.
In hormone research, however, the truth is seldom plain
and never simple. Genetic inferences taken from
Arabidopsis mutants have never been reconciled easily with
physiological studies on hormone action. The application
of a single hormone often affects many different plant
processes and conversely different hormones can modulate
the same developmental process, suggesting a complex
interaction of hormone signaling in plants.
Perhaps the differences between physiological and genetic
experiments are beginning to be resolved by recent studies
that report the identification of known hormone response
genes through screens that were not designed to find them.
Genetic analysis suggests that abscisic acid (ABA) and
ethylene closely interact and both function to modulate the
overall carbon status during early seedling growth and
development [2•–7•]. The publication of recent reviews on
interactions between metabolic sensing and hormonal
signaling has allowed us to focus on the genetic approaches
used and possibly explain why these previously identified
genes have been uncovered in new screens [8,9]. This
review discusses genetic interactions between ethylene and
ABA signalling, and how recent findings in the field of
sugar sensing relate to these two hormones.
Signaling, all the world’s a mutant
Ethylene screens, having a gas
Ethylene gas is involved in a wide variety of plant
processes, ranging from fruit ripening and leaf senescence
to abiotic and biotic stress responses. Using a combination
of ethylene insensitive (ein) and constitutive triple response (ctr)
mutants it appears ethylene binds to the ETHYLENE
RECEPTOR 1 (ETR1) family of two-component receptor
kinases and this event stops the ETR1 receptors from
activating CTR1, a downstream Raf-like serine/threonine
kinase [10,11]. Lack of CTR1 activation releases positive
regulators, such as EIN2 and the transcriptional activator
EIN3, from the negative regulation of CTR1, thereby
allowing an ethylene response [12].
One component of the ethylene response pathway that
functions outside of ethylene action is encoded by the
EIN2 gene. Although originally discovered through ethylene insensitivity screens, new ein2 alleles have also been
identified in screens involving auxin transport inhibitors
[13], cytokinin [14], ABA [2•,3•] and delayed senescence
[15]. Moreover, molecular dissection of this gene has
shown that EIN2 responses regulated by jasmonate are
separable from the EIN2 responses regulated by ethylene, indicating that this molecule can function in at
least two different signaling pathways [16]. The EIN2
gene encodes a novel protein, whose amino-terminal
region shows weak homology to the mammalian family of
NRAMP (natural resistance-associated macrophage protein)
metal transporters. Interestingly, the cytoplasmic carboxyl
terminus, which is absent in the NRAMP family but is
necessary and sufficient to activate downstream ethylene
components of the pathway, has some overall structural
topology to the yeast glucose sensor Snf3 [16,17]. If EIN2
functions as a sensor in non-ethylene mediated processes,
it is also possible that the ethylene response pathway itself
functions in the absence of ethylene. Possibly, in the
absence of the gas, the ETR1 pathway is positively activated to regulate cell growth. Inhibition of ETR1 by
ethylene leads to inactivation of the pathway, which in
turn inhibits cell expansion. In this scenario, it is easy to
see how a variety of positive growth signals could integrate
with ethylene through the ETR1 pathway to modulate
cell growth.
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Cell signalling and gene regulation
Table 1
Sugar insensitive Arabidopsis mutants that are affected in
hormone action.
Mutant
Gene affected
Reference
gin (glucose insensitive)
gin1
gin5
gin6
ABA2
Unknown
ABI4
[7•]
[4•]
[4•]
sis (sugar insensitive)
sis1
sis4
sis5
CTR1
ABA2
ABI4
[7•]
[5•]
[5•]
sun (sucrose-uncoupled)
sun6
ABI4
[6•]
ABA screens, spreading your seed
ABA plays a major role in late seed development and adaptation to environmental stresses. To date, mutations that
decrease sensitivity of Arabidopsis seed to ABA have
identified five ABA-insensitive genes (ABI1–ABI5), but
only mutations in ABI1 and ABI2 affect both vegetative
and seed ABA responsiveness (reviewed in [18,19]). The
ABI1 and ABI2 genes encode homologous type 2C protein
phosphatases, and reduction-of-function mutations in
either of these genes suggest that dephosphorylation
negatively regulates ABA signaling [20,21]. The ABI3,
ABI4 and ABI5 genes encode transcription factors of the
B3 domain, APETALA2 (AP2) domain and bZIP factor
classes, respectively, but mutations at these loci only
influence seed ABA responsiveness [22,23,24•]. Analysis of
these three genes using a combination of overexpression
and loss-of-function alleles suggests that these transcription
factors work in combination to regulate seed ABA response
and late embryogenesis [25].
mutations in components that interact with ABA rather than
for genes that are directly involved in the ABA signaling
pathway. Perhaps screens involving another aspect of ABA
signaling, such as water stress or ABA-specific gene expression, may be more insightful. Genetic screens that are based
on ABA-reporter genes have been developed [33], and
screens involving aberrant gene expression under osmotic
stress find mutants that show increased sensitivity of gene
expression to ABA [34]. Interestingly, these mutants are
altered only in a subset of ABA responses, suggesting that
ABA signaling is complex.
ABA–ethylene interactions, the chicken and the egg
In the past year, two independent screens designed to
identify mutants involved in perturbing ABA responsiveness identified previously characterized ethylene signaling
mutants [2•,3•]. era3 mutants, which were originally identified as ABA hypersensitive, were found to be allelic to ein2.
Furthermore, ctr1 and ein2 mutants were identified as
enhancers and suppressors of abi1 mutants, respectively.
Other ethylene insensitive mutants also showed increased
ABA responsiveness leading to the conclusion that ethylene
is a negative regulator of ABA signaling in Arabidopsis seeds
[2•,3•]. Unexpectedly, the same ethylene insensitive
mutants that showed increased seed ABA responsiveness
exhibited reduced root ABA responsiveness [2•,3•]. More
perplexing, it was found that increased ethylene synthesis
conferred a similar ABA-insensitive root phenotype,
although exogenous ABA did not induce ethylene synthesis.
How a reduction of ethylene response or an increase in
ethylene synthesis can cause the same ABA response
phenotype in the root is unclear, but once again it raises
the possibility that the ETR1 response pathway does
regulate some ethylene-independent signal in Arabidopsis.
Sugar screens, the sweet smell of success
Mutants with enhanced response to ABA at the level of
germination (i.e. era mutants) have identified a protein
farnesyl transferase (ERA1) as an attenuator of both seed
and vegetative ABA sensitivity [26,27]. However, the
pleiotrophy of era1 and the large number of potential
farnesylated proteins in the Arabidopsis genome have made
it difficult to identify which farnesylated target(s) is involved
in ABA signaling [28–31].
Although ABA response mutants exist, a simple ABA
signaling pathway has not been defined. This may reflect a
more complex signaling topology or perhaps indicates that
not enough response genes have been molecularly
identified. It is also possible that the assay for identifying
ABA-responsive mutants is not focused enough on ABA
action. Unlike the ‘triple response’, which appears to be
ethylene specific, germination efficiency in the presence of
exogenous ABA can be influenced by a myriad of factors; for
example, both gibberellin and ethylene response mutants
have altered seed ABA responsiveness [2•,3•,32]. Hence,
screens involving germination may enrich more for
Externally supplied sugar has different effects on various
stages of early growth in Arabidopsis. Whereas low concentrations can stimulate wild-type germination, higher
concentrations repress both cotyledon, early seedling
development and photosynthetic gene expression. By taking
advantage of the effects of high sugar concentrations on
Arabidopsis seedling growth, a number of groups have
identified mutants that have been classified as defective
in sugar response (reviewed in [35–37]). Further analysis
on many of these lines, however, showed they were
defective in ABA biosynthesis, ABA sensitivity or ethylene
response (Table 1; [4•–7•]).
Numerous experiments have now suggested a close interaction between the germination and growth of young
seedlings on exogenous sugar and ABA/ethylene action.
Young seedlings deficient in ABA biosynthesis (i.e. aba1,
aba2 and aba3) or ABA sensitivity (i.e. abi4 and abi5) are
insensitive to high levels of sugar and, unlike wild-type
plants, these mutants do not show sugar-dependent
repression of photosynthetic gene expression. In addition,
Genetic interactions between ABA, ethylene and sugar signaling pathways Gazzarrini and McCourt
germination on high sugar increases ABA levels in wildtype plants [4•]. Conversely, low concentrations of
exogenous sugar relieve the inhibitory effects of ABA on
wild-type seed germination, although these seedlings fail
to green or develop true leaves [38,39]. Thus, low sugar
levels interfere with the inhibitory effects of ABA on
germination, whereas inhibition of seedling development
post-germination by high sugar concentrations is dependent
on ABA synthesis.
The inhibitory effect of high sugar levels on early seedling
growth is confined to approximately two days post-germination; hence, there is a post-germination, sugar-sensitive
developmental window that affects the seedlings response
to ABA [7•]. Once a seedling is photosynthetically competent, sensitivity to ABA may decrease, resulting in a
plantlet that is relatively insensitive to sugar-induced ABA
synthesis after this point (Figure 1). Interestingly, ABI5
expression studies suggest that this transcription factor
functions in a short post-germination developmental
window [40•]. This time frame may define the same
sensitive stage used to screen for sugar mutants.
High glucose-induced repression of cotyledon and shoot
development can also be overcome by the addition of the
ethylene precursor 1-aminocyclopropane-1-carboxylate
(ACC), suggesting that ethylene can antagonize glucose
inhibition of early seedling growth [41]. Moreover, ethylene
overproducing (eto1) and ethylene constitutive signaling
(ctr1) mutants are insensitive to high glucose levels, whereas
ethylene insensitive mutants (etr1) are hypersensitive [7•,41].
These experiments suggest that increasing ethylene
concentrations work to decrease the sensitivity of early
seedlings to glucose. As glucose inhibition functions at
least partially through ABA, ethylene may decrease ABA
biosynthesis or sensitivity (Figure 1). Consistent with this
idea, epistatic analysis between etr1 (sugar hypersensitive)
and aba2 (sugar insensitive), indicates that ABA functions
at or downstream of the ETR1 signaling pathway during
early seedling development on high glucose [7•,41].
Mutations that reduce ethylene signaling do increase ABA
concentrations in Arabidopsis [2•], thus it is possible that
high glucose levels could signal through the ethylene
pathway to regulate ABA biosynthesis. Alternatively, sugarinduced ABA synthesis or sensitivity may be antagonized
by ethylene, as is seen in the earlier ABA–ethylene germination interaction [2•,3•].
Conclusions
Genetic analysis indicates that hormone signaling pathways
functionally intersect with each other and with possibly
many other signaling pathways. However, questions still
remain. The lack of sugar-related phenotypes for abi1, abi2
and abi3 suggests that reducing seed ABA sensitivity alone
is not enough to confer a sugar-insensitive phenotype.
This paradox has led to the placement of ABI4 and ABI5 in
a separate ABA signaling pathway. However, this placement
is confounded by the observation that abi5 mutants lose
389
Figure 1
High sugar
Ethylene
ABA
State 1
Lipid breakdown
State 2
Photosynthesis
Sugar
Current Opinion in Plant Biology
Hypothetical model of the effects of sugar and hormones on early
seedling growth in Arabidopsis. The carbon required for early seedling
growth is dependent on the catabolism of lipids and proteins stored in
the embryo (State 1). When seedlings are in State 1 they are highly
sensitive to ABA. As the seedlings become photosynthetically
competent (State 2), the sensitivity to ABA decreases. Exogenous
application of non-physiological concentrations of sugar during various
stages of seedling growth results in an increase in the endogenous
levels of ABA. However, depending on the developmental state, ABA
causes an inhibition of seedling growth in State 1 but has little effect
during State 2. Sensitivity of early seedling growth towards high sugar
concentrations is negatively regulated by ethylene, which, as shown by
epistatic studies, acts at or upstream of the ABA signaling pathway.
their glucose insensitivity in the presence of exogenous
ABA [4•]. The recent finding that ABI5 is post-translationally
modified in an ABA-dependent manner does imply that
some downstream factors may require ABA to function,
and may explain some of the ABA dependence of sugar
sensing [40•]. However, signaling complexities also raise
concerns about how well the genetic interactions observed
through these screens reflect the in vivo situation. As with
hormone response screens, the timing of application and
the concentrations of sugar used in many experiments are
artificial. Sugars can both stimulate and inhibit processes
in a development-dependent manner; hence, caution must
be used in the interpretation of experiments that involve
continuous sugar application.
Both ethylene and ABA are stress-induced hormones, so
perhaps the connection of these compounds to high sugar
concentrations exists only under developmentally irrelevant stress conditions. For example, the production of high
ABA due to the exogenous application of glucose could
encourage a germinating embryo that is younger than
two days to re-enter late embryogenesis, a developmental
390
Cell signalling and gene regulation
decision that ordinarily does not occur. If this is true, a
signaling interaction is created between ABA and sugar
that is not developmentally appropriate. Both the ABA and
ethylene mutants identified in these sugar screens are also
resistant to high osmolytes and new abi4 alleles have been
identified in salt-stress screens [5•,7•,42]. Although the
osmo-tolerant phenotype of sugar-insensitive mutants could
be the result of insensitivity to high sugar, it is also possible
that intracellular accumulation of sugar could protect them
against osmotic stress. Thus, screens using high exogenous
sugars might select for osmo-tolerant mutants.
The correct anatomy of a signaling network is essential as
its structure always affects its function. The diagrams
defined by genetics not only tell us how information is
transferred throughout the organism but also indicate the
robustness and stability of the transmission. With the
advent of complete sets of mutant knockout lines and
global transcript profiling, we are entering a stage in which
all the elements involved in these pathways will be known.
It is, therefore, essential that the mutants identified in genetic
screens give us a physiologically and developmentally
relevant blueprint of wild-type signaling.
abrogates the sugar-induced upregulation of ABI4. This study also demonstrates that sensitivity to high exogenous sugar in Arabidopsis requires ABA
and that high sugar in the medium induces ABA synthesis.
5.
•
Laby RJ, Kincaid MS, Kim D, Gibson SI: The Arabidopsis sugarinsensitive mutants sis4 and sis5 are defective in abscisic acid
synthesis and response. Plant J 2000, 23:587-596.
The sugar-insensitive mutants sis4 and sis5, isolated by their ability to
germinate and grow on 0.3 M sucrose, were found to be allelic to aba2 and
abi4, respectively. However, other ABA-responsive mutants (abi1, abi2, abi3
and abi5) showed wild-type response to high sugar during germination,
indicating that not all ABA-response mutants are sugar defective.
6.
•
Huijser C, Kortstee A, Pego J, Weisbeek P, Wisman E, Smeekens S:
The Arabidopsis sucrose uncoupled-6 gene is identical to abscisic
acid insensitive-4: involvement of abscisic acid in sugar
responses. Plant J 2000, 23:577-585.
Using a gene reporter screen rather than seedling growth, sucrose-uncoupled
mutants (sun) were identified. The sun6 mutant, which showed reduced
sugar-mediated repression of photosynthetic gene expression, was a new
ABI4 allele. As in the work described in [5•], other ABA-responsive mutants
(abi1, abi2, abi3 and abi5) did not display sugar-insensitive phenotypes.
7.
•
Gibson SI, Laby RJ, Kim D: The sugar-insensitive1 (sis1) mutant of
Arabidopsis is allelic to ctr1. Biochem Biophys Res Commun 2001,
280:196-203.
The isolation of mutants resistant to 0.3 M sucrose during germination
identified sis1, a new allele of ctr1. Whereas constitutive ethylene response
mutants are insensitive to the inhibitory effect of high sugar on early seedling
growth, ethylene-insensitive mutants showed a sugar-hypersensitive phenotype.
This paper linked ethylene and sugar responses.
8.
Gibson SI: Plant sugar response pathways. Part of a complex
regulatory web. Plant Physiol 2000, 124:1532-1539.
9.
Coruzzi G, Zhou L: Carbon and nitrogen sensing and signaling in
plants: emerging ‘matrix effect’. Curr Opin Plant Biol 2001,
4:247-253.
Update
Recently, Rook et al. [43•] have shown that although ABA
is unable to induce expression of the ADP-glucose
pyrophosphorylase Apl3 gene it enhances the induction of
this gene by sugar. The authors suggest that sugar-induced
ABA synthesis makes the seedling more sensitive to ABAdependent sugar signals, a hypothesis that is consistent
with the model proposed in Figure 1.
Acknowledgement
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that is assayed. Ethylene appears to be a negative regulator of ABA action
in the seed but positively regulates some aspects of ABA action in the root.
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gene ABI5 encodes a basic leucine zipper transcription factor.
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•
developmental arrest checkpoint is mediated by abscisic acid and
requires the ABI5 transcription factor in Arabidopsis. Proc Natl
Acad Sci USA 2001, 98:4782-4787.
The authors of this paper demonstrate that ABI5 works in a short developmental window post-germination to regulate the ABA responsiveness of
the seedling. Furthermore, ABI5 is post-translationally modified in an ABAdependent manner, demonstrating, for the first time, a molecular mechanism
linking an ABI transcription factor with ABA signaling.
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The isi3 and isi4 mutants, impaired in the sugar induction of the starch
biosynthetic Apl3 gene, were found to be allelic to abi4 and aba2, respectively.
Interestingly, ABA alone is unable to induce Apl3 expression, but strongly
enhances its induction by sugar, suggesting that ABA influences how tissues
respond to subsequent sugar signals.