Escolar Documentos
Profissional Documentos
Cultura Documentos
High glucose-induced repression of cotyledon and shoot Hypothetical model of the effects of sugar and hormones on early
development can also be overcome by the addition of the seedling growth in Arabidopsis. The carbon required for early seedling
ethylene precursor 1-aminocyclopropane-1-carboxylate growth is dependent on the catabolism of lipids and proteins stored in
(ACC), suggesting that ethylene can antagonize glucose the embryo (State 1). When seedlings are in State 1 they are highly
sensitive to ABA. As the seedlings become photosynthetically
inhibition of early seedling growth [41]. Moreover, ethylene competent (State 2), the sensitivity to ABA decreases. Exogenous
overproducing (eto1) and ethylene constitutive signaling application of non-physiological concentrations of sugar during various
(ctr1) mutants are insensitive to high glucose levels, whereas stages of seedling growth results in an increase in the endogenous
ethylene insensitive mutants (etr1) are hypersensitive [7•,41]. levels of ABA. However, depending on the developmental state, ABA
causes an inhibition of seedling growth in State 1 but has little effect
These experiments suggest that increasing ethylene during State 2. Sensitivity of early seedling growth towards high sugar
concentrations work to decrease the sensitivity of early concentrations is negatively regulated by ethylene, which, as shown by
seedlings to glucose. As glucose inhibition functions at epistatic studies, acts at or upstream of the ABA signaling pathway.
least partially through ABA, ethylene may decrease ABA
biosynthesis or sensitivity (Figure 1). Consistent with this
idea, epistatic analysis between etr1 (sugar hypersensitive) their glucose insensitivity in the presence of exogenous
and aba2 (sugar insensitive), indicates that ABA functions ABA [4•]. The recent finding that ABI5 is post-translationally
at or downstream of the ETR1 signaling pathway during modified in an ABA-dependent manner does imply that
early seedling development on high glucose [7•,41]. some downstream factors may require ABA to function,
Mutations that reduce ethylene signaling do increase ABA and may explain some of the ABA dependence of sugar
concentrations in Arabidopsis [2•], thus it is possible that sensing [40•]. However, signaling complexities also raise
high glucose levels could signal through the ethylene concerns about how well the genetic interactions observed
pathway to regulate ABA biosynthesis. Alternatively, sugar- through these screens reflect the in vivo situation. As with
induced ABA synthesis or sensitivity may be antagonized hormone response screens, the timing of application and
by ethylene, as is seen in the earlier ABA–ethylene germi- the concentrations of sugar used in many experiments are
nation interaction [2•,3•]. artificial. Sugars can both stimulate and inhibit processes
in a development-dependent manner; hence, caution must
Conclusions be used in the interpretation of experiments that involve
Genetic analysis indicates that hormone signaling pathways continuous sugar application.
functionally intersect with each other and with possibly
many other signaling pathways. However, questions still Both ethylene and ABA are stress-induced hormones, so
remain. The lack of sugar-related phenotypes for abi1, abi2 perhaps the connection of these compounds to high sugar
and abi3 suggests that reducing seed ABA sensitivity alone concentrations exists only under developmentally irrele-
is not enough to confer a sugar-insensitive phenotype. vant stress conditions. For example, the production of high
This paradox has led to the placement of ABI4 and ABI5 in ABA due to the exogenous application of glucose could
a separate ABA signaling pathway. However, this placement encourage a germinating embryo that is younger than
is confounded by the observation that abi5 mutants lose 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 abrogates the sugar-induced upregulation of ABI4. This study also demon-
strates that sensitivity to high exogenous sugar in Arabidopsis requires ABA
signaling interaction is created between ABA and sugar and that high sugar in the medium induces ABA synthesis.
that is not developmentally appropriate. Both the ABA and 5. Laby RJ, Kincaid MS, Kim D, Gibson SI: The Arabidopsis sugar-
ethylene mutants identified in these sugar screens are also • insensitive mutants sis4 and sis5 are defective in abscisic acid
resistant to high osmolytes and new abi4 alleles have been synthesis and response. Plant J 2000, 23:587-596.
The sugar-insensitive mutants sis4 and sis5, isolated by their ability to
identified in salt-stress screens [5•,7•,42]. Although the germinate and grow on 0.3 M sucrose, were found to be allelic to aba2 and
osmo-tolerant phenotype of sugar-insensitive mutants could abi4, respectively. However, other ABA-responsive mutants (abi1, abi2, abi3
and abi5) showed wild-type response to high sugar during germination,
be the result of insensitivity to high sugar, it is also possible indicating that not all ABA-response mutants are sugar defective.
that intracellular accumulation of sugar could protect them 6. Huijser C, Kortstee A, Pego J, Weisbeek P, Wisman E, Smeekens S:
against osmotic stress. Thus, screens using high exogenous • The Arabidopsis sucrose uncoupled-6 gene is identical to abscisic
acid insensitive-4: involvement of abscisic acid in sugar
sugars might select for osmo-tolerant mutants. 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
The correct anatomy of a signaling network is essential as sugar-mediated repression of photosynthetic gene expression, was a new
its structure always affects its function. The diagrams ABI4 allele. As in the work described in [5•], other ABA-responsive mutants
(abi1, abi2, abi3 and abi5) did not display sugar-insensitive phenotypes.
defined by genetics not only tell us how information is
transferred throughout the organism but also indicate the 7. Gibson SI, Laby RJ, Kim D: The sugar-insensitive1 (sis1) mutant of
• Arabidopsis is allelic to ctr1. Biochem Biophys Res Commun 2001,
robustness and stability of the transmission. With the 280:196-203.
advent of complete sets of mutant knockout lines and The isolation of mutants resistant to 0.3 M sucrose during germination
identified sis1, a new allele of ctr1. Whereas constitutive ethylene response
global transcript profiling, we are entering a stage in which mutants are insensitive to the inhibitory effect of high sugar on early seedling
all the elements involved in these pathways will be known. growth, ethylene-insensitive mutants showed a sugar-hypersensitive phenotype.
This paper linked ethylene and sugar responses.
It is, therefore, essential that the mutants identified in genetic
screens give us a physiologically and developmentally 8. Gibson SI: Plant sugar response pathways. Part of a complex
regulatory web. Plant Physiol 2000, 124:1532-1539.
relevant blueprint of wild-type signaling.
9. Coruzzi G, Zhou L: Carbon and nitrogen sensing and signaling in
plants: emerging ‘matrix effect’. Curr Opin Plant Biol 2001,
Update 4:247-253.
Recently, Rook et al. [43•] have shown that although ABA 10. Hua J, Meyerowitz EM: Ethylene responses are negatively
is unable to induce expression of the ADP-glucose regulated by a receptor gene family in Arabidopsis thaliana. Cell
1998, 94:261-271.
pyrophosphorylase Apl3 gene it enhances the induction of
11. Gamble R, Coonfield, Schaller GE: Histidine kinase activity of the
this gene by sugar. The authors suggest that sugar-induced ETR1 ethylene receptor from Arabidopsis. Proc Natl Acad Sci USA
ABA synthesis makes the seedling more sensitive to ABA- 1998, 95:7825-7829.
dependent sugar signals, a hypothesis that is consistent 12. Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker J: CTR1, a
with the model proposed in Figure 1. negative regulator of the ethylene response pathway in
Arabidopsis, encodes a member of the RAF family of protein
kinases. Cell 1993, 72:427-441.
Acknowledgement 13. Fujita H, Syono K: Genetic analysis of the effects of polar auxin
This work was supported by a grant from the Natural Sciences and inhibitors on root growth in Arabidopsis thaliana. Plant Cell
Engineering Research Council (NSERC). Physiol 1996, 37:1094-1101.
14. Su W, Howell SH: A single genetic locus, ckr1, defines
Arabidopsis mutants in which root growth is resistant to low
References and recommended reading concentrations of cytokinin. Plant Physiol 1992, 99:1569-1574.
Papers of particular interest, published within the annual period of review,
have been highlighted as: 15. Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG: Identification
of three genetic loci controlling leaf senescence in Arabidopsis
• of special interest thaliana. Plant J 1997, 12:527-535.
•• of outstanding interest
16. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker J: EIN2, a
1. McCourt P: Genetic analysis of hormone signaling. Annu Rev Plant bifunctional transducer of ethylene and stress responses in
Physiol Plant Mol Biol 1999, 50:219-243. Arabidopsis. Science 1999, 284:2148-2152.
2. Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, 17. Özcan S, Dover J, Johnston M: Glucose sensing and signaling by
• McCourt P: Regulation of abscisic acid signaling by the ethylene two glucose receptors in the yeast Saccharomyces cerevisiae.
response pathway in Arabidopsis. Plant Cell 2000, 12:1117-2000. EMBO J 1998, 17:2566-2573.
This study and work by Beaudoin et al. [3•] demonstrate that many ethylene
response mutants also have altered ABA responses, depending on the tissue 18. Leung J, Giraudat J: Abscisic acid signal transduction. Annu Rev
that is assayed. Ethylene appears to be a negative regulator of ABA action Plant Physiol Plant Mol Biol 1998, 49:199-222.
in the seed but positively regulates some aspects of ABA action in the root. 19. Bonetta D, McCourt P: Genetic analysis of ABA signal transduction
These studies suggest that correct signaling in a variety of ABA modulated pathways. Trends Plant Sci 1998, 3:231-235.
pathways in plants requires a functional ETR1 response pathway.
20. Gosti F, Beaudoin N, Serizet C, Webb AAR, Vartanian N, Giraudat J:
3. Beaudoin N, Serizet C, Gosti F, Giraudat J: Interaction between ABI1 protein phosphatase 2C is a negative regulator of abscisic
• abscisic acid and ethylene signaling cascades. Plant Cell 2000, acid signaling. Plant Cell 1999, 11:1897-1909.
12:1103-1115.
See annotation [2•]. 21. Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J: The ABI1 and
ABI2 protein phosphatase 2C act in a negative feedback
4. Arenas-Huetero F, Arroyo A, Zhou L, Sheen J, Leaon P: Analysis of regulatory loop of the abscisic acid signaling pathway. Plant J
• Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a 2001, 25:295-303.
central role of the plant hormone ABA in the regulation of plant
vegetative development by sugar. Genes Dev 2000, 14:2085-2096. 22. Giraudat J, Hauge B, Valon C, Smalle J, Parcy F, Goodman H:
A glucose-insensitive mutant gin6, selected for the ability to grow on 7% Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant
glucose, carried a T-DNA insertion in the promoter of the ABI4 gene, which Cell 1992, 4:1251-1261.
Genetic interactions between ABA, ethylene and sugar signaling pathways Gazzarrini and McCourt 391
23. Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM: The 34. Xiong L, Ishitani M, Lee H, Zhu JK: HOS5 — a negative regulator of
Arabidopsis abscisic acid response locus ABI4 encodes an osmotic stress-induced gene expression in Arabidopsis thaliana.
APETALA2 domain protein. Plant Cell 1998, 10:1043-1054. Plant J 1999, 19:569-578.
24. Finkelstein RR, Lynch TJ: The Arabidopsis abscisic acid response 35. Smeekens S, Rook F: Sugar sensing and sugar-mediated signal
• gene ABI5 encodes a basic leucine zipper transcription factor. transduction in plants. Plant Physiol 1997, 115:7-13.
Plant Cell 2000, 12:599-609.
The molecular identification of ABI5, along with previous studies showing 36. Smeekens S: Sugar regulation of gene expression in plants. Curr
that ABI3 and ABI4 are also transcription factors [22,23], shows the Opin Plant Biol 1998, 1:230-234.
importance of transcriptional regulation during embryogenesis in determining
ABA responsiveness to the seed. Furthermore, the homology of ABI5 to a 37. Sheen J, Zhou L, Jang JC: Sugar as signaling molecules. Curr Opin
bZIP domain is intriguing as TRAB1, a maize bZIP transcription factor, has Plant Biol 1999, 2:410-418.
been shown to interact with maize VP1, the ABI3 ortholog. 38. Garraciubo A, Legaria JP, Covarrubias AA: Abscisic acid inhibits
25. Söderman EM, Brocard IM, Lynch TJ, Finkelstein RR: Regulation and germination of mature Arabidopsis seeds by limiting the
function of the Arabidopsis ABA-insensitive4 gene in seed and availability of energy and nutrients. Planta 1997, 203:182-187.
abscisic acid response signaling networks. Plant Physiol 2000, 39. Finkelstein RR, Linch TJ: Abscisic acid inhibition of radicle
124:1752-1765. emergence but not seedling growth is suppressed by sugars.
26. Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P: A protein Plant Physiol 2000, 122:1179-1186.
farnesyl transferase involved abscisic acid signal transduction in 40. Lopez-Molina L, Mongrand S, Chua NH: A postgermination
Arabidopsis. Science 1996, 273:1239-1241. • developmental arrest checkpoint is mediated by abscisic acid and
27. Pei ZM, Ghassemian M, Kwak CM, McCourt P, Schroeder JI: Role of requires the ABI5 transcription factor in Arabidopsis. Proc Natl
farnesyltransferase in ABA regulation of guard cell anion Acad Sci USA 2001, 98:4782-4787.
channels and plant water loss. Science 1998, 282:287-290. The authors of this paper demonstrate that ABI5 works in a short devel-
opmental window post-germination to regulate the ABA responsiveness of
28. Bonetta D, Bayliss P, Sun S, Sage T, McCourt P: Farnesylation is the seedling. Furthermore, ABI5 is post-translationally modified in an ABA-
involved in meristem organization in Arabidopsis. Planta 2000, dependent manner, demonstrating, for the first time, a molecular mechanism
211:182-190. linking an ABI transcription factor with ABA signaling.
29. Yalovsky S, Rodriguez-Concepcion M, Bracha K, Toledo-Ortiz G, 41. Zhou L, Jang JC, Jones TL, Sheen J: Glucose and ethylene
Gruissen W: Prenylation of the floral transcription factor signal transduction crosstalk revealed by an Arabidopsis
APETALA1 modulates its function. Plant Cell 2000, 12:1257-1266. glucose-insensitive mutant. Proc Natl Acad Sci USA 1998,
95:10294-10299.
30. Ziegelhoffer EC, Medrano LJ, Meyerowitz EM: Cloning of the
Arabidopsis WIGGUM gene identifies a role for farnesylation in 42. Quesada V, Ponce MR, Micol J: Genetic analysis of salt-tolerant
meristem development. Proc Natl Acad Sci USA 2000, 97:7633-7638. mutants in Arabidopsis thaliana. Genetics 2000, 154:421-436.
31. Nambara E, McCourt P: Protein farnesylation in plants: a greasy 43. Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW: Impaired
tale. Curr Opin Plant Biol 1999, 2:388-392. • sucrose-induction mutants reveal the modulation of sugar-
32. Steber CM, Cooney SE, McCourt P: Isolation of the GA-response induced starch biosynthetic gene expression by abscisic acid
mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana. signalling. Plant J 2001, 26:421-433.
Genetics 1998, 149:509-521. 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.
33. Foster R, Chua NH: An Arabidopsis mutant with deregulated ABA Interestingly, ABA alone is unable to induce Apl3 expression, but strongly
gene expression: implication for negative regulator function. enhances its induction by sugar, suggesting that ABA influences how tissues
Plant J 1999, 17:363-372. respond to subsequent sugar signals.