JXB Advance Access originally published online on December 12, 2003
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Journal of Experimental Botany, Vol. 55, No. 395, pp. 247-251, January 1, 2004
© 2004 Oxford University Press
Signalling in Abiotic Stress |
Hormone signalling from a developmental context
Received 5 October 2003; Accepted 14 October 2003
Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada
* To whom correspondence should be addressed. Fax: +1 416 978 5978. E-mail: mccourt{at}botany.utoronto.ca
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Abstract |
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 Top Abstract IntroductionHormone signalling or a...Development and the hormone,...ConclusionReferences |
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The influence of hormones on plant growth and development has been clearly documented over the past 50 years. Now, with molecular genetics, the genes that convert changes in hormone levels into a cellular response are beginning to be identified. However, recent studies have demonstrated that the developmental context in which the hormones act plays a large influence on their synthesis and action. In this review, examples are given where known hormone response genes have been shown to have broader developmental roles as well as examples where genes that regulate developmental decisions, such as differentiation and fate, also influence hormone metabolism. The early conclusion of these studies is that an understanding of hormone signal transduction cannot be achieved in the absence of a developmental framework.
Key words: Cross-talk, hormones, plant development, signal transduction,
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Introduction |
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TopAbstractIntroductionHormone signalling or a...Development and the hormone,...ConclusionReferences |
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Although hormones regulate a diverse range of processes, it is still unclear how these small organic molecules can influence so many aspects of plant growth and development. Recently, the concept of cross-talk between hormones has attracted much attention, with the idea that hormone signalling pathways make up a complex interacting web of informational transfer that allows a variety of stimuli to cause a plethora of overlapping responses (Gazzarrini and McCourt, 2003). Much of the evidence for signalling cross-talk in hormone biology comes from genetic studies using the model plant Arabidopsis thaliana (arabidopsis). Often mutations that alter this plant’s responsiveness to one hormone cause other hormonal responses to be altered. A number of molecular mechanisms have been identified that explain the interactions between hormones. Genetic perturbations of one hormone response can cause changes in the synthesis or degradation of another hormone (Vogel et al., 1998). Alternatively, hormone signalling pathways can share signalling components so that both pathways are disrupted by a single mutation (Alonso et al., 1999).
In this review a third influence on hormone signalling in plants that also can impinge on hormone cross-talk is discussed. This is the dimension of developmental context on hormone responsiveness. For example, the amount of exogenous gibberellin (GA) required to rescue defective seed germination of an arabidopsis GA auxotroph is many fold higher than the amount needed to rescue the GA-dependent vegetative dwarf phenotype. Although this may simply reflect that embryos have more receptors for a particular hormone or perhaps may have different levels of hormones, how the developmental context of the cell influences hormone action has seldom been questioned in hormone signalling. An attempt is made to review some limited examples of where an original mutation was first defined as a hormone signalling gene and later shown to be a developmental regulator. Conversely, some select examples have been chosen of known developmental mutations that affect cell differentiation or cell fate, that were later shown to influence hormone synthesis. This review is not exhaustive and examples are limited to arabidopsis studies as the aim is to inform plant biologists of the growing relationship between hormone signalling and developmental studies with the intention of demonstrating that developmental context is required for a full understanding of how a hormone functions.
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Hormone signalling or a case of mistaken identity? |
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TopAbstractIntroductionHormone signalling or a...Development and the hormone,...ConclusionReferences |
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Turning a hormone into a cellular response is often described as involving three phases: perception of the input signal at a receptor, propagation of the signal through molecular commands, and change in a specific output response. Within this framework, mutational analysis in combination with epistasis using double mutant analysis has often led to the production of a linear signalling pathway (McCourt, 1999). Nowhere has this analysis been more successful than in the establishment of the ethylene signal transduction pathway in arabidopsis (for review, see Alonso and Ecker, 2001). In dark-germinated arabidopsis seedlings, ethylene induces the triple response that entails an exaggerated apical hook, radial swelling of the hypocotyl, and inhibition of root and hypocotyl elongation. Using this ethylene-dependent assay, two mutant classes were identified based on opposite phenotypes: those that failed to display the triple response (ethylene-insensitive; ein and etr) and those with a constitutive triple response (ctr1). The construction of double mutants with opposite phenotypes in combination with biochemical studies defined a genetic pathway in which ethylene binds to the ETR1 family of two-component receptor kinases. This binding prevents the activation of the downstream Raf-like protein kinase, CTR1, which in turn is needed to release positive regulators such as EIN2 (a modular integral membrane protein) and EIN3 (a transcription factor) to induce the ethylene-responsive gene expression.
Much of the success of genetic analysis of ethylene signalling has hinged on the specificity of the triple response, which appears to be exclusive to ethylene application. However, such simple and specific physiological response assays are not available for other hormones. For example, germination initially appeared to be a well suited assay for genetic analysis of the ABA pathway, since ABA inhibits seed germination at physiological concentrations. Mutants insensitive or supersensitive to ABA as measured by germination response identified a collection of genes that would appear to function in a signalling pathway (for a review, see Finkelstein et al., 2002). However, because germination efficiency is dependent on many internal and external factors it soon became uncertain as to which of these ‘ABA response genes’ were directly involved in the ABA signalling pathway. For example, to date, over 50 loci when mutated have been shown to affect ABA responsiveness. The chances that all these genes are required for primary ABA signalling seems remote, which begs the question why do so many genes when mutated affect the ABA germination response? Some are genes that are known to be involved in other hormone responses such as ethylene and GA synthesis and signalling (Steber et al., 1998; Beaudoin et al., 2000; Ghassemian et al., 2000). While screens have identified genes that function in many pathways, this makes their function in ABA signalling difficult to interpret. For example, mutations in the ERA1 gene of arabidopsis originally identified a role for a protein farnesyl transferase as a negative regulator of ABA signalling (Cutler et al., 1996; Pei et al., 1998). However, mutations that originally identified a gene (wiggum) based on their defects in floral organ numbers were eventually found to be mutations in the same farnesyl transferase (Running et al., 1998; Ziegelhoffer et al., 2000). Further phenotypic characterization of era1 showed that many phenotypes exist in this mutant background that do not appear to be directly regulated by ABA, including alterations in floral morphology, inflorescence branching and pollen development, and an increased number of lateral roots (Bonetta et al., 2000; Brady et al., 2003). The pleiotropic effects of the era1 mutation, however, are easily explained since this enzyme has many potential targets in the arabidopsis genome. Which, if any, of these farnesylated targets directly functions in ABA signalling is still unknown.
The third type of mutation that may alter hormone responsiveness, but may not directly affect an ABA signalling pathway, occurs in genes that encode developmental regulators. An example of a gene in this class is ABI3 of arabidopsis. Loss-of-function mutations in the ABI3 gene were first identified as causing the embryo to terminate development prematurely, resulting in a highly non-dormant ABA-insensitive seed. Although originally classified as a seed-specific ABA signalling component, recent studies have shown other roles for this transcription factor outside seed development. More importantly, ectopic expression of ABI3 or its maize orthologue VP1 causes leaf cells to take on a more embryonic pattern of gene expression in the presence of exogenous ABA, suggesting that this gene is a regulator of embryo differentiation (Parcy et al., 1994; Suzuki et al., 2001). Thus the change in ABA sensitivity resulting from genetic perturbations in ABI3 can be explained by a change in the developmental fate of the leaf cell rather than a change in ABA signal transduction.
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Development and the hormone, the chicken and the egg? |
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TopAbstractIntroductionHormone signalling or a...Development and the hormone,...ConclusionReferences |
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The interface between hormone signalling and development has, until quite recently, not been a concern of molecular genetic studies. Researchers studying classic developmental questions such as differentiation or cell fate have seldom concerned themselves with the role of plant hormones in these processes. In part, this was because the first task was to identify the key regulators involved in a developmental process of interest. For example, to understand how a hormone can influence flowering time first required the identification of the genes that regulate floral timing. Once the transcription factor LEAFY (LFY) was identified in arabidopsis and shown to be a regulator in the transition from a vegetative to a reproductive meristem, it became possible to study how GA induction of LFY can influence floral timing (Blázquez et al., 1998). As more regulators of meristem function are identified, it is becoming clear that these genes are not only influenced by changes in hormone concentrations but they also regulate hormone biosynthesis and sensitivity. For example, the shoot apical meristem (SAM) founder cells in the central region maintain their meristem identity through the KNOX (KNOTTED1-like homeobox-containing) genes. Recessive mutations in the maize KNOTTED1 gene and arabidopsis orthologue SHOOTMERISTEMLESS (STM) gene result in the failure to develop and maintain the SAM (Long et al., 1996; Kerstetter et al., 1997). Conversely, ectopic expression of KNOX genes results in the formation of adventitious meristems on leaves (Sinha et al., 1993; Chuck et al., 1996). Ectopic expression of KNOX genes from many species also results in the accumulation of cytokinins (Tamaoki et al., 1997; Kusaba et al., 1998a; Hewelt et al., 2000; Frugis et al., 2001). Similarly, plants that endogenously overproduce cytokinins increase KNAT1 and STM transcript levels in shoot meristems (Rupp et al., 1999). Moreover, overexpression of KNOX genes also results in the alteration of other hormone levels. For example, IAA and ABA levels in tobacco plants overexpressing the rice homeobox gene OSH1 exhibit decreased levels of IAA in phenotypically mild plants, while the level of ABA is greatly increased in both mild and severe transgenic plants (Kusaba et al., 1998a). The mechanism of how KNOX genes regulate cytokinin, auxin and ABA levels is unknown.
More is known about how KNOX genes regulate GA levels. When ectopically expressed, rice and tobacco homeobox genes cause decreased GA levels (Kusaba et al., 1998a, b; Sakamoto et al., 2001). The decreased levels of GA correlate with the severity of leaf shape and plant stature, and the application of exogenous GA can rescue these phenotypes (Kusaba et al., 1998a; Hay et al., 2002). The decreased GA levels correlate with a suppression of GA, 20-oxidase gene expression, suggesting that overexpression of KNOX genes regulates GA levels through GA biosynthesis. Sakamoto et al. (2001) showed that the tobacco KNOX protein NTH15 directly binds a sequence in the GA biosynthetic gene for GA 2-oxidase Ntc12. Mutational analysis of this Ntc12 sequence abolished binding and NTH15-dependent suppression of Ntc12::LUC expression in the SAM, showing that KNOX proteins can directly regulate GA biosynthesis in the SAM.
Misexpression of KNAT1 also appears to influence other hormone functions in higher plants. For example, when KNAT1 is fused to a senescence-inducible promoter the resulting transgenic plants show delayed senescence and an increase in cytokinin content in mature leaves (Ori et al., 1999). In the rough sheath2 (rs2) mutant of maize that displays ectopic expression of three KNOX genes, auxin transport has been shown to be defective (Tsiantis et al., 1999). Because these results are based on constitutive misexpression it is difficult to determine cause and effect. For example, does the decrease in GA synthesis due to KNAT1 misexpression cause the increase in cytokinin levels or are these independently regulated KNAT1 events. As mentioned below, one solution to this problem is to use controlled misexpression of a gene using an experimentally regulated promoter such as a glucocorticoid inducible system (Aoyama and Chua, 1997).
Another KNOX gene (KNAT2) appears to affect ethylene-related phenotypes (Hamant et al., 2002). In this study, DEX-inducible KNAT2 overexpressing lines display delayed leaf senescence. This phenotype is normally inhibited by ethylene perception (Oh et al., 1997). Induced overexpression of KNAT2 also inhibits hypocotyl elongation, induces epinastic cotyledons, and increases leaf lobing. Each of these phenotypes can be suppressed by the application of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC). Similarly, these phenotypes induced by KNAT2 overexpression were suppressed in a ctr1 mutant background, suggesting that KNAT2 acts antagonistically with ethylene in the seedling. Hamant et al. (2002) also looked at the relationship of ethylene and KNAT2 in the SAM. Uninduced lines on ACC resulted in a decrease in the number of cells in the SAM (similar to that observed in the ctr1 mutant). Induction of KNAT2 on ACC increases the number cells in the SAM, further emphasizing an antagonistic relationship between ethylene and KNAT2. Although cytokinins are known to induce ethylene biosynthesis, this does not appear to be the case here since cytokinin and ethylene appear to have opposite effects on KNAT2 in the SAM (Hamant et al., 2002). Although caution is required in interpreting phenotypes associated with ectopic expression, it is striking that such dramatic effects on a whole suite of hormones occurs by altering the level of a single KNOX gene.
Another developmental gene that regulates hormone levels is AMP1 (altered meristem program; Chaudhury et al., 1993). Originally isolated in a screen for embryo patterning mutants as hauptling (hpt; Jurgens et al., 1991), other alleles have been recovered for increased cotyledon number and leaf growth (amp1); constitutive photomorphogenesis (cop2; Hou et al., 1993); conversion of leaves into cotyledons (Conway and Poethig, 1997); and affected primordia timing (pt; Mordhorst et al., 1998). Additional phenotypes observed in amp1 include reduced apical dominance (Chaudhury et al., 1993), an enlarged shoot meristem (Conway and Poethig, 1997) and early flowering (Chaudhury et al., 1993). The high endogenous levels of cytokinins in amp1 can explain many of these phenotypes. Mutations in AMP1 cause increased levels of both zeatin and dihydrozeatin (Chaudhury et al., 1993), which could result in phenotypes associated with photomorphogenesis, an enlarged meristem, and loss of apical dominance. AMP1 has been cloned and found to be similar to human glutamate carboxypeptidases (Helliwell et al., 2001). Although no enzymatic activity has been shown, AMP1 has a number of conserved residues including the N-terminal membrane span, zinc-binding residues and a glutamate important for catalysis (Helliwell et al., 2001). In humans, this class of enzymes acts on small acidic peptides and folate polyglutamate. These potential targets suggest that AMP1 does not directly regulate cytokinin biosynthesis, which is consistent with the observation that not all amp1 phenotypes are phenocopied by cytokinin application and that genes with altered expression in amp1 are not similarly affected by cytokinin (Helliwell et al., 2001). Thus, although mutations in AMP1 clearly affect cytokinin levels, it is not known how this occurs.
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Conclusion |
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TopAbstractIntroductionHormone signalling or a...Development and the hormone,...ConclusionReferences |
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The genetic studies of a number of hormone response mutants indicate that although these mutations were originally defined as hormone response genes, more careful analysis in a developmental context can result in a new interpretation of the primary function of the genes. In part, the interpretation of many hormone response mutants in arabidopsis is conceived in the paradigm of mutational analysis using unicellular organisms like yeast and E. coli. In these model genetic systems, genetic analysis of signalling has been extremely successful because the phenotypes generated are in the context of a single developmental cell type. In the case of multicellular organisms such as arabidopsis, however, the number of cell types is orders of magnitude higher. Thus, phenotypes are more likely to be complicated and dependent on a developmental context (Fig. 1). A single hormone can affect a range of processes throughout the plant life cycle; at the same time, multiple hormones can affect the same tissue types. Moreover, although a plant may encounter a single hormone input signal, there may simultaneously be many outputs due to the mixture of cell types. For example, low concentrations of ABA stimulate primary root growth in young seedlings and inhibit lateral root formation (Ghassemian et al., 2000; De Smet et al., 2003). Also, under conditions of low water potential, ABA simultaneously inhibits shoot growth while promoting root growth in maize plants (Saab et al., 1990). Similarly, the ABA response of one developmental tissue may be quite different from another. The embryo responds to ABA by synthesizing seed storage proteins and lipids while guard cells respond by activating anion channels (for a review, see Finkelstein et al., 2002). Also, mutations in EIN2 result in hypersensitivitiy to ABA in germinating seeds yet insensitivity to ABA in the roots of young seedlings (Beaudoin et al., 2000; Ghassemian et al., 2000). Thus in the case of analysing ABA mutants, as with other hormone response mutants, phenotypic analysis may be complicated by the effect of a single input on a combination of cell types as well as the developmental status of the cells.
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