Auxin as a Model for the Integration of Hormonal Signal Processing and Transduction
Institute of Biology II, Faculty of Biology, University of Freiburg, D-79104 Freiburg, Germany
a Dipartimento di Agronomia Ambientale e Produzioni Vegetali, Agripolis, University of Padova, viale dell'Università 16, 35020 Legnaro, Italy
1 To whom correspondence should be addressed. E-mail klaus.palme{at}biologie.uni-freiburg.de
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Abstract |
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 TOP Abstract INTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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The regulation of plant growth responds to many stimuli. These responses allow environmental adaptation, thereby increasing fitness. In many cases, the relay of information about a plant's environment is through plant hormones. These messengers integrate environmental information into developmental pathways to determine plant shape. This review will use, as an example, auxin in the root of Arabidopsis thaliana to illustrate the complex nature of hormonal signal processing and transduction. It will then make the case that the application of a systems-biology approach is necessary, if the relationship between a plant's environment and its growth/developmental responses is to be properly understood.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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The evolution of plants and animals has been driven by unique sets of selection pressures. In plants, several cellular signaling mechanisms have diverged from those adopted by the animal kingdom to meet the distinct constraints of a sessile lifestyle. A range of unique signaling molecules convert environmental information into a cellular context, regulating a wide range of processes. A complicated, partially overlapping array of important environmental factors such as light (quality, direction and day length), water availability, gravitational orientation and biotic stress are sensed by various receptors and signal transduction systems and integrated into developmental responses. These responses allow plants to adapt to both predictable and exceptional conditions. As many of these decisions result in irreversible growth responses, the use of scarce resources in response to stimuli must be integrated in order to maximize fitness (Trewavas, 2005).
Environmental signals often influence cellular concentrations of, and sensitivity to, plant hormones. As internal signals, hormones have for a long time been attractive research targets. They are derived, for example, from aromatic amino acids, steroids, or carotenoids. However, both biosynthetic and signal transduction pathways seem to have diverged radically between plant and animal lineages (Chow and McCourt, 2006). Plant steroids, for example, are perceived at the plasma membrane by a Ser/Thr receptor kinase with no counterpart in animals (Kinoshita et al., 2005). Similarly, the gaseous hormone ethylene and the cell division regulating group of cytokinins are perceived by unique receptors sharing some similarities with bacterial two-component receptor systems. In contrast, auxin and gibberellin influence elements of the proteolytic control machinery to attenuate the half-life time of transcriptional regulators (Weiss and Ori, 2007). Plant hormones affect overlapping processes. The result of plant hormone action depends on specific hormone combinations and rarely on the specific activities of each. As many highly conserved pathways regulate intracellular signal transmission, we will discuss here the architecture of classic hormone pathways (e.g. abscisic acid, auxin, brassinosteroids, cytokinin, ethylene, gibberellin) and how they are integrated into plant development. Hormone interactions may occur at a biosynthetic level, a signaling level, or via a common action on a specific process. Understanding and modeling successfully the signaling pathways that drive plant development requires quantifying the extents to which these signaling pathways influence each other. To illustrate the complexity of the task, we will focus on the action of auxin in the developing root of Arabidopsis thaliana. Here, complex hormone interactions regulate growth and development in response to internal and external stimuli.
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AUXIN AND BRASSINOSTEROIDS |
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TOPAbstractINTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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Auxin controls root growth and development. A broad range of root developmental processes ranging from cell elongation and the response to gravity to the initiation of lateral branches have been shown to be highly dependent on auxin homeostasis. However, recent studies have indicated significant influences of other plant growth regulators, such as brassinosteroids (BR).
Auxin and brassinosteroids probably have a relatively complex relationship (Hardtke, 2007). It has been shown (using Arabidopsis hypocotyl elongation assays) that the auxin response mutants axr1 (Lincoln et al., 1990), axr2 (Timpte at al., 1994), axr3 and tir1 (Nemhauser et al., 2004) have significant resistance to brassinosteroids. The brassinosteroid response is therefore dependent on a functional auxin signal transduction pathway. Conversely, weak brassinosteroid-signaling bri1 mutants were also unresponsive to temperature-induced hypocotyl elongation, suggesting that the auxin response is dependent on a functional brassinosteroid signal transduction pathway (Nemhauser et al., 2004). This auxin/brassinosteroid physiological interdependency (Mandava, 1988) was shown to be mirrored at the transcriptional level (Clouse et al., 1992; Zurek and Clouse, 1994; Nemhauser et al., 2004; Kim et al., 2006). Goda and colleagues reported 48 genes that were regulated by both auxin and brassinolide (Goda et al., 2004). When they analyzed the frequency of the TGTCTC element, a core element of the previously reported auxin response element (Ulmasov et al., 1995; Sabatini et al., 1999; Casimiro et al., 2001), they found no enrichment in genes specifically regulated by IAA, but a significant enrichment in those up-regulated by both IAA and BRs (Goda et al., 2004; Nemhauser et al., 2004). This suggests that IAA-induced genes are also induced by brassinosteroids, at least in part, via the activation of the auxin responsive element (Nakamura et al., 2003).
Brassinosteroids also regulate root development; this activity is concentration-dependent. Low concentrations (up to 0.1 nM) of exogenous brassinosteroids stimulate root growth in wild-type plants and normalize the root length deficit of brassinosteroid-deficient mutants, while higher concentrations are inhibitory (Müssig et al., 2003). The growth-stimulating effect of exogenous brassinosteroids is not reduced by the auxin transport inhibitor 2,3,5-triidobenzoic acid (Müssig et al., 2003) and 100 nM of epi-brassinolide, the most bioactive brassinosteroid, drastically inhibits root growth of the auxin-insensitive axr1 mutant (Clouse et al., 1993). These observations suggest that root elongation is controlled distinctly by brassinosteroids and auxin, respectively. However, recently, Kim and colleagues found that expression of the Aux/IAA genes AXR3/IAA17, AXR2/IAA7, SLR/IAA14 and IAA28 was induced significantly in roots upon treatment with epi-brassinolide (Kim et al., 2006). As the transcription of several AUX/IAA genes involved in root development was significantly decreased in the brassinosteroid biosynthetic mutant det2 and in the brassinosteroid-signaling mutant bri1, these authors suggested AUX/IAA genes to be the point at which brassinosteroids and auxin-signaling pathways converge during root development (Kim et al., 2006). Moreover, in plants that are either treated with brassinosteroids or defective in brassinosteroid synthesis or signaling, the transcription of PIN genes, which facilitate functional auxin transport, was affected in a rather complicated manner, with both tissue- and dose-dependent modulation of transcript levels (Nakamura et al., 2004; Li et al., 2005). For example the abundance of PIN4 and PIN7 transcripts decreased in dose-dependent manner, while no obvious decrease was observed for PIN2 after wild-type plants were treated with brassinolide (Nakamura et al., 2004). However, brassinolide enhanced plant tropic responses by promoting the accumulation of PIN2 from the root tip to the elongation zone, thus implying an altered distribution of endogenous auxin (Li et al., 2005). The details of exactly when and how brassinosteroid signaling modifies auxin transport are still mysterious (Li et al., 2005).
Significant progress in understanding auxin/brassinosteroid interdependence came recently from the functional characterization of BREVIS RADIX (BRX)—a gene required for optimal embryonic and post-embryonic root growth (Mouchel et al., 2004, 2006). It appears now that brassinosteroid synthesis and auxin signaling are connected through a feedback loop that involves BRX (Mouchel et al., 2006). A feedback loop was proposed in which BRX maintains the expression of the CONSTITUTIVE PHOTOMORPHOGENESIS AND DWARF (CPD) gene to keep brassinosteroid biosynthesis above a critical threshold (Mouchel et al., 2006). This threshold level permits optimal auxin action, which, in turn, maintains BRX expression at a level required for proper CPD activity (Mouchel et al., 2006). Proper brassinosteroid levels, thus, might be rate-limiting for the auxin-induced transcriptional responses required for optimal root growth.
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AUXIN AND GIBBERELLIN |
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TOPAbstractINTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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Auxin and gibberellin (GA) both regulate cell expansion and differentiation and organ expansion, growth and development. For a long time, auxin and gibberellin were thought to act through mainly independent mechanisms. Recently, interactions between GA and auxin have been clearly demonstrated (Ross et al., 2000; Fu and Harberd, 2003). Studies have revealed interactions of at least two types: auxin contributes to growth regulation through (i) the regulation of GA biosynthesis, and (ii) the control of DELLA protein expression, with a subsequent modulation of the GA response (for a recent review, see Weiss and Ori, 2007).
Auxin has been shown to regulate GA biosynthesis in pea (Ross et al., 2000; O'Neill and Ross, 2002), tobacco (Wolbang and Ross, 2001), Arabidopsis (Frigerio et al., 2006) and rice (Cui et al., 2005), although possibly via the regulation of different enzymes in each species. For example, IAA significantly up-regulated PsGA3ox1 transcript levels after 2 h of application (O'Neill and Ross, 2002), down-regulated expression of PsGA2ox1 (a gene encoding a GA-inactivating dioxygenase), but had no or little effect on expression of the PsGA20ox1 gene. However, up-regulation of the PsGA3ox1 gene was inhibited after application of protein synthesis inhibitor cycloheximide (CHX), leading to a suggestion that the gene is not a primary auxin-response gene. It was also shown that regulation of GA metabolism is mediated by Aux/IAA genes. All gain-of-function lines tested (axr2-1/iaa7, axr3-1/iaa17, msg2-1/iaa19 and shy2-2/iaa3) showed defects in transcript levels of GA biosynthesis genes. Recently, a novel mutant, pax1-1 (partial suppressor of axr3-1), in which almost every aspect of the axr3-1 phenotype was suppressed, exhibited defects in GA response. Since pax1-1 positively regulates axr3/iaa17 transcription and interacts with other AUX/IAA genes, it was suggested that PAX1 might also control GA metabolism through alteration of DELLA protein turnover (Tanimoto et al., 2007). The regulation by auxin of GA biosynthetic enzyme-encoding genes does not require DELLA proteins (Frigerio et al., 2006), since both AtGA20ox1 and AtGA20ox2 were induced efficiently in both gai and rga mutants. Expression of the reporter gene GUS driven by AtGA2ox2, AtGA2ox4 and AtGA20ox2 promoters suggests that the auxin effect on GA biosynthesis is tissue-specific.
The GA–DELLA protein interaction mediates plant growth and development. DELLA proteins are members of the GRAS family of transcription factors and are represented by five genes in Arabidopsis (GA INSENSITIVE, GAI; REPRESSOR OF GA1-3, RGA; RGA-LIKE, RGL1; RGL2; and RGL3). Products of these genes are nuclear proteins whose stability and expression are regulated by GA. Either the exogenous application of GA or the removal of GAI or RGA proteins suppresses the phenotype of the GA-deficient ga1-3 mutant. Fu and Harberd (2003) demonstrated that decapitated ga1-3 seedlings were significantly less responsive to GA than intact seedlings. Application of IAA to the site of decapitation recovered the GA response in ga1-3 roots by promoting GA-mediated DELLA protein destabilization. Furthermore, suppression of AtPIN1 (a mediator of polar auxin transport), as well as application of 1-naphthylphthalamic acid (NPA) (a polar auxin transport inhibitor), affected GA-mediated RGA degradation and elongation of root cells. Thus, auxin and its polar transport are involved in the regulation of DELLA proteins.
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AUXIN AND CYTOKININS |
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TOPAbstractINTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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Investigations into cross-talk among plant hormones are underpinned by early discoveries on the antagonistic effects of auxin and cytokinins—a precedent for hormone interaction in plant development (Skoog and Miller, 1957). Cytokinins themselves are signaling molecules that exert a widespread influence over plant growth and development (Mok, 1994). In Arabidopsis, cytokinin signaling involves a two-component system, which is composed of two elements—a histidine kinase and a response regulator ARR (reviewed by Ferreira and Kieber, 2005). Cytokinins promote meristem cell differentiation (Kyozuka, 2007). Analysis of the ATP/ADP isopentenyltransferase (AtIPT) family of cytokinin biosynthetic enzymes, using both mutant analysis and exogenous cytokinin application, it was found that cytokinins control root meristem size through cell differentiation (Dello Ioio et al., 2007). It was found that root apical meristem size was increased in an ipt3, ipt5, ipt7 triple mutant. These plants showed a simultaneous decrease in the differentiation rate of meristematic cells. The conclusion was drawn that cytokinins control the rate of meristematic cell differentiation by acting in a restricted region of the root meristem (Dello Ioio et al., 2007). These findings are significant to auxin-signaling pathways, as auxin is a crucial signal in root apical meristems, establishing and maintaining stem cell identity (Aida et al., 2004).
Usually, cytokinins are negative regulators of root growth and development. Transgenic plants, which over-express cytokinin oxidase/dehydrogenase (CKX) genes, have lowered cytokinin levels, and display a variety of phenotypes, including enlarged root meristems, the formation of lateral roots in closer proximity to the apical meristem, increased root branching, and the promotion of adventitious root formation (Werner et al., 2003). Moreover, Lohar et al. (2004) showed a specific reduction in cytokinin levels in early lateral root primordia (Lohar et al., 2004). After an analysis of the expression of cyclin genes during lateral root formation, Li et al. reported that cytokinins inhibit the initiation of lateral roots through blocking the pericycle founder cells cycling at the G2 to M phase transition (Li et al., 2006). Auxin is also thought to exert control over the cell cycle by regulating key genes (del Pozo et al., 2002; Blilou et al., 2002). The cell cycle is therefore under the influence of both hormones. The relative significance of each and the extent of their interaction represent important unanswered questions.
In contrast to cytokinins, auxin promotes the formation of lateral roots (Guo et al., 2005; Woodward and Bartel, 2005) and adventitious roots (Falasca et al., 2004; Sorin et al., 2005). Cytokinins and IAA have antagonistic roles in root development; the auxin:cytokinin ratio is important for the control of many developmental processes, including organ regeneration from tissue culture (Skoog and Miller, 1957). Auxin can regulate cytokinin biosynthesis in Arabidopsis (Nordström et al., 2004). This work showed that auxin can reduce the pool size of major cytokinin intermediates. Here, the effect of auxin on cytokinin biosynthesis was demonstrated with two auxin-resistant mutants—axr1 and axr4. These plants did not have increased cytokinin levels, when compared with wild-type plants upon treatment with 1-NAA. It was also shown that in Arabidopsis plants with glucocorticoid-inducible over-expression of selected IPT genes, cytokinin levels could be significantly increased, but, unlike wild-type plants, the rate of auxin synthesis was not affected (Nordström et al., 2004).
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AUXIN AND ABSCISIC ACID |
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TOPAbstractINTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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Far from being linear, abscisic acid (ABA) signaling can be viewed as a complex mesh of interdependent secondary messengers which serve to alter the cellular concentration of Ca2+. These secondary messengers include phospholipid-derived signals, NO and H2O2 (Hirayama and Shinozaki, 2007). Though some of these molecules have also been implicated in auxin signaling, reports of a more direct cross-talk between ABA and auxin have focused on genetic analysis of the hormones’ transcriptional responses.
VIVIPAROUS1 (VP1)—a gene which encodes a transcription factor involved in ABA signaling in maize—is able to complement fully its Arabidopsis ortholog ABI3, when driven by the constitutive 35S promoter. Though the phenotype of these plants is largely normal, unlike wild-type plants, in the presence of ABA, they are unable to form lateral roots after auxin application (Suzuki et al., 2001). An enhancement of the ABA response by auxin, via the action of VP1, indicated a possible point at which the two hormones interact to regulate lateral root development. Further experiments showed that ABI3 itself is auxin-inducible in lateral root primordia (Brady et al., 2003).
ABA signaling is negatively regulated by a prenylated protein, as the phenotype of era1 (a locus encoding a beta-subunit of farnesyl transferase) shows an enhanced response to ABA (Cutler et al., 1996; Pei et al., 1998). ERA1 has been placed in an ABA-signaling cascade downstream of the protein phosphatases ABI1 and ABI2 (which confer sensitivity to ABA), and upstream of ABI3 (Brady et al., 2003). The role of lipid modification in auxin signal transduction is not yet well defined. However, possible connections have been proposed between ABA-mediated protein prenylation and auxin signaling (Johnson et al., 2005). IAA4 (a member of a family of negative regulators of auxin signaling) is prenylated in vitro (Caldelari et al., 2001). Also, prenylated small GTPases have been associated with auxin transport in the case of the Rab family (Ueda et al., 2004), and auxin signaling in the case of the Rop family (Tao et al., 2002). Indeed, besides era1, knockouts of a partially redundant geranylgeranyl transferase, ggb, which display an ABA-insensitive phenotype in guard cells, show increased lateral root formation in response to the application of exogenous auxin (Johnson et al., 2005).
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AUXIN AND ETHYLENE |
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TOPAbstractINTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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Ethylene is synthesized throughout the plant in response to a wide range of environmental and developmental stimuli, eliciting many growth responses (Wang et al., 2002). The most characteristic of these (and one much exploited by plant biologists)—the triple response of dark-grown seedlings to ethylene—shows a characteristically exaggerated apical hook. It is also defined by an inhibition of main root and hypocotyl elongation, a swelling of the hypocotyl, and an impaired gravity response (Guzmán and Ecker, 1990). Ethylene is perceived by a class of five trans-membrane receptors, which are related to bacterial two-component histidine kinases. Ethylene can act directly, for example to regulate cell division in the quiescent centre (Ortega-Martínez et al., 2007), or indirectly, for example to inhibit the response to gravity through affecting rates of flavonoid biosynthesis and accumulation (Buer et al., 2006). Ethylene-induced signaling also draws responses in cooperation with a range of other plant hormones. One of these hormones is auxin. The effects the two hormones have in common are particularly well studied. Auxin and ethylene act together to regulate many aspects of plant development, but, crucially in the root meristem, their interplay has been recently shown to act on cell expansion (Swarup et al., 2007; R
i
a et al., 2007). Classical physiological measurements have demonstrated that ethylene inhibits both polar auxin transport (Morgan and Gausman, 1966; Burg and Burg, 1967) and the interaction is significant for the root gravitropic response (Chadwick and Burg, 1970). A plant's response to gravity is mediated by unequal rates of cell expansion on either side of the growing root tip. Genetic evidence for this relationship came with the agravitropic phenotype of eir1—one of the several ethylene-insensitive mutants identified to date (Roman et al., 1995). The eir1 locus was found to encode the auxin transporter AtPIN2, linking ethylene perception and the polar transport of auxin in the root meristem (Luschnig et al., 1998; Müller et al., 1998). With this link came the confirmation that root gravitropism is not under the exclusive control of auxin, but also involves ethylene signaling. PIN2-dependent redistribution of auxin to the lower side of roots is required for gravitropism (Ottenschläger et al., 2003). However, the resulting inhibition of cell expansion requires the coordinated action of both auxin and ethylene. Another auxin transporter, AUX1, is also required for correct gravitropic response and ethylene sensitivity in the roots (Pickett et al., 1990). Furthermore, ethylene inhibits the gravity response by modulating the synthesis of flavonoids, which have been shown to be prime candidates for endogenous auxin transport inhibitors (Buer et al., 2006). These facts indicate the presence of an intimate connection between auxin transport and ethylene signaling.
Three recent studies have shown conclusively that auxin and ethylene signaling is interdependent, suggesting multiple mechanisms by which the hormones are able to mediate each other's action (Swarup et al., 2007; Stepanova et al., 2007; Ria et al., 2007). The coordination of auxin and ethylene signaling is complex and acts at many levels. For example, ethylene up-regulates auxin biosynthesis in the root apex but also requires auxin transport and responses if it is to inhibit root growth (Swarup et al., 2007). Transcript profiling has revealed a complex relationship between auxin and ethylene, with the hormones not only interacting on a biosynthetic level (auxin also regulates ethylene production) and on converging signaling pathways, but also acting independently on the same target genes (Stepanova et al., 2007). A recent model places the regulation of auxin biosynthesis and transport by ethylene at the centre of its effect on Arabidopsis root growth (Ria et al., 2007).
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AUXIN AND NUTRIENTS |
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TOPAbstractINTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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Roots are uniquely responsive to environmental change. How a plant senses the environment and how this signal is relayed to a growth response have long been important questions for plant physiologists and plant breeders alike. Nutrients are certainly a key factor. In many natural and agricultural systems, the availability of nitrogen, phosphorus, sulphur, and potassium often limits growth and reproduction Schulze et al., 1997; Zhang et al., 1998). This provides a strong driving force for the evolution of adaptive mechanisms to sub-optimal nutrient conditions.
Such adaptation has influenced main root growth, lateral root formation, and root hair formation—events which are all regulated by auxin. Therefore, the question arises as to whether or not this type of adaptation is directly related to auxin signaling. This question is not an easy one to answer, as many nutrients can be classified as both metabolites and signaling molecules.
Significant progress in dissecting the distinct signaling and metabolic roles of nutrients was made with the help of non-metabolizable analogs: turanose for sugars (Gonzali et al., 2005), phosphite for phosphate (Carswell et al., 1996, 1997), and mutants, such as a NR-deficient mutant for nitrate (Scheible et al., 1997).
There are at least three sugar-signaling pathways (Jang et al., 1997): (i) a hexokinase (HXK)-dependent pathway in which HXK acts as a sugar sensor; (ii) a glycolysis-dependent pathway in which certain metabolites downstream of hexose phosphorylation could serve as signaling molecules; and (iii) an HXK-independent pathway, possibly involving a sugar receptor on the plasma membrane. The HKX-dependent pathway acts in close conjunction with the auxin-signaling pathway (Moore et al., 2003). Mutation of gin2/hkx1 induces defects in root formation and auxin-induced cell proliferation, although no difference in endogenous auxin levels was found between hkx1 and wild-type (Moore et al., 2003). The gin2/hkx1 mutant lacks the ability to respond to auxin, either endogenous or when applied exogenously (Moore et al., 2003). These data agree with the observation that the auxin-resistant mutants tir1, axr1, and axr2 are also insensitive to growth inhibition by glucose (Rolland et al., 2006).
The ethylene-dependent regulation of ARF2 has been shown to require HOOKLESS1 (HLS1)—a protein with similarity to a family of N-acetyl transferases (Li et al., 2004). HLS1 regulates apical hook formation in dark-grown seedlings (Lehman et al., 1996). HLS1 may also be involved in sugar signaling, controlling HXK activity—a common factor in both the HKX-dependent and the glycolysis-dependent sugar-signaling pathways (Ohto et al., 2006). The hls1 mutation not only enhanced the auxin-induced expression of several auxin-responsive genes, but also increased the expression of sugar-responsive genes after exogenous sucrose application. This suggests that HLS1 negatively regulates both sugar and auxin signaling. The fact that auxin partially suppressed sugar-induced gene expression, and that this suppression was less pronounced in hls1 than in the wild-type, suggests that the negative effect of auxin on sugar signaling is mediated at least in part by auxin response factors (ARFs) in a HLS1-dependent manner (Ohto et al., 2006).
Another molecular target of cross-talk between auxin and sugars is WOX5 (WUSCHEL-related homeobox gene) (Gonzali et al., 2005). Both sucrose (Takahashi et al., 2003) and the non-metabolizable sugar analog turanose (Gonzali et al., 2005) trigger auxin accumulation in the hypocotyls and induce the production of adventitious roots (a response which is also observed after auxin application). WOX5 is expressed in the quiescent centre (QC) cells of the root meristem, and co-localizes with the root auxin concentration maximum. Here, WOX5 allows the maintenance of the auxin maximum by repressing the conjugation of IAA as well as by increasing auxin synthesis through inhibition of the SUR2 pathway (Gonzali et al., 2005). Furthermore, WOX5 expression is induced by auxin and turanose. However, in plants expressing a WOX5-TIN (turanose-insensitive) chimera in the tin mutant background, only auxin and not turanose was able to induce WOX5 expression, suggesting that turanose induction of WOX5 is mediated by auxin (Gonzali et al., 2005). Invertase is a possible target of cross-talk between auxin and sugar metabolism in the plants. Auxin redistribution increases asymmetrically invertase expression and activity. This increase results in the asymmetrical accumulation of hexoses and differential cell elongation across the pulvinus (Long et al., 2002).
By manipulating sucrose and nitrogen concentration in the culture medium, Malamy and Ryan demonstrated that a key factor in the regulation of lateral root inhibition is the ratio of sucrose to nitrogen (Malamy and Ryan, 2001). In this situation, the auxin response is not blocked, as repressive growth conditions of this kind can be overcome by the addition of exogenous 1-NAA (Malamy and Ryan, 2001). Visualization of auxin distribution with help of DR5 reporter lines suggested that in these inhibitory conditions, auxin transport was blocked at the hypocotyl–root junction, causing auxin accumulation in the hypocotyl.
Localized phosphate (Pi) starvation is a signal that strongly influences the root system (Linkohr et al., 2002). Auxin supplementation inhibits primarily root growth and mimics the phenotype of Pi-deprived seedlings (Lopez-Bucio et al., 2002), but, in the primary root at least, it appears the two signals are not interdependent. Here, auxin does not trigger a loss of meristematic activity, as does Pi starvation. A similar inference was drawn by demonstrating the inability of auxin either to mimic or rescue the root phenotype of the pdr2 mutant, which has a disrupted local Pi-sensing mechanism (Ticconi et al., 2004). Furthermore, primary root growth in the auxin-resistant mutants axr1, axr2, and axr4 were similar to wild-type responses both when Pi is sufficient and under Pi deficiency (Williamson et al., 2001; Lopez-Bucio et al., 2002; Al-Ghazi et al., 2003). Whilst Pi deficiency-induced growth modulation is auxin-independent for the primary root, it is auxin-dependent for lateral root development (Jain et al., 2007). Using a DR5::uidA-responsive promoter, it was shown that Pi deprivation induces a shift in auxin responsiveness from the primary root to lateral roots that suggests a redistribution of auxin during Pi deprivation (Nacry et al., 2005; Jain et al., 2007). A significantly lower number of lateral roots emerge under Pi deprivation in the pgp19 mutant (which exhibits reduced basipetal auxin transport) (Geisler et al., 2003, 2005) than in wild-type. This suggests that Pi deficiency induces the sensitivity of the roots to basipetally transported auxin (Jain et al., 2007). Here, then, is another example that demonstrates a change in nutrient conditions affecting not only auxin signaling, but also auxin transport and distribution.
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OUTLOOK |
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TOPAbstractINTRODUCTIONAUXIN AND BRASSINOSTEROIDSAUXIN AND GIBBERELLINAUXIN AND CYTOKININSAUXIN AND ABSCISIC ACIDAUXIN AND ETHYLENEAUXIN AND NUTRIENTSOUTLOOK |
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Plants have acquired novel signaling mechanisms that allow them to control actively the efficient exploitation of environmental resources. The complexity of these mechanisms is such that understanding them remains a considerable challenge for plant physiologists. Plants have minimized tissue and cell functional specialization; but, still, a high degree of phenotypic plasticity (governed by a network of active and resting meristems with no overarching control system) leads to a shape that efficiently mines light, minerals, and water. If we are to understand the overall organization of how plants sense the timing, direction and quantity of environmental physical and internal chemical signals, and how they turn them into cellular responses, we must capture correctly the relevant interactions using quantitative measurements under a variety of conditions. When compared to the dominant reductionist approach in plant research, the field of systems biology provides unique opportunities for the future. Systems biology aims to use a multidimensional approach by extracting information from quantitative multivariate experiments to build models that incorporate the diverse datasets for simulations. This is why systems biology, aided by the arrival of today's ‘omics’ approaches, computer technologies, and computational-based statistical methods, provides the opportunity to extract not only the maximum amount of information from experiments involving genome-scale data, but also enables the design of new experiments and simulation-based models. Testing such model-based predictions in vivo with plant mutants will make the circle complete by integrating and modeling the cellular activity of the genes and proteins that function in plant hormone-signaling networks. We expect that this will not only highlight instances of cross-talk between different signals under various conditions, but also help to devise predictive models that may identify the crucial regulators, hubs, and integrators involved. However, in large, complex signaling networks, the construction of precise quantitative models is precluded by the huge amount of required (but generally unavailable) data. Thus, new tools and techniques need to be developed to obtain information on gene function, physical associations, and quantitative biochemical parameters. When and how do the different proteins interact, and what are the connectivity and the clustering coefficients that provide topological characteristics of proteins in protein interaction networks? How are hormonal nodes connected to their interacting partners, and what are the clustering coefficients that define the cliquishness of each node? How do network motifs in integrated cellular networks describe transcriptional regulation and protein–protein interactions? Though often held back by the technically demanding process of gathering accurate, detailed data from plant systems, modeling approaches have offered new insights with increasing frequency (Merks et al., 2007; Palme, 2006). Especially encouraging progress has been made in a recent attempt to model auxin distribution. Here, a dynamic and robust auxin distribution in the Arabidopsis root tip has been shown to be independent of the source of auxin (Grieneisen et al., 2007). The resulting inferred auxin concentration gradient (the direct detection of which has so far proved elusive) influences the expression of the PLETHORA family of transcription factors, which regulate root development in a dose-dependent manner (Galinha et al., 2007). In turn, PLETHORA proteins regulate auxin concentration gradients via expression of the PIN family of auxin efflux transporters (Galinha et al., 2007) in a system which looks set to become an early testing ground for the applicability of a systems approach to plant growth and development.
The systems analysis of an intracellular network consists of two steps. The first step is the network reconstruction of the relevant chemical and molecular compounds and reactions. The second step is the analysis of this reconstructed network using computational techniques. These two steps are highly interconnected, and, as each computational process is sequentially rebuilt, constant analysis of the network generates hypotheses for further interrogation. The reconstruction process involves the integration of various high-throughput experimental data, and each dataset provides only one perspective on intracellular mechanisms and activities. The large number of components, the degree of interconnectivity, the differences in spatio-temporal scales, and the complex control of signaling networks are becoming evident in the integrated genomic and proteomic analyses that are emerging. Whole-network analyses are necessary to elucidate the global properties amidst the complexity of signaling systems.
A brief survey of the structure and dynamics of auxin-signaling networks in the Arabidopsis root has been discussed here, but more data need to be generated on cellular signaling networks that affect transcriptional regulation. Many other processes are connected and must be considered, such as mechanotransduction, cytoskeletal organization, organelle assembly, vesicular trafficking, and metabolism. In particular, describing mathematically the coupling between mechanical and biochemical processes poses significant challenges that will require the departure from causal, small-scale descriptions to systematic reconstructions of signaling networks. Only then can these reconstructed networks be modeled, allowing us to make quantitative predictions. Although mathematical formulation of these networks is important, by no means can it be argued that a network can be reduced to a set of differential equations. The level of detail of a cellular signaling network can range from inclusion of every moiety involved, to coarse-grained descriptions of key processes. The biological context and expected quantitative outcome will then dictate the degree of detail necessary in the reconstructed biochemical network.
The next years are likely to produce an explosion of data on hormone-mediated signaling pathways using gene microarray technologies, protein–protein interaction studies, fluorescent microscopy, and mass spectrometry. Systematic analysis will focus on the generation of quantitative, computational frameworks for analyzing the properties of signaling systems, and the integration of biological information across temporal and spatial scales. For example, expression array data can indicate which genes are on or off at a given time point, but cannot indicate which protein products interact with one another. Reconstructions should provide a framework by which such events can be integrated.
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We thank members of the Palme lab for critical reading of the manuscript. Our work was supported by the Deutsche Forschungsgemeinschaft (SFB 592), BMBF, DLR, ESA, EU, FCI and the Landesstiftung Baden-Württemberg GmbH. No conflict of interest declared.
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