JXB Advance Access originally published online on August 28, 2007
Journal of Experimental Botany 2008 59(1):67-74; doi:10.1093/jxb/erm134
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SPECIAL ISSUE REVIEW PAPER |
Hormonal control of shoot branching
Department of Biology, University of York, PO Box 373, York YO10 5YW, UK
* To whom correspondence should be addressed. E-mail: hmol1{at}york.ac.uk
Received 27 March 2007; Revised 4 May 2007 Accepted 15 May 2007
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Abstract |
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 Top Abstract IntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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Shoot branching is the process by which axillary buds, located on the axil of a leaf, develop and form new flowers or branches. The process by which a dormant bud activates and becomes an actively growing branch is complex and very finely tuned. Bud outgrowth is regulated by the interaction of environmental signals and endogenous ones, such as plant hormones. Thus these interacting factors have a major effect on shoot system architecture. Hormones known to have a major influence are auxin, cytokinin, and a novel, as yet chemically undefined, hormone. Auxin is actively transported basipetally in the shoot and inhibits bud outgrowth. By contrast, cytokinins travel acropetally and promote bud outgrowth. The novel hormone also moves acropetally but it inhibits bud outgrowth. The aim of this review is to integrate what is known about the hormonal control of shoot branching in Arabidopsis, focusing on these three hormones and their interactions.
Key words: Auxin, cytokinin, DAD, MAX, RMS, shoot branching
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Introduction |
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TopAbstractIntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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The plant shoot system is derived from the primary shoot apical meristem, which is established during embryogenesis. The meristem consists of a group of undifferentiated cells that initiates the leaves of the plant at its flanks and the elongating stem at its base. The point at which each leaf connects to the stem is called the node. In the axil of each leaf, at the base of the leaf petiole, one or more secondary axillary meristems can form. The primary shoot is formed by the repetition of a stem segment with a node carrying a leaf and one or more axillary meristems.
The axillary meristems have the same developmental potential as the primary shoot apical meristem, and each can therefore form an entire secondary shoot. However, they frequently form only a few leaves before arresting to form a dormant axillary bud. The buds can subsequently reactivate, producing a branch. This flexibility in axillary meristem activity makes possible substantial variation in shoot system architecture, allowing the plant to adapt its architecture to the prevailing environmental conditions. Hence it is not surprising that axillary bud activity is regulated by a wide range of environmental inputs such as the levels and quality of light (Snowden and Napoli, 2003; Cline, 1996), and nutrient availability (Cline, 1991). These environmental signals are likely to be relayed through the action of plant hormones. Of particular importance are auxin and cytokinin, as well as a new carotenoid-derived hormone which has yet to be chemically defined, but the existence of which is supported by the analysis of a series of shoot branching mutants in Arabidopsis, pea, and petunia (Beveridge, 2000; Booker et al., 2005; Simons et al., 2007). This review focuses on the understanding of the control of shoot branching by these three hormones.
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Auxin |
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TopAbstractIntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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Auxin was the first hormone to be linked to the regulation of shoot branching, and it has been in the spotlight for more that 100 years. It was known that the apex of the plant inhibits axillary bud outgrowth in some way because, when the apex is removed, axillary buds that have been dormant activate and the plant starts branching. The first experiment that linked this phenomenon with auxin was carried out by Thimann and Skoog (1934). They showed that auxin, applied to the top of a decapitated plant mimics the effect of the removed apex, preventing bud outgrowth.
Since Thimann and Skoog, many researchers over the years have contributed to the understanding of how auxin represses bud outgrowth and controls shoot branching (Leyser, 2003, 2005). Indole-3-acetic acid (IAA), the most abundant type of auxin in plants, has been shown to be abundantly synthesized in the shoot apex and young expanding leaves (Ljung et al., 2001); thus removal of the shoot apex removes a major auxin source. The auxin is transported basipetally down the shoot in a polar manner by active transport in the polar transport stream in the vascular parenchyma (Blakeslee et al., 2005). Several protein families are involved in active auxin transport, such as the influx facilitators AUXIN INFLUX CARRIER PROTEIN 1 (AUX1)/LIKE-AUX1 (LAX) proteins (Parry et al., 2004), the p-glycoprotein auxin efflux carriers (PGP) (Geisler and Murphy, 2006), and the PIN-FORMED auxin efflux carriers (PIN) (Paponov et al., 2005). In the Arabidopsis main shoot PIN1 appears to be particularly important for polar auxin transport, since loss of function of this single gene results in a substantial reduction in transport (Okada et al., 1991). Consistent with this role, the PIN1 protein is polarly localized in the plasma membrane at the base of xylem parenchyma cells (Gälweiler et al., 1998).
Although it is clear that apical auxin moving in the polar transport stream inhibits bud outgrowth, its mechanism of action in this process is still unclear. It is known that radiolabelled auxin applied apically does not enter the bud in any quantity (Prasad et al., 1993; Booker et al., 2003), and in fact the levels of auxin in buds frequently increase when the buds activate (Gocal et al., 1991). This is perhaps not surprising given that active shoot apices are prolific in auxin synthesis. Furthermore, direct auxin application onto the bud does not inhibit outgrowth (Brown et al., 1979). Thus the auxin moving in the stem must act indirectly.
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Cytokinin |
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TopAbstractIntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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Another hormone that is involved in shoot branching is cytokinin (Ck) (Cline, 1991). In contrast to the indirect inhibitory action of auxin, Cks directly promote bud growth. Exogenous Ck applied to buds promotes their outgrowth (Sachs and Thimann, 1967; Miguel et al., 1998) and Ck levels increase in buds as they activate (Emery et al., 1998).
Three different cytokins are the most abundant in higher plants: isopentenyladenine (iPT), zeatin (Z), and dihydrozeatin (DZ). Cks are synthesized in both the root and shoot (Chen et al., 1985; Nordström et al., 2004) and can move acropetally through the plant in the transpiration stream in the xylem.
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A novel branch-inhibiting hormone |
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TopAbstractIntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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One approach that enables us to understand the complex process of shoot branching regulation is the analysis of mutants. In Arabidopsis, the more axillary growth mutants (max1, max2, max3, and max4); in pea, the ramosus mutants (rms1, rms2, rms3, rms4, and rms5), and in petunia, the decreased apical dominance mutants (dad1, dad2, and dad3), have each been described (Beveridge et al., 1994, 1996, 1997; Napoli, 1996; Morris et al., 2001; Stirnberg et al., 2002; Booker et al., 2004, 2005; Sorefan et al., 2003; Snowden et al., 2005; Simons et al., 2007). Loss of function at any of these loci produces more branching shoots compared with wild-type (WT) (Fig. 1). Furthermore, for a subset of the mutants, including rms1, rms5, dad1, dad3, max1, max3, and max4 the branching phenotype of the mutant shoots can be restored to wild-type by grafting to wild-type rootstocks, suggesting that the mutants lack a graft transmissible branch inhibitor (Napoli, 1996; Morris et al., 2001; Turnbull et al., 2002; Sorefan et al., 2003; Simons et al., 2007). The production of this inhibitor can occur either in the shoot or in the root, because wild-type shoots grafted to mutant roots also have wild-type branching.
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In Arabidopsis, double mutant analysis and reciprocal grafting experiments with max1, max2, max3, and max4 demonstrate that the four genes act in the same pathway, with MAX1, MAX3, and MAX4 necessary for the production of a proposed novel hormone, and MAX2 involved in its signal transduction (Booker et al., 2005). The reciprocal grafting results suggest that MAX1 acts on a mobile intermediate downstream of MAX3 and MAX4, which are predicted to have immobile substrates.
All the MAX genes have been cloned (Stirnberg et al., 2002; Sorefan et al., 2003; Booker et al., 2004, 2005). MAX3 (At2g44990) was identified as a plastidic carotenoid cleavage dioxygenase (CCD) (Booker et al., 2004; Auldridge et al., 2006). When expressed in E. coli it has been shown to cleave a range of carotenoid substrates (Booker et al., 2004; Schwartz et al., 2004). MAX4 (At4g32810) is also a CCD, although substantially divergent from MAX3 (Sorefan et al., 2003). In E. coli MAX4 also shows CCD activity (Auldridge et al., 2006) and is able to cleave one of the products of the MAX3 carotenoid cleavage reaction (Schwartz et al., 2004). MAX1 (At2g26170) encodes a cytochrome P450 family member. MAX1 belongs to the Class III cytochrome P450s and the substrate of this class is often generated by dioxygenases, consistent with the proposed position for MAX1 downstream of MAX3 and MAX4 in the synthesis of the branching-inhibiting substance. Finally, MAX2 (At2g42620) also known as ORE9 (Woo et al., 2001), belongs to the F-box protein LRR family. Members of this family act as the substrate-selecting subunit of SCF-type ubiquitin–protein ligases, which catalyse the polyubiquitination of selected substrate proteins, usually marking them for degradation by the 26S proteosome (Ciechanover et al., 2000; Stirnberg et al., 2007). This probable biochemical function is also consistent with the predicted action of this gene in signal transduction of the novel hormone.
Double mutant analysis and reciprocal grafting experiments conducted in pea and petunia reveal a broadly similar picture, although with some interesting differences (see below). Consistent with this, the molecular analysis of the MAX genes has allowed a demonstration of orthology between some members of the MAX, RMS, and DAD gene families. Specifically MAX4, RMS1, and DAD1 are orthologous (Sorefan et al., 2003; Foo et al., 2005; Snowden et al., 2005), as are MAX3, RMS5 (Johnson et al., 2006), and possibly DAD3 (Simons et al., 2007). MAX2 is orthologous to RMS4 (Johnson et al., 2006), but in addition in pea there is a second gene, RMS3, predicted to act in the signal transduction of the novel hormone (Beveridge et al., 1996). In petunia, the predicted signal transduction mutant, dad2, does not affect the petunia MAX2/RMS4 homologue (Simons et al., 2007), and therefore an attractive hypothesis is that it is orthologous to RMS3. Thus far there are no mutations in the pea or petunia MAX1 homologues and no branching mutants in Arabidopsis that could be equivalent to rms3 or dad2. Recently, mutations in rice orthologues to MAX3/RMS5 and MAX2/RSM4 have been described as resulting in increased tillering (Ishikawa et al., 2005; Zou et al., 2006), suggesting that the pathway is conserved widely, at least in seed plants. Database searches reveal closely related genes across the plant kingdom.
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Interactions |
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TopAbstractIntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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Interactions between auxin and cytokinin
The indirect mechanism of action of auxin contrasts with the direct effects of cytokinin on bud growth. Interestingly, there is good evidence that auxin can regulate cytokinin biosynthesis. Application of auxin rapidly reduces flux through the isopentenyladenosine-5'-monophosphate-independent cytokinin biosynthetic pathway (Nordström et al., 2004). This effect of auxin appears to be mediated by the well-characterized auxin signal transduction pathway involving the AXR1, TIR1, and the other AFB genes (Leyser, 2006; Quint and Gray, 2006; Teale et al., 2006). For example, the effect of exogenous auxin on cytokinin synthesis is reduced in loss-of-function mutants in the AXR1 gene (Nordström et al., 2004). This auxin signalling pathway is also required for inhibition of branching. The same axr1 mutants have increased branching and their axillary buds are resistant to the inhibitory effects of apical auxin (Lincoln et al., 1990; Stirnberg et al., 1999). Using tissue-specific promoters and grafting experiments, it has been shown that the main site of action for AXR1 in bud inhibition is the xylem parenchyma and/or in the interfascicular sclerenchyma of the stem (Booker et al., 2003). These tissues encompass the main site for polar auxin transport in the stem (Blakeslee et al., 2005), suggesting that auxin levels in the polar transport stream are monitored by this pathway and may be read out through regulation of cytokinin synthesis to regulate bud outgrowth.
Consistent with this model, various lines of evidence suggest that apically derived auxin affects cytokinin synthesis both at the node and in the root, and that the level of cytokinin from these sources correlates with bud activity. For example, in pea, it has been reported that auxin reduced Ck synthesis by repressing the expression of the genes encoding the cytokinin biosynthetic enzyme adenosine-phosphate-isopentenyl transferase (IPT) in the stem (Tanaka et al., 2006). In chickpeas it has been reported that, after decapitation, Ck from the root accumulates in the bud (Mader et al., 2003); and there is evidence in pea and bean that, after decapitation, the levels of Ck exported from the root increase, but they can be restored to the levels found in the intact plant by application of auxin to the decapitated stump (Li et al., 1995; Bangerth, 1994; Bangerth et al., 2000).
Taken together these data suggest that one mechanism for auxin-mediated bud inhibition is through down-regulation of cytokinin synthesis, limiting cytokinin supply to the bud and reducing bud outgrowth. Consistent with this idea, basal supply of cytokinin through the transpiration stream can release Arabidopsis buds from inhibition imposed by apical auxin (Chatfield et al., 2000).
Auxin and the novel hormone
An intimate connection between the Arabidopsis MAX pathway and auxin has been proposed. Firstly, max mutant buds are resistant to the inhibitory effects of apical auxin (Sorefan et al., 2003; Bennett et al., 2006), suggesting that the pathway is required for full auxin-mediated bud inhibition. Furthermore, there is strong evidence to suggest that the MAX pathway acts by regulating auxin transport capacity in the main stem. This is achieved at least in part by modulation of the levels of PIN auxin efflux carriers (Bennett et al., 2006). In max mutants, there is an accumulation of PIN1 protein and the transcripts of several other auxin transporters have also been shown to be up-regulated (Lazar and Goodman, 2006). This results in an increase in auxin transport capacity in the stem of the mutants (Bennett et al., 2006). The increase in transport capacity apparently causes the increased shoot branching since, if auxin transport levels are reduced back to WT, either chemically with pharmacological transport inhibitors or genetically in the pin1 mutant background, the characteristic bushy phenotype is restored to WT. Furthermore, transport inhibitors can also restore wild-type auxin responses to max mutant buds.
These results link high auxin transport to high shoot branching. This paradox can be resolved by proposing a model in which the apical meristems on the shoot compete for limited auxin transport capacity in the stem. The assumptions of the model are that active shoot apical meristems must be able to export auxin, and that there is limited sink strength for auxin in the main stem of Arabidopsis. The first assumption is based on a strong correlation between bud activity and auxin export from the bud that has been known for many years (Morris, 1977; Li and Bangerth, 1999). Interestingly, recent results on the role of auxin in pattern leaf initiation at the shoot apex (Reinhardt et al., 2003) suggest an explanation as to why auxin export may be needed for meristem function. Leaves are initiated in the meristem at the convergence point of PIN protein orientation in the epidermal cell layer, suggesting auxin movement towards the site of leaf initiation. As the leaf is specified, additional PIN expression is observed in sub-epidermal layers with orientation suggesting the internalization of auxin. This domain of PIN expression predicts the future vascularization of the leaf. It is possible that this auxin internalization is required for continued meristem activity and that, in turn, it requires sufficient auxin transport capacity in the main stem to be established and maintained. The second assumption—that, in Arabidopsis, the auxin transport capacity in the WT stem is limiting is derived from the analysis of the max mutants, in which increased transport capacity is accompanied by increased branching (Bennett et al., 2006).
Thus this model suggests a second mode of action of apically derived auxin in the inhibition of bud outgrowth that relies on competition for limited auxin transport capacity in the main stem (Fig. 2). In the WT situation, auxin transport capacity (for example, PIN protein levels) in the main stem is limited, and becomes rapidly fully occupied by apically-derived auxin. Thus new auxin sources, i.e. axillary meritesm, are unable to establish an auxin transport stream out into the main stem. By contrast, in the max mutants, PINs and other auxin transport components over-accumulate and the auxin transport capacity of the stem is not saturated, allowing most of the axillary buds to export auxin into the stem and consequently to develop into new branches, showing the characteristic max bushy phenotype.
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This additional mode of action for auxin is distinct from that described above in which auxin concentration in the stem is monitored through the AXR1/AFB pathway and read out to regulate cytokinin production. The independence of these pathways is supported by the observation that auxin transport capacity in axr1 mutants is not different from wild-type, and axr1 max double mutants have additive phenotypes, with respect to both branch number and bud auxin response (Bennett et al., 2006).
Despite the clear distinction between these two auxin-related pathways, the situation is further complicated by the fact that the AXR1/AFB pathway interacts more directly with the MAX pathway through auxin-regulated MAX gene expression. In Arabidopsis, auxin is able to up-regulate a MAX4 promoter–reporter GUS fusion in the root tip and in the hypocotyl, and this up-regulation requires AXR1 (Bainbridge et al., 2005). Interestingly, in pea, much stronger auxin regulation of RMS1 and RMS5 expression has been observed using quantitative real-time PCR (qRT-PCR) in stem segments (Foo et al., 2005; Johnson et al., 2006). For RMS1, the most dramatic effects come from the reduction in basal expression levels by decapitation and hence presumably auxin removal. RMS1 transcript levels can be maintained by the addition of auxin to the decapitated stump. This difference might be due to differences in the regulation of the network between pea and Arabidopsis, or it might be due to the different sensitivities of the GUS and qRT-PCR systems. Certainly, it is not possible to detect GUS activity in most tissues in the MAX4 promoter::GUS reporter lines (Bainbridge et al., 2005), so detecting reductions in expression with auxin removal would clearly not be possible.
The MAX pathway and cytokinin
In pea, there is excellent evidence that the RMS pathway regulates cytokinin levels through a feedback signal that can move from the shoot to the roots (Foo et al., 2007). Xylem sap cytokinin is significantly below wild-type in the rms1, rms3, rms4, and rms5 mutants, and this effect can be mediated by the shoot, because when rms4 or rms3 scions are grafted to WT rootstocks, this low xylem sap Ck from the root is still observed (Beveridge, 2000). Recently, it has been shown that a similarly reduced level of cytokinin is present in max mutant xylem sap (Foo et al., 2007).
Interestingly, in the pea rms2 mutant, which shows the characteristic increased shoot branching of rms mutants, xylem sap Ck levels are normal or slightly elevated compared with WT. This has led to the proposal that the RMS2 gene is required in some way for the action of the downwardly mobile feedback signal. (Beveridge et al., 1997; Beveridge, 2000; Foo et al., 2007).
The idea of a basipetally moving feedback signal that requires RMS2 for its action is further supported by analysis of the expression of the RMS1 and RMS5 genes in other rms mutant backgrounds (Foo et al., 2005; Johnson et al., 2006). These genes are massively up-regulated in all the other rms backgrounds except rms2, where levels of RMS1 and RMS5 transcript are reduced. In Arabidopsis, this effect could not be detected using the MAX4 promoter::GUS fusion except in the hypocotyl of max2 mutants (Bainbridge et al., 2005). Here again, this might be due to differences between the systems or to differences in the sensitivity of the techniques used. Interestinly, in petunia the DAD1 gene, a MAX4 orthologue, is up-regulated in the stems of dad mutants but not in the roots (Snowden et al., 2005).
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The nature of the feedback signal |
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TopAbstractIntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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As briefly outlined above, the detailed analysis of the pea RMS system has clearly demonstrated the existence of a basipetally moving feedback signal that regulates both xylem sap Ck levels and RMS1 and RMS5 transcript abundance. It is possible that this signal is novel, but an alternative hypothesis is that this signal is, in fact, auxin. In this hypothesis, the RMS2 gene would be predicted to be involved in auxin signal transduction in some way, such that candidate Arabidopsis orthologues would include AXR1, AFB etc. Certainly there are striking similarities between the properties of the feedback signal and auxin, and between the phenotype and genetic behaviours of the rms2 and axr1 mutants.
If the feedback signal is auxin, then the hormonal network in question might resemble the diagram in Fig. 3. In this model, auxin, produced at the active primary shoot apex, is transported down the plant in the polar transport stream. In the stem, it has two distinct effects. One is to down-regulate cytokinin biosynthesis via the AXR1/AFB pathway, and one is to occupy limited auxin transport capacity, preventing establishment of auxin export from dormant axillary meristems. In rms1/dad1/max4 mutants, the lack of the unknown upwardly mobile signal results in enhanced auxin transport capacity in the main stem, allowing auxin export from the buds. This results in both increased bud outgrowth and increased auxin in the polar transport stream. The increased auxin in the polar transport stream would have several consequences. Firstly, it would result in a down-regulation of cytokinin synthesis, and secondly it would result in the up-regulation of RMS1/DAD1/MAX4 expression; both effects of the predicted feedback signal. In the axr1 mutant, auxin response is reduced, such that Ck levels are elevated, and auxin is unable to up-regulate MAX4 expression. The effects on branching and bud auxin response are additive with max mutants (Bennett et al., 2006). These results are similar to those observed in the rms2 mutant (Beveridge et al., 1997; Foo et al., 2005, 2007).
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Various arguments against the feedback signal being auxin have been raised, such as rms2, which lacks feedback regulation, and has higher IAA levels than the other rms mutants (Beveridge et al., 1996; Morris et al., 2001). However, if rms2 is an auxin signalling mutant, like axr1, this characteristic would be expected. In addition, measured auxin levels in the rms mutants are near WT (Beveridge, 2000). However, if high auxin content was restricted to the polar transport stream as suggested for Arabidopsis (Bennett et al., 2006), then whole tissue differences might be obscured. Auxin transport rates are not affected in rms or max mutants, but capacity appears to be affected in both (Beveridge, 2000; Bennett et al., 2006). However, in axr1 and rms2 the transport capacity is similar to WT.
It is worth mentioning that one of the differences between axr1 and rms2 mutants is that shoot branching in rms2 shoots is restored to wild-type when WT roots are grafted to the mutant scion (Morris et al., 2001). In contrast, with axr1, mutant scions cannot be rescued by WT roots (Booker et al., 2003). This difference, and others such as apparently WT auxin responses of rms2 mutants in some assays, demonstrate that there are significant differences between the two mutants.
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Future directions |
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TopAbstractIntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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The chemical identity of the novel branch-inhibiting hormone is still unknown and it is one of the priorities in this research area. The analysis of this pathway in Arabidopsis, pea, and petunia shows similarities between them, but there are also differences. The analysis of the pathway in a wider range of species, such as rice, Medicago, etc. will allow a better understanding of the pathway and its evolution. Another challenge ahead is the understanding of how the environment, such as nutrients and light quality, feed into the system.
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Conclusions |
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TopAbstractIntroductionAuxinCytokininA novel branch-inhibiting...InteractionsThe nature of the...Future directionsConclusionsReferences |
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The process of shoot branching is an important determinant of the plant's shape. After buds are formed, decisions are made within the plant as to whether to produce new branches or not. These decisions are based on environmental signals received, and endogenous signals produced. Many of the molecules that act and interact in this finely tuned network of communication are already known, and new findings are being incorporated in order to build a complete picture of the control of the shoot branching process. The unlocking of the signal transduction processes involved is the challenge that was set more than a century ago, and we are still being driven by it today.
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Acknowledgements |
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VO is funded by a BBSRC grant to OL. Thanks to Patrick Crozier for proofreading the manuscript.
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