Journal of Experimental Botany, Vol. 51, No. 342, pp. 51-59,
January 2000
© 2000 Oxford University Press
Regulation of Arabidopsis root development by nitrate availability
Biochemistry and Physiology Department, IACR-Rothamsted, Harpenden, UK
Received 26 February 1999; Accepted 10 June 1999
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Abstract |
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 Top Abstract IntroductionA localized supply of...The stimulation of LR...Evidence for an overlap...[IMAGE] also has a...Summary--a ‘dual...References |
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When the root systems of many plant species are exposed to a localized source of nitrate (
they respond by proliferating their lateral roots to colonize the nutrient-rich zone. This study reviews recent work with Arabidopsis thaliana in which molecular genetic approaches are being used to try to understand the physiological and genetic basis for this response. These studies have led to the conclusion that there are two distinct pathways by which modulates root branching in Arabidopsis. On the one hand, meristematic activity in lateral root tips is stimulated by direct contact with an enriched source of (the localized stimulatory effect). On the other, a critical stage in the development of the lateral root (just after its emergence from the primary root) is highly susceptible to inhibition by a systemic signal that is related to the amount of absorbed by the plant (the systemic inhibitory effect). Evidence has been obtained that the localized stimulatory effect is a direct effect of the ion itself rather than a nutritional effect. A -inducible MADS-box gene (ANR1) has been identified which encodes a component of the signal transduction pathway linking the external supply to the increased rate of lateral root elongation. Experiments using auxin-resistant mutants have provided evidence for an overlap between the auxin and response pathways in the control of lateral root elongation. The systemic inhibitory effect, which does not affect lateral root initiation but delays the activation of the lateral root meristem, appears to be positively correlated with the N status of the plant and is postulated to involve a phloem-mediated signal from the shoot. Key words: lateral roots, nitrate, plasticity, root architecture, signalling.
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Introduction |
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TopAbstractIntroductionA localized supply of...The stimulation of LR...Evidence for an overlap...[IMAGE] also has a...Summary--a ‘dual...References |
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The development of a plant's root system is highly responsive to the availability and distribution of mineral nutrients within the soil. The plasticity of root development is seen most clearly when roots are exposed to localized sources of certain nutrients, which leads to a ‘foraging’ response in which lateral roots (LRs) are stimulated to proliferate specifically within the nutrient-rich zone (Leyser and Fitter, 1998
). This response, which is seen to varying degrees in a wide range of plant species, has important implications for a plant's ability to compete with its neighbours for limiting supplies of nutrients (Robinson, 1994). Root development is also affected by the general availability of nutrients in the soil, being favoured by nutrient-poor conditions and inhibited in nutrient-rich soils (Ericsson, 1995).
The classical experiments on nutrients and root branching were done with barley (Hordeum vulgare) (Drew, 1973, 1975; Drew and Saker, 1975, 1978). Drew and colleagues found that locally concentrated supplies of 
or inorganic Pi (but not K+) stimulated both initiation and elongation of LRs within the nutrient-rich zone. The consensus view has been that these effects are related, either directly or indirectly, to the nutritional properties of the respective ions. For example, it has been suggested that assimilation of locally at its site of uptake leads to an increased influx of photosynthate and/or auxin which then stimulates LR growth in that region (Wiersum, 1958; Drew, 1973; Granato and Raper, 1989; Sattelmacher et al., 1993).
An alternative suggestion was put forward by Trewavas (Trewavas, 1983), who proposed that the ion is an important regulatory molecule in plants and that its stimulation of LR initiation is one of a number of direct effects that it exerts on plant development. The idea of as an environmental signal molecule has since gained wider acceptance (Redinbaugh and Campbell, 1991; Crawford, 1995), although until recently the evidence for signalling in plants was restricted to its role in the induction of the genes for enzymes directly or indirectly involved in assimilation (Pouteau et al., 1989; Gowri et al., 1992; Ritchie et al., 1994).
The first clear evidence for a role of in regulating plant development came from studies with Nicotiana plumbaginifolia mutants deficient in nitrate reductase (NR), in which it was shown that accumulation of high concentrations of in the shoot was correlated with a marked inhibition of root growth (Scheible et al., 1997a, b). Here data from recent studies with Arabidopsis are reviewed which provide further evidence for signalling in plant development and indicate that regulates root development in this species through two distinct pathways involving an external positive signal and an internal negative signal.
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A localized supply of specifically stimulates LR elongation in Arabidopsis
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TopAbstractIntroductionA localized supply of...The stimulation of LR...Evidence for an overlap...[IMAGE] also has a...Summary--a ‘dual...References |
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Arabidopsis offers a number of advantages for studying root development, notably its amenability to molecular genetic analysis, the ever-increasing database of genetic and sequence information, and its small size. Using a novel technique for applying localized nutrient treatments to Arabidopsis roots (the SAP technique) (Fig. 1A
), it was established that the response of Arabidopsis to a locally enriched supply of (1 mM KNO3 when the rest of the root system received 10 µM NH4NO3) is similar to that seen in other species, i.e. an increased production of LRs specifically within the -rich zone (Zhang and Forde, 1998). More detailed studies established that this was specifically due to a 2–3-fold increase in the mean rate of LR elongation, there being no increase in the numbers of first order LRs (Zhang et al., 1999). This differs from results obtained with barley and wheat (Triticum aestivum) where a similar treatment elicited an increase in both the elongation rate and the numbers of both first and second order LRs (Hackett, 1972; Drew, 1973). Surprisingly, even concentrations of as low as 50 µM in the -enriched zone (just 40 µM higher than in the -deprived zones) were able to stimulate LR elongation by about 50%, while 100 µM KNO3 was sufficient to elicit almost the maximal response (Zhang et al., 1999).
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) or 1 mM KCl (control, 
) was applied to the primary root of seedlings of the GUS marker line, END199 (Malamy and Benfey, 1997b
). Laterals that already existed at the time of transfer were measured at 24 h intervals to determine their elongation rates. Bars indicate standard errors (n=16)It can be shown that a localized
treatment has no effect on the rate of progression through the early stages of LR development. This experiment was made possible by use of a ß-glucuronidase (GUS) marker line which allows the early stages of LR development to be visualized by histochemical staining. The marker line used was END199, an enhancer trap line which expresses GUS activity in developing LRs from a very early stage just after LR initiation (Malamy and Benfey, 1997b). For the purposes of the experiment, the developing LRs were classified as Stage A, up to 3–5 cell layers; Stage B, up to the point of emergence; Stage C, 0.5 mm in length; Stage D, >0.5 mm in length. The transition from Stage C to Stage D approximately corresponds to the final stage of LR development when the LR meristem becomes activated and elongation of the mature LR begins (Malamy and Benfey, 1997a). A 1.5 cm segment of the primary root of each seedling was exposed to a localized supply of 1 mM KNO3, or (as control) 1 mM KCl, and the number of LRs at each of these stages assessed at daily intervals after the start of the experiment. As shown in Fig. 1B, there were no significant differences between the two treatments in the numbers of LRs at each stage. It is concluded that the stimulatory effect of a localized treatment comes into effect only after elongation of the mature LR begins.
It has been demonstrated that the increased rate of LR elongation associated with a localized treatment is not correlated with a significant increase in the size of the mature root cells (Zhang et al., 1999). The significance of this observation is that it shows that the higher rates of LR elongation must result from an increase in the rate of cell production within the LR meristem. A preliminary cytological analysis of -stimulated and control LRs indicates that this increased rate of cell production is at least partly due to an increase in the number of cells in the LR meristem, although the possibility that also accelerates progression of the meristematic cells through the cell cycle could not be eliminated (A Williams, PW Barlow and BGF, unpublished results).
The question has been asked whether a localized treatment can stimulate LR elongation if applied after the LR has already matured. Seedlings were grown for longer than usual on the basal level of (10 µM NH4NO3) and a localized supply of 1 mM KNO3 was then applied to a 1.5 cm zone of the root that had already developed LRs. The rate of elongation of the LRs in the -rich middle segment of the plate and in the top segment was monitored. The results (Fig. 1C) show that the delayed treatment was still capable of stimulating LR elongation compared to control roots treated with 1 mM KCl, and that this stimulation was specific to the LRs directly exposed to the . Similar results were obtained by Hackett (Hackett, 1972), who found that could only stimulate LR initiation in wheat if applied at or close behind the primary root tip, whereas LR elongation could be stimulated even if the treatment was delayed until after the LRs had appeared.
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The stimulation of LR elongation by : a nutritional or a signalling event?
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TopAbstractIntroductionA localized supply of...The stimulation of LR...Evidence for an overlap...[IMAGE] also has a...Summary--a ‘dual...References |
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Two lines of evidence suggest that the increased rate of LR elongation seen in
-enriched zones is a response to the ion itself and does not involve its role as a N source. Firstly, it was found that when localized supplies of other N sources (
and glutamine) were substituted for they failed to elicit the LR response (Zhang et al., 1999). This result differs from what has been reported in barley (Drew, 1975), where 
had a similar effect on LR proliferation as . However, as the barley experiments were not done under aseptic conditions there is the possibility that some nitrification of the occurred in this case.
The second line of evidence was obtained using an NR-deficient double mutant (nia1nia2), which has only 0.5% of wild-type NR activity (Wilkinson and Crawford, 1993). LR elongation rates in the NR mutant were found to respond to in a similar way as the wild type (Zhang and Forde, 1998), indicating that the response is not dependent on the plant's ability to assimilate the .
These observations do not support the hypothesis that the LRs directly exposed to a localized source of are stimulated because they benefit most from the increased N supply (Hackett, 1972). Nor do they support the suggestion that the elevated rates of assimilation within the -rich zone, and the resultant increase in metabolic activity in those roots, leads to a growth-stimulating influx of carbohydrates and auxin (Wiersum, 1958; Drew, 1973; Granato and Raper, 1989; Sattelmacher et al., 1993). It appears that the LRs are responding directly to a signal from the ion itself and that this signal is perceived only by the root tips that are directly exposed to the higher concentration (Zhang and Forde, 1998; Zhang et al., 1999).
There is good evidence from other studies that roots are able to sense the presence of in the environment and use it as a signal to modulate gene expression. NR genes in plants are -inducible and their induction is very rapid (within minutes) and is not dependent on the synthesis of new proteins (Gowri et al., 1992). Studies with N. plumbaginifolia have shown that, even in plants in which NR activity has been abolished by tungstate treatment (Deng et al., 1989) or by mutation (Pouteau et al., 1989), is still able to induce the accumulation of high levels of NR protein and mRNA. This indicates that the ion, and not one of the products of its assimilation, is the signal molecule that elicits the induction of the NR gene.
In Escherichia coli the signal is sensed and transduced by a ‘two component’ regulatory system, which consists of a transmembrane ‘sensor kinase’ and a ‘response regulator’ (Merrick and Edwards, 1995). Members of the same ‘two component’ regulator family are found in higher plants and are known to be involved in sensing ethylene and cytokinin (Chang et al., 1993; Kakimoto, 1996). Recently evidence has been obtained which suggests that a response regulator homologue in maize (Zea mays) leaves (ZmCip1) (Sakakibara et al., 1998) and related genes in Arabidopsis (Taniguchi et al., 1998), may have a role in N signalling. However, the signalling pathway in this instance appears to involve a long-distance cytokinin-mediated signal which stimulates expression of ZmCip1 in the shoot in response to the supply of either or ammonium to the roots. Whether another member of the ‘two component’ regulator family plays a part in the sensing of in the root is still unknown. Evidence for the existence of an external receptor in plant roots has been discussed elsewhere (Forde and Clarkson, 1999).
Identification of a MADS-box gene specifying a component of the response pathway
As one approach to finding genes involved in signalling in Arabidopsis roots, a screen for mRNAs that are rapidly induced by was initiated (H Zhang and BG Forde, unpublished results). RNA was extracted from roots that had been starved of N and then treated for 60 min with either KNO3 or KCl, and a subtractive hybridization procedure (Sharma et al., 1993) was used to generate a cDNA probe specifically enriched in -induced sequences. A number of cDNA clones representing novel -inducible genes were identified in this way, and one of these (pANR1) was found to encode a member of the MADS-box family of transcription factors (Zhang and Forde, 1998). In higher plants, most MADS-box genes identified to date are expressed in flowers and play a key role in controlling floral organ identity (Riechmann and Meyerowitz, 1997). However, members of the same family of transcription factors also occur in yeast and in mammalian cells where they are involved in converting external signals into developmental or metabolic responses (Shore and Sharrocks, 1995), indicating ancient regulatory functions unrelated to floral organogenesis.
ANR1 was shown to be expressed mainly or exclusively in roots and to be rapidly induced (<30 min) when N-starved roots are treated with (Zhang and Forde, 1998). It was also established that phosphate or K+ starvation followed by re-addition of the appropriate nutrient had no effect on ANR1 expression, indicating that the gene is not under some kind of general nutritional control. Using an ordered array of YAC clones (Zachgo et al., 1996) the ANR1 gene has been mapped to a locus adjacent to the centromere of chromosome 2 (H Zhang and BG Forde, unpublished results).
ANR1 belongs to a MADS-box subfamily that currently has three other members (Fig. 2). The founding member of this subfamily is AGL17, another root-specific MADS-box gene from Arabidopsis (Rounsley et al., 1995). Also in this group is nmhC5, an alfalfa (Medicago sativa) gene which is specifically expressed in root nodules (Heard et al., 1997). The fourth member, the pollen-specific DEFH125 gene from Antirrhinum majus (Zachgo et al., 1997), is the only current member of the subfamily that is expressed in aerial tissues. The functions of AGL17, nmhC5 and DEFH125 have not been established.
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The role of the ANR1 gene product was investigated by generating a set of antisense and co-suppressed Arabidopsis lines in which the gene was down-regulated to varying degrees (Zhang and Forde, 1998
). LR growth in the most strongly down-regulated lines was found no longer to respond to the stimulatory effect of a localized supply of , i.e. these lines lacked the ability to forage for . It was concluded that ANR1 is a component of the signal transduction pathway by which modulates the activity of the LR meristem (Zhang and Forde, 1998; Zhang et al., 1999). A number of other MADS-box genes of unknown function are expressed in vegetative tissues (Riechmann and Meyerowitz, 1997), with many more likely to be awaiting discovery, and it may be that some or all of these have a similar role to ANR1 in regulating plant development in response to environmental cues.
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Evidence for an overlap between the response pathways for auxin and
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TopAbstractIntroductionA localized supply of...The stimulation of LR...Evidence for an overlap...[IMAGE] also has a...Summary--a ‘dual...References |
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It is well established that exogenous auxin treatments can either stimulate or inhibit the initiation and elongation of LRs, depending on the concentration supplied (Evans et al., 1994
). Mutants which overproduce auxin or which are auxin-resistant also show altered LR phenotypes (Hobbie, 1998). In maize, the increase in LR elongation rates and in the frequency of LR initiation associated with a localized supply of was correlated with an increase in the endogenous IAA content in the roots in the zone of supply (Sattelmacher et al., 1993), but this leaves open the question of whether the IAA is responsible for stimulating LR proliferation or is a consequence of the increased growth.
Evidence for an overlap between the signal transduction pathways for auxin and in Arabidopsis has been obtained using a number of auxin-resistant mutants (Zhang et al., 1999): one of three mutants tested (axr4) showed no increase in LR elongation rates on exposure to a localized supply of . Two other auxin-resistant mutants (aux1 and axr2) showed wild-type responses to the treatment, indicating that their gene products are not involved in the response. The interpretation of these results is made easier by the fact that axr4, unlike other auxin mutants, is not cross-resistant to other plant hormones such as cytokinin or ethylene (Hobbie and Estelle, 1995). However, because the exact role of the AXR4 gene product is unknown it is unclear in what way the and auxin response pathways might interact.
It has been tentatively suggested that AUX1 and AXR4 may be part of the same auxin response pathway, at least with respect to the effect of auxin on root elongation (Hobbie and Estelle, 1995; Leyser, 1997). On this assumption, and taking into account the differing sensitivities of the aux1 and axr4 mutants to , it has been suggested that the overlap with the response pathway may occur downstream of AUX1 and upstream of AXR4 (Zhang et al., 1999).
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also has a systemic inhibitory effect on LR development
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TopAbstractIntroductionA localized supply of...The stimulation of LR...Evidence for an overlap...[IMAGE] also has a...Summary--a ‘dual...References |
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In addition to its ability to stimulate LR elongation when supplied locally,
has been shown to exert a separate inhibitory effect on LR development (Zhang et al., 1999). This inhibition, which does not affect the primary root, was first noted when high concentrations (>10 mM) were applied to the whole Arabidopsis root system (Zhang and Forde, 1998). It was subsequently established that the inhibitory effect of is distinct in a number of key ways from its stimulatory effect: (1) it is systemic rather than localized to the zone exposed to the treatment; (2) the extent of the inhibitory effect is related not only to the external supply of , but also to how much of the root system is exposed to the supply, indicating that it depends on the total amount of absorbed by the root system rather than the external concentration per se; (3) while the stimulatory effect acts specifically on elongation of mature LRs, the inhibitory effect acts only on immature LRs during a discrete phase just after their emergence from the primary root.
Nitrate's inhibitory effect is seen most clearly when seedlings are grown on media containing a low sucrose concentration (0.5%) and 50 mM KNO3 (Fig. 3A). Under these conditions the primary root grows normally but LR development is strongly suppressed, to the extent that even up to 14 d after germination no LRs are visible (Zhang et al., 1999; Fig. 3A). Closer inspection, however, reveals that the numbers of LRs initiated do not differ from those on roots cultured on 1 mM KNO3, but they only develop to a stage where they are c. 0.2–0.5 mm in length. Detailed analysis of the initiation and early progression of the LRs on 1 mM and 50 mM KNO3 established that the earlier stages up to the point of emergence are unaffected by the concentration (Zhang et al., 1999). Furthermore, shift experiments in which LRs were allowed to develop normally on 1 mM KNO3 before the seedlings were transferred to 50 mM KNO3, show that LRs that had progressed beyond the 0.5 mm stage grew at the same rate at 50 mM as they did at 1 mM (Fig. 3B). Similarly, many of the stunted LRs that develop on 50 mM will begin growth almost immediately if transferred to 1 mM or, if left for several weeks at 50 mM , will eventually grow out and elongate at normal rates (Fig. 3B). Thus they differ from the stunted LRs that develop on roots of the alf3 (‘aberrant lateral root formation’) mutant which are essentially dead (Celenza et al., 1995).
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These results suggest that the stage of LR development just after emergence has a special significance in the interaction between N availability and root branching. LR development in Arabidopsis has been studied in detail and shown to be a multistage process (Celenza et al., 1995
; Laskowski et al., 1995; Malamy and Benfey, 1997a, b). The process begins when a small group of founder cells in the pericycle initiate a programme of periclinal and anticlinal cell divisions to produce a LR primordium which eventually takes on the organized structure characteristic of a LR meristem. However, emergence of this primordium from the primary root occurs principally through cell expansion and it is not until after emergence that cell numbers near the tip of the LR primordia begin to increase, an indication that the LR meristem has become functional (Malamy and Benfey, 1997a). The phenotype of the rml (‘root meristemless’) mutants provides additional evidence that activation of the LR meristem only occurs after emergence (Cheng et al., 1995). In the rml1 mutant, the primary root stops growing soon after germination and LRs are arrested soon after emergence. 3H-thymidine labelling revealed that this blockage is caused by failure of the meristem to begin dividing. Thus the period when LRs become sensitive to the inhibitory effect of appears to coincide with a critical phase in LR development, just before or during the process of activation of the LR meristem.
How is the inhibitory signal generated? There is some evidence to suggest that the accumulation of itself within the plant plays an important role in inhibiting LR development. An increase in external concentration from 1 mM to 50 mM leads to a 3-fold increase in the content of both roots and shoots (H Zhang, A Jennings, BG Forde, unpublished results). Furthermore, it was found that LR development in the nia1nia2 mutant is more sensitive to inhibition by external than the wild type, indicating that it is the internal concentration rather than the products of N assimilation which is critical (Zhang et al., 1999). However, the same study found that high concentrations of glutamine in the medium also inhibited LR development preferentially, suggesting that N compounds other than itself can also contribute to generating the inhibitory signal.
It has similarly been reported that the accumulation of high concentrations of which occurs in shoots of tobacco plants with low NR activity is correlated with a marked inhibition of root growth and an increase in the shoot : root ratio (Scheible et al., 1997a, b). Detailed biochemical analysis of these plants revealed a strong inhibition of starch synthesis and turnover in the leaves and decreased levels of sugars in the root, and led to the conclusion that these changes of carbon allocation could be at least partly responsible for the effects on root growth (Scheible et al., 1997b). Since the pattern of LR development was not analysed in the low NR tobacco plants, it is not clear whether the phenomenon is identical to the one described in Arabidopsis.
The observation that it is possible partially to alleviate the inhibitory effect of 50 mM KNO3 by increasing the sucrose concentration in the medium from 0.5% to 2% (Zhang et al., 1999) would seem to be consistent with the conclusions of Scheible et al. (Scheible et al., 1997a, b). However, it has been argued that the remarkably specific effect that can exert on LR development in Arabidopsis, together with the absence of any effect on primary root growth, is difficult to reconcile with the kind of general inhibitory effect on root growth that would be expected if the supply of sucrose to the roots was limiting (Zhang et al., 1999). It seems more likely that either the increased sucrose supply leads to a reduction in tissue levels (by stimulating assimilation), or that the C/N ratio is a critical factor in generating the inhibitory signal.
There is good evidence that plants have mechanisms for monitoring N status and/or the C/N ratio. For example, studies on the regulation of expression of genes for NR and nitrite reductase have shown that they are repressed by glutamine and that their induction by is enhanced by sucrose (Vincentz et al., 1993; Sivasankar et al., 1997), while asparagine synthetase is regulated in the opposite way by the relative availability of N and C (Chevalier et al., 1996). In bacteria, the balance between C and N metabolism, as reflected by the glutamine : 2-oxoglutarate ratio, is monitored by the two-component ntr system (Merrick and Edwards, 1995; Böhme, 1998). An Arabidopsis gene for a homologue of the PII protein, which is a key component of the N regulatory system in enterobacteria and cyanobacteria, has recently been cloned (Hsieh et al., 1998). This gene (GLB1) encodes a chloroplast-targeted protein and the abundance of its mRNA in leaves was increased by light and sucrose and decreased by amino acids such as asparagine, glutamine and glutamate. Transgenic Arabidopsis plants in which the GLB1 gene was constitutively expressed under the control of the CaMV 35S promoter were less responsive to N availability in the regulation of anthocyanin accumulation (Hsieh et al., 1998). Whether the GLB1 gene product has any role in the regulatory pathway leading to inhibition of LR development remains to be established.
The concept that physiological processes in roots are regulated by the N status of the shoot is well established for both uptake (Imsande and Touraine, 1994; Lainé et al., 1995) and symbiotic N2 fixation (Parsons et al., 1993), but the exact nature of the signal that passes from shoot to root is completely unknown (Stitt and Scheible, 1998). If, as seems likely, the inhibitory signal that affects LR development is carried in the phloem, then it may be significant that the earliest symplastic connections between the phloem and the LR primordium are established at around the time of LR emergence (Oparka et al., 1995).
A morphological screen has been used to identify Arabidopsis mutants that are altered in their ability to regulate LR development in response to the N status (H Zhamg, A Jennings, BG Forde, unpublished results). Over 5000 EMS-mutagenized M2 seedlings were screened by growing them on vertical nutrient agar plates containing 50 mM KNO3 and 0.5% sucrose. Seventeen lines were identified in which LR development showed reduced sensitivity to the inhibitory effect of the high concentration and in which the mutant phenotype was heritable. Further analysis of these mutants should help to elucidate the mechanisms that plants use to monitor their N status, and the signalling mechanism that allows the shoot to direct physiological and developmental processes in the root.
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Summary—a ‘dual pathway’ model for the regulation of LR development by
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TopAbstractIntroductionA localized supply of...The stimulation of LR...Evidence for an overlap...[IMAGE] also has a...Summary--a ‘dual...References |
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Based on the studies described above a model has been put forward to explain how root branching in Arabidopsis is modulated according to antagonistic signals from the external
supply and the internal N status (Zhang et al., 1999>). This ‘dual pathway’ model, illustrated in Fig. 4, consists of a localized stimulatory effect that depends on the external concentration and acts on the mature LR tip to increase meristematic activity, and a systemic inhibitory effect that depends on the internal N status of the plant and acts on a critical stage of LR development prior to activation of the LR meristem. Remarkably, both effects are specific to the LRs, growth of the primary root being largely insensitive to the supply of (Zhang and Forde, 1998).
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The localized stimulatory effect is thought to begin with perception of the
signal by a sensor (possibly on the plasma membrane), with the signal being transduced through a pathway that involves the products of the ANR1 and AXR4 genes. Because the ANR1 gene is induced by in a similar time-scale to the genes for NR and the transporters it seems plausible that a common regulatory mechanism is responsible for the induction of each of these -inducible genes. The homology of the ANR1 gene to the MADS-box family of transcription factors suggests that its role is to activate the transcription of a set of genes that are somehow involved in modulating meristematic activity in the LR tip. A possible analogy is with the serum response factor (SRF), a human MADS-box transcription factor that is involved in the control of cell proliferation in response to extracellular signals from growth factors (Shore and Sharrocks, 1995). The role of the auxin-sensitivity gene AXR4 and whether it lies upstream or downstream of ANR1 in the signal transduction pathway are under investigation.
The systemic inhibitory effect requires the uptake of by the plant and the strength of the inhibitory signal seems to be related to the amount of absorbed, not to the external concentration per se. Although organic N compounds may play a role in generating the inhibitory signal, evidence from experiments with an NR-deficient Arabidopsis mutant suggests that the plant has a mechanism for monitoring the internal pool. The nature of the inhibitory signal is unknown, but is thought likely to originate in the shoot: preliminary experiments have shown that applying 50 mM KNO3 to one half of a split root system leads to the suppression of LR development in both halves (H Zhang, BG Forde, unpublished results). The inhibitory signal appears to be sensed specifically during a critical phase of LR development after emergence from the parent root and just prior to the point at which the cells of the newly differentiated LR meristem become activated and elongation of the mature LR begins.
These two opposing effects of provide an integrated regulatory system that enables root branching to be modulated to take into account both the plant's N status and the external availability and distribution of . In this way the intensity of the response to a localized source (i.e. the foraging response) can be adjusted according to the plant's demand for N, so that resource allocation within the plant as a whole can be optimized.
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Acknowledgments |
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We thank P Benfey for providing seed of the END199 line. This work was supported in part by a grant from the European Union (contract no. BIO4-CT97-2231) in the Biotech programme of Framework IV. IACR receives grant-aided support from the Biotechnology and Biological Sciences Research Council.
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Notes |
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1 Present address and to whom correspondence should be sent: Department of Biological Sciences, University of Lancaster, Lancaster LA1 4YQ, UK. Fax: +44 1524 843854. E-mail b.g.forde@lancaster.ac.uk
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