JXB Advance Access originally published online on November 17, 2003
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Journal of Experimental Botany, Vol. 55, No. 394, pp. 27-34, January 1, 2004
© 2004 Oxford University Press
Plant Carbon-Nitrogen Interactions from Rhizospheres to Planet |
Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake
Received 19 May 2003; Accepted 11 August 2003
1Université Montpellier II, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR 113 UM2/IRD/CIRAD/INRA/ENSAM, CC 02, Place E Bataillon, 34095 Montpellier cedex 05, France
* To whom correspondence should be addressed. Fax: +33 4 6714 3637. E-mail: touraine{at}univ-montp2.fr
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Abstract |
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 Top Abstract IntroductionIs the primary effect...Root morphogenesis as affected...Do PGPB affect the...ConclusionReferences |
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Plant growth-promoting bacteria (PGPB) and NO–3 availability both affect NO–3 uptake and root architecture. The presence of external NO–3 induces the expression of NO–3 transporter genes and elicits lateral root elongation in the part of the root system exposed to the NO–3 supply. By contrast, an increase in NO–3 supply leads to a higher plant N status (low N demand), which represses both the NO–3 transporters and lateral root development. The effects of PGPB on NO–3 uptake and root development are similar to those of low NO–3 availability (concomitant stimulation of NO–3 uptake rate and lateral root development). The mechanisms responsible for the localized and long-distance regulation of NO–3 uptake and root development by NO–3 availability are beginning to be elucidated. By contrast, the signalling and transduction pathways elicited by the rhizobacteria remain totally unknown. This review will compare the effects of NO–3 availability and PGPB on root morphogenesis and NO–3 uptake, in order to determine whether interactions exist between the NO–3-dependent and the PGPB-dependent regulatory pathways.
Key words: N demand, nitrate uptake, plant growth-promoting bacteria, plasticity, rhizosphere, root development.
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Introduction |
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TopAbstractIntroductionIs the primary effect...Root morphogenesis as affected...Do PGPB affect the...ConclusionReferences |
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The rhizosphere is the portion of the soil that forms the complex habitat of plant roots, and the composition of which is altered by root activity (Hiltner, 1904). An important component of the rhizosphere is the actively growing microbial population which thrives due to the provision of organic nutrients in root exudates. In turn, the microorganisms that colonize the rhizosphere profoundly affect root and plant biology in relation to nutrition, development and health. Current knowledge of root development and physiology, however, essentially comes from studies that did not take into account the effects of the rhizosphere. On the one hand, the wealth of literature and an understanding of root biology has demonstrated the strength of investigations that avoid microbial interactions in order to decipher the underlying mechanisms involved in nutrient uptake and root development. On the other hand, the influence of the rhizosphere microflora on root biology is so important that it is crucial to evaluate how the basic nutritional and developmental processes of the plant are affected.
Micro-organisms that colonize the rhizosphere can be classified according to their effects on plants and the way they interact with roots. Some of these micro-organisms are plant pathogens whereas others trigger beneficial effects. Among the latter, one can distinguish two large categories. First, mycorrhizal fungi and bacteria belonging to the genera Rhizobium and Frankia are able to establish a symbiotic relationship with the roots of host plants (Harley and Smith, 1983; Broughton and Perret, 1999). Such interactions lead to morphologically distinct structures, namely mycorrhizes and nodules, that are sites with enhanced nutritional functions that neither partner would carry out alone (Hadri et al., 1998; Albrecht et al., 1999; Martin and Plassard, 2001; Trinchant et al., 2001). Second, a subset of bacteria, referred to as plant growth-promoting bacteria (PGPB; Bashan and Holguin, 1998), have beneficial effects on plants without developing such symbiotic associations. While the mechanisms involved in pathogenicity and symbiosis have been extensively studied, the interactions between PGPB and plant roots are not clearly defined (Glick, 1995).
PGPB are usually classified into two groups according to whether they affect plant growth indirectly or directly, referred to as biocontrol PGPB and PGPB, respectively (Bashan and Holguin, 1998). It is worthwhile to mention that most PGPB are likely to elicit both biocontrol, that prevents deleterious effects of phytopathogenic microorganisms, and plant growth promotion. The mechanisms involved in biocontrol by rhizosphere bacteria have been reviewed elsewhere (Whipps, 2001; Persello-Cartieaux et al., 2003) and will not be discussed here. The occurrence of direct effects on plant growth has been demonstrated using gnotobiotic culture systems where a single bacteria strain interacts with the host plant (Lifshitz et al., 1987; Bertrand et al., 2001). The plant response to PGPB is obviously a very complex phenomenon resulting from the combination of mechanisms which affect several aspects of mineral nutrition and root development (Cleyet-Marel et al., 2001). Considering the quantitative importance of nitrogen in plant mineral nutrition and given that nitrogen availability and PGPB are known to trigger changes in both plant nutrition and root development, this review focuses on the possible interactions between the plant responses to these abiotic and biotic factors.
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Is the primary effect of PGPB on plants a nutritional or a developmental effect? |
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TopAbstractIntroductionIs the primary effect...Root morphogenesis as affected...Do PGPB affect the...ConclusionReferences |
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Many of the PGPB described to date are free-living diazotrophs that can convert molecular nitrogen into ammonia in a free state by virtue of the nitrogenase enzyme complex (Postgate, 1982). Another feature that has been reported for PGPB is the production of phytohormones, which could affect root development directly. Since nutritional capacity and developmental control are very much dependent on each other and because they both affect the growth rate of the plant, one can ask whether the PGPB primarily act on one or the other.
It was attractive to explain the positive effect of PGPB on plant growth by the provision of nitrogen fixed by the bacteria to the host plant. This ‘biofertilization’ hypothesis was all the more attractive since N availability is the main yield-limiting factor in many agricultural situations and the leaching of N fertilizers into groundwater causes environmental problems. Experiments using acetylene reduction measurements and the 15N isotope dilution technique provided conflicting results. For instance, large contributions to the plant N budget from plant-associated bacterial N2-fixation have been reported with sugar cane (Urquiaga et al., 1992; Mirza et al., 2001) and mangrove (Bashan et al., 1998). Furthermore, gene reporter fusions demonstrated that the Nif genes of Azospirillum and Azoarcus rhizobacteria strains are expressed (enhanced?) when associated with the roots of wheat and rice, respectively (Vande Broek et al., 1993; Egener et al., 1998, 1999). However the expression of Nif genes or active N2 fixation by the rhizobacteria do not imply that there is a large transfer of newly fixed nitrogen to the plant. On the contrary, evidence that growth promotion by PGPB does not rely on the N2-fixation process have been obtained for tomato seedlings associated with an Azospirillum brasilense mutant strain totally deficient in N2-fixation capacity (Bashan et al., 1989b). Overall, most of the inoculation experiments reported in the literature failed to show a significant contribution of N2 fixation by PGPB to the plant N status (Lethbridge et al., 1982; Boddey et al., 1986; Okon and Kapulnik, 1986; Bremner et al., 1995). This is in complete contrast to symbiotic associations where relatively large amounts of atmospheric N reach the plant as ammonia released by the bacteroids. By contrast, most of the ammonia produced in PGPB by the nitrogenase-catalysed N2 fixation would be assimilated by the rhizobacteria through the glutamine synthetase/glutamate synthase (GS/GOGAT) pathway. Considering the high cost of the N2-fixation reaction (Phillips, 1980), the bacteria tend to limit the loss of fixed N. The leak of ammonia out of the bacteria cells may be minimized by virtue of the GS/GOGAT pathway operating at a high rate (Steenhoudt and Vanderleyden, 2000). In addition, ammonium transporters found in several PGPB strains are thought to be involved in the reabsorption of NH+4 released as a consequence of NH3 diffusion through the bacterial membrane (Van Dommelen et al., 1997). The inoculation of tomato roots with a wild-type strain, but not with nif mutant strains, of Azospirillum brasilense induced the tomato LeAmt1.2 gene coding for an ammonium transporter (Becker et al., 2002). This suggests that due to its N2-fixation activity the bacteria excrete NH+4 in quantities consistent with the induction of the LeAmt1.2 gene, i.e. in the micromolar range (higher concentrations reduces LeAmt1.2 mRNA levels). Quantification of N transfer would be necessary to assess whether the ammonium released by the bacteria is used as an N source by the plant. Alternatively, the authors proposed that NH+4 ions play a signalling role in the interactions between PGPB and plants (Becker et al., 2002).
The positive effects of PGPB on plant growth are always correlated with remarkable changes in root morphology, namely increased lateral root length and root hair number and length (Tien et al., 1979; de Freitas and Germida, 1989; Pacovsky, 1990; Okon and Vanderleyden, 1997; Bertrand et al., 2000). It is generally assumed that these developmental responses are triggered by phytohormones produced by the bacteria (Bloemberg and Lugtenberg, 2001; Persello-Cartieaux et al., 2003). Among the plant growth regulators, auxin may play a major role supported by the fact that a screen for Arabidopsis thaliana mutants insensitive to Pseudomonas rhizobacteria resulted in the isolation of two mutants altered in the Aux1 auxin influx transporter (Persello-Cartieaux et al., 2001). One must keep in mind that the effect of auxin largely depends upon its concentration. Consistent with the hypothesis of an auxin-mediated effect of the Pseudomonas strains, inoculation with increasing doses of these rhizobacteria had a positive impact on rooting up to a certain concentration of bacteria above which deleterious effects were observed (Persello-Cartieaux et al., 2003). Other phytohormones including cytokinins and gibberellins may be involved in the effect of PGPB on root morphogenesis (Steenhoudt and Vanderleyden, 2000). Furthermore, some PGPB strains have been shown to have an aminocyclopropane carboxylate deaminase (Shah et al., 1998), an enzyme that hydrolyses ACC. Such bacteria are likely to divert ACC, the precursor of ethylene, from the plant root, which has the effect of reducing the inhibition of root growth by ethylene (Glick et al., 1998). Considering the numerous interactions that exist between the different hormone signalling pathways in plants, it is difficult to assess which of these pathways is the primary target of PGPB. More likely, the rhizobacteria alters not just a single, but several, hormonal pathways, which could account for the different morphological changes observed, for example, lateral root elongation and root hair development.
An increase in the root surface area and the volume of soil foraged by the root, which leads to an enhanced nutrient uptake, is the most commonly proposed explanation for the beneficial effects of PGPB on plant growth. The improvement in mineral nutrition would explain the promotion of shoot growth. This rationale is consistent with the observation that plants inoculated with Azopsirillum take up N, P, K, and microelements more efficiently from the soil (Okon and Vanderleyden, 1997). However, PGPB may enhance mineral uptake, not only as a consequence of the increase in root surface area but also by stimulating the ion uptake systems. Considering the relationship between the effects of PGPB on root morphology and nutrient uptake, the experimental data published is mainly correlative. The different responses of plants to PGPB include stimulation of root branching and root hair development, stimulation of total nutrient uptake (especially that of nitrogen), and an increase in biomass accumulation. How these different responses are related mechanistically is not known. Considering nitrogen nutrition, a priori plants can acquire N under two mineral forms, namely nitrate (NO–3) and ammonium (NH+4). However, because the concentration of NH+4 in the soil is generally much lower than that of NO–3 (Marschner, 1995) and because the development of most plants is optimal on NO–3 rather than on NH+4 (cf. the ammonium syndrome, Mehrer and Mohr, 1989), the favoured source for N uptake is NO–3. On the other hand, NO–3 availability is known to affect both root branching and NO–3 uptake itself (Forde, 2002). Because NO–3 availability and PGPB affect the same developmental and physiological processes in plant roots, the question is whether the responses share a mechanistic basis. Two points will be addressed in this review: (1) Are the responses of root morphogenesis to NO–3 and to PGPB independent of each other? (2) Do PGPB affect NO–3 uptake directly or is the gain in plant N only a consequence of the increase in root surface area?
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Root morphogenesis as affected by both nitrate availability or PGPB inoculation |
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TopAbstractIntroductionIs the primary effect...Root morphogenesis as affected...Do PGPB affect the...ConclusionReferences |
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As mentioned above, one of the more characteristic effects of PGPB is an increased elongation rate, and perhaps initiation rate, of lateral roots resulting in a more branched root system architecture (Kapulnik et al., 1985a; Lifshitz et al., 1987).
Modifications of root architecture similar to those elicited by PGPB are triggered by the changes in NO–3 available in the medium (Wiersum, 1958). These plastic responses have been characterized in detail using culture devices with uneven distribution of NO–3 (vertical layers, split root systems) (Drew et al., 1973; Drew, 1975; Friend et al., 1990; Burns, 1991). Molecular studies performed in Arabidopsis thaliana (Zhang and Forde, 1998; Zhang et al., 1999) showed that a dual pathway process operates in plants: a localized control, that senses the presence of exogenous NO–3, induces lateral root elongation; a systemic control inhibits root growth in plants with a high N status. The model proposes that with uneven NO–3 supplies (e.g. a plant which only has a portion of the root system in the presence of NO–3), the systemic inhibition of lateral root growth would be released, and lateral root growth enhanced, but only for those roots that develop in the NO–3-containing zones.
Two genes of the signalling pathway that links external NO–3 to increased rates of lateral root elongation have been identified, namely the MADS-box transcription factor ANR1 and the AXR4 gene involved in the auxin transduction pathway (Zhang et al., 1999). By contrast, the systemic pathway remains far more obscure. Neither the sensors of N status in the shoot, nor the signal translocated in the phloem, nor the transduction pathway responding to this signal in the roots have been identified. At the morphological level, high NO–3 concentrations lead to a less branched root system, corresponding to fewer visible lateral roots (Zhang and Forde, 1998; Zhang et al., 1999; Tranbarger et al., 2003a). Studies performed with nitrate reductase-deficient Arabidopsis and tobacco mutants revealed that this response is related to a nitrate pool in the leaf (Scheible et al., 1997; Stitt and Feil, 1999; Zhang et al., 1999). However, since NO–3 is not translocated in the phloem, another signal must serve to pass the information about the shoot’s N status to the roots. In the case of the systemic control of NO–3 uptake by the plant’s N demand, the phloem-translocated signals are thought to be glutamine or other amino acids (Imsande and Touraine, 1994; Vidmar et al., 2000; Nazoa et al., 2003). However, the amino acid pools are unlikely to be involved in the control of root development. This is indicated by the observation that the addition of glutamine or asparagine to the nutrient medium did not reduce the number and length of Arabidopsis lateral roots as high NO–3 concentrations did (Tranbarger et al., 2003a, b). Recently, it has been proposed that hormones like auxin and ABA would act as the long-distance signals responsible for the systemic control of lateral root development (Forde, 2002; Casimiro et al., 2003). Also two transcription factor genes, the expression of which, in roots, correlated with the systemic plasticity response of the roots of Arabidopsis thaliana, have been identified (Tranbarger et al., 2003a). These genes are putative candidate targets of the long-distance N status signals arising in the shoot that regulate lateral root development.
The localized and systemic responses of root branching to NO–3 appear to be exerted at different steps of lateral root development. The external presence of NO–3 stimulates lateral root elongation by increasing the meristematic activity in lateral root tips (Zhang et al., 1999), while the accumulation of NO–3 in shoot leads to a reduction in the number of lateral roots by stunting their development at some stage just before or after emergence (Zhang et al., 1999; Tranbarger et al., 2003a). Compared with what is known for NO–3, the manner in which lateral root development is affected by PGPB is much less characterized. In the literature, positive effects of PGPB have been mentioned for both the length or elongation rate and the number of lateral roots (Kapulnik et al., 1985b; Frommel et al., 1991; Sarig et al., 1992). Preliminary studies performed with a new strain of Phyllobacterium isolated from the rhizosphere of oilseed rape (Bertrand et al., 2001) indicated that these rhizobacteria have a marked effect on the length rather than the number of lateral roots (Larcher, et al., 2003). With the present state of knowledge, the possibility that the different PGPB strains may affect lateral root development at different stages cannot be ruled out. In addition, the morphological descriptions currently available are not detailed enough to determine whether NO–3 and PGPB can affect the same step of lateral root development or not.
As mentioned above, the effect of PGPB on root morphogenesis is usually attributed to the release of phytohormones by the rhizobacteria, auxin being the most cited of these plant growth factors. Since a link between the signalling pathway involved in the localized response to NO–3 and the auxin pathway has been reported (Zhang et al., 1999), there is speculation whether NO–3 and PGPB effects on root morphogenesis share common steps or not. As far as is known, no experimental data are available to date to address this question. Nevertheless, because NO–3 is often present in the soil, especially in agricultural conditions, but at varying concentrations, a more interesting consideration than the possible interactions between PGPB and the localized NO–3 response pathway are the interactions between PGPB and the systemic NO–3 response pathway. Again, no physiological, cellular or molecular data are available to respond unambiguously. However, a recent study performed with Arabidopsis with the Phyllobacterium strain isolated by Bertrand et al. (2001) suggests that high N status and PGPB affect lateral root development independently from each other: the rhizobacteria promoted lateral root growth whatever the NO–3 concentration in the nutrient medium; conversely, increasing the NO–3 concentration repressed lateral root growth whether the plants were inoculated or not (unpublished results).
A priori, one could envisage that PGPB could interfere with the NO–3 effect on lateral root development via changes either in the rhizosphere NO–3 concentration or the plant’s N status. Some PGPB have been shown to have a nitrate reductase activity (Bothe et al., 1992; Larcher et al., 2003) suggesting that they can use NO–3 as an N source. No evidence exists, but it is possible that NO–3 used by the PGPB decreases the NO–3 concentration at the root cell surface. By contrast, plants inoculated with PGPB generally have a higher N content than the uninoculated plants (Saudibet et al., 2002; authors’ unpublished results), although this is not always observed (Dobbelaere et al., 2002). Decreasing NO–3 concentration at the root surface per se is expected to have no effect on lateral root growth as long as NO–3 concentration remains sufficient for ANR1 induction. An increase in N status inhibits, not stimulates, lateral root development. Therefore, if changes in the NO–3 rhizosphere concentration or the plant’s N status due to PGPB are ever high enough to trigger significant effects on lateral root development, these effects would be negative, not positive as regularly observed.
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Do PGPB affect the NO–3 uptake systems? |
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TopAbstractIntroductionIs the primary effect...Root morphogenesis as affected...Do PGPB affect the...ConclusionReferences |
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It is generally assumed that PGPB trigger an increase in root surface area which results in an increased mineral uptake and, in turn, enhances shoot biomass accumulation. An enhanced plant ‘nutrient uptake’ by PGPB is widely described (Okon, 1985; Okon and Kapulnik, 1986; Bertrand et al., 2000), however, what uptake means must be clarified. Uptake refers to a function, namely the transport of a nutrient through the plasma membrane of root cells, i.e. the net flux from the growth medium to the plant that should theoretically be expressed per unit absorbing surface. Because of the difficulty in measuring this surface, it is usually expressed per unit of root weight. Therefore, if the increase in the amount of nutrient taken up from the medium in PGPB-inoculated plants were simply due to an increase in root surface, the effect of PGPB would be entirely dependent on root development, and not on the uptake function. NO–3 uptake is known to be tightly regulated by the plant’s N demand (Imsande and Touraine, 1994; Touraine et al., 1994), changes in which normally result in opposite variations of the rates of root growth and NO–3 uptake. This has been shown with lettuce plants grown in a split root device (Burns, 1991). The supply of an N-free nutrient solution to 90% of the root system first led to an increase of NO–3 uptake by the 10% of the roots that remained supplied with NO–3. However, subsequently the NO–3 uptake rate decreased while the proportion of root biomass in the NO–3-containing part increased. It would thus be expected that the increase of root surface area in PGPB-inoculated plants be accompanied by a decrease of NO–3 uptake rate, in order to maintain the total amount of NO–3 taken up by the plant at the same level as in non-inoculated plants. Conversely, for the NO–3 uptake rate to remain constant while the root surface increases, it would be required that the N demand regulation does not operate. This would imply that either the regulation of NO–3 uptake in PGPB-inoculated plants differs from that in non-inoculated plants, or that N nutrition limits plant growth so that NO–3 uptake is not down-regulated by the plant’s N status. Considering the variety of culture conditions used in the different studies published, plant N nutrition is unlikely to be limited when plant growth promotion by rhizobacteria is observed. Furthermore, it was observed that Arabidopsis thaliana grown on non-limiting mineral nutrient medium inoculated with a Phyllobacterium strain had a positive effect on plant growth, while increasing the concentration of NO–3 in the medium resulted in either no effects or even negative effects on plant growth (unpublished data).
If the increase in root surface alone cannot explain the gain in the plant’s N status, then the possible effects of PGPB on NO–3 uptake has to be considered. The data published on this question are very scarce. Azospirillum brasilense and A. irakense strains stimulated overall plant growth, including root development and grain yield of spring wheat and maize (Dobbelaere et al., 2002), but neither of the rhizobacteria changed the N concentration in plants or grains. The authors concluded that the inoculation did not enhance the uptake of minerals into the plant. By contrast, another study (Saudibet et al., 2002) led to the conclusion that NO–3 uptake by the roots of spring wheat is stimulated by another A. brasilense strain. This conclusion was based on the observations that both the shoot:root ratio and the plant NO–3 and N contents were higher in the inoculated plants so that the N accumulated:root biomass ratio was higher in inoculated plants. The effect of PGPB on NO–3 uptake was investigated in oilseed rape inoculated with an Achromobacter strain using an electrophysiological approach (Bertrand et al., 2000). As frequently observed with PGPB, this strain led to a higher increase of shoot biomass than root biomass, resulting in a higher shoot:root ratio. This implies that the effect of PGPB on root branching and the resulting increase in root surface is not sufficient to explain the increase in total NO–3 uptake since this latter increased more than the root surface did. Two different working hypotheses can be proposed: (1) PGPB could induce an increase in NO–3 uptake rate, leading to stimulated shoot growth rate driven by the improved N nutrition; (2) PGPB could stimulate shoot growth rate by an alternative mechanism, leading to an increased NO–3 uptake rate driven by the nutritional demand. In both hypotheses, whether it is a cause or a consequence of shoot growth stimulation, the NO–3 uptake rate itself is expected to be higher in the roots of inoculated plants. Using ion-specific microelectrodes, it has been shown that the uptake rates of NO–3 in the seminal root of oilseed rape increased in response to the inoculation with Achromobacter (Bertrand et al., 2000). It is remarkable that the uptake rate of the other ion tested, K+, and the efflux of H+ also increased, as described by others (Bashan et al., 1989a; Bashan, 1990). These findings suggest that the rhizobacteria affect mineral ion uptake globally due to a stimulation of the proton pump ATPase activity. Alternatively the Achromobacter strain could enhance the activity of several ion transporters, either directly by affecting the processes involved in their regulation in roots or indirectly via an increased nutritional demand as envisaged in hypothesis (2). Such changes in the plant’s nutritional demand are known to trigger changes in mineral uptake rate. For instance, changing the growth rate of a plant, and hence the N demand, by modifying one environmental factor while the supply of NO–3 to roots was kept constant, resulted in changes of NO–3 uptake rate (Gastal and Saugier, 1989; Touraine et al., 1994).
Beside the possible direct effect of PGPB on NO–3 uptake and the indirect effect via the increased root surface area due to the stimulation of lateral root development, the effect on root hair development has to be considered. Several PGPB strains have been shown to increase root hair size and number (de Freitas and Germida, 1989; Okon and Vanderleyden, 1997; Bertrand et al., 2000), and these tubular extensions of root epidermal cells can be involved in mineral uptake capacity in two ways. First, root hairs represent a large surface available for ion uptake and, second, they are believed to play an important role in nutrient uptake. The role of root hairs in mineral absorption, however, is usually largely overestimated. Indeed, anatomical observations and fluorescent dye experiments have shown that the epidermal cell layer forms a symplastic domain separated from the rest of the root symplasm due to a very low density of plasmodesmata (Morot-Gaudry and Touraine, 2000). Due to this anatomical feature, the main site where mineral ions enter the root symplasm for further transport to the other plant organs would be the outer cortical cell layers, not the epidermis. This assumption is supported for NO–3 by the results of a compartmental analysis performed in barley. This study indicated that the roots contain two different NO–3 pools, a small metabolic pool which does not supply NO–3 for xylem secretion, and a larger pool exchanging with the medium at one end and with the xylem sap at the other end (Siddiqi et al., 1991). The role of cortical cells in NO–3 uptake is further supported by the finding that the high affinity NO–3 transporter NRT2.1 in Arabidopsis is expressed at higher levels in these cells than in the epidermal cells (Nazoa et al., 2003).
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Conclusion |
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TopAbstractIntroductionIs the primary effect...Root morphogenesis as affected...Do PGPB affect the...ConclusionReferences |
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Despite their ability to fix atmospheric nitrogen, PGPB are unlikely to provide large amounts of this nitrogen to the plants. However, they have a great impact on nitrogen nutrition by increasing NO–3 uptake capacity, indirectly as a consequence of stimulated lateral root development and possibly directly by stimulating NO–3 transport systems. The question of the ability of PGPB to stimulate NO–3 uptake, however, remains to be addressed directly. Although NO–3 transporters are likely to be post-translationally regulated, the results of numerous expression studies suggest that NO–3 uptake is primarily regulated at the transcriptional level (Forde, 2000; Vidmar et al., 2000; Touraine et al., 2001; Glass et al., 2002; Nazoa et al., 2003). The molecular tools available in Arabidopsis should, therefore, help to determine whether PGPB have an effect on NO–3 transporters per se, directly or indirectly, or if the increased N efficiency is only due to the increase of root surface area elicited by the PGPB.
The effect of PGPB on root morphogenesis does not appear to be antagonistic to the effect exerted on root architecture by NO–3. To investigate whether the two underlying regulatory pathways are totally independent or if they share some common elements will require more detailed knowledge of the individual signalling pathways. In addition, the rapid progress of knowledge on the hormonal transduction pathways in plants will provide tools to determine which steps of these transduction pathways are targets of the PGPB.
Finally, the response processes of root development and mineral uptake to NO–3 availability and PGPB inoculation are probably independent of each other. If this is true, the effects of these abiotic and biotic factors must be additive, i.e. the total root length would be the highest in inoculated plants grown with low N fertilization. This conclusion is consistent with the observation that the effects of inoculation are the highest in fields with low N fertilizer supply (Okon, 1985; Dobbelaere et al., 2002).
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Acknowledgements |
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We are grateful to Marièle Larcher, Jean-Claude Cleyet-Marel and Timothy Tranbarger for fruitful discussions about the subject discussed in this review. Sophie Mantelin was supported by a PhD grant from the Institut National de la Recherche Agronomique (INRA) and the Centre Technique Interprofessionnel des Oléagineux Métropolitains (CETIOM).
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