Journal of Experimental Botany, Vol. 53, No. 373, pp. 1495-1502,
June 2002
© 2002 Oxford University Press
Original Papers |
An inducible activator produced by a Serratia proteamaculans strain and its soybean growth-promoting activity under greenhouse conditions
Department of Plant Science, Macdonald Campus of McGill University, 21,111 Lakeshore Road, Ste Anne de Bellevue, Quebec, Canada H9X 3V9
Received 23 October 2001; Accepted 20 February 2002
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Abstract |
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Serratia proteamaculans 1-102 (1-102) promotes soybean–bradyrhizobia nodulation and growth, but the mechanism is unknown. After adding isoflavonoid inducers to 1-102 culture, an active peak with a retention time of about 105 min in the HPLC fractionation was isolated using a bioassay based on the stimulation of soybean seed germination. The plant growth-promoting activity of this material was compared with 1-102 culture (cells) and supernatant under greenhouse conditions. The activator was applied to roots in 83, 830 and 8300 HPLC microvolts (µV) per seedling when plants were inoculated with bradyrhizobia or sprayed onto the leaves in same concentrations at 20 d after inoculation. The root-applied activator, especially at 1 ml of 830 µV per seedling, enhanced soybean nodulation and growth at the same level as 1-102 culture under both optimal and sub-optimal root zone temperatures. Thus, this activator stimulating soybean seed germination is also responsible for the plant growth-promoting activity of 1-102 culture. However, when sprayed onto the leaves, the activator did not increase growth and in higher concentrations decreased average single leaf area. The results suggest that this inducible activator might be a lipo-chitooligosaccharide (LCO) analogue. LCOs act as rhizobia-to-legume signals stimulating root nodule formation. The activator could provide additional ‘signal’, increasing in the signal quality (the signal-to-noise ratio, SNR) of the plant–rhizobia signal exchange process.
Key words: Inducible activator, plant growth-promoting rhizobacteria, Serratia proteamaculans, soybean.
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Introduction |
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Legume nodulation is a complex process involving interactions between the host plants and rhizobia. This process is also affected by many biotic and abiotic environmental factors (Hungria and Stacey, 1997
; Valdssak and Vanderleyden, 1997). The first stage in the establishment of the symbiotic system is signal exchange between legume plants and rhizobia. The plant-to-bacteria signals are isoflavonoids which induce bradyrhizobial nod gene expression and in the case of soybean are mainly genistein and daidzein (Rao and Cooper, 1994). The rhizobia-to-plant return signals are lipo-chitooligosaccharides (LCOs), so-called Nod factors, which play pivotal roles in root nodule formation. LCOs are oligosaccharides of ß-1,4-linked N-acetyl-D-glucosamine and of some specifically modified side groups. LCOs are synthesized via sophisticated biochemical processes catalysed by a series of nod gene encoded enzymes (Perret et al., 2000). All individual rhizobial strains produce specific structurally diverse LCO mixtures (Spaink, 1996) and the major LCO molecule produced by Bradyrhizobium japonicum 532C is Nod Bj V (C18:1; MeFuc) (Prithiviraj et al., 2000).
During the signal exchange process, environmental factors affecting either signal production or signal perception can affect nodulation and subsequent nitrogen fixation. Sub-optimal (15–17.5 °C) root zone temperatures (RZTs), pH stress and mineral nitrogen inhibit the production of isoflavonoids by soybean roots as well as subsequent nodulation and nitrogen fixation (Streeter, 1988; Cho and Harper, 1990; Zhang and Smith, 1994, 1996a; Pan and Smith, 1998). High temperature (39 °C) increases the release of the isoflavonoid signals from soybean seeds during the first 24 h, but the compounds released have decreased nod gene-inducing activities (Hungria and Stacey, 1997). The addition of genistein to the inoculant or the rhizosphere could at least partially alleviate the deleterious effects of these environmental factors (Zhang and Smith, 1995, 1996b, 1997; Smith and Zhang, 1996; Hungria and Stacey, 1997; Pan et al., 1998). Besides inhibiting the synthesis and excretion of isoflavonoids by soybean roots, low RZTs also suppress bacterial nod gene expression, and this also could be partially overcome by genistein application (Zhang et al., 1996a). In addition, LCOs are sensitive to chitinase and related hydrolases which cleave and inactivate Nod factors in the host rhizosphere (Perret et al., 2000). When Sinorhizobium fredii and S. meliloti were transconjugated with a chitinase gene from a Serratia marcescens strain, the enzyme was expressed and nodulation of soybean and alfalfa were impeded (Krishnan et al., 1999).
Many plant growth-promoting rhizobacteria (PGPR) have beneficial effects on legume growth, and at least some PGPR strains enhance legume nodulation and nitrogen fixation by affecting signal exchange between the plants and rhizobia. Co-inoculation of some Pseudomonas and Bacillus strains, along with effective Rhizobium spp., stimulates chickpea growth, nodulation and nitrogen fixation (Parmar and Dadarwal, 1999). Seed colonization by these PGPR or application of the ethyl acetate extract of the culture supernatant increase the concentration of flavonoid-like compounds in roots, and the rhizobacteria themselves are capable of producing fluorescent flavonoids similar to those produced by the plant (Parmar and Dadarwal, 1999). These lines of evidence indicate that PGPR may produce signal molecule analogues and/or stimulate the plant to produce more signal molecules. It may also be reasonable to postulate that some rhizobacteria produce LCO analogues or improve conditions for signal exchange.
Some Serratia strains, such as S. proteamaculans 1-102 and S. liquefaciens 2-68, have beneficial effects on legume plant growth (Chanway et al., 1989; Zhang et al., 1996b). They are both partially able to overcome the effects of sub-optimal RZT on soybean nodulation and N2 fixation. Strain 1-102 generally performed better than 2-68 at sub-optimal RZTs (Zhang et al., 1996b). Their culture supernatants had the same beneficial effects on soybean plants as the bacterial cultures, although not under sub-optimal conditions (Dashti, 1997). Combined application of these PGPR and genistein improved N2 fixation in soybean at suboptimal root zone temperatures (Dashti et al., 2000). Given their effects on soybean plants, it is hypothesized that the PGPR strains exert their influence via the production of specific compounds after they have been inoculated into plant rhizospheres. In testing this hypothesis, a series of experiments were designed and carried out with S. proteamaculans 1-102. A plant growth-stimulating substance (activator) in the HPLC fractions from 1-102 culture treated with isoflavonoid inducers was first isolated through a bioassay for its ability to stimulate soybean seed germination and then its activity in promoting soybean growth and nodulation was further evaluated under greenhouse conditions. The objective of the results presented here was to demonstrate that the inducible activator produced by 1-102 was the compound responsible for the bacterial promotion of soybean plant growth and nodulation under both optimal and suboptimal RZT conditions.
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Materials and methods |
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Activator preparation
PGPR strain Serratia proteamaculans 1-102 (1-102) was cultured in King's Medium B (Atlas, 1995
). The initial broth inoculum was inoculated with slant material and cultured in 250 ml flasks containing 100 ml of medium for 72 h on a shaker (Model 4530 Table Top Orbital Shaker, Forma Scientific Inc., Mariotla, Ohio, USA) at 150 rev min-1 and 28 °C. Subcultures were then inoculated with the initiation broth inoculum at a 1% inoculation ratio and cultured in 4.0 l flasks containing 1.0 l of medium for 96 h under the same conditions as the initial culture. During the culture period, isoflavonoid inducers (Sigma-Aldrich Canada Ltd., Oakville, Canada), including genistein (G6766), naringenin (N5893), apigenin (A9914), and luteolin (L9283) were added at final concentrations of 1 µM each (Kosslak et al., 1987). At the end of the 96 h culture period, the culture broth was extracted with butanol at a 40% (v/v) final concentration. The organic phase was collected and evaporated in a low-pressure rotary evaporation system (Yamota RE500, Yamato, USA) at 50 °C. The residue was re-suspended in 18% acetonitrile (AcN/H2O, v/v) as a crude preparation. This crude preparation was further purified through HPLC fractionation, using a Waters system equipped with two model 510 pumps, a WISP 712 auto-sampler, a model 441 absorbance detector and a fraction collector (Waters, MA, USA). The crude sample was loaded onto a C18 reverse-phase column (Vydac 218TP54, 300 Å, 5 µm, 4.6x250 mm). The elution was performed as follows: 0–45 min with isocratic 18% acetonitrile; 45–110 min with a gradient from 18% to 60.7% acetonitrile; 110–115 min with a gradient from 60.7% to 100% acetonitrile; 115–120 min, with a reversed gradient from 100% to 18% acetonitrile. The absorbance of the eluted fractions was monitored at 214 nm. The HPLC elutes were collected as 120 fractions, 1 min of elution time per fraction, and maintained at 4 °C until use. Besides 1-102 culture treated with the inducers, the culture without added inducers, and the culture medium alone (culture medium that had never grown cells) were also subjected to the same extraction procedures described above. All the 120 HPLC fractions from these three samples were tested with a bioassay method based on soybean seed germination as a test for the presence of activator.
Bioassay for the active HPLC peak
The bioassay of the active peak was conducted by following a 3-step focusing strategy. In the first step, all the 120 fractions were divided to three parts: I-i, 0–40 min; I-ii, 41–80 min and I-iii, 81–120 min, and tested for ability to stimulate soybean seed germination. In the second step, the selected active part I-iii (81–120 min) was further divided into four parts: II-i, 80–90 min; II-ii, 91–100 min, II-iii; 101–110 min; and II-iv, 111–120 min and bioassayed, and part II-iii (101–110 min) was identified. In the third bioassay step, part II-iii was subdivided to three parts: III-i, 101–103 min; III-ii, 104–106 min; and III-iii, 107–110 min. In the bioassay, soybean seeds (cultivar OAC Bayfield) were surface-sterilized in sodium hypochloride (2% solution containing 4 ml l-1 of Tween 20) (Bhuvaneswari et al., 1980). A filter paper disc was put in the bottom of each sterilized Petri dish (100x15 mm, Fisher Scientific, Ontario, Canada) in order to have an even distribution of the added solution. Ten soybean seeds were placed on the filter paper of each dish. Each treatment was replicated five times in five separate dishes, and the entire experiment was conducted twice. At each step the treatment solution was prepared as follows: all of the 1 min samples corresponding to a section of the HPLC chromatogram that was to be assayed were combined and the resulting material was serially diluted with distilled water to 1:500, 1:5000 and 1:50 000. Ten ml of each solution was added to each of a set of five dishes. The time of solution addition was taken as the beginning of the germination period. All the dishes were kept in an incubator (Conviron E15 Growth Chamber, Controlled Environments Ltd., Winnipeg, Canada) at 26±1 °C, with 70–80% humidity, good ventilation and without lighting. A seed was judged to be germinated when the root tip had clearly penetrated the seed coat. The number of germinated seed in each dish was recorded periodically during the 66 h germination process. The germination rate was expressed as a percentage of the total number of seeds in the dish. The bioassay eventually identified part III-ii, 104–106 min as the potential activator. This peak was only present in cultures where the 1-102 cells had been treated with flavonoid inducers. The relative concentration of the activator was given as the area under the HPLC peak, measured in microvolts (µV). The applied active solutions were equal to 8300 µV ml-1 (1:500), 830 µV ml-1 (1:5000) and 83 µV ml-1 (1:50 000). In the following greenhouse experiments, only selected activator from culture treated with inducers was tested in these three relative concentrations.
Greenhouse experiments
The effect of the activator on soybean plant growth was evaluated under greenhouse conditions by comparison with 1-102 cultures, and 1-102 culture supernatant. The experiment was conducted in both pot (20 cm diameter) and pouch (15x16 cm, Mega International, Minneapolis, MN) culture systems. When pouch culture was adopted, the RZT was controlled by water bath systems at 25 °C and 15 °C. The greenhouse air temperature was 25±2 °C with additional illumination of 300 µM m-2 s-1 supplied by high pressure sodium lamps (P. L. Light System, Montreal, Canada) for a photoperiod of 16/8 h day/night. The inocula used in the experiment were Bradyrhizobium japonicum 532C (532C), 532C plus 1-102 culture, 532C plus 1-102 culture supernatant, 532C plus activator at three relative concentrations (83, 830 and 8300 µV plant l-1). In the pot experiment, as described below, all three concentrations of the activator were also sprayed onto seedling leaves.
The soybean seeds (OAC Bayfield) were surface-sterilized in sodium hypochloride (Bhuvaneswari et al., 1980) and planted in trays containing Vermiculite and germinated in the greenhouse. Three to four day old healthy seedlings, at the VE stage (Fehr et al., 1971), were transplanted into pots containing Vermiculite (VIL Vermiculite Inc., Montreal and Toronto, Canada) or pouches suspended in a water bath. Inoculation was conducted when the seedlings were 10-d-old, at the early VC stage.
B. japonicum 532C was cultured in yeast extract mannitol culture medium (YEM) (Vincent, 1970) on a shaker (Model 4580 Refrigerated Console Incubater Orbital Shaker; Forma Scientific Inc., Marietla, Ohio, USA) at 150 rev min-1 and 28 °C. The initial culture was inoculated with slant material and cultured for 7 d. The subculture time was 72–96 h. The cell concentration of the B. japonicum 532C culture was estimated by spectrophotometry at 620 nm (Bhuvaneswari et al., 1980). The B. japonicum culture was diluted with distilled water to A620nm=0.08 (approximately 108 cells ml-1), and the inoculation dose was 108 cells per seedling (Zhang and Smith, 1994).
S. proteamaculans 1-102 was produced in the same way as for activator preparation but for only 24 h and no isoflavonoid inducer was applied. The cell concentration of the 1-102 culture was estimated by spectrophotometry at 420 nm (Pan et al., 1999). The culture was diluted with distilled water to A420nm=0.10 (approximately 108 cells ml-1) and the inoculation dose for 1-102 was also 108 cells per seedling. The culture supernatant was prepared from a 24 h culture by centrifugation at 4000 rev min-1 for 15 min. When it was co-inoculated with 532C, it was diluted with distilled water at the same rate as the culture inoculant.
When the purified activator was applied to roots by co-inoculation with the bradyrhizobia or the leaves by spraying, it was diluted with distilled water to final concentrations of 83 µV ml-1 (Act1), 830 µV ml-1 (Act2) or 8300 µV ml-1 (Act3). The activator solutions were applied at 1 ml per plant, either to roots or the leaves. The sprayings of the activator in the pot experiment were conducted at 20 d after inoculation (DAI). When the spraying was conducted, the pots were far enough apart that the seedlings did not touch each other.
The plants were cultured without application of any mineral nitrogen and harvested at 50 DAI. During the growth period, the plants were watered with N-free Hoagland's solution (Hoagland and Arnon, 1950), in which Ca(NO3)2 and KNO3 were replaced with 1 mM K2HPO4 and 1 mM KH2PO4. After harvesting, data were collected on leaf number and leaf area (not applicable to 15 °C RZT samples as most of the leaves had senesced by then), nodule number, nodule weight, root weight, and shoot weight. The weights of nodules, shoots and roots were collected after they had been dried at 70–80 °C for not less than 48 h.
Data analysis
All the data were analysed statistically with the SAS system (Littell et al., 1991). When analysis of variance indicated differences, comparisons among treatment means were conducted with an ANOVA protected least significance difference (LSD) test (Steel and Torrie, 1980). In general, differences were considered significant at P
0.05. However, in some cases differences significant at probabilities between 0.05 and 0.1 are described. When this happens the P values are given in the text.
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Results |
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The HPLC profiles of the three extracted materials, 1-102 culture with the inducers, 1-102 culture without the inducers and the culture medium alone, are shown in Fig. 1
. The 1-102 culture with the inducers had a novel peak with retention time 104.83 min (Fig. 1A). At the same position, as well as in the neighbouring regions, the medium control had no peak (Fig. 1C). The 1-102 culture without inducers had a peak with retention time 103.15 min (Fig. 1B), and this peak disappeared in the culture with the inducers (Fig. 1A). After the three-step bioassay, based on stimulation of soybean seed germination, the study focused on fraction III-ii, with a retention time 104–106 min, in which the novel peak in Fig. 1A was included. The final bioassay results with 104–106 min fractions are shown in Fig. 2. Compared with the medium alone control, the fraction from both cultures with and without the inducers resulted in a higher germination rate. Although all three tested concentrations were active, the lowest, 1:50 000 (83 µV ml-1) caused the greatest stimulation of germination (Fig. 2, III).
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In the pouch experiment, co-inoculation of 1-102 culture increased nodule number by 30%, nodule weight by 45.5% and plant weight by 31.3% under 25 °C RZT, and nodule number by 81.1% and plant weight by 14.6% under 15 °C RZT, compared with the 532C-alone control (Table 1
). Addition of the PGPR supernatant to the B. japonicum inoculant increased nodule weight by 53.7% and plant weight by 31.2% under 25 °C RZT, that is at essentially the same level with co-inoculation of B. japonicum with the 1-102 culture. However, at 15 °C RZT, the application of 1-102 supernatant failed to cause an increase in the plant weight, although nodule number was increased.
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In the pouch experiment, addition of the activator, Act2 at 830 µV plant-1, to the B. japonicum inoculant caused the largest increases of all the treatments. It increased all the measured variables at both RZTs. Thus, the effects of the activator were similar to co-inoculation of 1-102 culture with B. japonicum cells. Act2 increased nodule number by 31.9% and 80.2%, nodule weight by 81.2% and 46.6%, and plant weight by 39.2% and 27.2% under 25 °C and 15 °C RZT, respectively (Table 1
). Act1 at 83 µV plant-1 and Act3 at 8300 µV plant-1 had little positive effect at 25 °C RZT in the pouch experiment. However, at 15 °C RZT it increased nodule number and plant weight at levels similar to co-inoculation of 1-102 culture. Act1 also increased nodule weight at 15 °C RZT (Table 1). Thus, soybean plants are more sensitive to this activator higher RZT, in the pouch experiment.
In the pot experiment, Act2 resulted in the largest increases in nodule number (50%), nodule weight (47.5%) and plant weight (35%) (Fig. 3), relative to the 532C-alone control. In spite of these large numerical increases, the levels of these variables for this treatment were not different from those resulting from treatment with the 1-102 culture, 1-102 supernatant, Act1, and the Act3. Spray treatment with the activator, Act1LS at 83 µV plant-1 increased nodule number (P=0.06), but the other two spray treatments, Act2LS and Act3LS, did not increase any of the measured variables (Fig. 3). Act2LS and Act3LS decreased single leaf area (Table 2), although the leaf number per plant and the total leaf area per plant were not different between leaf-applied activator treatments and the control (data not shown). The higher the concentration of the activator applied on leaves, the more the average single leaf area was decreased.
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Discussion |
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Numerous publications have reported that co-inoculation of PGPR with rhizobia improves legume nodulation and nitrogen fixation, however, in only a few cases has the mechanism of PGPR stimulation been investigated (Derylo and Skrupska, 1993
; Srinivasan et al., 1996; Parmar and Dadarwal, 1999). Finding the mechanisms by which PGPR promote legume growth and nodulation remains a major challenge. Recent progress in the understanding of legume–rhizobia interactions (Perret et al., 2000) has encouraged an approach to the PGPR mechanisms with new and more specific questions. The work included in this paper showed that root application of the activator had essentially the same efficacy as live 1-102 cells in promoting soybean plant growth and nodulation. This strongly suggested that the activator is the compound responsible for the PGPR efficacy and that the hypothesis that the live cells in the rhizosphere produce the activator after being activated by the isoflavonoid inducers secreted by plant roots is correct.
In the greenhouse experiments, promotion of soybean plant growth and nodulation by the 1-102 culture supernatant only at an RZT in the optimum range confirms other results (Dashti, 1997). Regardless of culture system or RZT, Act1, the 1-102 supernatant and the 1-102 culture were not different from each other (Table 1; Fig. 3). This suggested that even without the application of inducers, the PGPR cells produce low concentrations of the activator during the culture process. This was supported by the variable effectiveness of applications of the activator at the different concentrations. Among the three applied concentrations, Act2 performed the best: both the higher and the lower doses, Act3 and Act1, showed diminished effectiveness in promoting plant growth and nodulation. Thus, Act2 was the optimal concentration and it may well be that the concentration of the activator in the supernatant was lower than this, being sufficient to promote plant growth and nodulation at an optimal RZT, but insufficient for this growth promotion under the lower RZT condition. The activity of 1-102 cells at the lower RZT indicates that they were able to produce sufficient activator for soybean plant growth stimulation; presumably isoflavonoid inducers produced by soybean roots played a role in activating bacterial biosynthesis of the activator. The purified activator caused stimulation of soybean plant growth at all concentrations and at both optimal and suboptimal RZTs, suggesting that even the lowest concentration of isolated activator was greater than the concentration in the culture supernatant.
Bioassay methods are generally more sensitive in detecting physiologically active substances than the physico-chemical analyses. In these bioassay experiments, besides fraction III-ii, which contained the active peak (104.85 min) from 1-102 culture with the inducers, the same fraction from cultures without inducers also showed activity in stimulating seed germination, although it displayed no obvious peak in the profile (Fig. 1). This could be explained by a very low concentration of the activator, below detection by HPLC. This is possible. For instance, LCOs show high activity in the stimulation of nodulation in soybean systems at 10-8 M, but this is well below the level of HPLC detection. For stimulation of root hair deformation, LCO activity has been seen at concentrations as low as 10-11 M (Relic et al., 1993).
The efficacy of root applications of the activator was constant in both pouch and pot experiments. However, the leaf applications were not as effective as the root applications. When the activator was sprayed on soybean leaves, decreased leaf area per leaf and the lack of increased plant growth and nodulation were observed. That the activator, which would normally be produced in the rhizosphere, has effects on plant development when applied on the leaves is interesting. These experimental results showed that decreases in average single leaf area occurred only at higher concentrations of activator, Act2LS and Act3LS. Besides activator concentration, activator effectiveness may also be related to the plant development stage when the spray was conducted. For soybean seedlings grown in the greenhouse under N-free culture conditions, 20 DAI is the beginning of the period of rapid leaf area expansion (personal observations). When leaf area is increasing, it may become a competitive sink for both nitrogen and carbohydrate. If the activator stimulates translocation from the leaves to other sinks, leaf area expansion will be limited by the spray application. This could, in turn, diminish total plant photosynthesis and, subsequently, nitrogen fixation through plant auto-regulation mechanisms for maintaining nitrogen–carbon balance (Shantharam and Mattoo, 1997).
Rhizobia produce a series of LCOs with different substitutions and/or modifications of the basic structure of three to five 1,4-ß-linked N-acetylglucosaminosyl fragments (Hungria and Stacey, 1997). Besides playing a key role in legume root nodule formation, LCOs are also involved in other plant morphogenesis activities, such as induction of cell cycle genes in suspension cell cultures and induction of mitosis in the protoplast cultures, and even in some aspects of animal morphogenesis (Spaink, 1996). There is increasing evidence that some plants and animals are also capable of producing and recognizing signal molecules that structurally resemble the rhizobial LCOs, i.e. LCO analogues (Spaink, 1996). These results imply that the activator in question could be an LCO analogue. As with LCOs from rhizobia, the activator was produced in measurable amounts following exposure of the cells to the isoflavonoid inducers. The activator and LCO were prepared by following a similar extraction procedure. Their HPLC purification programmes were also very similar (following the same procedure LCO Bj V [C18:1 MeFuc] has an HPLC retention time of 83–86 min), and both of them were monitored with UV light of 214 nm wavelength. Both the activator and LCOs stimulate soybean seed germination (B Prithiviraj, LCOs stimulate soybean and other crop seed germination, personal communication). If this is the case, it not only supports the initial hypothesis, but also allows the mechanism of the plant growth-promoting activity by Serratia proteamaculans 1-102 to be described further.
During signal communication, signal quality is described in terms of signal-to-noise ratio (SNR). Only when the SNR becomes greater than a critical value does the communication succeed. The plant–bacteria signal exchange process is a two-way molecular conversation occurring in the rhizosphere (Fisher and Long, 1992). The SNR concept may also be applicable to the legume–rhizobia signal exchange. An LCO analogue might increase the SNR of the molecular conversation between legume and rhizobia. LCOs have multiple functions in inducing root nodule formation and other responses related to the infection process in host plants (Prithiviraj et al., 2000). An LCO analogue might perform any one or a number of these multiple functions. Furthermore, besides the host plant (Perret et al., 2000; Prithiviraj et al., 2000), other rhizobacteria may also produce LCO hydrolases in the rhizosphere. LCO analogues may act as competitive substrates of hydrolysis enzymes.
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1 To whom correspondence should be addressed. Fax: +1 514 398 7897. E-mail: dsmith{at}macdonald.mcgill.ca
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References |
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