Journal of Experimental Botany, Vol. 53, No. 376, pp. 1929-1934,
September 1, 2002
© 2002 Oxford University Press
The major Nod factor of Bradyrhizobium japonicum promotes early growth of soybean and corn
Received 10 July 2001; Accepted 10 May 2002
Department of Plant Science, Macdonald Campus, McGill University, 21,111 Lakeshore Road, Ste Anne de Bellevue, QC, Canada H9X 3V9
1 To whom correspondence should be addressed: Fax: +1 514 398 7897. E-mail: dsmith{at}macdonald.mcgill.ca
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Abstract |
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Greenhouse experiments were conducted to evaluate the effect of Nod factor Nod Bj-V (C18:1, MeFuc) of Badyrhizobium japonicum on the growth of soybean and corn. Three-day-old seedlings of soybean and corn were grown in hydroponic solutions containing four concentrations (0, 10–7, 10–9 or 10–11 M) of Nod factor. After 7 d of treatment, Nod factor enhanced soybean and corn biomass. Nod factor elicited profound effects on root growth resulting in 34–44% longer roots in soybean. More detailed analyses of the roots, using a scanner based image analysis system, revealed that Nod factor increased the total length, projected area and surface area of the roots and decreased the diameter of soybean roots, while it increased the total length of corn roots. Stem injection of soybean plants with 10–7 M Nod factor resulted in increased dry matter accumulation. These results suggest that Nod factor, besides mediating early stages of nodulation, has more general plant growth-promoting effects.
Key words: Key words: Corn, lipo-chito-oligosaccharide, Nod factor, nodulation, soybean.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Nod factors are bacteria-to-plant signal molecules produced by bacteria of the genera Bradyrhizobium, Rhizobium, Azorhizobium, Allorhizobium, Mesorhizo bium, and Sinorhizobium during the formation of the rhizobia–legume N2-fixing symbiosis (Spaink, 1992). These signal molecules are induced in response to plant-to-bacteria signal molecules, which are usually flavonoids and isoflavonoids found in legume root exudates. Nod factors are lipo-chito-oligosaccharides (LCOs) and are generally composed of three to five 1-4ß-linked acetyl glucosamine residues with the N acetyl group of the terminal non-reducing end replaced by an acyl chain. However, various modifications to this basic structure are possible and each of the rhizobia produces a specific set of Nod factors. A number of studies have implicated Nod factors as a possible candidate in the host specificity of rhizobia (Spaink et al., 1991; Cohn et al., 1998; Stougaard, 2000). The Nod factors produced by Bradyrhizobium japonicum are pentameric molecules with C18:1, C16:0, and C16:1 fatty acid chains at the non-reducing end and 2-O-methylfucose at the reducing end of the chitin backbone (Carlson et al., 1993).
Nod factors as well as synthetic LCOs are known to affect a number of host physiological processes. For example, they induce root hair deformation (Spaink, 1996), ontogeny of complete nodule structures (Fisher and Long, 1992; Denarie and Cullimore, 1993), and cortical cell division (Sanjuan et al., 1992), indicating that LCOs are mitogenic and morphogenic agents and invoke the same effect as cytokinins (BAP, 2iP or kinetin) or inhibitors of auxin transport (Relic et al., 1993). LCOs and Nod factors also induce the expression of host nodulin genes essential for infection thread formation (Horvath et al., 1993; Minami et al., 1996), and have been shown to activate defence-related enzymes (Inui et al., 1997).
In non-host plants, Nod factors have been shown to elicit several physiological responses. They induce rapid and transient alkalinization of tobacco (Baier et al., 1999) and tomato cells (Staehelin et al., 1994) in suspension cultures. De Jong et al. (1993) found that Nod factors restored cell division and embryo development in a temperature-sensitive carrot mutant. Somatic embryo cultures of Norway spruce (Picea abies) also resumed cell division when Nod factors were added to the medium, even in the absence of auxin and cytokinin (Dyachok et al., 2000). However, the effect of Nod factors on whole plant systems of host and non-host plants have not been studied. Therefore, the present research was conducted to study the effect of the Nod factor of Bradyrhizobium japonicum, Nod Bj-V (C18:1, MeFuc), on the growth of soybean and corn in the greenhouse.
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Materials and methods |
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Bacterial culture
The Bradyrhizobium japonicum strain 532C was obtained from Liphatech (Milwaukee, USA), and was maintained on slants with Yeast Extract Mannitol Agar (mannitol 10 g, K2HPO4 0.5 g,MgSO4.7H2O 0.2 g, NaCl 0.1 g, yeast extract 0.4 g, distilled water 1000 ml) (Vincent, 1970).
Extraction and purification of Nod factor
The bacteria were cultured in 2.0 l flasks containing YEM broth shaken at 150 rpm at 28 °C. At the end of the exponential growth phase (5–7 d), the biosynthesis of Nod factor was induced by the addition of the isoflavonoid genestein (Sigma Chemical Co. MO, USA) to a final concentration of 5 µM. After 48–96 h of treatment with genistein the culture was extracted with 0.4 vol. of the HPLC-grade 1-butanol (Fisher Scientific, Canada). The upper butanol layer was collected and rotary-evaporated at 50 °C under vacuum. The residue was redissolved in 18% acetonitrile and fractionated by HPLC using a Vydac C18 reversed phase column (0.46x25 cm; 5 µM) (The Separation Group Inc, Hesperia, CA, USA) with a gradient of acetonitrile from 18% to 60%. The chromatographic peak corresponding to Nod factor Nod Bj-V (C18:1, MeFuc) was identified by comparing it with the retention time of an LCO standard, Nod Bj-V (C18:1), MeFuc, prepared from Bradyrhizobium japonicum strain USDA110 (a generous gift from Professor G Stacey, University of Tennessee, Knoxville, USA). The material was further purified by HPLC and freeze-dried. The purity of the Nod factor was confirmed by subjecting a sample of a collected peak for chemical identity by FAB-MS (Dr RW Carlson, Complex Carbohydrate Research Centre, University of Georgia, USA), the activity of each batch was confirmed by a root hair deformation bioassay, conducted with soybean (Prithiviraj et al., 2000).
Effects of Nod Bj-V (C18:1, MeFuc)
Experiments were conducted in the greenhouse of the Macdonald Campus of McGill University. Seeds of soybean [Glycine max (L.) Merr] cv. OAC Bayfield and corn (Zea mays L.) hybrid Pioneer 3921 were surface-sterilized with 2% hypochlorite for 2 min and rinsed with five changes of sterile distilled water. The seeds were then placed in sterile moist germination paper (Anchor Papers Inc., USA) in 9 cm Petri dishes at the rate of 10 seeds per Petri dish and incubated at 25±2 °C in the dark for 3 d. After 72 h seedlings with uniform growth were selected and transferred onto the covers of 350 ml glass bottles. The covers were made of plastic with holes of 5 mm diameter drilled through them. The seedlings were suspended through these holes such that the roots were immersed in water containing different concentrations (0: control, 10–7, 10–9 and 10–11 M) Nod factor. The required concentrations of the Nod factor were made by dissolving freeze-dried Nod factor in a small amount (100 µl) of 50% acetonitrile in water (Stokkermans et al., 1995) and further dilutions were made with distilled water. The diameter of the bottle was 5 cm and each bottle had five seedlings placed equidistantly. The bottles were uniformly aerated using a compressor and plastic tubing (Prithiviraj et al., 2000). Each treatment was done in triplicate and the experiment was organized in a completely randomized design. A 14 h photoperiod, a PAR of 1000 µmol m–2 s–1, temperature at 25±2 °C and 70% humidity were maintained throughout the experiment. The experiment was repeated three times.
After 7 d soybean and corn plants were harvested and shoots were excised, placed in paper bags and dried at 90 °C for 48 h. The roots were stained with 0.1% Toluidine Blue O (Sigma, USA) and root morphology variables (total length, projected and surface area, average diameter, number of tips and forks) were measured using the WinRHIZO version 3.2, an optical-scanner-based image analysis system (Regent instrument Inc., Quebec, Canada) using a method described earlier (Costa et al., 2001).
Stem injection experiment
Soybean seeds were surface-sterilized in 2% hypochlorite for 2 min, rinsed in five changes of sterile distilled water and germinated in sterile vermiculite. At the V1 stage (fully developed leaves at unifoliate nodes), the seedlings were transplanted into plastic pots (15 cm diameter) containing a mixture of 1:1 (v/v) turface (an inert calcined clay, Applied Industrial Materials Corp., IL, USA) and sand. Three days after transplanting 1 ml of B. japonicum strain 532C suspension, equivalent to 108 cells ml–1, was applied to the root zone. The plants were watered regularly using Hoagland’s solution (Hoagland and Arnon, 1950) and grown until the V3 stage (three nodes on the stem with fully expanded leaves beginning with the unifoliate node) (Fehr et al., 1971). The photoperiod, air temperature and relative humidity were as described above. At the V3 stage, an injection system was established for each plant following the method of Abdin et al. (2001). The system was composed of two main parts: (i) a supporting stand, and (ii) a solution injection system. The supporting stand consisted of a 30x31 cm plywood platform with two 59 cm lengths of steel pipe (20 cm apart, 1.22 cm o.d., bottom end threaded) attached to one side. These were attached with two circular metal bases, threaded on the inside and attached to the plywood, near the back of the plywood platform, with wood screws. Three holes were drilled in a second sheet of plywood (22.5x 8.5 cm), and two of these were fitted over the two steel pipes attached to the first sheet of plywood. The second sheet rested on two pipe clamps, about 15 cm above ground level. A 5 ml syringe was suspended through a hole in the middle of the second plywood sheet. Standard (22.5x8.5x7 cm) ceramic three-hole construction bricks (approximately 2.7 kg each) provided a pressure source and the steel pipes provided support for the bricks; the two steel pipes fitted through the two outside holes.
The injection tubing consisted of a 35 cm long flexible plastic tube (Tygon i.d. 0.8 mm, o.d. 2.4 mm) connected at one end to a standard disposable 18-gauge 1
needle (Becton Dickinson and Company, Franklin Lakes, NJ), and at the other end to a 25-gauge 
vacutainer needle (Vacutainer, Becton Dickinson and Company, Rutherford, NJ). The original vacutainer needle tubing was replaced with the stronger Tygon tubing as preliminary testing revealed that the original tubing ruptured under high pressure.
Using masking tape, a triangular cup was formed around the stem of each soybean seedling, about 1 cm above the soil surface. Using the vacutainer needle end of the injection tubing, the 25-gauge needle was inserted into the stem of a soybean plant at a location inside the masking tape cup, so that at least half the needle length was inside the stem. After needle insertion, the cup was filled with fluid latex (Vultex, General Latex Canada, Candiac, Quèbec) and was left to dry for a period of 5 d, in order to ensure a solid seal at the injection site. The pots were then placed on the injection stand, and the other end of the injection tubing was connected to a 5 ml syringe, that contained about 2 ml of the solution pertinent to the treatment under study. In order to replace the air present in the Tygon tubing with the injected solution, the syringe piston was pulled back, drawing plant sap into the tubing and replacing all the air. The syringe piston was then gradually released, so that liquid could flow freely into the tube. The syringe was then disconnected from the tubing, and filled completely (5 ml) with the treatment solution, placed in its designated place on the injection stand, and reconnected with the injection tubing. After assembling the injection system, pressure was applied to the syringe by placing a standard construction-type ceramic brick (approximately 2.7 kg) on top of the syringe plunger. One brick was added each day until reasonable flow rates were achieved. This never required more than four bricks. Given that the internal diameter of the syringe barrel was 1.2 cm, the mass of one brick was 2.7 kg, and that pressure placed on the 5 ml syringe barrel and on the 25-gauge 3/4 needle inserted into soybean stem are the same, the pressure based on the transverse area of syringe barrel would have been approximately 0.2 MPa per brick at the site of injection.
Approximately three times the number of experimental units required were initially established, so as to achieve the required number of working systems with no leaks or obstructions. The injection of the tested solutions (water, 10–7 M Nod factor) continued from the V3 stage to the R4 stage (pod 2 cm long at one of the four uppermost nodes on the main stem with a fully developed leaf) (Fehr et al., 1971). On average 0.1 ml of test solution was injected per plant per day for 34 d. At this stage plants were harvested, separated into leaves, stems and roots, placed in paper bags, dried at 90 °C for 48 h and weighed. Each treatment had five replications.
Data analysis
Data were analysed using the Statistical Analysis System (SAS Institute Inc., 1989). Means of the dry weight data were compared by Student’s t-test at P <0.05. Treatment means of the root morphology data were compared with a GLM protected LSD test. Only differences between means significant at P <0.05 were considered to be significant differences.
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Results and discussion |
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Nod factor, when present in the hydroponic solution, enhanced the growth of soybean plants; shoot length of plants treated with 10–7 and 10–9 M Nod factor were 9% and 5% greater, respectively, than those of the control (Fig. 1). The effect of Nod factor was more pronounced for the roots. The primary roots of soybean plants treated with 10–7 and 10–9 M LCO were 1.44 and 1.34-fold longer than the control. The lowest concentration of Nod factor (10–11M) did not show any effect. The dry weights of the plants were also increased by Nod factor treatment; biomass of soybean plants at 10–7 and 10–9 M Nod factor were 6.6% and 3.9% greater, respectively, than the control, and this increase was due to the gains in the root weight (Table 1).
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A more detailed analysis of soybean roots using a scanner-based image analysis system showed that the application of 10–7, 10–9 and 10–11 M Nod factor increased the total length of roots by 26%, 22% and 10%, respectively (Table 2). In addition, the Nod factor treatments stimulated branching of the roots: the numbers of tips were 11–14% higher than for control plants. At 10–7, 10–9 and 10–11 M LCO, the root projected and surface areas were 22%, 19% and 8% larger than the control. However, LCO treatment decreased the root average diameter and this effect was more obvious at 10–7 than at 10–9 and 10–11 M (Table 2).
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The long-term injection of 10–7 M Nod factor into the stem of soybean also increased total plant dry matter by 8% (Table 3). Therefore, chronic injection of 10–7 M Nod factor, Nod Bj-V (C18:1), MeFuc, promoted the growth of soybean. Although the dry weight of pods was less in the LCO treatment, this treatment had more pods (33±1.5) as compared to the control (30±0.6), so that pod dry weight might have been greater for Nod factor-treated plants by maturity. Interestingly, there was a significant increase in the nodule dry weight for Nod factor-injected plants as compared to control (water-injected) plants; this increase was due to an increase in the weight per nodule and was not due to increase in the total number of nodules.
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Addition of Nod factor to the hydroponic growth medium of corn had positive effects on plant biomass accumulation (11% and 7% increases at 10–7 and 10–11 M Nod factor) (Table 4). Interestingly, this increase in dry matter was due to increases in shoot weight, but not root weight, contrary to the situation with soybean.
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Relative changes of corn shoot height and root length at 10–7 M Nod factor were different. The above-ground portion of corn plants was 7% longer and the below-ground part was 13% shorter than those of control plants (results not shown). The roots were thick with more branching. A more detailed analysis of the root system showed a 12% increase in the total root length due to 10–7 M Nod factor. Lower concentrations did not affect the root growth of corn (Table 5).
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The LCO-induced increases in plant growth demonstrated in the experiments could be caused by ‘hormone-like’ effects of Nod factor. Nod factors are potent inducers of cell division through the induction of cell cycle genes in plants. Purified Nod factors, when targeted through a microballistic approach, resulted in the induction of cell division at the site of contact (Schlaman et al., 1997). Further, appropriate Nod factors per se can induce de novo organogenesis of nodules in a variety of legumes (Cohn et al., 1999). Similarly, induction of cell division by Nod factors in non-legumes has been reported (De Jong et al., 1993; Dyachock et al., 2000). Thus, the observed effect of Nod Bj-V (C18:1, MeFuc) on soybean and corn might be due to an LCO-elicited increase in cell division. During studies on the formation of pseudonodules on roots of Macroptilium atropurpureum it was shown that LCO application mimics modification in the cytokinin-auxin balance provoked by the application of cytokinins (Relic et al., 1993). Like most phytohormones, Nod factors are active over a very wide range of concentrations. In this report, soybean root variables (total length, projected and surface areas, average diameter) were affected by LCO at concentrations from 10–7 to 10–9 M. These data, showing that the application of Nod factor stimulated biomass accumulation and changes in plant structure and morphology, support a view of Nod factors as ‘hormone-like’ molecules.
Interestingly, the Nod factor elicited positive effects on corn, a non-host species. Nod factor responsive genes ENOD12 and homologues of ENOD40 have been characterized in rice, a non-legume (Kouchi et al., 1999; Reddy et al., 1998) suggesting that the perception of Nod factor might be conserved among a wide variety of plants, and the present result supports this view. In previous experiments B. japonicum Nod factors accelerated germination of soybean and corn seeds, however, the pentamer of chitin failed to elicite such effects (unpublished results) suggesting that the structure of Nod factor is involved in specificity for the physiological activity. Strains of Rhizobium leguminosarum bv. trifolii have been isolated as endophytes of rice (Oryza sativa) and this association improves the growth of rice under laboratory conditions and could improve grain yield of some cultivars under field conditions (Yanni et al., 1997). Recently, Prayitno et al. (1999) studied the association between rice and rhizobia using gfp tagged Rhizobium strains and concluded that these bacteria were intimate epiphytic micro-organisms that multiply on the surface and produce plant growth-stimulating molecules which, it is thought, might be Nod factors. Non-host plants could also induce the nod genes of rhizobia (Hungria and Stacey, 1997). Expression of R. meliloti nodA nodB genes under diverse promoters in tobacco altered plant growth and development, illustrating that the product of these genes can cause strong morphogenetic effects (Schmidt et al., 1993).
Given the minute concentration of Nod factors required for the observed effects it is reasonable to assume the presence of specific receptors for LCO in the plant. Two classes of Nod Factor Binding Sites (NFBS) have been characterized in Medicago spp: NFBS1 has low affinity for Nod factors while NFBS2 had higher affinity (Gressent et al., 1999). These putative receptors did not discriminate between sulphuryl substitution needed for in vivo activity. Internalization of LCO in plant cells have been reported (Philip-Hollingsworth et al., 1997) suggesting that the perception of LCO signal in plants might be more complex.
Perturbation of the auxin–cytokinin balance has a profound effect on plant growth and development (Relic et al., 1993). LCO is known to affect auxin transport and this may affect the hormone balance of the plant resulting in the observed effect. Further, the products of some Nod factor-responsive genes are known to have phytohormone activity (Minami et al., 1996). It has also been proposed that LCO and LCO-like compounds might be endogenous plant hormones and the addition of this might cause an increase in the concentration of such compounds, resulting in the enhanced growth of the plant.
To date, the mechanism of the hormone-like activity of LCOs has not been investigated. The addition of various LCOs to soybean roots has been shown to cause rapid induction of ENOD40 expression (Minami et al., 1996) and it was postulated that ENOD40 can function in plants as a cytoplasmic RNA to control phytohormone balance. Therefore, the external application of LCO may modify the control of the balance of phytohormones (e.g. auxin–cytokinin ratio) and provoke large changes in plant growth and development as has been found in these experiments.
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Acknowledgements |
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The research reported in this paper was funded in part by a grant from the Natural Sciences and Engineering Research Council of Canada and Bios Agriculture Inc., Quebec, Canada to DLS. The authors are grateful to Professor Gary Stacey, University of Tennessee at Knoxville for the Nod factor standard and Professor RW Carlson, Complex Carbohydrate Research Center, Universtiy of Georgia, Athens, USA for confirming the chemical identity of the Nod factor reported in this study. Work at the Complex Carbohydrate Research Center is supported, in part, by a Department of Energy Grant DE-FG09-93-ER20097.
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C. Robert, M.-O. Bancal, P. Nicolas, C. Lannou, and B. Ney Analysis and modelling of effects of leaf rust and Septoria tritici blotch on wheat growth J. Exp. Bot., May 1, 2004; 55(399): 1079 - 1094. [Abstract] [Full Text] [PDF]
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