Published online 7 February 2006
Published in Agron J 98:289-294 (2006)
DOI: 10.2134/agronj2005.0132
© 2006 American Society of Agronomy
677 S. Segoe Rd., Madison, WI 53711 USA
Biological Nitrogen Fixation
Bradyrhizobium japonicum Preincubated with Methyl Jasmonate Increases Soybean Nodulation and Nitrogen Fixation
Fazli Mabood,
Xiaomin Zhou and
Donald Smith*
Plant Science Dep., Macdonald Campus of McGill Univ., 21111 Lakeshore Road, Sainte Anne de Bellevue, QC, Canada, H9X 3V9
* Corresponding author (Donald.Smith{at}McGill.ca)
Received for publication May 3, 2005.
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ABSTRACT
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Jasmonates (jasmonic acid and methyl jasmonate) are naturally occurring plant hormones biosynthesized in response to wounding and biotic and abiotic stresses. Besides their role in planta, they can act as signaling molecules in soybean (Glycine max)–Bradyrhizobium symbioses by inducing the transcription of nodulation genes. Previous studies have shown that inoculation of soybean with Bradyrhizobium japonicum preinduced with genistein (Ge) or methyl jasmonate (MeJA) promoted soybean nodulation and N fixation under controlled environment conditions. We conducted two separate field experiments in the year 2002 to study the effect of preinducing B. japonicum strains with methyl jasmonate (MeJA), alone or in combination with Ge, on nodulation and N fixation under field conditions. Two B. japonicum strains (532C and USDA3) and four inducer treatments (control, MeJA, Ge, and MeJA plus Ge) were formulated. Genistein and MeJA increased nodule number, nodule dry weight per plant, and seasonal N fixation, as compared with the control treatment, inoculated with uninduced B. japonicum. These results demonstrate that methyl jasmonate alone or in combination with Ge can be used to promote soybean nodulation and N fixation under short-season field conditions.
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INTRODUCTION
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THE LEGUME-RHIZOBIA SYMBIOSIS is the most important source of biological N fixation in agricultural systems (Kahindi et al., 1997). Rhizobia invade root cortical cells where they induce the formation of a new plant organ, the nodule (Broughton et al., 2003). Inside these nodules, rhizobia are able to fix atmospheric dinitrogen into ammonia (Hungria and Stacey, 1997). Soybean plants are able to fix 100 to 200 kg ha–1 yr–1 of atmospheric dinitrogen (N2) while in symbiotic association with B. japonicum (Smith and Hume, 1987).
Jasmonates (JA) are naturally occurring growth regulators found in all higher plants (Meyer et al., 1984). In plants, JA is produced from linoleic and linolenic acids, which are produced from membrane lipid breakdown through the action of phospholipase. These fatty acids are converted into 13-hydroperoxylinolenic acid, which is then converted into 12,13epoxy-octadecatrienoic acid. It is then catalyzed into 12-oxo-phytodienoic acid, which, after a reduction and three steps of ß-oxidation, produces (+)-7-iso-JA (Creelman and Mullet, 1997). JA plays an active role in leaf abscission and senescence and in plant growth and development (Creelman and Mullet, 1997). In addition, JA is involved in the signal transduction cascade of induced disease resistance (Gundlach et al., 1992), wounding, and osmotic stress (Kramell et al., 1995). Besides its roles in planta, JA can act as a signaling molecule in Bradyrhizobium-soybean symbiosis. We have recently shown that jasmonates are able to induce the expression of nodulation genes of B. japonicum and that preincubation of B. japonicum with jasmonates promotes nodulation and N fixation in soybean under controlled environment conditions (Mabood and Smith, 2005).
Genistein, exuded from soybean plant roots, is an important signal molecule in the Bradyrhizobium-soybean symbiosis. It initiates the first step in the symbiosis by inducing the transcription of B. japonicum nodulation genes (Kosslak et al., 1987). In response, B. japonicum produce Nod factors, the bacteria-to-plant signal molecules. Successful completion of this signal exchange allows for root hair infection, leading to the formation of N fixing nodules (Broughton et al., 2003). Low root zone temperature disrupts this interorganismal signaling by inhibiting the biosynthesis and rhizosecretion of genistein (Ge) (Zhang and Smith, 1996a) and expression of the bacterial nodulation genes (Zhang et al., 1996). In an investigation of ways to promote nodulation and N fixation under low root zone temperature conditions, Zhang and Smith (1995) have shown that preincubation of B. japonicum with Ge before inoculation onto soybean roots can promote soybean nodulation and N fixation.
Genistein is added to some commercial inoculants to increase soybean yield, especially under suboptimal root zone temperature (RZT) conditions. However, Ge is costly and, at the concentrations needed to overcome low RZT inhibition of soybean nodulation, is inhibitory to the growth of B. japonicum cultures (Mabood and Smith, 2005). Inducers that are less expensive and not damaging to B. japonicum cells would be much more suitable for commercial production of inoculants and could prove beneficial for industrial inoculant producers and soybean crop producers. Methyl jasmonate (MeJA) is an effective nod gene inducer of B. japonicum, is substantially cheaper than Ge, is commercially available, and does not harm B. japonicum cells (Mabood and Smith, 2005). In the present study, we investigated the effect of B. japonicum preincubated with MeJA, alone or in combination with Ge, on soybean nodulation and N fixation under short-season field conditions.
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MATERIALS AND METHODS
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Experimental Design
The experiment was organized as a randomized complete block design with four blocks. There were two factors (inducer molecules and B. japonicum strains) in the experiment. The inducer molecule treatments were B. japonicum cells pre-incubated with 20 µM Ge, with 50 µM MeJA, with 20 µM Ge plus 50 µM MeJA, and with no inducer molecule(s). To determine the amount of N fixed by the B. japonicum-soybean symbiosis, a non-nodulating Evans line was included in the experiment. Each block had one plot of non-nodulating Evans randomly assigned.
The B. japonicum strains were 532C and USDA3. B. japonicum 532C was used because it performs well under cool Canadian soil conditions (Hume and Shelp, 1990), USDA3 was selected due to it greater sensitivity to inducer molecules (unpublished data).
Field Conditions and Plant Material
The experiment was conducted at two sites at the Emile A. Lods Research Center (45°25'45'' N; 73°56'00'' W) of the Macdonald Campus of McGill University, Montreal, Canada in the year 2002. The soil at one site was a sandy-loam (fine silty, mixed, nonacid, frigid Humaquept), and the crop during the previous year was barley (Hordeum vulgare L.). The second site was a clay-loam soil (fine, mixed, nonacid, frigid Humaquept) where the previous crop was corn (Zea mays L.). At both the sites, the soybean cultivar OAC Bayfield was sown.
Each plot was 5 by 1.4 m (row length of 5 m and width of 0.20 m with seven rows in each plot). Soybean seeds were sown by hand. The plant population was 350 plants per plot (450 000 plants ha–1), with an approximate plant-to-plant distance of 10 cm within the row. Soybean seeds were sown on 21 May 2002 and 25 May 2002 at the clay-loam site and sandy-loam sites, respectively.
Preparation of the Bacterial Inoculants and Inoculation
B. japonicum strains 532C and USDA3 were cultured from Petri plate colonies in 500 mL flasks containing 100 to 200 mL yeast extract mannitol culture medium (Vincent, 1970). The cultures were shaken at 150 rpm at 28°C. The initial culture time was 7 d, which was followed by subculturing for a further 5 d in 4-L flasks containing 2 L of bacterial culture. Filter sterilized Ge (Sigma, Mississauga, ON, Canada) and MeJA (Aldrich, Mississauga, ON, Canada) stock solutions were prepared in dimethyl sulfoxide and added to the subcultures so that final Ge and MeJA concentrations were 20 and 50 µM, respectively. The control flasks of each strain were not induced. The sub-cultures were shaken for another 24 h. Before inoculation of the seeds in the field, the cell density of the subculture was determined by spectrophotometer at 620 nm and diluted with distilled water to an OD of 0.1 [(A620 nm reading of 0.1 indicates approximately 108 cells mL–1 (Bhuvaneswari et al., 1980)]. Soybean seeds were sown into open rows and covered with soil immediately after the inoculants were added. The inoculant was applied to the seeds in the open furrows using a 60-mL sterile plastic syringe. Sixty milliliters of inoculant was applied evenly to each row, and the row was then closed immediately. No inoculant was applied to the control (no inoculant treatment) or non-nodulating plots.
Data Collection
Daily average air temperature and precipitation were recorded at the Macdonald Campus weather station. The classification of soybean growth stages followed those of Fehr et al. (1971). Plants were harvested at three developmental stages during the season: (i) V3, three nodes on the main stem with fully developed leaves beginning with the unifoliate nodes (7 July 2002); (ii) R3, at the early pod development stage (12 Aug. 2002); and (iii) R8, harvest maturity stage (28 Sept. 2002). At each harvest, plant samples (10 plants randomly selected) were harvested from each plot for data collection. The plants were separated into shoots and roots, and the roots were washed with tap water. Nodules were removed from the roots, and the number of nodules per plant was recorded. The nodules were oven dried at 70°C for at least 48 h, and nodule dry weight (mg) per plant was recorded. At each harvest, shoots and roots were oven dried at 70°C for at least 48 h, and the N concentration was determined separately using an elemental analyzer (Model NC2500; CE Instruments, Milan, Italy). For seed N determination, 10 plants were randomly selected from each plot at the end of the growing season (R8 stage), harvested, and oven dried at 70°C for at least 48 h. The seeds of these plants were threshed by hand, and the N concentration was determined using an elemental analyzer (Model NC2500; CE Instruments, Milan, Italy). Samples from the non-nodulating Evans line were also collected and used for detecting the differences in amount of N fixed by various B. japonicum treatments. The total amount of seed N fixed was calculated by N difference method (total seed N fixed = total N in seeds of nodulating plants – total N in seeds of non-nodulating plants). Seed N is a suitable way to assess the effects of various treatments on total N fixation because the N harvest index (proportion of plant N in the seeds) is generally about 0.8 (Smith et al., 1988). Relative leaf chlorophyll content was measured by taking SPAD (Soil Plant Analysis Device) meter readings at two plant development stages (V3 and R3).
Data Analysis
The data collected were analyzed by analysis of variance using the statistical analysis system computer package (SAS Inst., 1988). Means were compared by Duncan's multiple range test and orthogonal contrasts (Steel and Torrie, 1980) to test responses to inducer molecules (contrast 1: comparison between controls [532C control + USDA3 control] and the inducer molecule treatments applied to both strains {Ge + MeJA + [Ge + MeJA]}), between strains (contrast 2: comparison between strain 532C and USDA3), between control and the inducer molecules applied to strain 532C (contrast 3: comparison between control and {Ge + MeJA + [Ge + MeJA]}), and between control and the inducer molecules applied to strain USDA3 (contrast 4: comparison between control and {Ge + MeJA + [Ge + MeJA]}). Differences were declared significant at P < 0.05.
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RESULTS AND DISCUSSION
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Daily temperature and precipitation during the 2002 growing season (May–September) are shown in Fig. 1
. The average monthly temperature and monthly precipitation for the past 57 yr (1945–2002) are given in Fig. 2
. The first 2 mo of 2002 were cooler and wetter, whereas the remaining 3 mo were hotter and drier, than the 57-yr average (Fig. 2). The average temperature at planting (11.29°C, May) was 1.81°C below the 57-yr average (13.1°C), whereas the average precipitation in the month of May (128.5 mm) was much higher (55.94 mm, or 77%) than the 57-yr average (72.56 mm). Thus, during early plant growth and development (June), the conditions were wetter and cooler than the long-term average (Fig. 2).
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Fig. 2. Monthly average temperature and total monthly precipitation during the 2002 growing season and 57-yr average (1945–2002).
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Nodulation
The results of our study indicated that Ge, MeJA, and both inducer molecules together consistently increased nodule number and nodule dry weight over the untreated control (inoculated with uninduced B. japonicum only) at both sites (Table 1). In general, plants receiving both inducers produced more nodules with more dry weight (Table 1).
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Table 1. Effect of preincubation of Bradyrhizobium japonicum with genistein (Ge) (20 µM) and methyl jasmonate (MeJA) (50 µM) alone or in combination on soybean nodule number and dry weight at two sites with contrasting soil types and different planting dates.
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At the sandy loam site, plants inoculated with strain 532C and treated with inducers had 60.7% (V3 stage) and 10.8% (R3 stage) more nodules than the noninduced control; there were 83.6% (V3 stage) and 25.2% (R3 stage) increases over control in the case of USDA3. Nodule dry weight increased by 28.1% (V3 stage) and 9.2% (R3 stage) over the noninduced control for strain 532C; the increases were 36.0% (V3 stage) and 8.2% (R3 stage) for induced USDA3 as compared with the noninduced control. At the clay-loam site, plants inoculated with induced strain 532C had 72.5% (V3 stage) and 44.7% (R3 stage) more nodules than the noninduced control, whereas the increases were 85.2% (V3 stage) and 60.4% (R3 stage) over the control in the case of USDA3. Nodule dry weight increased by 59.4% (V3 stage) and 22.9% (R3 stage) over control with strain 532C, whereas the increases were 106.2% (V3 stage) and 14.6% (R3 stage) when using preincubated USDA3 with inducers, as compared with the noninduced control.
There was often no difference (P < 0.05) between the two tested strains (532C and USDA3) for nodule number and nodule dry weight per plant at either harvest. The exceptions were nodule dry weight at the V3 stage (sandy-loam site) and nodule dry weight at the R3 stage (clay-loam site), where inoculation with strain 532C resulted in 8.6 and 10.7% increases in nodule dry weight over USDA3 at the sandy-loam (V3) and clay-loam sites (R3), respectively (Table 1). The superior performance of strain 532C under low spring soil Canadian conditions has been documented (Hume and Shelp, 1990).
Our finding that Ge increased nodulation is consistent with previously published results (Belkheir et al., 2000; Pan et al., 2002, 1998; Zhang and Smith 1997, 1995). Earlier publications found increased nodule number and weight after preincubation of B. japonicum with Ge. Our data indicate that inoculation of soybean plants with bradyrhizobial cells incubated with MeJA alone or in combination with Ge increased soybean nodule number and weight. The mechanism by which MeJA enhances soybean nodulation is probably similar to that of Ge. Application of Ge (Kosslak et al., 1987) and MeJA (Mabood and Smith, 2005) to B. japonicum cultures induces the expression of nod genes, leading to higher levels of Nod factor production by B. japonicum cells. Soybean plants inoculated with B. japonicum cells that had been pre-incubated with Ge, MeJA, or both formed more nodules with more dry weight than plants treated with noninduced inoculant. This is the first report that MeJA-induced B. japonicum increased nodule number and nodule weight under the complex regime of field conditions. We have previously shown that MeJA-preincubated B. japonicum increased nodule number and weight under optimal and suboptimal RZT conditions under controlled environment conditions (Mabood and Smith, 2005). Preincubation of B. japonicum with MeJA also promoted soybean plant growth and grain yield under field conditions (Mabood et al., 2005).
Low temperatures inhibit GE biosynthesis and rhizosecretion from soybean roots (Zhang and Smith, 1996a). They also inhibit the expression of nod genes by B. japonicum (Zhang et al., 1996), thus reducing the production of Nod factors (also known as lipo-chitooligosaccharides) (Zhang et al., 2002; McKay and Djordjevic, 1993). Previous studies have shown that preincubation of Bradyrhizobium with GE helps overcome low soil temperature inhibition of soybean nodulation under controlled environment conditions (Zhang and Smith, 1995) and low-temperature spring field conditions (Zhang and Smith, 1997). Because the spring and early summer of 2002 were cooler than the long-term average (Fig. 2), the preincubation of bacterial cells with Ge, MeJA, or both might have been effective in increasing soybean nodule number and weight.
Nodule number and dry weight were different between plants at the two sites (Table 1). Plants growing at the sandy-loam site had more nodules and more nodule dry weight at both harvests than plants growing at the clay-loam site (Table 1), indicating that differences in soil type and/or planting date resulted in different plant nodulation patterns. Physical and chemical properties of soil are known to affect nodule formation and subsequent nodule growth (Gibson, 1971).
Shoot Nitrogen Yield and Total Nitrogen Fixed at the R3 Stage
At the R3 developmental stage, there was a difference (P < 0.05) among inducer treatments for shoot N yield at either site. Preincubation of B. japonicum with Ge, MeJA, and both increased shoot N yield at the sandy- and clay-loam sites, as compared with the uninduced control treatment (receiving B. japonicum inoculant only) (Table 2). At the clay-loam site, preincubation of B. japonicum strain 532C with Ge, MeJA, or both resulted in 11.8, 19.8, and 10.1% increases, respectively, for shoot N yield over the control treatment, whereas preincubation of strain USDA3 with Ge, MeJA, or both caused 18.1, 9.0, and 23.3% increases, respectively, for shoot N yield over the control. At the sandy-loam site, strain 532C preincubated with Ge, MeJA, or both resulted in 9.5, 12.8, and 12.8% increases, respectively, for shoot N yield, whereas for strain USDA3, the corresponding figures were 7.9, 5.9, and 16.0%, respectively (Table 2). Given that the amount of N extracted from the soil should be similar for control and inducer treatments, the differences between the two amount to the difference in total N fixed. There was no difference (P < 0.05) in shoot N yield between the two tested strains at either site (Table 2).
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Table 2. Effect of pre-incubation of Bradyrhizobium japonicum with genistein (Ge) (20 µM) and methyl jasmonate (MeJA) (50 µM) alone or in combination on soybean shoot N content (kg ha–1) and total fixed N (kg ha–1) at R3 developmental stage at two sites with contrasting soil types and different planting dates.
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Total N fixation was affected (P < 0.05) by inducer treatments at both sites. At the clay-loam site, preincubation of B. japonicum with Ge, MeJA, or both resulted in 10.9, 19.6, and 12.2% increases, respectively, for total N fixed over the control treatment, whereas preincubation of strain USDA3 with Ge, MeJA, or both caused 18.2, 11.8, and 23.1% increases, respectively, for total N fixed over the control. At the sandy-loam site, strain 532C preincubated with Ge, MeJA, or both resulted in 7.5, 6.1, and 8.1% increases, respectively, for total N fixed, whereas for strain USDA3, these figures were 9.4, 10.5, and 20.1%, respectively (Table 2). The increased N fixation by plants receiving bacterial cultures induced with Ge, MeJA, or both was related to increases in nodule number and nodule dry matter per plant (Table 1). At both sites, the amount of N fixed was related to nodule number per plant (R2 = 0.6461, P < 0.05 at the sandy-loam site; R2 = 0.6308, P < 0.05 at the clay-loam site) and nodule dry weight per plant (R2 = 0.7614, P < 0.05 at the sandy-loam site; R2 = 0.5606, P < 0.05 at the clay-loam site). We have previously shown that preincubation of B. japonicum with methyl jasmonate enhanced the amount of N fixed by soybean plants under controlled environment conditions (Mabood and Smith, 2005). There was no difference (P < 0.05) in shoot N fixed between the two tested strains at either site (Table 2).
Our data showed that site had a large effect on the ability of soybean plants to fix N. Plants growing at the sandy-loam site fixed more N than plants growing at the clay-loam site (Table 2). The superior performance of plants at the sandy-loam soil was probably due, for the most part, to the greater nodule number and dry weight (Table 1) at this site as compared with the clay-loam site.
Seed Nitrogen Yield and Nitrogen Fixed
Inducer molecule treatments increased seed N yield and seed N fixed at both sites (P < 0.05). There was no difference between the two tested strains for seed N yield and seed N fixed at either site (Table 3). At both sites, the highest seed N yield and seed N fixed were obtained for the plants receiving inoculants induced with Ge + MeJA. The control plants had the lowest N yield and seed N fixed. At the sandy-loam site, incubation of B. japonicum strain 532C with inducers showed 12.37, 13.42, and 37% increases in seed N fixed, for Ge, MeJA, and both over control, whereas incubation of strain USDA3 with inducers resulted in 8.4, 6.6, and 10.78% increases for Ge, MeJA, and both over the control. At the clay-loam site, incubation of B. japonicum strain 532C with inducers resulted in 9.19, 10.73, and 1.61% more seed fixed N than the control for Ge, MeJA, and both, respectively, whereas incubation of strain USDA3 with inducers resulted in 9.53, 10.89, and 4.35% more than the control, for Ge, MeJA, and both, respectively.
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Table 3. Effect of pre-incubation of Bradyrhizobium japonicum with genistein (Ge) (20 µM) and methyl jasmonate (MeJA) (50 µM) alone or in combination on soybean seed N yield (kg ha–1) and N fixed (kg ha–1) at the harvest maturity stage (R8) of soybean plants at two sites with contrasting soil types and different planting dates.
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The increase in seed N yield due to Ge treatment corroborates previous findings (Belkheir et al., 2000; Pan et al., 1998; Zhang and Smith, 1996b). Because the mechanism of action of MeJA is similar to that of Ge, we speculate that MeJA-induced increases in seed N yield are due to a more rapid nodulation and onset of N fixation, as previously reported with Ge. When bacterial cells were induced simultaneously with Ge and MeJA, there was some synergy between these inducers for seed N yield. These findings, and especially the increases in N in plant tissues, argue strongly that the effect of Ge and MeJA inducers followed from an earlier onset of N2 fixation and increased total N fixation.
Site had a large effect on the soybean seed N yield. Plants growing at the sandy-loam site had greater seed N yields and N fixed than those growing at the clay-loam site (Table 3). The increased seed N yield and seed N fixed by plants growing at the sandy-loam site was probably related to nodule number and nodule dry weight (Table 1) per plant. At both sites, there was a relationship between nodule number per plant (R2 = 0.4440, P < 0.05 at the sandy-loam site; R2 = 0.4775, P < 0.05 at the clay-loam site), nodule dry weight per plant (R2 = 0.6996, P < 0.05 at the sandy-loam site; R2 = 0.7454, P < 0.05 at the clay-loam site), and the amount of seed N fixed. The amount of seed N fixed was also correlated with grain yield at both sites (R2 = 0.6257, P < 0.05 at the sandy-loam site; R2 = 0.6424, P < 0.05 at clay-loam site). Grain yield data are reported in Mabood et al. (2005).
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CONCLUSIONS
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The stimulative effect of Ge on N fixation and growth of soybean plants under field conditions is well documented; however, there has been no previous study investigating the use of B. japonicum inoculum induced with MeJA, alone or in combination with Ge, on soybean nodulation and N fixation. From this experiment we provide data from two different field experiments conducted on different soil types with contrasting physical properties and different planting dates to demonstrate the stimulative effects of MeJA alone or in combination with Ge on nodulation and N fixation by soybean plants. Our results show that Ge (20 µM), MeJA (50 µM), or both inducers together increased plant nodulation, N fixation, and growth.
Site had large effects on the ability of plants to produce nodules and fix N. Plants growing at the sandy-loam site produced more nodules with more nodule dry weight, leading to enhanced N fixation. Plants growing at the clay-loam site produced comparatively fewer nodules with less nodule weight than the sandy-loam site. Thus, the amount of N fixed was lower than the sandy-loam site.
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ACKNOWLEDGMENTS
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We thank the Natural Science and Engineering Research Council of Canada for Discovery grant funds to support this work.
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