Rhizobium leguminosarum bv. viciae sp. inoculation improves the agronomic efficiency of N of common bean (Phaseolus vulgaris L.)
© Argaw and Akuma. 2015
Received: 27 March 2015
Accepted: 7 July 2015
Published: 25 July 2015
Due to common bean derives lower nitrogen (N) from symbiotic N2-fixation, it requires N either from inorganic fertilizer or soil N. Field experiments were conducted at four locations to evaluate the effect of Rhizobium leguminosarum bv. phaseoli inoculation on agronomic efficiency of N of common bean var. Dursitu major growing areas of eastern Ethiopia.
Six levels of inorganic N (0, 20, 40, 60, 80 and 100 kg N ha−1) and two inoculation treatments (uninoculated and inoculated) were factorially combined and laid out in randomized completely block design, replicated three times.
AE-N, nodule number per plant (NN) and nodule dry weight per plant (NDW) decreased with N rates of application beyond 20 kg N ha−1. The highest AE-Ns at Babillae, Fedis and Haramaya sites were obtained from 20 kg N ha−1 applied with Rhizobium inoculation while 40 kg N ha−1 supplied with Rhizobium inoculation at Hirna site. Regardless of experimental sites, inoculation improved AE-N. A positive relationship between AE-N and NDW was also observed in all experimental sites. Significant increase in grain yield with increasing rates of N application was also observed.
Hence, it can be concluded that inoculation is recommendable to increases the efficient utilization of applied Mineral N.
Common bean (Phaseolus vulgaris L.) is the most important food legume worldwide, providing the main source of protein for more than 300 million people, supplying about 20% of the protein intake per person (CIAT 2001; Broughton et al. 2003). Despite the fact that some grain yield gain recorded over the last decades, common bean production is still very low in many regions of sub-Saharan African (SSA). Average dry bean yield in most developing countries are very much less than that of potential, indicating that common bean production could be improved by increasing yields per unit land area (Yan et al. 1995). In Ethiopia, common bean is one of the major grain legumes cultivated, with its production centred in small farmers’ fields where the use of N fertilizer is limited and average yields are low, usually less than 1 ton ha−1 (CSA 2013). While under experimental condition, the productivity of common bean at experimental site has obtained up to 4,517 kg ha−1 (IAR 1997, 1998; Assefa et al. 2006). The main causes of low productivity at farmer fields are a poor technology level, utilization of low agricultural input and cropping in low fertility soils, especially with low N content (Haile 1990; Beebe et al. 2013). Low soil fertility is one of the most important yield-limiting factors in most of the bean-producing regions of Ethiopia (Tana and Fininsa 2006). Among essential plant nutrients, nitrogen (N) is the most important limiting nutrient for crop production in the tropics, including Ethiopia (Sanchez 1976). In Latin American, the yield losses due to N deficiency has been recorded up to 45% when compared to the N fertilized plants (Thung and Rao 1999). This indicates the need for inorganic N application and/or a search for more effective rhizobial strains to enhance the growth and grain yield of common bean.
Use of nitrogenous fertilizers by smallholder farmers to increase crop production in SSA has been limited due to unaffordable by many subsistent farmers. Beside the fact that common bean recovered usually less than 50% of the applied N fertilizer (dos Santos and Fageria 2007, 2008). These conditions have therefore necessitated an approach to crop production that emphasizes biological N2 fixation (BNF), with programs for rhizobial strain selection with superior symbiotic performance at a low cost. However, common bean is a promiscuous legume able to form symbioses with many rhizobial species and this nature result in poor N2 fixing plant compared to other grain legumes (Hardarson et al. 1993). N2 fixation in common bean can be increased through inoculation with certain highly efficient strains of Rhizobium leguminosarum biovar phaseoli (Hungria et al. 2000). Hungria et al. (2003) found comparable yield of common bean at 60 kg N ha−1 and Rhizobium tropici inoculated plants. Mulas et al. (2011) observed that inoculation of effective rhizobia attenuated intrinsic soil characteristics through the production of plant growth promoting properties beside N2 fixation (Atzorn et al. 1988; Ahemad and Khan 2011; Stajkovic et al. 2011). Studies, however, indicated that the performance of Rhizobium inoculation alone in the field conditions is not satisfactory (Graham 1981; Buttery et al. 1987). This indicates the need of some mineral N application even though fertilized with N owing to poor nodulation and lack of responses to inoculation under field conditions (Graham et al. 2003). Studies indicated that low rates of inorganic N application have been shown to enhance nodule formation and function but are not sufficient to achieve maximum yields (da Silva et al. 1993; Hungria et al. 2003). These authors also indicate that low levels of N fertilizer associated with the inoculation with selected rhizobial strains, can stimulate plant growth, N2 fixation and grain yield. Under these circumstances, inoculation trials must emphasize not only the benefits of bean inoculation, but also of the combination of that practice with N fertilization, in order to achieve a decrease in mineral N input whilst still obtaining maximum yields. However, there is little information on the effect of inoculation of elite Rhizobium sp. on use efficiency of N by common bean. Therefore the objectives of this experiment were to evaluate the effect of inoculation of elite Rhizobium sp. on use efficiency of N, nodulation and productivity of common bean in four representative experimental sites of Eastern Ethiopia.
Four major common bean growing areas of eastern Ethiopia were selected to determine the effect of Rhizobium on use efficiency of N, nodulation and yield of common bean. The experimental fields are located in the Hirna [N09°13.157″ and E041°06.488″ at an altitude of 1,808 m above sea level (m.a.s.l.)], Fedis (N09°06.941″ and E042°04.835″ at an altitude of 1,669 m.a.s.l.), Babillae (N09°13.234″ and E042°19.407″ at 1,669 m.a.s.l.) and Haramaya (N09°24.954″ and E042°02.037″ at an altitude of 2,020 m.a.s.l.) agricultural research centers. These experiments were conducted during 2012 cropping season.
Soil analysis of experimental sites before sowing
pH in H2O
EC (mS cm−1)
Organic carbon (%)
Total nitrogen (%)
Available P (mg kg−1)
Zn (mg kg−1)
B (mg kg−1)
NH4–N (mg kg−1)
NO3–N (mg kg−1)
Clay (g kg−1)
Silt (g kg−1)
Sand (g kg−1)
Sandy clay loam
Silty clay loam
Number of indigenous rhizobia of common bean g−1 soil
1.1 × 104
2.8 × 103
2.5 × 102
The population density of indigenous rhizobia nodulating common bean in the soils was determined by a plant infection technique (Vincent 1970). The seeds of common bean var. Dursitu were surface sterilized and germinated in petri dish that contained moist filter paper. One seedling was placed on pouches that contained Jensen’s N-free nutrient solution. Each seedling was inoculated with 1.0 ml of soil solution 2 weeks afterwards. Nodulation was examined 21 days after inoculation. The total numbers of nodulated seedling were converted into most probable number of indigenous rhizobia nodulating common bean g−1 of soil.
Sources of seeds and Rhizobium strain
A common bean var. Dursitu was supplied by Lowland pulses research project, Haramaya University, Ethiopia. Variety was selected based on their yield, their maturity time and recentness of year of release. Strain of Rhizbium spp. (HUPvR-16) was obtained from bio fertilizer research and production project, Haramaya University.
Agar slope of strain of Rhizobium was supplied by Soil microbiology research laboratory, Haramaya University. For purification, the isolate was preliminarily cultured in yeast extract mannitol agar medium (YEMA) (10 g mannitol, 1 g yeast-extract, 1 g KH2P04, 0.1 g NaCl, and 0.2 g MgS04·7H20 per liter, pH 6.8) and incubated at 28°C for 5 days. The pure colony of the isolate was later transferred to YEM broth medium with gentle shaking at 120 rpm for 5 days. By this procedure, the Rhizobium culture reached the middle or late logarithmic phase, and cell density in the culture was estimated by measuring optical density (OD) using spectrophotometer at 540 nm. Rhizobium inoculant was prepared by mixing 30 g of sterilised decomposed filter-mud with 15 ml of broth cultures of the appropriate Rhizobium strain in polyethylene bags. The moisture content of the inocula was 35% (w/w). After incubating the inoculated filer-mud for 2 weeks at 28°C, the count of the Rhizobium was 1 × 109 g−1 carrier material. Populations of rhizobia in the inoculants were determined by duplicate plate counts (Vincent 1970).
Field trials were conducted in order to investigate the effects of dual application of inorganic N fertilizer with different rate with and without inoculations of Rhizobium strain on Agronomic efficiency of N of common bean. The treatments of this experiment t were obtained by factorially combined six levels of inorganic N (0, 20, 40, 60, 80 and 100 kg N ha−1) and two inoculation treatments (inoculated and uninoculated). Then, the treatments were arranged in split plot with randomized complete block design (RCBD) with three replications. N rates of application were assigned as main plot treatment. Rhizobium treatments were applied as sub-plot treatments. N fertilizer in each level was divided into two equal parts; the first part of the N (20 kg N ha−1) was applied along the furrow by hand and incorporated before planting time, and the remaining parts were used in the flowering stages.
Results and discussion
Agronomic efficiency of N
Agronomic efficiency of N of common bean var. Dursitu obtained from selected areas of eastern Ethiopia with and without Rhizobium leguminosarum. bv. vicieae inoculation
Agronomic efficiency of N (%)
20 kg N ha−1
40 kg N ha−1
60 kg N ha−1
80 kg N ha−1
100 kg N ha−1
At Babillae site, the highest AE-N (10.16 and 11.6 kg kg−1) from inoculated and uninoculated treatments was obtained at 40 and 20 kg N ha−1, respectively. At Fedis site, 20 kg N ha−1 resulted in the highest AE-N (9.4 and 19.15 kg kg−1) along uninoculated and inoculated treatments, respectively. Similarly at Haramaya site, 20 kg N ha−1 application gave the highest AE-N (8.7 and 24.2 kg kg−1) along uninoculated and inoculated treatments, respectively. At Hirna site, 40 kg N ha−1 gave the highest AE-N (9.49 and 14.70 kg kg−1) among uninoculated and inoculated treatments, respectively. This indicates the need of inoculation to boost grain yield at Fedis site. This also indicates the need of lower rate of N when inoculated common bean with effective Rhizobium sp. for the highest AE-N. All study locations, the AE-N obtained from uninoculated treatment were ranged from 3.9 to 11.8 kg kg−1 which was previously reported for common bean by Fageria et al. (2013). They found the range of AE-N between 3.9 and 11.8 kg kg−1.
The highest AE-N of common bean at Babillae, Fedis and Haramaya were 15.29, 19.15 and 24.20 kg kg−1, respectively, all obtained from Rhizobium inoculation in conjunction with 20 kg N ha−1 application. The highest AE-N (14.70) from Hirna site was recorded from Rhizobium inoculation with 40 kg N ha−1 application. The lowest AE-N observed at Babillae and Hirna were 6.44 and 2.52 kg kg−1, respectively, from combined application of inoculation and 80 kg N ha−1. The lowest AE-N (2.48 and 3.50 kg kg−1) at 80 and 100 kg N ha−1, were obtained from Fedis and Haramaya sites, respectively.
Agronomic efficiency of N and nodulation
Nodule number per plant of common bean var. Dursitu obtained from selected areas of eastern Ethiopia with and without Rhizobium leguminosarum. bv. vicieae inoculation
Nodule number per plant
20 kg N ha−1
40 kg N ha−1
60 kg N ha−1
80 kg N ha−1
100 kg N ha−1
Nodule dry weight of common bean var. Dursitu obtained from selected areas of eastern Ethiopia with and without Rhizobium leguminosarum. bv. vicieae inoculation
Nodule dry weight (g/plant)
20 kg N ha−1
40 kg N ha−1
60 kg N ha−1
80 kg N ha−1
100 kg N ha−1
At Babile site, statistically higher NN and NDW was produced at 20 kg N ha−1 alone and in combination with inoculation of Rhizobium. This study, however indicated the non-significant difference of NDW obtained from 20 kg N ha−1 and the control treatment (without N application). The highest NN produced at Babile site was 161.67 at 20 kg N ha−1 with Rhizobium inoculation. At Fedis site, significantly higher NN and NDW were observed at 20 and 40 kg N ha−1 applications along uninoculated treatment. Along Rhizobium inoculation treatment, the control treatment induced the highest NN and NDW. Likewise, at Haramaya site, 20 kg N ha−1 application without inoculation resulted in significantly higher NN and NDW than the other treatments. Along Rhizobium inoculated, the control treatment produced the highest NN, although this NN was statistically similar with those NN produced at 20 and 40 kg N ha−1. At Haramaya site, 20 kg N ha−1 produced significantly higher NDW than those treatment of N application greater than 20 kg N ha−1. These results indicate that the inoculated isolate could fulfill the N needs of the plant in addition to the native soil total N at Fedis and Haramaya site as previously observed by Mnasri et al. (2007). The result obtained in these three sites agreed with previously reported by Daba and Haile (2000) who found that starter N with Rhizobium inoculation recommended to improve nodulation and yield of common bean in eastern Ethiopia. The application of a small amount of fertilizer N (15–30 kg N ha−1) enhances nodulation of different legume crops (da Silva et al. 1993; Tsai et al. 1993b; Hungria et al. 2003). The better performance of common bean in nodulation in inoculated treatments might be related with plant growth promoting activities of inoculated isolate, beside N2 fixation (Atzorn et al. 1988). They also found that plant growth hormones biosynthesis genes are closely linked to the genes for nodulation and N fixation. Wani et al. (2007) found that plant growth promoting rhizobia improved the nodule number by 23%.
The highest NN at Fedis and Haramaya were 146.67 and 282.00, respectively, at 20 kg N ha−1 application. Combined application of 20 kg N ha−1 and Rhizobium inoculation produced the higher NDW at Babillae and Haramaya, indicating the needs of Rhizobium inoculation and starter N to improve the nodule formation and development at these sites. Sole application of 20 kg N ha−1 resulted in the highest NDW at Fedis site, implying that this site could have higher native rhizobia nodulating common bean, thus inhibiting the effectiveness of inoculated isolate (Giller et al. 1998).
Regardless of the inoculation treatments, the highest NN and NDW at Hirna site were observed at the control treatments. The highest NN (216.67) at Hirna site was obtained from the control treatments with no inoculation of Rhizobium sp. This may indicate that soil had sufficient and effective number of rhizobia nodulating common bean (Theuri et al. 2006) and sufficient inherent soil N until the plant start fix N. Similar finding was reported by Chemining’wa et al. (2007) who found reduction in nodule number and nodule dry of common bean when added starter N fertilizer and improvement of these traits when inoculated Rhizobium alone.
Total biomass yield
Total biomass yield of common bean var. Dursitu obtained from selected areas of eastern Ethiopia with and without Rhizobium leguminosarum. bv. vicieae inoculation
Total biomass yield (kg ha−1)
20 kg N ha−1
40 kg N ha−1
60 kg N ha−1
80 kg N ha−1
100 kg N ha−1
The highest TBY (3,648.1 kg ha−1) at Babillae was produced at 100 kg N ha−1 applied with Rhizobium inoculation. This TBY was 387.3 kg ha−1 over that obtained from 100 kg N ha−1 alone. Similarly, at 100 kg N ha−1 supplied with Rhizobium sp. inoculation had the highest TBY (4,740.7 kg ha−1) at Fedis site. At Haramaya site, however, the highest TBY (6,474.1 kg ha−1) was obtained from 100 kg N ha−1 applied alone, indicating the presence of competitive and/or effective rhizobia in Haramaya soil. While at Hirna site, 100 kg N ha−1 with Rhizobium inoculation had the highest TBY (8,000.0 kg ha−1) which was 988.4 kg ha−1 over that obtained from 100 kg N ha−1 alone. This indicates that common bean cultivated at this site highly responded to Rhizobium inoculation in comparison to uninoculated treatment, although the soil had higher soil N and native rhizobia nodulating common bean. The lowest TBY at Babillae, Fedis, Haramaya and Hirna sites were 1,787.0, 2,077.0, 48.19.8 and 5,051.3 kg ha−1 respectively. The control treatment without inoculation gave the lowest TBY at Fedis, Haramaya and Hirna sites. While at Babillae site, the control treatment with inoculation resulted in the lowest TBY, indicating the non-responsiveness of common bean for inoculation without starter N.
Grain yield of common bean var. Dursitu obtained from selected areas of eastern Ethiopia with and without Rhizobium leguminosarum. bv. vicieae inoculation
Grain yield (kg ha−1)
20 kg N ha−1
40 kg N ha−1
60 kg N ha−1
80 kg N ha−1
100 kg N ha−1
N rated between 20 and 100 kg N ha−1 was exhibited non-significant effect on GY at Haramaya sites. In both inoculation treatments, the result indicated increases in GY with increasing rates of N application, although N rates of application reduced NN and NDW. Similar finding was observed on soybean by Osborne and Riedell (2011). At Hirna site, a significant increase in GY with increasing rates of N application without inoculation was observed. While along Rhizobium inoculation treatment, a significant improvement of GY was observed up to 40 kg N ha−1 but the rates above 40 kg N ha−1 exhibited a significant reduction of GY. The presence of competitive and efficient indigenous rhizobia (Thies et al. 1991) and high soil total N (Gan et al. 2009) could be the causes of need of low N application when applied in conjuction with inoculation.
The highest GY (2,089.54 kg ha−1) at Babillae site was obtained from 100 kg N ha−1 applied with Rhizobium inoculation. This GY was 259.45 kg ha−1 over those obtained from 100 kg N ha−1 alone. Similarly, at Fedis site, the highest GY (1,653.89 kg ha−1) was produced from 100 kg N ha−1 applied with Rhizobium inoculation. Similar finding on chickpea has been previously reported by Namvar et al. (2011) who found that inoculation together with N application gave better yield of chickpea than those obtained from N applied without inoculation. The highest GY (2,475.28 kg ha−1) at Haramaya site was obtained from sole application of 100 kg N ha−1. Similarly, improvement of common bean seed yield has been previously observed by Soratto et al. (2004) and Pelegrin et al. (2009). They found that the highest GY of common bean was obtained at 130 and 182 kg N ha−1 of N application in different tillage practices. Rhizobium inoculation applied with 40 kg N ha−1 gave the highest GY (2,441.57 kg ha−1) at Hirna site. Similarly, Hungria et al. (2003) found the highest common bean production at low rates of N applied with Rhizobium inoculation. On the other hand, the lowest GY at Babillae, Fedis and Haramaya were 996.39, 1,005.37 and 2,029.91 kg ha−1 obtained from Rhizobium inoculated without N application. This indicates that Rhizobium inoculation without N application in these experimental sites is insufficient to increase common bean yield even though, it was improved significantly the NN and NDW. However, the lowest GY (1,767.29 kg ha−1) at Hirna site was produced at the control treatment without inoculation implies that the native rhizobia are not effective in N2 fixation.
Plant total tissue N
Plant total tissue N of common bean var. Dursitu obtained from selected areas of eastern Ethiopia with and without Rhizobium leguminosarum. bv. vicieae inoculation
Plant total tissue N (%)
20 kg N ha−1
40 kg N ha−1
60 kg N ha−1
80 kg N ha−1
100 kg N ha−1
The result of this experiment indicated that inoculation of elite isolate of Rhizobium leguminosarum bv. Phaseoli improves the use efficiency of N by common bean in all experimental locations. Similarly the AE-N of common bean showed direct and positive relationship with nodule dry eight common beans, indicating the importance of nodulation and the consecutive output of this biological process on to improve efficient utilization of applied mineral N fertilizer. Accordingly, the starter amount of N fertilizer is recommended for all experimental sites to get the highest AE-N of common bean. Beside this, the soil inherent soil fertility status and indigenous rhizobia nodulating common bean affects effectiveness of sole application of N fertilizer and in combination with Rhizobium inoculation on the productivity of common bean. Rhizobium inoculation reduced the need of exogenous N application to get maximum common bean yield in the study sites.
Both of us participated starting from the development of the research idea, writing proposal and competing research grant and development of this manuscripts. But, mine was more participated in the management and collection of data from the field experiment that is way; I am the first author of this manuscript. Both authors read and approved the final manuscript.
This study received the financial support from Ethiopia Institute of Agricultural Research under the project ‘National Biofertilizer Development Project’. We also thank Girmaye Mekonnen, Berhanu Mengistu and Dejene Ayenew for the field experimental support and Dr. Mashilla Dejene for editorial support while writing the manuscript.
Compliance with ethical guidelines
Competing interests This research was funded by two governmental higher institutes. Haramaya University and Ethiopia Institute of Agricultural Research were provided and fully funded and covered the cost of this research. We, as author and principal investigator of this research, acknowledged and say thanks for those institutes supported this project. Both authors declare that they have no competing interests.
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