Determining Nodulation Regulatory (Rj) Genes of Myanmar Soybean Cultivars and Their Symbiotic Effectiveness with Bradyrhizobium japonicum USDA110


Soybean (Glycine max L.) plays an essential role in human nutrition as a protein source, and in plant nutrition as a N source. The rate of N fixation varies depending on the cultivars and compatibility between the inoculated Rhizobium strain and the host cultivar. Characterizing the nodulation regulatory (Rj) genes is necessary to determine the compatibility of cultivars and Rhizobium strains. Rj genes were previously identified based on inoculation tests and PCR analyses. The six cultivars Yezin-3, Yezin-7, Yezin-11, Shan Seine (Local), Madaya (Local), and Hinthada (Local) were identified as harboring the Rj4 gene. Two cultivars, Yezin-6 and Yezin-8, were classified as non-Rj-gene harboring. Two other cultivars, Yezin-9 and Yezin-10, were identified as Rj3- and Rj2Rj3-gene harboring, respectively. Ours is the first report on Rj3- and Rj2Rj3-gene harboring cultivars in Myanmar. We evaluated Myanmar soybean cultivars for symbiotic effectiveness, relying on the standard strain Bradyrhizobium japonicum USDA110. In our first experiment, the soybean cultivar Yezin-11 (Rj4) showed the highest N fixing potential. Based on their potential for fixing N and nodulation, the top six soybean cultivars were Yezin-11 (Rj4), Yezin-9 (Rj3), Yezin-6 (non-Rj), Yezin-8 (non-Rj), Yezin-3 (Rj4) and Yezin-10 (Rj2Rj3). These cultivars were selected for a second experiment, which revealed that the N fixation, nodulation, and plant growth of Yezin-11 (Rj4) *Corresponding author. A. Z. Htwe et al. 2800 were superior to the other cultivars. We conclude that Yezin-11 (Rj4) is the most efficient cultivar for nodulation and N fixation when inoculated with B. japonicum USDA110.

Share and Cite:

Htwe, A. , Saeki, Y. , Moe, K. and Yamakawa, T. (2015) Determining Nodulation Regulatory (Rj) Genes of Myanmar Soybean Cultivars and Their Symbiotic Effectiveness with Bradyrhizobium japonicum USDA110. American Journal of Plant Sciences, 6, 2799-2810. doi: 10.4236/ajps.2015.618276.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] MOAI (2013) Myanmar Agriculture in Brief. Ministry of Agriculture and Irrigation, Naypyitaw.
[2] CSO (2006) Myanmar Agricultural Statistics (1992-1993 to 2004-2005). Central Statistical Organization, Ministry of National Planning and Economic Development, Yangon.
[3] Unkivich, M.J. and Pate, J.S. (2000) An Appraisal of Recent Field Measurements of Symbiotic N2 Fixation by Annual Legumes. Field Crop Research, 65, 211-228.
[4] van Kessel, C. and Hartley, C. (2000) Agricultural Management of Grain Legumes: Has It Led to An Increased in Nitrogen Fixation? Field Crop Research, 65, 165-181.
[5] Van, K., Kim, M.Y. and Lee, S.H. (2007) Genomic of Root Nodulation. Genomic-Assisted Crop Improvement, 2, 435-452.
[6] Hayashi, M., Saeki, Y., Haga, M., Harada, K., Kouchi, H. and Umehara, Y. (2012) A Review: Rj (rj) Genes Involved in Nitrogen-Fixing Root Nodule Formation in Soybean. Breeding Science, 61, 544-553.
[7] Williams, L.F. and Lynch, D.L. (1954) Inheritance of a Non-Nodulating Character in the Soybean. Agronomy Journal, 46, 28-29.
[8] Caldwell, B.E. (1966) Inheritance of a Strain-Specific Ineffective Nodulation in Soybeans. Crop Science, 6,427-428.
[9] Caldwell, B.E., Hinson, K. and Johnson, H.W. (1966) A Strain-Specific Ineffective Nodulation Reaction in the Soybean Glycine max L. Merrill. Crop Science, 6, 495-496.
[10] Vest, G. (1970) Rj3-A Gene Conditioning Ineffective Nodulation. Crop Science, 10, 34-35.
[11] Vest, G. and Caldwell, B.E. (1972) Rj4—A Gene Conditioning Ineffective Nodulation in Soybean. Crop Science, 12, 692-693.
[12] Trese, A.T. (1995) A Single Dominant Gene in McCall Soybean Prevents Effective Nodulation with Rhizobium fredii USDA257. Euphytica, 81, 279-282.
[13] Ishizuka, J., Suemasu, Y. and Mizogami, K. (1991) Preference of Rj-Soybean Cultivars for Bradyrhizobium japonicum for Nodulation. Soil Science and Plant Nutrition, 37, 15-21.
[14] Ishizuka, J., Yokoyama, A. and Suemasu, Y. (1991) Relationship between Serotypes of Bradyrhizobium japonicum and Their Compatibility with Rj-Cultivars for Nodulation. Soil Science and Plant Nutrition, 37, 23-30.
[15] Minami, M., Yamakawa, T., Yamamoto, A., Akaso, S. and Saeki, Y. (2009) Estimation of Nodulation Tendency among Rj-Genotype Soybeans Using Bradyrhizobial Community Isolated from an Andosol. Soil Science and Plant Nutrition, 55, 65-72.
[16] Saeki, Y., Akagi, I., Takaki, H. and Nagatomo, Y. (2000) Diversity of Indigenous Bradyrhizobium Strains Isolated from Three Different Rj-Soybean Cultivars in Terms of Randomly Amplified Polymorphic DNA and Intrinsic Antibiotic Resistance. Soil Science and Plant Nutrition, 46, 917-926.
[17] Saeki, Y., Kaneko, A., Hara, T., Suzuki, K., Yamakawa, T., Nguyen, M.T., Nagatomo, Y. and Akao, S. (2005) Phylogenetic Analysis of Soybean Nodulating Rhizobia Isolated from Alkaline Soils in Vietnam. Soil Science and Plant Nutrition, 51, 1043-1052.
[18] Saeki, Y., Minami, M., Yamamoto, A. and Akao, S. (2008) Estimation of the Bacterial Community Diversity of Soybean-Nodulating Bradyrhizobia Isolated from Rj-Genotype Soybeans. Soil Science and Plant Nutrition, 54, 718-724.
[19] Soe, K.M., Yamakawa, T., Hashimoto, S. and Sarr, P. (2013) Phylogenetic Diversity of Indigenous Soybean Bradyrhizobia from Different Agro-Climatic Regions in Myanmar. Science Asia, 39, 574-583.
[20] Soe, K.M. and Yamakawa, T. (2013) Evaluation of Effective Myanmar Bradyrhizobium Strains Isolated from Myanmar Soybean and Effects of Coinoculation with Streptomyces griseoflavus P4 for N Fixation. Soil Science and Plant Nutrition, 59, 361-370.
[21] Soe, K.M. and Yamakawa, T. (2013) Low-Density Co-Inoculation of Myanmar Bradyrhizobium yuyanmingense MAS34 and Streptomyces griseoflavus P4 to Enhance Symbiosis and Seed Yield in Soybean Varieties. American Journal of Plant Science, 4, 1879-1892.
[22] Yamakawa, T., Eriguchi, M., Hussain, A.K.M.A. and Ishizuka, J. (1999) Soybean Preference for Bradyrhizobium japonicum for Nodulation: Nodulation by Rj2Rj3Rj4-Genotypes Isolated from the Progenies of a Cross between Soybean cv. ICA-2 (Rj2Rj3) and Hill (Rj4). Soil Science and Plant Nutrition, 45, 461-469.
[23] Yamakawa, T., Hussain, A.K.M.A. and Ishizuka, J. (2003) Soybean Preference for Bradyrhizobium japonicum for Nodulation Occupation of Serogroup USDA110 in Nodules of Soybean Plants Harboring Various Rj-Genes Grown in a Field. Soil Science and Plant Nutrition, 49, 835-841.
[24] Yang, S., Tang, F., Gao, M., Krishnan, H.B. and Zhu, H. (2010) R Gene-Controlled Host Specificity in the Legume- Rhizobia Symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 107, 18735-18740.
[25] Tang, F., Yang, S., Liu, J., Gao, M. and Zhu, H. (2014) Fine Mapping of the Rj4 Locus, a Gene Controlling Nodulation Specificity in Soybean. Molecular Breeding, 33, 691-700.
[26] Hayashi, M., Shiro, S., Kanamori, H., Mori-Hosokawa, S., Sasaki-Yamagata, H., Sayama, T., Nishioka, M., Takahashi, M., Ishimoto, M., Kataoyose, Y., Kaga, A., Harada, K., Kouchi, H., Saeki, Y. and Umehara, Y. (2014) A Thaumatin-Like Protein, Rj4, Controls Nodule Symbiotic Specificity in Soybean. Plant Cell Physiology, 55, 1679-1689.
[27] Ishizuka, J., Kim, S.D., Hussain, A.K.M.A. and Yamakawa, T. (1993) Soybean Preference for Bradyrhizobium japonicum for Nodulation: Isolation of Rj2Rj4-Lines from the Cross of Soybean cvs. IAC-2 (Rj2) and Hill (Rj4). Soil Science and Plant Nutrition, 39, 79-86.
[28] Nakano, Y., Yamakawa, T., Ikeda, M. and Ishizuka, J. (1997) Nodulation of Rj-Soybean Varieties with Rhizobium fredii USDA193 under Limited Supply of Nutrients. Soil Science and Plant Nutrition, 43, 929-932.
[29] Kuykendall, L.D. (1979) Transfer of R Factors to and between Genetically Marked Sublines of Rhizobium japonicum. Applied Environmental Microbiology, 37, 862-866.
[30] Klubeck, B.P., Hendrickson, L.L., Zablotowicz, R.M., Skwara, J.E., Varsa, E.C., Smith, S., Isleib, T.G., Maya, J., Valdes, M., Dazzo, F.B., Todd, R.L. and Walgenback, D.D. (1988) Competitiveness of Selected Bradyrhizobium japonicum Strains in Midwestern USA Soils. Soil Science Society American Journal, 52, 662-666.
[31] Somasegaran, P. and Hoben, H.J. (1994) Handbook for Rhizobia: Methods in Legumes-Rhizobium Technology. Springer-Verlag Inc, New York, 450.
[32] Denarie, J., Debelle, E. and Rosenberg, C. (1992) Signalling and Host Range Variation in Nodulation. Annual Review Microbiology, 46, 446-453.
[33] Perret, X., Staechelin, C. and Brouthton, W.J. (2000) Molecular Basis of Symbiotic Promiscuity. Microbiology and Molecular Biology Reviews, 64, 180-201.
[34] Boonkerd, N. and Singleton, P. (2002) Production of Rhizobium Biofertilizer. In: Kannaiyan, S., Ed., Biotechnology of Biofertilizers, Narosa Publishing House, New Delhi, 122-128.
[35] Devine, T.E. and Kuykendall, L.D. (1996) Host Genetic Control of Symbiosis in Soybean (Glycine max L.). Plant Soil, 186, 173-187.
[36] Devine, T.E. and Breithaupt, B.H. (1981) Frequencies of Nodulation Response Alleles, Rj2 and Rj4 in Soybean Plant Introductions and Breeding Lines. USDA Technical Bulletin No. 2618.
[37] Soe, K.M., Bhromsiri, A., Karladee, D. and Yamakawa, T. (2012) Effects of Endophytic actinomycetes and Bradyrhizobium japonicum Strains on Growth, Nodulation, Nitrogen Fixation and Seed Weight of Different Soybean Varieties. Soil Science and Plant Nutrition, 58, 319-325.
[38] Aung, T.T., Tittaburt, P., Boonkerd, N. and Herridge, D. (2013) Co-Inoculation Effects of Bradrhizobium japonicum and Azospirillum sp. on Competitive Nodulation and Rhizosphere Eubacterial Community Structures of Soybean under Rhizobia-Established Soil Conditions. African Journal of Biotechnology, 12, 2850-2862.
[39] Wani, S.P., Rupela, O.P. and Lee, K.K. (1995) Sustainable Agriculture in a Semiarid Tropic through Biological Nitrogen Fixation in Grain Legume. Plant Soil, 174, 29-49.
[40] Thabgaraju, M. and Werner, D. (2004) Indigenous Strains of Rhizobia and Their Performance in Specific Regions of India. In: Werner, D., Ed., Biological Resources and Migration, Springer-Verlag, Berlin, 174.
[41] Hungria, M. and Bohrer, T.R.J. (2000) Variability of Nodulation and Dinitrogen Fixation Capacity among Soybean Cultivars. Biology and Fertility of Soils, 31, 45-52.
[42] Nohara, T., Nakayama, N., Nakamura, T., Takahashi, M., Maruyama, S., Arihara, J. and Shimada, S. (2006) Cultivar Differences of Nitrogen Fixation Capacity and Its Contribution to Nitrogen Accumulation in Soybean Grown in the Field with a High Soil Nitrate Level. Japanese Journal of Crop Science, 75, 350-359.
[43] Htwe, A.Z., Yamakawa, T., Sarr, P.S. and Sakata, T. (2015) Diversity and Distribution of Soybean-Nodulation Bradyrhizobia Isolated from Major Soybean-Growing Regions in Myanmar. African Journal of Microbiology Research, 9, 2183-2196.

Copyright © 2022 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.