Morphological, genetic and symbiotic characterization of root nodule bacteria isolated from Bambara groundnuts (Vigna subterranea L. Verdc) from soils of Lake Victoria basin, western Kenya

Onyango Benson; Anyango Beatrice; Nyunja Regina; P. K. Koech; Robert A. Skilton; Stomeo Francesca

doi:10.7324/JABB.2015.3101

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Abstract

Low soil nitrogen (N) is a major constraint for sustainable crop production in smallholder farming systems in Africa. Grain legumes such as bambara groundnuts (Vigna subterranea L. Verdc). can form N fixing symbiotic association with root nodule bacteria collectively called ‘rhizobia’; in a process that can supply sufficient N for the legume and other crops under intercrop or in rotation. There is currently insufficient information on the diversity of indigenous rhizobial populations in the soils of Lake Victoria basin in western Kenya which associate with bambara groundnuts. In this study, one local bambara groundnut accession was used to trap root nodule bacteria from four soils obtained from farmers’ fields in Lake Victoria basin, western Kenya. Sixty four rhizobial isolates were obtained from the soils and morphologically characterized on Yeast Mannitol Extract Agar (YEMA) with Congo red and Bromothymol blue (BTB). Molecular evaluation was done using 16S rRNA genes to distinguish between the isolates. Results of morphological characterization showed majority (70%) of the isolates had very fast and fast growth rates on YEMA, 26% were intermediate while 3% were slow growers. The fast, very fast and some intermediates (70 %) showed positive acid reaction while the rest showed positive reaction in alkaline conditions on YEMA with BTB. The 16S rRNA gene sequences had greater than 97% similarity to diverse genera including Rhizobium sp., Bradyrhizobium sp., Burkholderia sp. and Agrobacterium sp. previously isolated from crop plants. Phylogenetic analysis of eighteen representative sequences showed the presence of three clades with Rhizobium and Agrobacterium type sequences occurring in a single clade while Bradyrhizobium and Burkholderia type sequences clustered into separate clades. In glasshouse experiments, seven isolates identified as Bradyrhizobium sp. and Burkholderia sp. and one Rhizobium sp. produced significantly (P≤0.05) higher nodule number per plant which were all effective with correspondingly high total biomass values of above 1.1 g per plant. The rest of the isolates showed significantly (P≤0.05) low levels of nodulation most of which were ineffective and resulted in significantly (P≤0.05) less plant dry matter. Isolates BAMKis12, BAMKis8, BAMKis4, BAMKbay8 and BAMsp3 genetically characterized as Bradyrhizobium sp. and Burkholderia sp. respectively can potentially be used as biofertilizers in inoculation programmes to improve the productivity of bambara groundnuts in the region.

Keyword: Bambara groundnut root nodule bacteria 16 rRNA genes symbiotic efficiency.

Citation:

Onyango BO, Koech PK, Anyango B, Nyunja RA, Skilton RA, Stomeo F. Morphological, genetic and symbiotic characterization of root nodule bacteria isolated from Bambara groundnuts (Vigna subterranea L. Verdc) from soils of Lake Victoria basin, western Kenya. J App Biol Biotech. 2015; 3 (01): 001-010. DOI: 10.7324/JABB.2015.3101

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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Reference

1. Sprent J. Nodulation in legumes. Kew, UK: Kew Publishing; 2001. p 156-157.
2. Chen W. M, Moulin L., Bontemps, C., Vandamme P., Bena G. and Boivin-Masson C. Legume symbiotic nitrogen fixation by beta-proteobacteria is wide spread in nature. Journal of Bacteriology. 2003; 185: 7266-7272. https://doi.org/10.1128/JB.185.24.7266-7272.2003
3. Mclean A. M., Finan T. M. and Sadowsky M. J. Genomes of the symbiotic nitrogen-fixing bacteria of the legumes. Plant Physiology. 2007; 144:615-622. https://doi.org/10.1104/pp.107.101634
4. Dai J., Liu X. and Wang Y. Genetic diversity and phylogeny of rhizobium isolated from Caraganamycrophylla growing in desert soils in Ningxia China. Genetic and Molecular Research. 2012; 11(3): 2683 – 2693. https://doi.org/10.4238/2012.June.25.5
5. Mothapo N.V., Grossman J. M., Maul J. E., Shi W. and Isleib T. Genetic diversity of resident soil rhizobia isolated from nodules of distinct hairy vetch (Viciavillosa Roth) genotypes. Applied Soil Ecology. 2013; 64: 201 – 213. https://doi.org/10.1016/j.apsoil.2012.12.010
6. Azam-Ali S. N., Sesay A., Karikari S. K., Massawe F. J., Aguitar-Manjarrez J., Bannayan M. and Hampson K. J. Assessing the potential of under-utilized crops: A case study using Bambara groundnut. Experimental Agriculture. 2001; 37: 433–472. https://doi.org/10.1017/S0014479701000412
7. Sprent J. I., Odee D. W and Dakora F. T. African legumes: A vital but under-utilized resource. Journal of Experimental Botany. 2010; 61 (5): 1257 – 1265. https://doi.org/10.1093/jxb/erp342
8. Mkandawire C. H. Review of Bambara groundnuts [Vigna subterranean (L.) Verdc.] production in Sub Saharan Africa. Agriculture Journal. 2007; 2(4): 464 – 470.
9. Jaetzold R., Schmidt H., Hortnez B. and Shisanya C. Ministry of Agriculture: Farm management handbook of Kenya Vol. 2 - Natural conditions and farm management information. 2ndEdtn Part A. West Kenya (Nyanza province). 2007; p. 1 – 81.
10. Doku E. V. and Karikari S. K. Bambara groundnut. Economic Botany. 1971; 25: 225 - 262. https://doi.org/10.1007/BF02860762
11. Gueye M., James E. K., Kierars M. and Sprent J. I. The development and structure of root nodules on bambara groundnuts [Voandzeia (Vigna) subterranea]. World Journal of Microbiology and Biotechnology. 1998; 4(3): 365-375. https://doi.org/10.1007/BF01096142
12. Kanu S. A. and Dakora F. D. Symbiotic nitrogen contribution and biodiversity of bacteria nodulating Psoralea species in the Cape Fynbos of South Africa. Soil Biology and Biochemistry. 2012; 54:68–76. https://doi.org/10.1016/j.soilbio.2012.05.017
13. Mohale C. K., Belane A. K. and Dakora F. D. Why is bambara groundnut able to grow and fix N2 under contrasting soil conditions in different agroecologies? A presentation at the 3rdinternational scientific conference on neglected and underutilized species on 26thSeptember, 2013 in Accra Ghana. 2013; p. 13-16.
14. Graham, P. H. Ecology of root nodule bacteria. In: Dilworth M. J., James E. K., Sprent I. J., and Newton E. W. (Eds), Nitrogen fixing leguminous symbioses. Springer Science+Business Media B. V., Dordrecht, Netherlands. 2008; pp 23 – 43.
15. Anyango B., Wilson K. J., Beynon J. L. and Giller K. E. Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Applied Environmental Microbiology. 1995; 61:4016-4021.
16. Chemining'wa G. and Vessey J. The abundance and efï¬cacy of Rhizobium leguminosarum bv. viciae in cultivated soils of the eastern Canadian prairie. Soil Biology and Biochemistry. 2006; 38: 294–302. https://doi.org/10.1016/j.soilbio.2005.05.007
17. Prevost D., Drouin P., Laberge S., Bertrand, A., Cloutier, J. and Levesque, G. Cold-adapted rhizobia for nitrogen fixation in temperate regions. Canadian Journal of Botany. 2003; 81:1153-1161. https://doi.org/10.1139/b03-113
18. Anderson J. M. and Ingram J. S. I. Tropical soil biology and fertility: A handbook of methods, 2nd edtn, CAB International, Wallingford, UK. 1993; P 85-93.
19. Giller K.E. Nitrogen fixation in tropical cropping systems. CAB International, Wallingford U.K. 2001; p. 423. https://doi.org/10.1079/9780851994178.0000
20. Bray R.H., and Kurtz L.T. Determination of total nitrogen, organic and available forms of phosphorus in soils. Soil Science. 1945; 59: 39 – 45. https://doi.org/10.1097/00010694-194501000-00006
21. Lindsay W. L. and Norvell W. A. Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Science Society of America Journal. 1978; 42: 421-428. https://doi.org/10.2136/sssaj1978.03615995004200030009x
22. Bala, A. Collection and maintenance of elite rhizobial strains: Milestone reference number 3.2.1 (N2 Africa: Putting Nitrogen fixation to work in smallholder farmers in Africa). www.N2Africa.org.
23. Woomer P. L., Karanja N., Kisamuli S. M., Murwira M. and Bala, A. A revised manual for rhizobium methods and standard protocols available in the project website: Milestone reference number 5.5.1 In: N2Africa: Putting Nitrogen fixation to work in smallholder farmers in Africa: www.N2Africa.org.
24. Eden P. A, Schmidt T. M, Blakemore R. P, Pace N. R Phylogenetic Analysis of Aquaspirillum magnetotacticum Using Polymerase Chain Reaction-Amplified 16S rRNA-Specific DNA. International Journal of Systematic Bacteriology. 1991; 41 (2): 324–325. https://doi.org/10.1099/00207713-41-2-324
25. Jiang H., Dong H., Zhang G., Yu B., Chapman L. R. and Fields M. W. Microbial diversity in water and sediment of Lake Chaka, an Athalassohaline Lake in Northwestern China. Applied and Environmental Microbiology. 2006; 72 (6): 3832–3845. https://doi.org/10.1128/AEM.02869-05
26. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., and Kumar S. MEGA6: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution. 2011; 28: 2731-2739. https://doi.org/10.1093/molbev/msr121
27. Tamura K. M., and Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences (USA). 2004; 101:11030-11035. https://doi.org/10.1073/pnas.0404206101
28. Lafay B. and Burdon J. J. Molecular diversity of rhizobia nodulating the invasive legume Cytisuss coparius in Australia. Journal of Applied Microbiology. 2006; 100: 1228-1238. https://doi.org/10.1111/j.1365-2672.2006.02902.x
29. Mierzwa B., Wdowiak-Wr\óbel S. and Malek W. Robinia pseudoacacia in Poland and Japan is nodulated by Mesorhizobium amorphae strains. Antonie van Leeuwenhoek. 2010; 97: 351-361. https://doi.org/10.1007/s10482-010-9414-8
30. Ulrich, A. & Zaspel, I. Phylogenetic diversity of rhizobial strains nodulating Robinia pseudoacacia L. Microbiology. 2000; 146:2997-3005. https://doi.org/10.1099/00221287-146-11-2997
31. Moschetti G., Peluso A., Protopapa A., Anastasio M., Pepe O. and Defez R. Use of nodulation pattern, stress tolerance, nodC gene amplification, RAPD-PCR and RFLP–16S rDNA analysis to discriminate genotypes of Rhizobium leguminosarum biovarviciae. Systematic and Applied Microbiology. 2005; 28: 619-631. https://doi.org/10.1016/j.syapm.2005.03.009
32. Martinez-Romero, E. Diversity of Rhizobium-Phaseolus vulgaris symbiosis: Overview and perspectives. Plant Soil. 2003; 252:11-23. https://doi.org/10.1023/A:1024199013926
33. Brockwell J., Pilka A. and Holliday R.A. Soil pH is a major determinant of the numbers of naturally occurring Rhizobium meliloti in non-cultivated soils in central New South Wales. Australian Journal of Experimental Agriculture. 1991; 31: 211-219. https://doi.org/10.1071/EA9910211
34. Slattery J. F., Pearce D. J., and Slattery W. J. Effects of resident rhizobial communities and soil type on the effective nodulation of pulse legumes. Soil Biology and Biochemistry. 2004; 36: 1339 -1346. https://doi.org/10.1016/j.soilbio.2004.04.015
35. Moulin L., Chen W. M., Béna G., Dreyfus B., and Boivin-Masson C. Rhizobia: The family is expanding. In: Nitrogen Fixation; Global perspectives. T. Finan, M. O'Brian, D. Layzell, K. Vessey and W. Newton. (Edts). CAB International. 2002; pp. 61-65.
36. Vandamme P., Goris J., Chen W. M., de Vos P. and Willems A. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp.nov., nodulate the roots of tropical legumes. Systematic and Applied Microbiology. 2002; 25: 507-512. https://doi.org/10.1078/07232020260517634
37. Chen W. M., James E. K., Chou J. H., Sheu S. Y., Yang S. Z. and Sprent, J.I. beta-Rhizobia from Mimosapigra, a newly discovered invasive plant in Taiwan. New Phytologist. 2005; 168: 661-675. https://doi.org/10.1111/j.1469-8137.2005.01533.x
38. Elliott G. N., Chen W. M., Chou J. H., Wang H. C., Sheu S. Y., Perin L., Reis M. V., Moulin L., Simon M. F., Bontemps C., Sutherland J. M., Bessi R., Faria S. M., Trinick M. J., Prescott A. R., Sprent J. I. and James E. K. Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytologist. 2007; 173: 168 –180. https://doi.org/10.1111/j.1469-8137.2006.01894.x
39. Ngugi G.W. Promoting the conservation and use of underutilized and neglected crops; A case study of Kenya. In: Bambara groundnut (Vigna subterranea L. Verdc.): Proceedings of the workshop on conservation and improvement of bambara groundnuts (Vigna subterranea L. Verdc.). Harare, Zimbabwe. Heller J. F. Begemann and Mushoga J. Edtrs. 1997; pp 84-112.
40. Bontemps C., Elliott G. N., Simon M. F., Dos Reis Junior F. B., Gross E., Lawton R. C., Neto N. E., de Fatima Loureiro M., De Faria S. M. Burkholderia species are ancient symbionts of legumes. Molecular Ecology. 2010; 19: 44–52. https://doi.org/10.1111/j.1365-294X.2009.04458.x
41. Young J. M., Kuykendall L. D., Martinez-Romero E., Kerr A. and Sawada H. A revision of Rhizobium (Frank, 1889), with an emended description of the genus and the inclusion of all species of Agrobacterium (Conn, 1942) and Allorhizobium undicola (de Lajudie et al., 1998) as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. International Journal of Systematic and Evolutionary Microbiology. 2001; 5: 89-103. https://doi.org/10.1099/00207713-51-1-89
42. Lindstrom K. and Young J. P. W. International committee on systematics of prokaryotes; Sub-committee on the taxonomy of Rhizobium and Agrobacterium. International Journal of Systematic and Evolutionary Microbiology. 2011; 61: 3089 – 3093. https://doi.org/10.1099/ijs.0.036913-0
43. Dilworth M. J., Howieson J. G., Reeve W. G., Tiwari R. P., and Glenn A. R. Acid tolerance in root nodule bacteria and selecting for it. Australian Journal of Experimental Agriculture. 2001; 41: 435-446. https://doi.org/10.1071/EA99155
44. Wang L. L., Wang E. T., Liu J., Li Y. and Chen W. X. Endophytic occupation of root nodules and roots of Melilotus dentatus by Agrobacterium tumefaciens. Microbiology and Ecology. 2006; 52: 436-443. https://doi.org/10.1007/s00248-006-9116-y
45. Howieson J. G., O'Hara G. W. and Carr S. J. Changing roles for legumes in Meditteranean Agriculture: Developments from an Australian perspective. Field Crops Research. 2000; 65: 107-122. https://doi.org/10.1016/S0378-4290(99)00081-7

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1. Sprent J. Nodulation in legumes. Kew, UK: Kew Publishing; 2001. p 156-157.

2. Chen W. M, Moulin L., Bontemps, C., Vandamme P., Bena G. and Boivin-Masson C. Legume symbiotic nitrogen fixation by beta-proteobacteria is wide spread in nature. Journal of Bacteriology. 2003; 185: 7266-7272. https://doi.org/10.1128/JB.185.24.7266-7272.2003

3. Mclean A. M., Finan T. M. and Sadowsky M. J. Genomes of the symbiotic nitrogen-fixing bacteria of the legumes. Plant Physiology. 2007; 144:615-622. https://doi.org/10.1104/pp.107.101634

4. Dai J., Liu X. and Wang Y. Genetic diversity and phylogeny of rhizobium isolated from Caraganamycrophylla growing in desert soils in Ningxia China. Genetic and Molecular Research. 2012; 11(3): 2683 – 2693. https://doi.org/10.4238/2012.June.25.5

5. Mothapo N.V., Grossman J. M., Maul J. E., Shi W. and Isleib T. Genetic diversity of resident soil rhizobia isolated from nodules of distinct hairy vetch (Viciavillosa Roth) genotypes. Applied Soil Ecology. 2013; 64: 201 – 213. https://doi.org/10.1016/j.apsoil.2012.12.010

6. Azam-Ali S. N., Sesay A., Karikari S. K., Massawe F. J., Aguitar-Manjarrez J., Bannayan M. and Hampson K. J. Assessing the potential of under-utilized crops: A case study using Bambara groundnut. Experimental Agriculture. 2001; 37: 433–472. https://doi.org/10.1017/S0014479701000412

7. Sprent J. I., Odee D. W and Dakora F. T. African legumes: A vital but under-utilized resource. Journal of Experimental Botany. 2010; 61 (5): 1257 – 1265. https://doi.org/10.1093/jxb/erp342

8. Mkandawire C. H. Review of Bambara groundnuts [Vigna subterranean (L.) Verdc.] production in Sub Saharan Africa. Agriculture Journal. 2007; 2(4): 464 – 470.

9. Jaetzold R., Schmidt H., Hortnez B. and Shisanya C. Ministry of Agriculture: Farm management handbook of Kenya Vol. 2 - Natural conditions and farm management information. 2ndEdtn Part A. West Kenya (Nyanza province). 2007; p. 1 – 81.

10. Doku E. V. and Karikari S. K. Bambara groundnut. Economic Botany. 1971; 25: 225 - 262. https://doi.org/10.1007/BF02860762

11. Gueye M., James E. K., Kierars M. and Sprent J. I. The development and structure of root nodules on bambara groundnuts [Voandzeia (Vigna) subterranea]. World Journal of Microbiology and Biotechnology. 1998; 4(3): 365-375. https://doi.org/10.1007/BF01096142

12. Kanu S. A. and Dakora F. D. Symbiotic nitrogen contribution and biodiversity of bacteria nodulating Psoralea species in the Cape Fynbos of South Africa. Soil Biology and Biochemistry. 2012; 54:68–76. https://doi.org/10.1016/j.soilbio.2012.05.017

13. Mohale C. K., Belane A. K. and Dakora F. D. Why is bambara groundnut able to grow and fix N2 under contrasting soil conditions in different agroecologies? A presentation at the 3rdinternational scientific conference on neglected and underutilized species on 26thSeptember, 2013 in Accra Ghana. 2013; p. 13-16.

14. Graham, P. H. Ecology of root nodule bacteria. In: Dilworth M. J., James E. K., Sprent I. J., and Newton E. W. (Eds), Nitrogen fixing leguminous symbioses. Springer Science+Business Media B. V., Dordrecht, Netherlands. 2008; pp 23 – 43.

15. Anyango B., Wilson K. J., Beynon J. L. and Giller K. E. Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Applied Environmental Microbiology. 1995; 61:4016-4021.

16. Chemining'wa G. and Vessey J. The abundance and efï¬cacy of Rhizobium leguminosarum bv. viciae in cultivated soils of the eastern Canadian prairie. Soil Biology and Biochemistry. 2006; 38: 294–302. https://doi.org/10.1016/j.soilbio.2005.05.007

17. Prevost D., Drouin P., Laberge S., Bertrand, A., Cloutier, J. and Levesque, G. Cold-adapted rhizobia for nitrogen fixation in temperate regions. Canadian Journal of Botany. 2003; 81:1153-1161. https://doi.org/10.1139/b03-113

18. Anderson J. M. and Ingram J. S. I. Tropical soil biology and fertility: A handbook of methods, 2nd edtn, CAB International, Wallingford, UK. 1993; P 85-93.

19. Giller K.E. Nitrogen fixation in tropical cropping systems. CAB International, Wallingford U.K. 2001; p. 423. https://doi.org/10.1079/9780851994178.0000

20. Bray R.H., and Kurtz L.T. Determination of total nitrogen, organic and available forms of phosphorus in soils. Soil Science. 1945; 59: 39 – 45. https://doi.org/10.1097/00010694-194501000-00006

21. Lindsay W. L. and Norvell W. A. Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Science Society of America Journal. 1978; 42: 421-428. https://doi.org/10.2136/sssaj1978.03615995004200030009x

22. Bala, A. Collection and maintenance of elite rhizobial strains: Milestone reference number 3.2.1 (N2 Africa: Putting Nitrogen fixation to work in smallholder farmers in Africa). www.N2Africa.org.

23. Woomer P. L., Karanja N., Kisamuli S. M., Murwira M. and Bala, A. A revised manual for rhizobium methods and standard protocols available in the project website: Milestone reference number 5.5.1 In: N2Africa: Putting Nitrogen fixation to work in smallholder farmers in Africa: www.N2Africa.org.

24. Eden P. A, Schmidt T. M, Blakemore R. P, Pace N. R Phylogenetic Analysis of Aquaspirillum magnetotacticum Using Polymerase Chain Reaction-Amplified 16S rRNA-Specific DNA. International Journal of Systematic Bacteriology. 1991; 41 (2): 324–325. https://doi.org/10.1099/00207713-41-2-324

25. Jiang H., Dong H., Zhang G., Yu B., Chapman L. R. and Fields M. W. Microbial diversity in water and sediment of Lake Chaka, an Athalassohaline Lake in Northwestern China. Applied and Environmental Microbiology. 2006; 72 (6): 3832–3845. https://doi.org/10.1128/AEM.02869-05

26. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., and Kumar S. MEGA6: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution. 2011; 28: 2731-2739. https://doi.org/10.1093/molbev/msr121

27. Tamura K. M., and Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences (USA). 2004; 101:11030-11035. https://doi.org/10.1073/pnas.0404206101

28. Lafay B. and Burdon J. J. Molecular diversity of rhizobia nodulating the invasive legume Cytisuss coparius in Australia. Journal of Applied Microbiology. 2006; 100: 1228-1238. https://doi.org/10.1111/j.1365-2672.2006.02902.x

29. Mierzwa B., Wdowiak-Wr\óbel S. and Malek W. Robinia pseudoacacia in Poland and Japan is nodulated by Mesorhizobium amorphae strains. Antonie van Leeuwenhoek. 2010; 97: 351-361. https://doi.org/10.1007/s10482-010-9414-8

30. Ulrich, A. & Zaspel, I. Phylogenetic diversity of rhizobial strains nodulating Robinia pseudoacacia L. Microbiology. 2000; 146:2997-3005. https://doi.org/10.1099/00221287-146-11-2997

31. Moschetti G., Peluso A., Protopapa A., Anastasio M., Pepe O. and Defez R. Use of nodulation pattern, stress tolerance, nodC gene amplification, RAPD-PCR and RFLP–16S rDNA analysis to discriminate genotypes of Rhizobium leguminosarum biovarviciae. Systematic and Applied Microbiology. 2005; 28: 619-631. https://doi.org/10.1016/j.syapm.2005.03.009

32. Martinez-Romero, E. Diversity of Rhizobium-Phaseolus vulgaris symbiosis: Overview and perspectives. Plant Soil. 2003; 252:11-23. https://doi.org/10.1023/A:1024199013926

33. Brockwell J., Pilka A. and Holliday R.A. Soil pH is a major determinant of the numbers of naturally occurring Rhizobium meliloti in non-cultivated soils in central New South Wales. Australian Journal of Experimental Agriculture. 1991; 31: 211-219. https://doi.org/10.1071/EA9910211

34. Slattery J. F., Pearce D. J., and Slattery W. J. Effects of resident rhizobial communities and soil type on the effective nodulation of pulse legumes. Soil Biology and Biochemistry. 2004; 36: 1339 -1346. https://doi.org/10.1016/j.soilbio.2004.04.015

35. Moulin L., Chen W. M., Béna G., Dreyfus B., and Boivin-Masson C. Rhizobia: The family is expanding. In: Nitrogen Fixation; Global perspectives. T. Finan, M. O'Brian, D. Layzell, K. Vessey and W. Newton. (Edts). CAB International. 2002; pp. 61-65.

36. Vandamme P., Goris J., Chen W. M., de Vos P. and Willems A. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp.nov., nodulate the roots of tropical legumes. Systematic and Applied Microbiology. 2002; 25: 507-512. https://doi.org/10.1078/07232020260517634

37. Chen W. M., James E. K., Chou J. H., Sheu S. Y., Yang S. Z. and Sprent, J.I. beta-Rhizobia from Mimosapigra, a newly discovered invasive plant in Taiwan. New Phytologist. 2005; 168: 661-675. https://doi.org/10.1111/j.1469-8137.2005.01533.x

38. Elliott G. N., Chen W. M., Chou J. H., Wang H. C., Sheu S. Y., Perin L., Reis M. V., Moulin L., Simon M. F., Bontemps C., Sutherland J. M., Bessi R., Faria S. M., Trinick M. J., Prescott A. R., Sprent J. I. and James E. K. Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytologist. 2007; 173: 168 –180. https://doi.org/10.1111/j.1469-8137.2006.01894.x

39. Ngugi G.W. Promoting the conservation and use of underutilized and neglected crops; A case study of Kenya. In: Bambara groundnut (Vigna subterranea L. Verdc.): Proceedings of the workshop on conservation and improvement of bambara groundnuts (Vigna subterranea L. Verdc.). Harare, Zimbabwe. Heller J. F. Begemann and Mushoga J. Edtrs. 1997; pp 84-112.

40. Bontemps C., Elliott G. N., Simon M. F., Dos Reis Junior F. B., Gross E., Lawton R. C., Neto N. E., de Fatima Loureiro M., De Faria S. M. Burkholderia species are ancient symbionts of legumes. Molecular Ecology. 2010; 19: 44–52. https://doi.org/10.1111/j.1365-294X.2009.04458.x

41. Young J. M., Kuykendall L. D., Martinez-Romero E., Kerr A. and Sawada H. A revision of Rhizobium (Frank, 1889), with an emended description of the genus and the inclusion of all species of Agrobacterium (Conn, 1942) and Allorhizobium undicola (de Lajudie et al., 1998) as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. International Journal of Systematic and Evolutionary Microbiology. 2001; 5: 89-103. https://doi.org/10.1099/00207713-51-1-89

42. Lindstrom K. and Young J. P. W. International committee on systematics of prokaryotes; Sub-committee on the taxonomy of Rhizobium and Agrobacterium. International Journal of Systematic and Evolutionary Microbiology. 2011; 61: 3089 – 3093. https://doi.org/10.1099/ijs.0.036913-0

43. Dilworth M. J., Howieson J. G., Reeve W. G., Tiwari R. P., and Glenn A. R. Acid tolerance in root nodule bacteria and selecting for it. Australian Journal of Experimental Agriculture. 2001; 41: 435-446. https://doi.org/10.1071/EA99155

44. Wang L. L., Wang E. T., Liu J., Li Y. and Chen W. X. Endophytic occupation of root nodules and roots of Melilotus dentatus by Agrobacterium tumefaciens. Microbiology and Ecology. 2006; 52: 436-443. https://doi.org/10.1007/s00248-006-9116-y

45. Howieson J. G., O'Hara G. W. and Carr S. J. Changing roles for legumes in Meditteranean Agriculture: Developments from an Australian perspective. Field Crops Research. 2000; 65: 107-122. https://doi.org/10.1016/S0378-4290(99)00081-7

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