A re-appraisal of the biology and terminology describing rhizobial strain success in nodule occupancy of legumes in agriculture

Plant and Soil

Volumn 348, Issue 1-2, 2011, Pages 255-267

  Yates, Ron John ^a,b   Howieson, John Gregory ^a   Reeve, Wayne Gerald ^a   O'Hara, Graham William ^a  

^a MURDOCH UNIVERSITY   (Australia)

^b DEPARTMENT OF AGRICULTURE AND FOOD WESTERN AUSTRALIA   (Australia)

Author keywords

Effectiveness; Legumes; Nitrogen fixation; Rhizobia; Selective nodulation

Indexed keywords

EXPERIMENTAL STUDY; GENOME; INOCULATION; LEGUME; NITROGEN FIXATION; NODULATION; RHIZOBACTERIUM; SOIL MICROORGANISM; SYMBIOSIS; TERMINOLOGY;

RHIZOBIACEAE;

EID: 80053565386     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-011-0971-z     Document Type: Review

References (129)

1. Aguilar OM, Riva O, Peltzer E (2004) Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centres of host diversification. Proc Nat Acad Sci USA 101: 13548-13553.
2. Amarger N (1981) Competition for nodule formation between effective and ineffective strains of Rhizobium meliloti. Soil Biol Biochem 13: 475-480.
3. Amarger N, Lobreau JP (1982) Quantitative study of nodulation competitiveness in Rhizobium strains. Appl Environ Microbiol 44: 583-588.
4. Anyango B, Wilson K, Giller K (1998) Competition in Kenyan soils between Rhizobium leguminosarum biovar phaseoli strain Kim5 and R. tropici strain CIAT899 using the gusA marker gene. Plant Soil 204: 69-78.
5. Baldwin IL, Fred EB (1929) Nomenclature of the root nodule bacteria of the Leguminosae. J Bact 17: 141-150.
6. Ballard RA, Charman N (2000) Nodulation and growth of pasture legumes with naturalised soil rhizobia 1. Annual Medicago spp. Aust J Exp Agric 40: 939-948.
7. Barran LR, Bromfield ESP (1997) Competition among rhizobia for nodulation of legumes. In: McKersie BD, Brown DCW (eds) Biotechnology and the Improvement of Forage Legumes. University Press, Cambridge, pp 343-374.
8. Bottomley PJ (1992) Ecology of Bradyrhizobium and Rhizobium. In: Stacy G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, NY, pp 293-348.
9. Boundy-Mills KL, Kosslack RM, Tully RE, Pueppke SG, Lohrke SM, Sadowsky MJ (1994) Induction of the Rhizobium fredii nod box-independent nodulation gene nolJ requires a functional nodD1 gene. Mol Plant-Micr Inter 7: 305-308.
10. Bringhurst RM, Cardon ZG, Gage DJ (2001) Galactosides in the rhizosphere: utilization by Sinorhizobium meliloti and development of a biosensor. Proc Nat Acad Sci USA 98: 4540-4545.
11. Brockhurst MA, Fenton A, Roulston B, Rainey PB (2006) The impact of phages on interspecific competition in experimental populations of bacteria. BMC Ecol 6: 19.
12. Brockwell J (2001) Sinorhizobium meliloti in Australian soils: population studies of the root-nodule bacteria for species of Medicago in soils of the Eyre Peninsula, South Australia. Aust J Exp Agric 41: 753-762.
13. Brockwell J, Katznelson J (1976) Symbiotic characteristics of Rhizobium trifolii from Israel in association with 10 species of Trifolium. Aust J Agric Res 27: 799-810.
14. Brockwell J, Bottomley PJ (1995) Recent advances in inoculant technology and prospects for the future. Soil Biol Biochem 27: 683-697.
15. Brockwell J, Hely FW, Neal-Smith CA (1966) Some symbiotic characteristics of rhizobia responsible for spontaneous, effective field nodulation of Lotus hispidus. Aust J Exp Agric Anim Hus 6: 365-370.
16. Brockwell J, Gault RR, Zorin M, Roberts MJ (1982) Effects of environmental variables on the competition between inoculum strains and naturalised populations of Rhizobium trifolium for nodulation of Trifolium subterraneum L. and on rhizobia persistence in the soil. Aust J Agric Res 33: 803-815.
17. Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174: 143-180.
18. Bromfield ESP (1984a) The preference for strains of Rhizobium meliloti by cultivars of Medicago sativa grown on agar. Can J Microbiol 30: 1179-1186.
19. Bromfield ESP (1984b) Variation in preference for Rhizobium meliloti within and between Medicago sativa cultivars grown in soil. Appl Environ Microbiol 48: 1231-1236.
20. Broughton WJ, Samprey U, Bohlool BB (1982) Competition for nodulation of Pisum sativum cv. Afghanistan requires live rhizobia and a plant component. Can J Microbiol 28: 162-168.
21. Broughton WJ, Jabbouri S, Perret X (2000) Keys to symbiotic harmony. J Bacteriol 182: 5641-5652.
22. Caldwell BE, Vest G (1968) Nodulation interactions between soybean (Glycine max) genotypes and serogroups of Rhizobium japonicum. Crop Sci 8: 680-682.
23. Chandra R, Pareek RP (1985) Role of host-genotype in effectiveness and competitiveness of chick pea (Cicer arientinum) rhizobium. Trop Agric (Trinidad) 62: 90-94.
24. Cregan PB, Keyser HH (1986) Host restriction of nodulation by Bradyrhizobium japonicum strain USDA 123 in soybean. Crop Sci 26: 911-916.
25. Date RA, Brockwell J (1978) Rhizobium strain competition and host interaction for nodulation. In: Wilson JR (ed) Plant relations in pastures. CSIRO press, Melbourne, Australia, pp 202-216.
26. Davis EO, Evans IJ, Johnston AWB (1988) Identification of nodX, a gene that allows Rhizobium leguminosarum bv. viciae strain TOM to nodulate Afghanistan peas. Mol Gen Genet 212: 531-535.
27. Denison RF (2000) Legume sanctions and the evolution of symbiotic cooperation by rhizobia. The Amer Natl 156: 567-576.
28. Denison RF, Kiers ET (2004) Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Let 237: 187.
29. Denton MD, Coventry DR, Howieson JG, Murphy PJ, Bellotti WD (2002) Competition between inoculated and naturalized R. leguminosarum bv. trifolii for nodulation of annual clovers in alkaline soils. Aust J Agric Res 53: 1019-1026.
30. Denton MD, Reeve WG, Howieson JG, Coventry DR (2003) Competitive abilities of common field isolates and a commercial strain of Rhizobium leguminosarum bv. trifolii for clover nodule occupancy. Soil Biol Biochem 35: 1039-1048.
31. Devine TE (1984) Inheritance of soybean nodulation response with a fast-growing strain of Rhizobium. J Heredity 75: 359-361.
32. Devine TE, Kuykendall LD (1996) Host genetic control of symbiosis in soybean (Glycine max L.). Plant Soil 186: 173-187.
33. Dowling DN, Broughton WJ (1986) Competition for nodulation of legumes. Ann Rev Microbiol 40: 131-157.
34. Downie JA, Parniske M (2002) Plant biology: locks, keys and symbioses. Nature 420: 369-370.
35. Ferrey ML, Graham PH, Russelle MJ (1994) Nodulation efficiency of Bradyrhizobium japonicum strains with genotypes of soybean varying in the ability to resist nodulation. Can J Microbiol 40: 456-460.
36. Firmin JL, Wilson KE, Carlson RW, Davies AE, Downie JA (1993) Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol Microbiol 10: 351-360.
37. George MLC, Robert F (1991) Autoregulatory response of Phaseolus vulgaris L. to symbiotic mutants of Rhizobium leguminosarum bv. phaseoli. Appl Environ Microbiol 57: 2687-2692.
38. Gibson AH (1968) Nodulation failure of Trifolium subterraneum L. cv. Woogenellup (syn. Marrar). Aust J Agric Res 19: 907-918.
39. Gibson AH, Curnow BC, Bergersen FJ, Brockwell J, Robinson AC (1975) Studies of field strains of Rhizobium trifolii associated with Trifolium subterraneum L. pastures in south-eastern Australia. Soil Biol Biochem 7: 95-102.
40. Graham PH (2008) Ecology of the root-nodule bacteria of legumes. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht, pp 23-43.
41. Hahn M, Studer D (1986) Competitiveness of a nif - Bradyrhizobium japonicum mutant against the wild-type strain. FEMS Microbiol Let 33: 143-148.
42. Hahn M, Hennecke H (1988) Cloning and mapping of a novel nodulation region from Bradyrhizobium japonicum by genetic complementation of a deletion mutant. Appl Environ Microbiol 54: 55-61.
43. Hardarson G, Jones DG (1979a) Effect of temperature on competition amongst strains of Rhizobium trifolii for nodulation of two white clover varieties. Ann Appl Biol 92: 229-236.
44. Hardarson G, Jones DG (1979b) The inheritance of preference for strains of Rhizobium trifolii by white clover (Trifolium repens). Ann Appl Biol 92: 329-333.
45. Hardarson G, Heichel GH, Vance CP, Barnes DK (1982a) Evaluation of alfalfa and Rhizobium meliloti for compatibility in nodulation and nodule effectiveness. Crop Sci 21: 562-567.
46. 2 fixation. Crop Sci 22: 55-58.
47. Hennecke H (1990) Nitrogen fixation genes involved in the Bradyrhizobium japonicum-soybean symbiosis. FEBS let 268: 422-426.
48. Herridge DF (2008) Inoculation technology for legumes. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht, pp 77-109.
49. Hogg B, Davies AE, Wilson KE, Bisseling T, Downie JA (2002) Competitive nodulation blocking of cv. Afghanistan pea is related to high levels of nodulation factors made by some strains of Rhizobium leguminosarum bv. viciae. Mol Plant Micro Intl 15: 60-68.
50. Holl FB (1975) Host plant control of the inheritance of dinitrogen fixation in the Pisum Rhizobium symbiosis. Euphytica 24: 767-770.
51. Holland AA (1966) Serological characteristics of certain root-nodule bacteria of legumes. Anton van Leeuwen J Micro Serol 32: 410-418.
52. Howieson JG, Ballard R (2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia - some contemporary thoughts. Soil Biol Biochem 36: 1261-1273.
53. Howieson JG, Ewing MA (1986) Acid tolerance in the Rhizobium meliloti-Medicago symbiosis. Aust J Agric Res 36: 55-64.
54. Howieson JG, Loi A, Carr SJ (1995) Biserrula pelecinus L. - a legume pasture species with potential for acid, duplex soils which is nodulated by a unique root-nodule bacteria. Aust J Agric Res 46: 997-1009.
55. Howieson JG, O'Hara GW, Carr SJ (2000) Changing roles for legumes in Mediterranean agriculture: developments from an Australian perspective. Field Crops Res 65: 107-122.
56. Hungria M, Franchini J, Campo R, Graham PH (2005) The importance of nitrogen fixation to soybean cropping in South America. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht, pp 25-42.
57. Ireland JA, Vincent JM (1968) A quantitative study of competition for nodule formation. Trans 9th Int Con Soil Sci Soc 2: 85-93.
58. Johnson HW, Means UM (1960) Interactions between genotypes of soybeans and genotypes of nodulating bacteria. Agr J 52: 651-654.
59. Jones DG, Russell PE (1972) The application of immunofluorescence techniques to host plant/nodule bacteria selectivity experiments using Trifolium repens. Soil Biol Biochem 4: 277-280.
60. Jones DG, Hardarson G (1979) Variation within and between white clover varieties in their preference for strains of Rhizobium trifolii. Ann Appl Biol 92: 221-228.
61. Jones DG, Morley SJ (1981) The effect of pH on host plant 'preference' for strains of Rhizobium trifolii using fluorescent ELISA for strain identification. Ann Appl Biol 97: 183-190.
62. Kiers ET, West SA, Denison RF (2008) Maintaining cooperation in the legume-rhizobia symbiosis: identifying selection pressures and mechanisms. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht, pp 59-76.
63. Laguerre G, Mazurier SI, Amarger N (1992) Plasmid profiles and restriction length polymorphism of Rhizobium leguminosarum bv. viciae in field populations. FEMS Micro Eco 101: 17-26.
64. Lewis-Henderson WR, Djordjevic MA (1991) nodT, a positively-acting cultivar specificity determinant controlling nodulation of Trifolium subterraneum by Rhizobium leguminosarum biovar trifolii. Plant Mol Biol 16: 515-526.
65. Lie TA (1978) Symbiotic specialization in pea plants: the requirement of specific Rhizobium strains for peas from Afghanistan. Annal App Biol 88: 462-465.
66. Lie TA (1984) Host genes in Pisum sativum L. conferring resistance to European Rhizobium leguminosarum strains. Plant Soil 82: 415-425.
67. Lindstrom K, Murwira M, Willems A, Altier N (2010) The biodiversity of beneficial microbe-host mutualism: the case of rhizobia. Res Microbiol 161: 453-463.
68. Lohrke SM, Orf JH, Martinez-Romero E, Sadowsky MJ (1995) Host-controlled restriction of nodulation by Bradyrhizobium japonicum strains in serogroup 110. Appl Environ Microbiol 61: 2378-2383.
69. Loi A, Howieson JG, Nutt BJ, Carr SJ (2005) A second generation of annual pasture legumes and their potential for inclusion in Mediterranean-type farming systems: a review. Aust J Exp Agric 45: 289-299.
70. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Natl Com 1: 1-12.
71. Marques Pinto C, Yao PY, Vincent JM (1974) Nodulating competitiveness amongst strains of Rhizobium meliloti and R. trifolii. Aust J Agric Res 25: 317-329.
72. Martinez-Romero E (2003) Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 252: 11-23.
73. Masterson CL, Sherwood MT (1974) Selection of Rhizobium trifolii by white and sub clovers. Irish J Agric Res 13: 91-99.
74. Materon LA, Vincent JM (1980) Host specificity and interstrain competition with soybean rhizobia. Field Crop Res 3: 215-224.
75. Materon LA (1994) Delayed inoculation and competition of Rhizobium meliloti in annual Medicago species. Appl Soil Ecol 1: 255-260.
76. McDermott TR, Graham PH (1989) Bradyrhizobium japonicum inoculant mobility, nodule occupancy, and acetylene reduction in the soybean root system. Appl Environ Microbiol 55: 2493-2498.
77. McInnes A, Haq K (2003) Contributions of rhizobia to soil nitrogen fertility. In: Abbott LK, Murphy DV (eds) Soil biological fertility: a key to sustainable land use in agriculture. Kluwer Academic Publishers, Dordrecht, pp 99-108.
78. McInnes A, Thies JE, Abbott LK, Howieson JG (2004) Structure and diversity among rhizobial strains, populations and communities-a review. Soil Biol Biochem 36: 1295-1308.
79. Meschini EP, Blanco FA, Zanetti ME, Beker MP, Küster H, Pühler A, Aguilar OM (2008) Host genes involved in nodulation preference in common bean (Phaseolus vulgaris)-Rhizobium etli symbiosis revealed by suppressive subtractive hybridization. Mol Plant-Microbe Interact 21: 459-468.
80. Mellor HY, Glen AR, Arwas R, Dilworth MJ (1987) Symbiotic and competitive properties of motility mutants of Rhizobium trifolii TA1. Archiv Microbiol 148: 34-39.
81. Michiels J, Dombrecht B, Vermeiren N, Xi C, Luyten E, Vanderleyden J (1998) Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiol Ecol 26: 193-205.
82. Montealegre C, Graham PH, Kipe-Nolt JA (1995) Preference in the nodulation of Phaseolus vulgaris cultivar RAB39. Can J Microbiol 41: 992-998.
83. Montealegre C, Graham PH (1996) Preference in the nodulation of Phaseolus vulgaris cv. RAB39. II. Effect of delayed inoculation or low cell representation in the inoculant on nodule occupancy by Rhizobium tropici UMR1899. Can J Microbiol 42: 844-850.
84. Mpepereki S, Javaheri F, Davis P, Giller KE (2000) Soyabeans and sustainable agriculture: promiscuous soybeans in southern Africa. Field Crop Res 65: 137-149.
85. Murphy PJ, Wexler M, Grzemski W, Rao JP, Gordon D (1995) Rhizopines: their role in symbiosis and competition. Soil Biol Biochem 27: 525-529.
86. Nandasena KG, O'Hara GW, Tiwari RP, Howieson JG (2006) Rapid in situ evolution of nodulating strains for Biserrula pelecinus L. through lateral transfer of a symbiosis island from the original Mesorhizobial inoculant. Appl Environ Microbiol 72: 7365-7367.
87. Nandasena KG, O'Hara GW, Tiwari RP, Sezmis E, Howieson JG (2007) In situ lateral transfer of symbiosis islands results in rapid evolution of diverse competitive strains of mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ Microbiol 9: 2496-2511.
88. Nandasena KG, O'Hara GW, Tiwari RP, Willems A, Howieson JG (2009) Mesorhizobium australicum sp. nov. and Mesorhizobium opportunistum sp. nov., isolated from Biserrula pelecinus L. in Australia. Int J Syst Evol Microbiol 59: 2140-2147.
89. Neilan J, Dowling DN, Dunican LK (1984) Host selection of Rhizobium trifolii on Trifolium repens (clover). Biochem Soc Trans 12: 492.
90. Nicol H, Thornton HG (1941) Competition between related strains of nodule bacteria and its influence on infection of the legume host. Proc Roy Soc Lond, Series B 130: 32-59.
91. O'Hara GW (2001) Nutritional constraints on root nodule bacteria affecting symbiotic nitrogen fixation: a review. Aust J Exp Agric 52: 417-433.
92. Parniske M, Downie JA (2003) Locks, keys and symbioses. Nature 425: 569-570.
93. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201.
94. Pueppke SG, Broughton WJ (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant-Microbe Interact 12: 293-318.
95. Robinson AC (1969a) Competition between effective and ineffective strains of Rhizobium trifolii in the nodulation of Trifolium subterraneum. Aust J Agric Res 20: 827-841.
96. Robinson AC (1969b) Host selection for effective Rhizobium trifolii by red clover and sub clover in the field. Aust J Agric Res 20: 1053-1060.
97. Roughley RJ, Blowes WM, Herridge DF (1976) Nodulation of Trifolium subterraneum by introduced rhizobia in competition with naturalized strains. Soil Biol Biochem 8: 403-407.
98. Russell PF, Jones DG (1975) Variation in selection of Rhizobium trifolii by varieties of red and white clover. Soil Biol Biochem 7: 15-18.
99. Rynne FG, Glenn AR, Dilworth MJ (1994) Effect of mutations in aromatic catabolism on the persistence and competitiveness of Rhizobium legvminosarum bv. trifolii. Soil Biol Biochem 26: 703-710.
100. Sadowsky MJ, Cregan PB (1992) The soybean Rj4 allele restricts nodulation by Bradyrhizobium japonicum serogroup 123 strains. Appl Environ Microbiol 58: 720-723.
101. Sadowsky MJ, Graham PH (1998) Soil biology of the Rhizobiaceae. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) Molecular biology of model plant-associated bacteria. Kluwer Academic Publishers, Dordrecht, pp 155-172.
102. Sadowsky MJ, Kosslak RM, Madrzak CJ, Golinska B, Cregan PB (1995) Restriction of nodulation by Bradyrhizobium japonicum is mediated by factors present in the roots of Glycine max. Appl Environ Microbiol 61: 832-836.
103. Sadowsky MJ, Tully RE, Cregan PB, Keyser HH (1987) Genetic diversity in Bradyrhizobium japonicum serogroup 123 and its relation to genotype-specific nodulation of soybeans. Appl Environ Microbiol 53: 2624-2630.
104. Sessitsch A, Howieson JG, Perret X, Antoun H, Martínez-Romero E (2002) Advances in Rhizobium research. Crit Rev Plant Sci 21: 323-378.
105. Sherwood MT, Masterson CL (1974) Importance of using the correct test host in assessing the effectiveness of indigenous populations of Rhizobium trifolii. Irish J Agric Res 13: 101-108.
106. Simms EL, Taylor DL (2002) Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integ Compar Biol 42: 369-380.
107. Simms EL, Taylor DL, Povich J, Shefferson RP, Sachs JL, Urbina M, Tausczik Y (2005) An empirical test of partner choice mechanisms in a wild legume-Rhizobium interaction. Proc Royal Soc London B 273: 77-81.
108. Singer M, Holding AJ, King J (1964) The response of Trifolium repens to inocula containing varying proportions of effective and ineffective rhizobia. 8th Intl Congr Soil Sci Bucharest, Romania, pp1021-1025.
109. Slattery JF, Coventry DR (1993) Variation of soil populations of Rhizobium leguminosarum bv. trifolii and the occurrence of inoculant rhizobia in nodules of sub clover after pasture renovation in north-eastern Victoria. Soil Biol Biochem 25: 1725-1730.
110. Streeter JG (1994) Failure of inoculant rhizobia to overcome the dominance of resident strains for nodule formation. Can J Microbiol 40: 513-522.
111. Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW (1995) Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci 92: 8985-8989.
112. Svenning MM, Gudmundssont J, Fagerli IL, Leinonen P (2001) Competition for nodule occupancy between introduced strains of Rhizobium leguminosarum bv. trifolii and its influence on plant production. Ann Botany 88: 781-787.
113. Talbi C, Delgado MJ, Girard L, Ramírez-Trujillo A, Caballero-Mellado J, Bedmar EJ (2010) Burkholderia phymatum strains capable of nodulating Phaseolus vulgaris are present in Moroccan soils. Appl Environ Microbiol 76: 4587-4591.
114. Thies JE, Bohlool BB, Singleton PW (1991a) Subgroups of the cowpea miscellany: symbiotic specificity within Bradyrhizobium spp. for Vigna unguiculata, Phaseolus lunatus, Arachis hypogaea, and Macroptilium atropurpureum. Appl Environ Microbiol 57: 1540-1545.
115. Thies JE, Singleton PW, Bohlool BB (1991b) Modelling symbiotic performance of introduced rhizobia in the field by use of indices of resident population size and nitrogen status of the soil. Appl Environ Microbiol 57: 29-37.
116. Toro N (1996) Nodulation competitiveness in the Rhizobium legume symbiosis. World J Microbiol Biotech 12: 157-162.
117. Trinick MJ (1980) Relationships amongst the fast growing rhizobia of Lablab purpureus, Leucaena leucocephala, Mimosa spp., Acacia farnesiana and Sesbania grandiflora and their affinities with other rhizobial groups. J Appl Microbiol 49: 39-53.
118. Trinick MJ (1982) Biology. Rhizobium. In: Broughton WJ (ed) Nitrogen Fixation, vol 2. Oxford University Press, Oxford, pp 76-146.
119. Triplett EW (1988) Isolation of genes involved in nodulation competitiveness from Rhizobium leguminosarum bv. trifolii T24. Proc Natl Acad Sci USA 85: 3810-3814.
120. Triplett EW, Sadowsky MJ (1992) Genetics of competition for nodulation of legumes. Ann Rev Microbiol 46: 399-428.
121. Valdivia B, Dughri MH, Bottomley PJ (1988) Antigenic and symbiotic characterization of resident Rhizobium leguminosarum bv. trifolii recovered from root nodules of Trifolium pratense L. sown into sub clover pasture soils. Soil Biol Biochem 20: 267-274.
122. Vargas AAT, Graham PH (1988) Phaseolus vulgaris cultivar and Rhizobium strain variation in acid-pH tolerance and nodulation under acid conditions. Field Crops Res 19: 91-101.
123. Vincent JM (1954) The root-nodule bacteria as factors in clover establishment in the red basaltic soils of the Lismore District, New South Wales. I. A survey of 'native' strains. Aust J Agric Res 5: 55-60.
124. Vincent JM, Waters LM (1953) The influence of the host on competition amongst clover root-nodule bacteria. J Gen Microbiol 9: 357-370.
125. Weaver RW, Frederick LR (1974) Effect of inoculum rate on competitive nodulation of Glycine max (L.) Merrill. II. Field studies. Agron J 66: 233-236.
126. Weber RW, Miller VL (1972) Effect of soil temperature on Rhizobium japonicum serogroup distribution in soy-bean nodules. Agron J 64: 796-798.
127. Yates RJ, Howieson JG, Real D, Reeve WG, Vivas-Marfisi A, O'Hara GW (2005) Evidence of selection for effective nodulation in the Trifolium spp. symbiosis with Rhizobium leguminosarum biovar trifolii. Aust J Exp Agric 45: 189-198.
128. Yates RJ, Howieson JG, Reeve WG, Nandasena KG, Law IJ, Braü L, Ardley JK, Nistelberger H, Real D, O'Hara GW (2007) Lotononis angolensis forms nitrogen fixing, lupinoid nodules with phylogenetically unique, fast-growing, pink-pigmented bacteria, which do not nodulate L. bainesii or L. listii. Soil Biol Biochem 39: 1680-1688.
129. Yates RJ, Howieson JG, Reeve WG, Braü L, Speijers J, Nandasena K, Real D, Sezmis E, O'Hara GW (2008) Host-strain mediated selection for an effective nitrogen-fixing symbiosis between Trifolium spp. and Rhizobium leguminosarum biovar trifolii. Soil Biol Biochem 40: 822-833.