Plant and Soil

, Volume 204, Issue 1, pp 57–67 | Cite as

Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: Effect on radishes (Raphanus sativus L.)

  • Hani Antoun
  • Chantal J. Beauchamp
  • Nadia Goussard
  • Rock Chabot
  • Roger Lalande


Bradyrhizobia and rhizobia are symbiotic bacterial partners forming nitrogen fixing nodules on legumes. These bacteria share characteristics with plant growth promoting rhizobacteria (PGPR). Nodule inducing bacteria, like other PGPR, are capable of colonizing the roots of non-legumes and produce phytohormones, siderophores and HCN. They also exhibit antagonistic effects towards many plant pathogenic fungi. The potential of nodule inducing bacteria to function as PGPR, was examined by using radish as a model plant. Three percent of the 266 strains tested were found to be cyanogens, while a majority (83%) produced siderophores. Fifty eight percent of the strains produced indole 3-acetic acid (IAA) and 54% solubilized phosphorus. Some of the bacterial species examined were found to have a deleterious effect while others were neutral or displayed a stimulatory effect on radishes. Bradyrizobium japonicum strain Soy 213 was found to have the highest stimulatory effect (60%), and an arctic strain (N44) was the most deleterious, causing a 44% reduction in radish dry matter yield. A second plant inoculation test, performed in growth cabinets, revealed that only strain Tal 629 of B. japonicum significantly increased (15%) the dry matter yield of radish. This indicates that specific bradyrhizobia have the potential to be used as PGPR on non-legumes.

Bradyrhizobium growth promotion radish Rhizobium 


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  1. Abd-Alla M H 1994 Use of organic phosphorus by Rhizobium leguminosarum bv. viciae phosphatases. Biol. Fertil. Soils 8, 216–218.Google Scholar
  2. Alexander D B and Zuberer D A 1991 Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol. Fertil. Soils 12, 39–45.Google Scholar
  3. Al-Mallah M K, Davey M R and Coking E C 1990 Nodulation of oilseedrape (Brassica napus) by rhizobia. J. Exp. Bot. 41, 1567–1572.Google Scholar
  4. Alström S 1991 Deleterious rhizosphere bacteria in relation to plants and other microorganisms. In Plant Growth-promoting Rhizobacteria-progress and Prospect. Eds. C Keel, B Koller and G Défago. pp 275–285. IOBC/WPRS Bulletin XIV (8).Google Scholar
  5. Alström S and Burns R G 1989 Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biol. Fertil. Soils 7, 232–238.Google Scholar
  6. Antoun H, Bordeleau L M and Sauvageau R 1984 Utilization of the tricarboxylic acid cycle intermediates and symbiotic effectiveness in Rhizobium meliloti. Plant Soil 77, 29–38.Google Scholar
  7. Antoun H, Bordeleau L M and Gagnon C 1978 Antagonisme entre Rhizobium meliloti et Fusarium oxysporum en relation avec l'efficacité symbiotique. Can. J. Plant Sci. 58, 75–78.Google Scholar
  8. Bakker A W and Schippers M 1987 Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp.-mediated plant growth-stimulation. Soil Biol. Biochem. 19, 451–457.Google Scholar
  9. Beauchamp C J 1993 Mode d'action des rhizobactéries favorisant la croissance des plantes et potentiel de leur utilisation comme agent de lutte biologique. Phytoprotection 74, 19–27.Google Scholar
  10. Beauchamp C J, Dion P, Kloepper J W and Antoun H 1991 Physiological characterization of opine-utilizing rhizobacteria for traits related to plant growth-promoting activity. Plant Soil 132, 273–279.Google Scholar
  11. Bordeleau L M, Antoun H and Lachance R A 1977 Effets des souches de Rhizobium meliloti et des coupes successives de la luzerne (Medicago sativa) sur la fixation symbiotique d'azote. Can. J. Plant Sci. 57, 433–439.Google Scholar
  12. Bric J M, Bostock R M and Silverstone S E 1991 Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl. Environ. Microbiol. 57, 535–538.Google Scholar
  13. Buonassisi A J, Copeman R J, Pepin H S and Eaton G W 1986 Effect of Rhizobium spp.on Fusarium f.sp. phaseoli. Can. J. Plant Pathol. 8, 140–146.Google Scholar
  14. Chabot R, Antoun H and Cescas M P 1993 Stimulation de la croissance du maïs et de la laitue romaine par des microorganismes dissolvant le phosphore inorganique, Can. J. Microbiol. 39, 941–947.Google Scholar
  15. Chabot R, Antoun H and Cescas M P 1996a Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Plant Soil 184, 311–321.Google Scholar
  16. Chabot R, Antoun H, Kloepper J W and Beauchamp C 1996b Root colonization of maize and lettuce by bioluminescent Rhizobium leguminosarum biovar phaseoli. Appl. Environ. Microbiol. 62, 2767–2772.PubMedGoogle Scholar
  17. de Britto Alvarez M A, Gagné S and Antoun H 1995 Effect of compost on rhizosphere microflora of the tomato and on the incidence of plant growth-promoting rhizobacteria. Appl. Environ. Microbiol. 61, 194–199.Google Scholar
  18. Ehteshamul-Haque S and Ghaffar A 1993 Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mungbean. J. Phytopathol. 138, 157–163.Google Scholar
  19. Gaur Y D, Sen A N and Subba Rao N S 1980 Improved legume-Rhizobium symbiosis by inoculating preceding cereal crop with Rhizobium. Plant Soil 54, 313–316.Google Scholar
  20. Glazerbrook J and Walker G C 1991 Genetic techniques in Rhizobium meliloti. In Bacterial Genetic Systems. Ed. J H Miller pp 398–418. Methods in Enzymology 204, Academic Press, New York.Google Scholar
  21. Goldstein A H 1986 Bacterial solubilization of mineral phosphates: historical perspective and future prospects. Am. J. Altern. Agric. 1: 51–57.Google Scholar
  22. Guerinot M L 1991 Iron uptake and metabolism in the rhizobia/legume symbioses. Plant Soil 130, 199–209.Google Scholar
  23. Halder A K and Chakrabartty P K 1993 Solubilization of inorganic phosphate by Rhizobium. Folia Microbiol. 38, 325–330.Google Scholar
  24. Höflich G, Wiehe W and Kühn G. 1994 Plant growth stimulation by inoculation with symbiotic and associative rhizosphere microorganisms. Experientia 50, 897–905.Google Scholar
  25. Howell R K 1987 Rhizobium induced mineral uptake in peanut tissues. J. Plant Nutr. 10, 1297–1305.Google Scholar
  26. Jadhav R S, Thaker N V and Desai A 1994 Involvement of the siderophore of cowpea Rhizobium in the iron nutrition of the peanut. World J. Microbiol. Biotechnol. 10, 360–361.Google Scholar
  27. Kloepper J W 1993 Plant growth-promoting rhizobacteria as biological control agents. In Soil Microbial Ecology. Ed. F B Metting, Jr. pp 255–274. Marcel Dekker, Inc., New York.Google Scholar
  28. Kloepper J W and Beauchamp C J 1992 A review of issues related to measuring colonization of plant roots by bacteria. Can. J. Microbiol 38, 1219–1232.Google Scholar
  29. Kloepper J W and Schroth M N 1978 Plant growth-promoting rhizobacteria on radishes. In Proc. 4th Int. Conf. Plant Pathogenic Bacteria. Vol 2, pp 879–882. INRA, Angers, France.Google Scholar
  30. Kucey R M N, Janzen, H H and Leggett M E 1989 Microbially mediated increases in plant-available phosphorus. Adv. Agron. 42, 199–228.Google Scholar
  31. Lalande R, Bigwaneza P C and Antoun H 1990 Symbiotic effectiveness of Rhizobium leguminosarum biovar phaseoli isolated from soils of Rwanda. Plant Soil 121, 41–46.Google Scholar
  32. Lalande R, Bissonnette N, Coutlée D and Antoun H 1989 Identification of rhizobacteria from maize and determination of their plant-growth promoting potential. Plant Soil 115, 7–11.Google Scholar
  33. Lalande R, Antoun H, Paré T and Joyal P 1986 Effets de l'inoculation avec des souches du Rhizobium leguminosarum bv. phaseoli sur le rendement et la teneur en azote du haricot(Phaseolus vulgaris). Naturaliste Can. (Rev. Écol. Syst.) 113, 337–346.Google Scholar
  34. Lemanceau P 1992 Effets bénéfiques de rhizobactéries sur les plantes: exemple des Pseudomonas. Agronomie 12, 413–437.Google Scholar
  35. Lippmann B, Leinhos V and Bergmann H 1995 Influence of auxin producing rhizobacteria on root morphology and nutrient accumulation of crops. I. Changes in root morphology and nutrient accumulation in maize (Zea mays L.) caused by inoculation with indole-3-acetic acid (IAA) producing Pseudomonas and Acinetobacter strains or IAA applied exogenously. Angew Bot. 69, 31–36.Google Scholar
  36. Liu L, Kloepper J W and Tuzun S 1995a Induction of systemic resistance in cucumber against Fusarium wilt by plant growth-promoting rhizobacteria. Phytopathology 85, 695–698.Google Scholar
  37. Liu L, Kloepper J W and Tuzun S 1995b Induction of systemic resistance in cucumber against bacterial angular leaf spot by plant growth-promoting rhizobacteria. Phytopathology 85, 843–847.Google Scholar
  38. Loper J E and Buyer J S 1991 Siderophores in microbial interactions on plant surfaces. Mol. Plant-Microbe Int. 4, 5–13.Google Scholar
  39. Malajczuk N, Pearse m and Litchfield R T 1984 Interactions between Phytophthora cinnamomi and Rhizobium isolates. Trans. Br. Mycol. Soc. 82, 491–500.Google Scholar
  40. McInroy J A and Kloepper J W 1995 Survey of indigenous endophytes from cotton and sweet corn. Plant Soil 173, 337–342.Google Scholar
  41. Noel T C, Sheng C, Yost C K, Pharis R P and Hynes M F 1996 Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can. J. Microbiol. 42, 279–283.PubMedGoogle Scholar
  42. O'Sullivan D J and O'Gara F 1992 Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiol. Rev. 56, 662–676.PubMedGoogle Scholar
  43. Peña-Cabriales J J and Alexander M 1983 Growth of Rhizobium in unamended soil. Soil Sci. Soc. Am. J. 47, 81–84.Google Scholar
  44. Plazinsky J, Innes R W and Rolfe B G 1985 Expression of Rhizobium trifolii early nodulation genes on maize and rice plants.J. Bacteriol. 163, 812–815.PubMedGoogle Scholar
  45. Plessner O, Klapatch T and Guerinot M L 1993 Siderophore utilization by Bradyrhizobium japonicum. Appl. Environ. Microbiol. 59, 1688–1690.Google Scholar
  46. Prévost D, Bordeleau L M, Caudry-Reznick S, Schulman H M and Antoun H 1987 Characteristics of rhizobia isolated from three legumes indigenous to the Canadian high arctic: Astragalus alpinus, Oxytropis maydelliana, and Oxytropis arctobia. Plant Soil 98, 313–324.Google Scholar
  47. Richardson A E 1994 Soil microorganisms and phosphorus availability. In Soil Biota. Management in Sustainable Farming Systems. Ed. C E Pankhurst. pp 50–62. CSIRO, Melbourne.Google Scholar
  48. Ridge R W, Rolfe B G, Jing Y and Cocking E C 1992 Rhizobium nodulation of non-legumes. Symbiosis 14, 345–357.Google Scholar
  49. Schloter M, Wiehe W, Assmus B, Steindl H, Becke H, Höflich G and Hartmann A 1997 Root colonization of different plants by plant-growth-promoting Rhizobium leguminosarum bv. trifolii R39 studied with monospecific polyclonal antisera. Appl. Environ. Microbiol. 63, 2038–2046.PubMedGoogle Scholar
  50. Shimshick E J and Hebert R R 1979 Binding characteristics of N2-fixing bacteria to cereal roots. Appl. Environ. Microbiol. 38, 447–453.Google Scholar
  51. Staehelin C, Granado J, Müller J, Wieken A, Mellor R B, Felix G, Regenass M, Broughton W J and Boller T 1994 Perception of Rhizobium nodulations factors by tomato cells and inactivation by root chitinases. Proc. Natl. Acad. Sci. USA 91, 2196–2200.PubMedGoogle Scholar
  52. Steel R G D and Torrie J H 1980 Principles and Procedures of Statistics. A Biometrical Approach. McGraw-Hill Publ. Co., Toronto.Google Scholar
  53. Suslow T V and Schroth M N 1982 Rhizobacteria of sugar beets: effects of seed application and root colonization on yield.Phytopathology 72, 199–206.Google Scholar
  54. Terouchi N and Syono K 1990 Rhizobium attachment and curling in asparagus, rice and oat plants. Plant Cell Physiol. 31, 119–127.Google Scholar
  55. Trinick M J 1973 Symbiosis between Rhizobium and the non-legume, Trema aspera Nature (Lond.) 244, 459–460.Google Scholar
  56. Trinick M J and Hadobas P A 1995 Formation of nodular structures on the non-legumes Brassica napus, B.campestris, B. juncea and Arabidopsis thaliana with Bradyrhizobium and Rhizobium isolated from Parasponia spp. or legumes grown in tropical soils. Plant Soil 172, 207–219.Google Scholar
  57. Valdés M, Reza-Aleman F and Furlan V 1993 Response of Leucaena esculenta to endomycorrhizae and Rhizobium inoculation. World J. Microbiol. Biotechnol. 9, 97–99.Google Scholar
  58. Vincent J M 1970 A manual for the practical study of the root-nodule bacteria. Int. Biol. Prog. Handbook No. 15. Blackwell Scientific Publications, Oxford.Google Scholar
  59. Wang T L, Wood E A and Brewin N J 1982 Growth regulators, Rhizobium and nodulation in peas. Indole-3-acetic acid from the culture medium of nodulating and non-nodulating strains of R. leguminosarum. Planta 155, 343–349.Google Scholar
  60. Werner D 1992 Symbiosis of Plants and Microbes. Chapman & Hall, London.Google Scholar
  61. Wiehe W and Höflich G 1995. Survival of plant growth promoting rhizosphere bacteria in the rhizosphere of different crops and migration to non-inoculated plants under field conditions in north-east Germany. Microbiol. Res. 150, 201–206.Google Scholar
  62. Xie Z-P, Staehlin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton W J, Vögeli-Lange R and Boller T 1995 Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soyabeans. Plant Physiol. 108, 1519–1525.PubMedGoogle Scholar
  63. Yanni Y G, Rizk R Y, Corich V, Squartini A and Dazzo F B 1995 Endorhizosphere colonization and growth promotion of Indica and Japonica rice varieties by Rhizobium leguminosarum bv. trifolii. In Proc. 15th North American Symbiotic Nitrogen-Fixation Conference. North Carolina State University, Raleigh, NC.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Hani Antoun
    • 1
    • 2
  • Chantal J. Beauchamp
    • 3
  • Nadia Goussard
    • 1
  • Rock Chabot
    • 1
  • Roger Lalande
    • 4
  1. 1.Recherches en Sciences de la vie et de la santé, Pavillon Charles-Eugène MarchandCanada
  2. 2.Département des Sols et de Génie AgroalimentaireCanada
  3. 3.Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Pavillon Paul-ComtoisUniversité LavalCanada
  4. 4.Centre de Recherches sur les Sols et les Grandes Cultures, Agriculture et Agro-Alimentaire CanadaCanada

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