Advertisement

European Journal of Plant Pathology

, Volume 119, Issue 3, pp 329–339 | Cite as

Promotion of plant growth by ACC deaminase-producing soil bacteria

  • Bernard R. Glick
  • Zhenyu Cheng
  • Jennifer Czarny
  • Jin Duan
Full Research Paper

Abstract

Plant growth-promoting bacteria that contain the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase facilitate plant growth and development by decreasing plant ethylene levels, especially following a variety of environmental stresses. In this review, the physiological basis for this growth-promotion effect is examined in some detail. In addition, models are presented that endeavour to explain (i) the seemingly paradoxical effects of ethylene on a plant’s response to stress, (ii) how the expression of this enzyme is transcriptionally regulated in many bacterial strains and (iii) how ACC deaminase-containing plant growth-promoting bacteria alter plant gene expression and positively modulate plant growth.

Keywords

ACC deaminase Ethylene Plant growth-promoting bacteria Plant stress Plant growth 

Abbreviations

ACC

1-Aminocyclopropane-1-carboxylate

AOA

Aminooxyacetic acid

AVG

L-α-(aminoethoxyvinyl)-glycine

CRP

Cyclic AMP receptor protein

FNR

Fumarate–nitrate reduction regulatory protein

IAA

Indole-3-acetic acid

Lrp

Leucine-responsive regulatory protein

1-MCP

1-Methylcyclopropene

PAHs

Polycyclic aromatic hydrocarbons

PCBs

Polycyclic biphenyls

RAP PCR

RNA arbitrarily primed PCR

Notes

Acknowledgements

The work described in this review was funded by the Natural Sciences and Engineering Research Council of Canada, to B.R.G. and a fellowship to J.C. We thank Dr. Elisa Gamalero for critically reading the manuscript.

References

  1. Abeles, F. B., Morgan, P. W., & Saltveit, M. E. Jr. (1992). Ethylene in plant biology. New York: Academic Press.Google Scholar
  2. Apse, M. P., Aharon, G. S., Snedden, W. A., & Blumwald, E. (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science, 285, 1256–1258.PubMedCrossRefGoogle Scholar
  3. Arshad, M., & Frankenberger, W. T. Jr. (2002). Ethylene: Agricultural sources and applications. Dordrecht, The Netherlands: Kluwer Academic/Plenum Publishers.Google Scholar
  4. Babalola, O. O., Osir, E. O., Sanni, A. I., Odhaimbo, G. D., & Bulimo, W. D. (2003). Amplification of 1-aminocyclopropane-1-carboxylic (ACC) deaminase from plant growth promoting rhizobacteria in Striga-infested soils. African Journal of Biotechnology, 2, 157–160.Google Scholar
  5. Belimov, A. A., Hontzeas, N., Safronova, V. I., Demchinskaya, S. V., Piluzza, G., Bullitta, S., & Glick, B. R. (2005). Cadmium-tolerant plant growth-promoting rhizobacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biology and Biochemistry, 37, 241–250.CrossRefGoogle Scholar
  6. Belimov, A. A., Safronova, V. I., Sergeyeva, T. A., Egorova, T. N., Matveyeva, V. A., Tsyganov, V. E., Borisov, A. Y., Tikhonovich, I. A., Kluge, C., Preisfeld, A., Dietz, K. J., & Stepanok, V. V. (2001). Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Canadian Journal of Microbiology, 47, 642–652.PubMedCrossRefGoogle Scholar
  7. Blaha, D., Prigent-Combaret, C., Mirza, M. S., & Moënne-Loccoz, Y. (2006). Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiology Ecology, 56, 455–470.PubMedCrossRefGoogle Scholar
  8. Burd, G. I., Dixon, D. G., & Glick, B. R. (1998). A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Applied and Environmental Microbiology, 64, 3663–3668.PubMedGoogle Scholar
  9. Burd, G. I., Dixon, D. G., & Glick, B. R. (2000). Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Canadian Journal of Microbiology, 46, 237–245.PubMedCrossRefGoogle Scholar
  10. Burg, S. P., & Burg, E. A. (1966). The interaction between auxin and ethylene and its role in plant growth. American Journal of Botany, 55, 262–269.Google Scholar
  11. Campbell, B. G., & Thomson, J. A. (1996). 1-Aminocyclopropane-1-carboxylate deaminase genes from Pseudomonas strains. FEMS Microbiology Letters, 138, 207-210.PubMedCrossRefGoogle Scholar
  12. Ciardi, J. A., Tieman, D. M., Lund, S. T., Jones, J. B., Stall, R. E., & Klee, H. J. (2000). Response to Xanthomonas campestris pv. vesicatoria in tomato involves regulation of ethylene receptor gene expression. Plant Physiology, 123, 81–92.PubMedCrossRefGoogle Scholar
  13. Dey, R., Pal, K. K., Bhatt, D. M., & Chauhan, S. M. (2004). Growth promotion and yield enhancement of peanut (Aracis hypoggaea L.) by application of plant growth-promoting rhizobacteria. Microbiological Research, 159, 371–394.PubMedCrossRefGoogle Scholar
  14. Dharmasiri, N., & Estell, M. (2004). Auxin signaling and regulated protein degradation. Trends in Plant Science, 9, 302–308.PubMedCrossRefGoogle Scholar
  15. Duan, J., Müller, K. M., Charles, T. C., Vesely, S., & Glick, B. R. (2006). 1-Aminocyclopropane-1-carboxylate (ACC) deaminase genes in Rhizobia: Isolation, characterization and regulation. Proceedings of the 7th International PGPR Workshop (50 pp). Amsterdam.Google Scholar
  16. Else, M. A., & Jackson, M. B. (1998). Transport of 1-aminocyclopropane-1-carboxylic acid (ACC) in the transpiration stream of tomato (Lycopersicon esculentum) in relation to foliar ethylene production and petiole epinasty. Australian Journal of Plant Physiology, 25, 453–458.CrossRefGoogle Scholar
  17. Farwell, A. J., Vesely, S., Nero, V., Rodriguez, H., Shah, S., Dixon, D. G., & Glick, B. R. (2006). The use of transgenic canola (Brassica napus) and plant growth-promoting bacteria to enhance plant biomass at a nickel-contaminated field site. Plant and Soil, 288, 309–318.CrossRefGoogle Scholar
  18. Ghosh, S., Penterman, J. N., Little, R. D., Chavez, R., & Glick, B. R. (2003). Three newly isolated plant growth-promoting bacilli facilitate the growth of canola seedlings. Plant Physiology and Biochemistry, 41, 277–281.CrossRefGoogle Scholar
  19. Glick, B. R. (1995). The enhancement of plant growth by free-living bacteria. Canadian Journal of Microbiology, 41, 109–117.Google Scholar
  20. Glick, B. R., Karaturovíc, D. M., & Newell, P. C. (1995). A novel procedure for rapid isolation of plant growth promoting pseudomonads. Canadian Journal of Microbiology, 41, 533–536.Google Scholar
  21. Glick, B. R., Patten, C. L., Holguin, G., & Penrose, D. M. (1999). Biochemical and genetic mechanisms used by plant growth promoting bacteria. London: Imperial College Press.Google Scholar
  22. Glick, B. R., Penrose, D. M., & Li, J. (1998). A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. Journal of Theoretical Biology, 190, 63–68.PubMedCrossRefGoogle Scholar
  23. Greenberg, B. M., Huang, X. D., Gurska, Y., Gerhardt, K. E., Wang, W., Lampi, M. A., Zhang, C., Khalid, A., Isherwood, D., Chang, P., Wang, H., Dixon, D. G., & Glick, B. R. (2006). Successful field tests of a multi-process phytoremediation system for decontamination of persistent petroleum and organic contaminants, Proceedings of the 29th Arctic and Marine Oil Spill Program Technical Seminar (Vol. 1, pp. 389–400).Google Scholar
  24. Grichko, V. P., Filby, B., & Glick, B. R. (2000). Increased ability of transgenic plants expressing the bacterial enzyme ACC deaminase to accumulate Cd, Co, Cu, Ni, Pb and Zn. Journal of Biotechnology, 81, 45-53.PubMedCrossRefGoogle Scholar
  25. Grichko, V. P., & Glick, B. R. (2000). Identification of DNA sequences that regulate the expression of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylate deaminase gene. Canadian Journal of Microbiology, 46, 1159–1165.PubMedCrossRefGoogle Scholar
  26. Grichko, V. P., & Glick, B. R. (2001a). Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiology and Biochemistry, 39, 11–17.CrossRefGoogle Scholar
  27. Grichko, V. P., & Glick, B. R. (2001b). Flooding tolerance of transgenic tomato plants expressing the bacterial enzyme ACC deaminase controlled by the 35S, rolD or PRB-1b promoter. Plant Physiology and Biochemistry, 39, 19–25.CrossRefGoogle Scholar
  28. Guinel, F. C., & Geil, R. D. (2002). A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment of these two symbioses. Canadian Journal of Botany, 80, 695–720.CrossRefGoogle Scholar
  29. Honma, M. (1985). Chemically reactive sulfhydryl groups of 1-aminocyclopropane-1-carboxylate deaminase. Agricultural and Biological Chemistry, 49, 567–571.Google Scholar
  30. Honma, M. (1993). Stereospecific reaction of 1-aminocyclopropane-1-carboxylate deaminase. In J. C. Pech, A. Latché, & C. Balagué (Eds.), Cellular and molecular aspects of the plant hormone ethylene (pp. 111–116). Dordrecht, The Netherlands: Kluwer Academic Publishers.Google Scholar
  31. Honma, M., & Shimomura, T. (1978). Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agricultural and Biological Chemistry, 42, 1825–1831.Google Scholar
  32. Hontzeas, N., Richardson, A. O., Belimov, A. A., Safranova, V. I., Abu-Omar, M. M., & Glick, B. R. (2005). Evidence for horizontal gene transfer (HGT) of ACC deaminase genes. Applied and Environmental Microbioogy, 71, 7556–7558.CrossRefGoogle Scholar
  33. Hontzeas, N., Zoidakis, J., Glick, B. R., & Abu-Omar, M. M. (2004a). Expression and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the rhizobacterium Pseudomonas putida UW4: A key enzyme in bacterial plant growth promotion. Biochimica et Biophysica Acta, 1703, 11–19.PubMedGoogle Scholar
  34. Hontzeas, N., Saleh, S. S., & Glick, B. R. (2004b). Changes in gene expression in canola roots induced by ACC deaminase-containing plant growth-promoting bacteria. Molecular Plant–Microbe Interactions, 17, 865–871.PubMedCrossRefGoogle Scholar
  35. Huang, X.-D., El-Alawai, Y., Gurska, J., Glick, B. R., & Greenberg, B. M. (2005). A multi-process phytoremediation system for decontamination of persistent total petroleum hydrocarbons (TPHs) from soils. Microchemical Journal, 81, 139–147.CrossRefGoogle Scholar
  36. Huang, X.-D., El-Alawi, Y., Penrose, D. M., Glick, B. R., & Greenberg, B. M. (2004). Responses of plants to creosote during phytoremediation and their significance for remediation processes. Environmental Pollution, 130, 453–463.PubMedCrossRefGoogle Scholar
  37. Hyodo, H. (1991). Stress/wound ethylene. In A. K. Mattoo, & J. C. Shuttle (Eds.), The plant hormone ethylene (pp. 65–80). Boca Raton: CRC Press.Google Scholar
  38. Jacobson, C. B., Pasternak, J. J., & Glick, B. R. (1994). Partial purification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Canadian Journal of Microbiology, 40, 1019–1025.CrossRefGoogle Scholar
  39. Jansonius, N. J. (1998). Structure, evolution and action of vitamin B6-dependent enzymes. Current Opinion in Structural Biology, 8, 759–769.PubMedCrossRefGoogle Scholar
  40. Jia, Y. J., Kakuta, Y., Sugawara, M., Igarashi, T., Oki, N., Kisaki, M., Shoji, T., Kanetuna, Y., Horita, T., Matsui, H., & Honma, M. (1999). Synthesis and degradation of 1-aminocyclopropane-1-carboxylic acid by Penicillium citrinum. Bioscience, Biotechnology and Biochemistry, 63, 542–549.CrossRefGoogle Scholar
  41. Klee, H. J., Hayford, M. B., Kretzmer, K. A., Barry, G. F., & Kishore, G. M. (1991). Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants. Plant Cell, 3, 1187–1193.PubMedCrossRefGoogle Scholar
  42. Klee, H. J., & Kishore, G. M. (1992). Control of fruit ripening and senescence in plants. United States Patent Number: 5,702,933.Google Scholar
  43. Leonard, P. M., Smits, S. H. J., Sedelnikova, S. E., Brinkman, A. B., de Vos, W. M., van der Oost, J., Rice, D. W., & Rafferty, J. B. (2001). Crystal structure of the Lrp-like transcrptional regulator from the archaeon Pyrococcus furiosus. EMBO Journal, 20, 990–997.PubMedCrossRefGoogle Scholar
  44. Li, J., & Glick, B. R. (2001). Transcriptional regulation of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene (acdS). Canadian Journal of Microbiology, 47, 359–367.PubMedCrossRefGoogle Scholar
  45. Li, Q., Shah, S., Saleh-Lakha, S., & Glick, B. R. (2006). Growth of tobacco in nickel-contaminated soil in the presence of the plant growth-promoting bacterium Pseudomonas putida UW4. Current Microbiology (in press).Google Scholar
  46. Ma, W., Charles, T. C., & Glick, B. R. (2004). Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Applied and Environmental Microbiology, 70, 5891–5897.PubMedCrossRefGoogle Scholar
  47. Ma, W., Guinel, F. C., & Glick, B. R. (2003b). The Rhizobium leguminosarum bv. viciae ACC deaminase protein promotes the nodulation of pea plants. Applied and Environmental Microbiology, 69, 4396–4402.PubMedCrossRefGoogle Scholar
  48. Ma, W., Sebestianova, S., Sebestian, J., Burd, G. I., Guinel, F., & Glick, B. R. (2003a). Prevalence of 1-aminocyclopropaqne-1-carboxylate in deaminase in Rhizobia spp. Antonie Van Leeuwenhoek, 83, 285–291.PubMedCrossRefGoogle Scholar
  49. Madhaiyan, M., Poonguzhali, S., Ryu, J., & Sa, T. (2006). Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocycloprpane-1-carboxylate deaminase-containing Methylobacterium fjisawaense. Planta, 224, 268–278.PubMedCrossRefGoogle Scholar
  50. Mayak, S., Tirosh, T., & Glick, B. R. (2004a). Plant growth-promoting bacteria that confer resistance to water stress in tomato and pepper. Plant Science, 166, 525–530.CrossRefGoogle Scholar
  51. Mayak, S., Tirosh, T., & Glick, B. R. (2004b). Plant growth-promoting bacteria that confer resistance in tomato to salt stress. Plant Physiology and Biochemistry, 42, 565–572.PubMedCrossRefGoogle Scholar
  52. Minami, R., Uchiyama, K., Murakami, T., Kawai, J., Mikami, K., Yamada, T., Yokoi, D., Ito, H., Matsui, H., & Honma, M. (1998). Properties, sequence, and synthesis in Escherichia coli of 1-aminocyclopropane-1-carboxylate deaminase from Hansenula saturnus. Journal of Biochemistry, 123, 1112–1118.PubMedGoogle Scholar
  53. Morgan, P. W., & Gausman, H. W. (1966). Effects of ethylene on auxin transport. Plant Physiology, 41, 45–52.PubMedCrossRefGoogle Scholar
  54. Nie, L., Shah, S., Burd, G. I., Dixon, D. G., & Glick, B. R. (2002). Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growth-promoting bacterium Enterobacter cloacae CAL2. Plant Physiology and Biochemistry, 40, 355–361.CrossRefGoogle Scholar
  55. Nukui, N., Ezura, H., Yuhashi, K., Yasuta, T., & Minamisawa, K. (2000). Effects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum. Plant Cell Physiology, 41, 893–897.PubMedCrossRefGoogle Scholar
  56. Nukui, N., Minamisawa, K., Ayabe, S. I., & Aoki, T. (2006). Expression of the 1-aminocyclopropane-1-carboxylic acid deaminase gene requires symbiotic nitrogen-fixing regulator gene nifA2 in Mesorhizobium loti MAFF303099. Applied and Environmental Microbiology, 72, 4964–4969.PubMedCrossRefGoogle Scholar
  57. Penrose, D. M., Moffatt, B. A., & Glick, B. R. (2001). Determination of 1-aminocyclopropane-1-carboxylic acid (ACC) to assess the effects of ACC deaminase-containing bacteria on roots of canola seedlings. Canadian Journal of Microbiology, 47, 77–80.PubMedCrossRefGoogle Scholar
  58. Pierik, R., Tholen, D., Poorter, H., Visser, E. J. W., & Voesenek, L. A. C. J. (2006). The Janus face of ethylene: Growth inhibition and stimulation. Trends in Plant Science, 11, 176–183.PubMedCrossRefGoogle Scholar
  59. Prayitno, J., Rolfe, B. G., & Mathesius, U. (2006). The ethylene-insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiology, 142, 168–180.PubMedCrossRefGoogle Scholar
  60. Reed, M. L. E., & Glick, B. R. (2005). Growth of canola (Brassica napus) in the presence of plant growth-promoting bacteria and either copper or polycyclic aromatic hydrocarbons. Canadian Journal of Microbiology, 51, 1061–1069.PubMedCrossRefGoogle Scholar
  61. Robison, M. M., Griffith, M., Pauls, K. P., & Glick, B. R. (2001a). Dual role of ethylene in susceptibility of tomato to Verticillium wilt. Journal of Phytopathology, 149, 385–388.CrossRefGoogle Scholar
  62. Robison, M. M., Shah, S., Tamot, B., Pauls, K. P., Moffatt, B. A., & Glick, B. R. (2001b). Reduced symptoms of Verticillium wilt in transgenic tomato expressing a bacterial ACC deaminase. Molecular Plant Pathology, 2, 135–145.CrossRefGoogle Scholar
  63. Sheehy, R. E., Honma, M., Yamada, M., Sasaki, T., Martineau, B., & Hiatt, W. R. (1991). Isolation, sequence, and expression in Escherichia coli of the Pseudomonas sp. strain ACP gene encoding 1-aminocyclopropane-1-carboxylate deaminase. Journal of Bacteriology, 173, 5260–5265.PubMedGoogle Scholar
  64. Sisler, E. C., & Serek, M. (1997). Inhibitors of ethylene responses in plants at the receptor level: Recent developments. Physiologia Plantarum, 100, 577–582.CrossRefGoogle Scholar
  65. Stearns, J., & Glick, B. R. (2003). Transgenic plants with altered ethylene biosynthesis or perception. Biotechnology Advances, 21, 193–210.PubMedCrossRefGoogle Scholar
  66. Stearns, J. C., Shah, S., Dixon, D. G., Greenberg, B. M., & Glick, B. R. (2005). Tolerance of transgenic canola expressing 1-aminocyclopropane-carboxylic acid deaminase to growth inhibition by nickel. Plant Physiology and Biochemistry, 43, 701–708.PubMedCrossRefGoogle Scholar
  67. Sturz, A. V., & Nowak, J. (2000). Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Applied Soil Ecology, 15, 183–190.CrossRefGoogle Scholar
  68. Suttle, J. C. (1988). Effect of IAA on polar IAA transport, net IAA uptake and specific binding of N-1-naphthylphthalkamic in tissues and microsomes isolated from etiolated pea epicotyls. Plant Physiology, 88, 795–799.PubMedGoogle Scholar
  69. Timmusk, S., & Wagner, E. G. H. (1999). The plant growth promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: A possible connection between biotic and abiotic stress responses. Molecular Plant–Microbe Interactions, 12, 951–959.PubMedCrossRefGoogle Scholar
  70. Uchiumi, T., Ohwada, T., Itakura, M., Mitsui, H., Nukui, N., Dawadi, P., Kaneko, T., Tabata, S., Yokoyama, T., Tejima, K., Saeki, K., Omori, H., Hayashi, M., Maekawa, T., Sriprang, R., Murooka, Y., Tajima, S., Simomura, K., Nomura, M., Suzuki, A., Shimoda, Y., Sioya, K., Abe, M., & Minamisawa, K. (2004). Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. Journal of Bacteriology, 186, 2439–2448.PubMedCrossRefGoogle Scholar
  71. Van Loon, L. C. (1984). Regulation of pathogenesis and symptom expression in diseased plants by ethylene. In Y. Fuchs, & E. Chalutz (Eds.), Ethylene: Biochemical, physiological and applied aspects (pp. 171–180). The Hague: Martinus Nijhoff/Dr W. Junk.Google Scholar
  72. Van Loon, L. C., Geraats, B. P. J., & Linthorst, H. J. M. (2006). Ethylene as a modulator of disease resistance in plants. Trends in Plant Science, 11, 184–191.PubMedCrossRefGoogle Scholar
  73. Van Loon, L. C., & Glick, B. R. (2004). Increased plant fitness by rhizobacteria. In H. Sandermann (Ed.), Molecular ecotoxicology of plants (pp. 177–205). Berlin: Springer-Verlag.Google Scholar
  74. Walsh, C., Pascal, R. A., Johnston, M., Raines, R., Dikshit, D., Krantz, A., & Honma, M. (1981). Mechanistic studies on the pyridoxal phosphate enzyme 1-aminocyclopropane-1-carboxylate from Pseudomonas sp. Biochemistry, 20, 7509–7519.PubMedCrossRefGoogle Scholar
  75. Wang, C., Knill, E., Glick, B. R., & Défago, G. (2000). Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth promoting and disease-suppressive capacities. Canadian Journal of Microbiology, 46, 898–907.PubMedCrossRefGoogle Scholar
  76. Wang, C., Ramette, A., Punjasamarnwong, P., Zala, M., Natsch, A., Moënne-Loccoz, Y., & Défago, G. (2001). Cosmopolitan distribution of phlD-containing dicotyledonous crop-associated pseudomonads of worldwide origin. FEMS Microbiology Ecology, 37, 105–116.CrossRefGoogle Scholar
  77. Yang, S. F., & Hoffman, N. E. (1984). Ethylene biosynthesis and its regulation in higher plants. Annual Review of Plant Physiology, 35, 155–189.CrossRefGoogle Scholar
  78. Yuhashi, K. I., Ichikawa, N., Ezura, H., Akao, S., Minakawa, Y., Nukui, N., Yasuta, T., & Minamisawa, K. (2000). Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum. Applied and Environmental Microbiology, 66, 2658–2663.PubMedCrossRefGoogle Scholar

Copyright information

© KNPV 2007

Authors and Affiliations

  • Bernard R. Glick
    • 1
  • Zhenyu Cheng
    • 1
  • Jennifer Czarny
    • 1
  • Jin Duan
    • 1
  1. 1.Department of BiologyUniversity of WaterlooWaterlooCanada

Personalised recommendations