Growth and biochemical responses of soybean to double and triple microbial associations with Bradyrhizobium, Azospirillum and arbuscular mycorrhizae

Applied Soil Ecology

Volumn 61, Issue , 2012, Pages 147-157

  Juge, C ^a   Prevost D ^a   Bertrand, A ^a   Bipfubusa, M ^a   Chalifour, F P ^b  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Arbuscular mycorrhizae; Azospirillum; Biochemical responses; Bradyrhizobium; Rhizosphere interactions; Soybean

Indexed keywords

ARBUSCULAR; AZOSPIRILLUM; BRADYRHIZOBIUM; FUNGI; GLYCINE MAX;

EID: 84864060092     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2012.05.006     Document Type: Article

References (69)

1. Antunes P.M., de Varennes A., Rajcan I., Goss M.J. Accumulation of specific flavonoids in soybean (Glycine max (L.) merr.) as a function of the early tripartite symbiosis with arbuscular mycorrhizal fungi and Bradyrhizobium japonicum (kirchner) jordan. Soil Biol. Biochem. 2006, 38:1234-1242.
2. Bagyaraj D.J., Manjunath A., Patil R.B. Interactions between a vesicular-arbuscular mycorrhiza and Rhizobium and their effects on soybean in the field. New Phytol. 1979, 82:141-145.
3. 2 on carbohydrate and ureide concentration in soybean inoculated with different strains of Bradyrhizobium japonicum. Botany 2011, 89:481-490.
4. Bethlenfalvay G.J., Brown M.S., Stafford A.E. Glycine-Glomus-Rhizobium symbiosis. II. Antagonistic effects between mycorrhizal colonization and nodulation. Plant Physiol. 1985, 79:1054-1058.
5. Bethlenfalvay G.J., Brown M.S., Ames R.N., Thomas R.S. Effects of drought on host and endophyte development in mycorrhizal soybeans in relation to water use and phosphate uptake. Physiol. Plant. 1988, 72:565-571.
6. Bethlenfalvay G.J. Mycorrhizal fungi in nitrogen-fixing legumes: problems and prospects. Methods in Microbiology, vol. 24(c) 1992, 375-389.
7. Blakeney A.B., Mutton L.L. A simple colorimetric method for the determination of sugars in fruits and vegetables. J. Sci. Food Agric. 1980, 31:889-897.
8. Brockwell J., Bottomley P.J. Recent advances in inoculant technology and prospects for the future. Soil Biol. Biochem. 1995, 27:683-697.
9. Catford J.G., Staehelin C., Lerat S., Piché Y., Vierheilig H. Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with nod factors. J. Exp. Bot. 2003, 54:1481-1487.
10. Chalk P.M., Souza R.D.F., Urquiaga S., Alves B.J.R., Boddey R.M. The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol. Biochem. 2006, 38:2944-2951.
11. Chebotar V.K., Asis C.A., Akao S. Production of growth-promoting substances and high colonization ability of rhizobacteria enhance the nitrogen fixation of soybean when coinoculated with Bradyrhizobium japonicum. Biol. Fertil. Soil 2001, 34:427-432.
12. Cohen S.A. Amino acid analysis using precolumn derivatization with 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate. Amino Acid Analysis Protocols 2007, vol. 159:39-47. Humana Press Inc., Totowa, NJ, USA. Cooper (Ed.).
13. CRAAQ Centre de référence en agriculture et agroalimentaire du Québec 2003, Guide de référence en fertilisation, 294 pp.
14. Crawford N., Kahn M., Leustek M.L., Long T.S.R. Nitrogen and sulphur. Biochemistry & Molecular Biology of Plants 2000, 786-849. American Society of Plant Physiologists. B. Buchaman, W. Gruissem, R. Jones (Eds.).
15. Curioni P.M.G., Hartwig U.A., Nöberger J., Schuller K.A. Glycolitic flux is adjusted to nitrogenase activity in nodules of detopped and argon-treated alfalfa plants. Plant Physiol. 1999, 119:445-453.
16. Dobbelaere S., Vanderleyden J., Okon Y. Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit. Rev. Plant Sci. 2003, 22:107-149.
17. Fortin J.A., Plenchette C., Piché Y. Les Mycorhizes. La nouvelle Révolution verte 2008, Multimondes/Quae, Québec, CA/France, ISBN: 978-2-89544-124-3/ISBN: 978-2-7592-0105-1.
18. Gherbi H., Markmann K., Svistoonoff S., Estevan J., Autran D., Giczey G., et al. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and frankia bacteria. PNAS 2008, 105:4928-4932.
19. Gleldhill A. Analysis of Soy Isoflavones From a Dietary Supplement Using UPLC with PDA and SQ Detection. Application Note 2007, Waters Corporation, Manchester, UK.
20. Hamel C., Plenchette C. Mycorrhizae in Crop Production 2007, Haworth Food & Agricultural Products Press, NY.
21. Hare P.D., Cress W.A. Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 1997, 21:79-102.
22. Hause B., Schaarschmidt S. The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 2009, 70:1589-1599.
23. Hayashi T., Banba M., Shimoda Y., Kouchi H., Hayashi M., Imaizumi-Anraku H. A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J. 2010, 63:141-154.
24. Hayat R., Ali S., Amara U., Khalid R., Ahmed I. Soil beneficial bacteria and their role in plant growth promotion: a review. Ann. Microbiol. 2010, 60:579-598.
25. Hodge A., Berta G., Doussan C., Merchan F., Crespi M. Plant root growth, architecture and function. Plant Soil 2009, 321:153-187.
26. Johansson J.F., Paul L.R., Finlay R.D. Microbial interactions in the mycorrhyzosphere and their significance for sustainable agriculture. FEMS Microbiol. Ecol. 2004, 48:1-13.
27. Juge C., Champagne A., Coughlan A.P., Juge N., Parrott L., Piché Y. Quantifying the growth of arbuscular mycorrhizal fungi: usefulness of the fractal dimension. Botany 2009, 87:387-400.
28. Kaschuk G., Kuyper T.W., Leffelaar P.A., Hungria M., Giller K.E. Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses?. Soil Biol. Biochem. 2009, 41:1233-1244.
29. Khan M.S., Zaidi A., Musarrat J. Microbes for Legume Improvement 2010, Springer Wien, New York.
30. Khasa D., Piché Y., Coughlan A.P. Advances in Mycorrhizal Science and Technology 2009, NRC Research Press, Ottawa.
31. King C.A., Purcell L.C. Soybean nodule size and relationship to nitrogen fixation response to water deficit. Crop Sci. 2001, 41:1099-1107.
32. 2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol. 2005, 137:1389-1396.
33. Kosslak R.M., Bookland R., Barkei J., Paaren H.E., Appelbaum E.R. Induction of Bradyrhizobium- jponicum common nod genes by isoflavones isolated from Glycine max. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:7428-7432.
34. Lerat S., Lapointe L., Gutjahr S., Piché Y., Vierheilig H. Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol. 2003, 157:589-595.
35. Lucy M., Reed E., Glick B.R. Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek. Int. J. Gen. Mol. Microbiol. 2004, 86:1-25.
36. Maillet F., Poinsot V., André O., Puech-Pagés V., Haouy A., Gueunier M., et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011, 469:58-64.
37. Mehnaz S., Lazarovits G. Inoculation effects of Pseudomonas putida Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb. Ecol. 2006, 51:326-335.
38. Mehnaz S., Weselowski B., Lazarovits G. Azospirillum canadense sp. nov., a nitrogen-fixing bacterium isolated from corn rhizosphere. Int. J. Syst. Evol. Microbiol. 2007, 57:620-624.
39. Miyauchi M.Y.H., Lima D.S., Nogueira M.A., Lovato G.M., Murate L.S., Cruz M.F., et al. Interactions between diazotrophic bacteria and mycorrhizal fungus in maize genotypes. Sci. Agric. 2008, 65:525-531.
40. Molla A.H., Shamsuddin Z.H., Halimi M.S., Morziah M., Puteh A.B. Potential for enhancement of root growth and nodulation of soybean co-inoculated with Azospirillum and Bradyrhizobium in laboratory systems. Soil Biol. Biochem. 2001, 33:457-463.
41. Morandi D., Bailey J.A., Gianinazzi-Pearson V. Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol. Plant Pathol. 1984, 24:357-364.
42. Negi M., Sachdev M.S., Tilak K.V.B.R. Influence of soluble phosphorus fertilizer on the interaction between a vesicular-arbuscular mycorrhizal fungus and Azospirillum brasilense in barley (Hordeum vulgare L.). Biol. Fertil. Soil 1990, 10:57-60.
43. Okon Y., Kapulnik Y. Development and function of Azospirillum-inoculated roots. Plant Soil 1986, 90:3-16.
44. Oldroyd G.E.D., Harrison M.J., Paszkowski U. Reprogramming plant cells for endosymbiosis. Science 2009, 324:753-754.
45. Pacovsky R.S., Fuller G., Paul E.A. Influence of soil on the interactions between endomycorrhizae and Azospirillum in sorghum. Soil Biol. Biochem. 1985, 17:525-531.
46. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 2008, 6:763-777.
47. Phillips J.M., Hayman D.S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 1970, 55:158-161.
48. Prévost D., Antoun H. Root nodule bacteria and symbiotic nitrogen fixation. Soil Sampling and Methods of Analysis 2007, 379-398. CRC Press, Florida. 2nd ed. E.G. Gregorich, M.R. Carter (Eds.).
49. 2 induces differences in nodulation of soybean depending on bradyrhizobial strain and method of inoculation. Plant Soil 2010, 331:115-127.
50. Requena N., Jimenez I., Toro M., Barea J.M. Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol. 1997, 136:667-677.
51. Roberts M.R. Does GABA act as a signal in plants?. Plant Signal. Behav. 2007, 2:408-409.
52. Saharan B.S., Nehra V. Plant growth promoting rhizobacteria: a critical review. Life Sci. Med. Res. 2011, 2011:1-30.
53. Saini V.K., Bhandari S.C., Tarafdar J.C. Comparison of crop yield, soil microbial C N and P, N-fixation, nodulation and mycorrhizal infection in inoculated and non-inoculated sorghum and chickpea crops. Field Crops Res. 2004, 89:39-47.
54. 2 fixation response to drought. J. Exp. Bot. 1999, 50:143-155.
55. Serraj R., Vadez V., Denison R.F., Sinclair T.R. Involvement of ureides in nitrogen fixation inhibition in soybean. Plant Physiol. 1999, 119:289-329.
56. Smith S.E., Read D.J. Mycorrhizal Symbiosis 2008, Academic Press, London, 804 pp. 3rd ed.
57. Sprent J.I., James E.K. Legume evolution: where do nodules and mycorrhizas fit in?. Plant Physiol. 2007, 144:575-581.
58. Streeter J.G. Carbohydrates in soybean nodules. II. Distribution of compounds in seedlings during the onset of nitrogen fixation. Plant Physiol. 1980, 66:471-476.
59. Steinkellner S., Lendzemo V., Langer I., Schweiger P., Khaosaad T., Toussaint J.-P., Vierheilig H. Flavonoids and stirolactones in root exudates as signals in symbiotic ant pathogenic plant-fungus interactions. Molecules 2007, 12:1290-1306.
60. Sulieman S. Does GABA increase the efficiency of symbiotic N2 fixation in legumes?. Plant Signal. Behav. 2011, 6:32-36.
61. 2 fixation efficiency in the model legume Medicago truncatula. Plant Cell Environ. 2010, 33:2162-2172.
62. Tennant D. A test of a modified line intersect method of estimating root length. J. Ecol. 1975, 63:995-1001.
63. Toro M., Azcón R., Herrera R. Effects on yield and nutrition of mycorrhizal and nodulated Pueraria phaseoloides exerted by P-solubilizing rhizobacteria. Biol. Fertil. Soil 1996, 21:23-29.
64. Valdenegro M., Barea J.M., Azcón R. Influence of arbuscular-mycorrhizal fungi Rhizobium meliloti strains and PGPR inoculation on the growth of Medicago arborea used as model legume for re-vegetation and biological reactivation in a semi-arid mediterranean area. Plant Growth Regul. 2001, 34:233-240.
65. Vierheilig H. Regulatory mechanisms during the plant - arbuscular mycorrhizal fungus interaction. Can. J. Bot. 2004, 82:1166-1176.
66. Vincent J.M. A manual for the practical study of root-nodule bacteria. Int. Biol. Programme Handbook 1970, vol. 15. Blackwell Sci., Oxford, UK.
67. Volpin H., Kapulnik Y. Interaction of Azospirillum with beneficial soil microorganisms. Azospirillum/plant associations 1994, 111-118. CRC Press, Florida. Y. Okon (Ed.).
68. 2 fixation in soybean. Plant Physiol. 1987, 85:137-144.
69. Xie Z.-P., Staehelin C., Vierheilig H., Wiemken A., Jabbouri S., Broughton W.J., et al. Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol. 1995, 108:1519-1525.