Plant and Soil

, Volume 245, Issue 1, pp 147–162 | Cite as

Breeding for better symbiosis

  • Z. Rengel


The present review gives a critical assessment of the literature dealing with symbiosis between rhizobia and legumes and between AM fungi and most plants. Associative N2 fixation (even though strictly speaking not a symbiotic relationship) does have some characteristics of symbiosis due to mutualistic dependence and usefulness of the relationship, and is therefore covered in this review. Nodulation in the rhizobia–legume symbiosis may be limited by an insufficient amount of the nod-gene inducers released from seed and/or roots. However, there is genotypic variation in the germplasm of legume species in all components of the signalling pathway, suggesting a prospect for improving nodulation by selecting and/or transforming legume genotypes for increased exudation of flavonoids and other signalling compounds. Deciphering chromosomal location as well as cloning nod, nif and other genes important in nodulation and N2 fixation will allow manipulation of the presence and expression of these genes to enhance the symbiotic relationship. Increased efficacy of symbiotic N2 fixation can be achieved by selecting not only the best host genotypes but by selecting the best combination of host genotype and nodule bacteria. As flavonoids exuded by legume seedlings may not only be nod-gene inducers, but also stimulants for hyphal growth of the AM fungi, selecting and/or transforming plants to increase exudation of these flavonoids may result in a double benefit for mycorrhizal legumes. Mutants unable to sustain mycorrhizal colonisation are instrumental in understanding the colonisation process, which may ultimately pay off in breeding for the more effective symbiosis. In conclusion, targeted efforts to breed genotypes for improved N2 fixation and mycorrhizal symbiosis will bring benefits in increased yields of crops under a wide range of environmental conditions and will contribute toward sustainability of agricultural ecosystems in which soil-plant-microbe interactions will be better exploited.

associative N2 fixation dinitrogen fixation genotype mycorrhiza nodulation rhizobia root exudation screening selection symbiosis 


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  1. Abd-Alla M H, Vuong T D and Harper J E 1998 Genotypic differences in dinitrogen fixation response to NaCl stress in intact and grafted soybean. Crop Sci. 38, 72-77.Google Scholar
  2. Al-Karaki G N 1998 Benefit, cost and water-use efficiency of arbuscular mycorrhizal durum wheat grown under drought stress. Mycorrhiza 8, 41-45.Google Scholar
  3. Al-Karaki G N and Al-Raddad A 1997 Drought stress and VA mycorrhizal fungi effects on growth and nutrient uptake of two wheat genotypes differing in drought resistance. Crop Res. (Hisar) 13, 245-257.Google Scholar
  4. Anderson G C, Fillery I R P, Dunin F X, Dolling P and Asseng S 1998 Nitrogen and water flows under pasture-wheat and lupin-wheat rotations in deep sands in Western Australia. 2. Drainage and nitrate leaching. Austr. J. Agric. Res. 49, 345-361.Google Scholar
  5. Andriolo J, Pereira P A A and Henson R A 1994 Variability among wild Phaseolus vulgaris lines for traits related to biological N2fixation. Pesquisa Agropecuaria Brasileira 29, 831-837.Google Scholar
  6. Armero J, Lopez-Valbuena R, Jorrin J and Tena M 1994 Contribution of different plant organs to the accumulation and secretion of phenolic compounds in glutathione-treated chickpea (Cicer arietinum) seedlings. Acta Hortic. 381, 506-509.Google Scholar
  7. Balaji B, Poulin M J, Vierheilig H and Piche Y 1995 Responses of an arbuscular mycorrhizal fungus, Gigaspora margarita, to exudates and volatiles from the Ri T-DNA-transformed roots of nonmycorrhizal and mycorrhizal mutants of Pisum sativum L. Sparkle. Exp. Mycol. 19, 275-283.Google Scholar
  8. Balota E L, Lopes E S, Hungria M and Dobereiner J 1995 Interactions and physiological effects of diazotrophic bacteria and arbuscular mycorrhizas on cassava. Pesquisa Agropecuaria Brasileira 30, 1335-1345.Google Scholar
  9. Baon J B, Smith S E and Alston A M 1993 Mycorrhizal responses of barley cultivars differing in P efficiency. Plant Soil 157, 97-105.Google Scholar
  10. Barker S J, Stummer B, Gao L, Dispain I, O'Connor P J and Smith S E 1998 A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation. Plant J. 15, 791-797.Google Scholar
  11. Becard G and Piche Y 1990 Physiological factors determining vesicular-arbuscular mycorrhizal formation in host and nonhost Ri T-DNA transformed roots. Can. J. Bot. 68, 1260-1264.Google Scholar
  12. Bell M J, Wright G C, Suryantini and Peoples M B 1994 The N2-fixing capacity of peanut cultivars with differing assimilate partitioning characteristics. Aust. J. Agric. Res. 45, 1455-1468.Google Scholar
  13. Bhagwat A A and Keister D L 1992 Identification and cloning of Bradyrhizobium japonicum genes expressed strain selectively in soil and rhizosphere. Appl. Environ. Microbiol. 58, 1490-1495.Google Scholar
  14. Blumenthal J M and Russelle M P 1996 Subsoil nitrate uptake and symbiotic dinitrogen fixation by alfalfa. Agron. J. 88, 909-915.Google Scholar
  15. Boivin C, Barran L R, Malpica C A and Rosenberg C 1991 Genetic analysis of a region of the Rhizobium meliloti pSym plasmid specifying catabolism of trigonelline, a secondary metabolite present in legumes. J. Bacteriol. 173, 2809-2817.Google Scholar
  16. Bolanos-Vasquez M C and Werner D 1997 Effects of Rhizobium tropici, R. etli, and R. leguminosarum bv. phaseoli on nod gene-inducing flavonoids in root exudates of Phaseolus vulgaris. Mol. Plant-Microbe Interact. 10, 339-346.Google Scholar
  17. Borisov A Y, Rozov S M, Tsyganov V E, Kulikova O A, Kolycheva A N, Yakobi L M, Ovtsyna A O and Tikhonovich I A 1994 Identification of symbiosis genes in pea (Pisum sativum L.) by means of induced mutagenesis. Genetika (Moskva) 30, 1484-1494.Google Scholar
  18. Boyetchko S M and Tewari J P 1995 Susceptibility of barley cultivars to vesicular-arbuscular mycorrhizal fungi. Can. J. Plant Sci. 75, 269-275.Google Scholar
  19. Bradbury S M, Peterson R L and Bowley S R 1993 Further evidence for a correlation between nodulation genotypes in alfalfa (Medicago sativa L.) and mycorrhiza formation. New Phytol. 124, 665-673.Google Scholar
  20. Burdman S, Volpin H, Kigel J, Kapulnik Y and Okon Y 1996 Promotion of nod gene inducers and nodulation in common bean (Phaseolus vulgaris) roots inoculated with Azospirillum brasilense Cd. Appl. Environ. Microbiol. 62, 3030-3033.Google Scholar
  21. Buttery B R, Park S J, Van Berkum P 1997 Effects of common bean (Phaseolus vulgaris L.) cultivar and rhizobium strain on plant growth, seed yield and nitrogen content. Can. J. Plant Sci. 77, 347-351.Google Scholar
  22. Caba J M, Lluch C and Ligero F 1993 Genotypic differences in nitrogen assimilation in Vicia faba: effect of nitrate. Plant Soil 151, 167-174.Google Scholar
  23. Castellanos J Z, Pena-Cabriales J J and Acosta-Gallegos J A 1996 15N-determined dinitrogen fixation capacity of common bean (Phaseolus vulgaris) cultivars under water stress. J. Agric. Sci. 126, 327-333.Google Scholar
  24. Christiansen-Weniger C, Groneman A F and Van Veen J A 1992 Associative N2 fixation and root exudation of organic acids from wheat cultivars of different aluminium tolerance. Plant Soil 139, 167-174.Google Scholar
  25. Cooper J E, Wood M and Bjourson A J 1985 Nodulation of Lotus peduncululatus in acid rooting solution by fast-and slow-growing rhizobia. Soil Biol. Biochem. 17, 487-492.Google Scholar
  26. Cordovilla M P, Ligero F, Lluch C and Cordovilla M P 1995 Influence of host genotypes on growth, symbiotic performance and nitrogen assimilation in faba bean (Vicia faba L.) under salt stress. Plant Soil 172, 289-297.Google Scholar
  27. Dakora F D, Joseph C M and Phillips D A 1993 Common bean root exudates contain elevated levels of daidzein and coumestrol in response to Rhizobium inoculation. Mol. Plant-Microbe Interact. 6, 665-668.Google Scholar
  28. Dangaria C J, Parameshwarappa R, Salimath P M and Annigeri B S 1994 Genetic divergence for nodulating characters in chickpea. Legume Research 17, 32-36.Google Scholar
  29. De Chueire L M and Hungria M 1997 N2-fixation ability of Brazilian soybean cultivars with Sinorhizobium fredii and Sinorhizobium xinjiangensis. Plant Soil 196, 1-5.Google Scholar
  30. De la Bastide P Y, Kropp B R and Piche Y 1995 Population structure and mycelial phenotypic variability of the ectomycorrhizal basidiomycete Laccaria bicolor (Maire) Orton. Mycorrhiza 5, 371-379.Google Scholar
  31. Dobereiner J 1997 Biological nitrogen fixation in the tropics: social and economic contributions. Soil Biol. Biochem. 29, 771-774.Google Scholar
  32. Dockendorff T C, Sanjuan J, Grob P and Stacey G 1994 NolA represses nod gene expression in Bradyrhizobium japonicum. Mol. Plant-Microbe Interact. 7, 596-602.Google Scholar
  33. Duc G 1995 Mutagenesis of faba bean (Vicia faba L.) and the identification of five different genes controlling no nodulation, ineffective nodulation or supernodulation. Euphytica 83, 147-152.Google Scholar
  34. Duc G, Trouvelot A, Gianinazzi-Pearson V and Gianinazzi S 1989 First report of non-mycorrhizal plant mutants (Myc?) obtained in pea (Pisum sativum L.) and faba bean (Vicia faba L.). Plant Sci. 60, 215-222.Google Scholar
  35. Duponnois R, Garbaye J, Bouchard D and Churin J L 1993 The fungus-specificity of mycorrhization helper bacteria (MHBs) used as an alternative to soil fumigation for ectomycorrhizal inoculation of bare-root Douglas-fir planting stocks with Laccaria laccata. Plant Soil 157, 257-262.Google Scholar
  36. Eisenschenk L, Diebold R, Perez-Lesher J, Peterson A C, Peters N K and Noel K D 1994 Inhibition of Rhizobium etli polysaccharide mutants by Phaseolus vulgaris root compounds. Appl. Environ. Microbiol. 60, 3315-3322.Google Scholar
  37. El-Ghachtouli N, Paynot M, Morandi D, Martin-Tanguy J and Gianinazzi S 1995 The effect of polyamines on endomycorrhizal infection of wild-type Pisum sativum, cv. Frisson (nod+myc+) and two mutants (nod-myc+ and nod-myc-). Mycorrhiza 5, 189-192.Google Scholar
  38. El-Shanshoury A R 1995 Interactions of Azotobacter chroococcum, Azospirillum brasilense and Streptomyces mutabilis, in relation to their effect on wheat development. J. Agron. Crop Sci. 175, 119-127.Google Scholar
  39. Espiritu B M, Lales E H and Palacpac N Q 1993 Interaction effects of Bradyrhizobium strain and cultivar in mungbean (Vigna radiata (L.) Wilczek). Philippine J. Biotechnol. 4, 61-68.Google Scholar
  40. Evans J, Chalk P M and O'Connor G E 1995 Potential for increasing N2 fixation of field pea through soil management and genotype. Biol. Agric. Hortic. 12, 97-112.Google Scholar
  41. Fedi S, Montaini P and Favilli F 1992 Chemotactic response of Azospirillum toward root exudates of C3 and C4 plants. Symbiosis 13, 101-105.Google Scholar
  42. Fesenko A N, Provorov N A, Orlova I F, Orlov V P and Simarov B V 1995 Selection of Rhizobium leguminosarum bv. viceae strains for inoculation of Pisum sativum L. cultivars: analysis of symbiotic efficiency and nodulation competitiveness. Plant Soil 172, 189-198.Google Scholar
  43. Fobert P R, Roy N, Nash J H E and Iyer V N 1991 Procedure for obtaining efficient root nodulation of a pea cultivar by a desired Rhizobium strain and preempting nodulation by other strains. Appl. Environ. Microbiol. 57, 1590-1594.Google Scholar
  44. Fyson A and Sprent J I 1982 The development of primary root nodules on Vicia faba L. grown at two temperatures. Ann. Bot. 50, 681-692.Google Scholar
  45. Gagnon H and Ibrahim R K 1997 Effects of various elicitors on the accumulation and secretion of isoflavonoids in white lupin. Phytochemistry 44, 1463-1467.Google Scholar
  46. Gagnon H and Ibrahim R K 1998 Aldonic acids: a novel family of nod gene inducers of Mesorhizobium loti, Rhizobium lupini, and Sinorhizobium meliloti. Mol. Plant-Microbe Interact. 11, 988-998.Google Scholar
  47. Garcia de Salamone I E, Dobereiner J, Urquiaga S and Boddey R M 1997 Biological nitrogen fixation in Azospirillum strain-maize genotype associations as evaluated by the 15N isotope dilution technique. Biol. Fertil. Soils 23, 249-256.Google Scholar
  48. Gemell L G and Roughley R J 1993 Field evaluation in acid soils of strains of Rhizobium leguminosarum bv. trifolii selected for their tolerance or sensitivity to acid soil factors in agar medium.Soil Biol. Biochem. 25, 1447-1452.Google Scholar
  49. Gianinazzi-Pearson V 1996 Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8, 1871-1883.Google Scholar
  50. Gianinazzi-Pearson V, Branzanti B and Gianinazzi S 1989 In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7, 243-255.Google Scholar
  51. Gianinazzi-Pearson V, Gollote A, Lherminier J, Tisserant B, Franken P, Dumas-Gaudot E, Lemoine M C, Van Tuinen D and Gianinazzi S 1995 Cellular and molecular approaches in the characterization of symbiotic events in functional arbuscular mycorrhizal associations. Can. J. Bot. 73, S526-S532.Google Scholar
  52. Godbold D L, Jentschke G, Wintr S and Marschner P 1998 Ectomycorrhizas and amelioration of metal stress in forest trees. Chemosphere 36, 757-762.Google Scholar
  53. Graham P H, Viteri S E, Mackie F, Vargas A T and Palacios A 1982 Variation in acid soil tolerance among strains of Rhiozobium phaseoli. Field Crops Res. 5, 121-128.Google Scholar
  54. Hardarson G, Bliss F A, Cigales-Rivero M R, Henson R A, Kipe-Nolt J A, Longeri L, Manrique A, Pena-Cabriales J J, Pereira P A A, Sanabria C A and Tsai S M 1993 Genotypic variation in biological nitrogen fixation by common bean. Plant Soil 152, 59-70.Google Scholar
  55. Harper J E, Corrigan K A, Barbera A C and Abd-Alla M H 1997 Hypernodulation of soybean, mung bean, and hyacinth bean is controlled by a common shoot signal. Crop Sci. 37, 1242-1246.Google Scholar
  56. Hartmann A, Giraud J J and Catroux G 1998 Genotypic diversity of Sinorhizobium (formerly Rhizobium) meliloti strains isolated directly from a soil and from nodules of alfalfa (Medicago sativa) grown in the same soil. FEMS Microbiol. Ecol. 25, 107-116.Google Scholar
  57. Hartwig U A, Joseph C M and Phillips D A 1991 Flavonoids released naturally from alfalfa seeds enhance growth rate of Rhizobium meliloti. Plant Physiol. 95, 797-803.Google Scholar
  58. Hernandez G, Vasquez H, Toscano V, Sanchez M, Penate-T, Franchi-Alfaro A, Mendez N and Drevon J J 1993 Nodulation and growth of common bean (Phaseolus vulgaris L.) cultivars in hydroponic culture and in the field. Trop. Agric. 70, 230-234.Google Scholar
  59. Hernandez G, Ramirez M, Suarez R and Fuentes S I 1995 Root exuded nod-gene inducing signals limit the nodulation capacity of different alfalfa varieties with Rhizobium meliloti. Plant Cell Rep. 14, 626-629.Google Scholar
  60. Heron D S, Ersek T, Krishnan H B and Pueppke S G 1989 Nodulation mutants of Rhizobium fredii USDA257. Mol. Plant-Microbe Interact. 2, 4-10.Google Scholar
  61. Honma M A, Asomaning M and Ausubel F 1990 Rhizobium meliloti nodD genes mediate host-specific activation of nodABC. J. Bacteriol. 172, 901-911.Google Scholar
  62. Howieson J G 1995 Characteristics of an ideotype acid tolerant pasture legume symbiosis in Mediterranean agriculture. Plant Soil 171, 71-76.Google Scholar
  63. Howieson J G, Ewing M A and D'Anuono M F 1988 Selection for acid tolerance in Rhizobium meliloti. Plant Soil 105, 179-188.Google Scholar
  64. Howieson J G, Robson A D and Abbott L K 1992 Acid-tolerant species of Medicago produce root exudates at low pH which induce the expression of nodulation genes in Rhizobium meliloti. Aust. J. Plant Physiol. 19, 287-296.Google Scholar
  65. Howieson J G, Loi A and Carr S J 1995 Biserrula pelecinus L.-a legume pasture species with potential for acid, duplex soils which is nodulated by unique root-nodule bacteria. Aust. J. Agric. Res. 46, 997-1009.Google Scholar
  66. Hungria M and Phillips D A 1993 Effects of a seed color mutation on rhizobial nod-gene-inducing flavonoids and nodulation in common bean. Mol. Plant-Microbe Interact. 6, 418-422.Google Scholar
  67. Hungria M, Boddey L H, Santos M A and Vargas M A T 1998 Nitrogen fixation capacity and nodule occupancy by Bradyrhizobium japonicum and B. elkanii strains. Biol. Fertil. Soils 27, 393-399.Google Scholar
  68. Hurek T, Tan Z, Egener T, Engelhard M, Gyaneshwar P, Ladha J K and Reinhold-Hurek B 1999 Novel nitrogen-fixing bacteria associated with the root interior of rice. In Proceedings of the Meeting of the Third Working Group on Biological Nitrogen Fixation in Rice, August 9-12, 1999. IRRI, Manila, Philippines.Google Scholar
  69. Ibrahim K K, Arunachalam V, Rao P S K and Tilak K V B R 1995 Seasonal response of groundnut genotypes to arbuscular mycorrhiza-Bradyrhizobium inoculation. Microbiol. Res. 150, 218-224.Google Scholar
  70. Ikeda K, Toyota K and Kimura M 1998 Role of extracellular pectinases in the rhizoplane competence of a rhizobacterium Burkholderia pickettii MSP3Rif. Soil Biol. Biochem. 30, 323-329.Google Scholar
  71. Jagnow G 1990 Differences between cereal crop cultivars in root-associated nitrogen fixation, possible causes of variable yield response to seed inoculation. Plant Soil 123, 255-259.Google Scholar
  72. James E K 2000 Nitrogen fixation in endophytic and associative symbiosis. Field Crops Res. 65, 197-209.Google Scholar
  73. Janczarek M, Urbanik-Sypniewska T and Skorupska A 1997 Effect of authentic flavonoids and the exudate of clover roots on growth rate and inducing ability of nod genes of Rhizobium leguminosarum bv. trifolii. Microbiol. Res. 152, 93-98.Google Scholar
  74. Jimenez-Zurdo J I, Garcia-Rodriguez F M and Toro N 1997 The Rhizobium meliloti putA gene: its role in the establishment of the symbiotic interaction with alfalfa. Mol. Microbiol. 23, 85-93.Google Scholar
  75. Kape R, Wex K, Parniske M, Gorge E, Wetzel A and Werner D 1992 Legume root metabolites and VA-mycorrhiza development. J. Plant Physiol. 141, 54-60.Google Scholar
  76. Karagiannidis N, Nikolaou N and Mattheou A 1995 Influence of three VA-mycorrhiza species on the growth and nutrient uptake of three grapevine rootstocks and one table grape cultivar. Vitis 34, 85-89.Google Scholar
  77. Katsunori I, Makie K, Perigio F B Jr and Shoichiro A 1995 Induction of nodule-like structures on oilseed rape by inoculation with rhizobia in the presence of helper bacteria. Soil Sci. Plant Nutr. 41, 313-320.Google Scholar
  78. Keyser H H and Cregan P B 1987 Nodulation and competition for nodulation of selected soybean genotypes among Bradyrhizobium japonicum serogroup 123 isolates. Appl. Environ. Microbiol. 53, 2631-2635.Google Scholar
  79. Kouchi H, Takane K, So R B, Ladha J K and Reddy P M 1999 Rice ENOD40: isolation and expression analysis in rice and transgenic soybean root nodules. Plant J. 18, 121-129.Google Scholar
  80. Kuykendall L D 1989 Influence of Glycine max nodulation on the persistence in soil of a genetically marked Bradyrhizobium japonicum strain. Plant Soil 116, 275-277.Google Scholar
  81. Ladha J K, De Bruijn F J and Malik K A (eds.) 1997 Opportunities for Biological Nitrogen Fixation in Rice and Other Non-Legumes. Kluwer Academic Publishers, Dodrecht.Google Scholar
  82. Ledgard S F 1989 Nitrogen fixation and transfer to associated grasses by white clover cultivars under dairy cow grazing. In Proceedings of the XVI International Grassland Congress, 4-11 October 1989, Nice, France. pp. 169-170.Google Scholar
  83. Leung K and Bottomley P J 1987 Influence of phosphate on the growth and nodulation characteristics of Rhizobium trifolii. Appl. Environ. Microbiol. 53, 2098-2105.Google Scholar
  84. Leung K and Bottomley P J 1994 Growth and nodulation characteristics of subclover (Trifolium subterraneum L.) and Rhizobium leguminosarum bv. trifolii at different soil water potentials. Soil Biol. Biochem. 26, 805-812.Google Scholar
  85. Leung K, Strain S R, De Bruijn F J and Bottomley P J 1994 Genotypic and phenotypic comparisons of chromosomal types within an indigenous soil population of Rhizobium leguminosarum bv. trifolii. Appl. Environ. Microbiol. 60, 416-426.Google Scholar
  86. Lohrke S M, Orf J H, Martinez-Romero E and Sadowsky M J 1995 Host-controlled restriction of nodulation by Bradyrhizobium japonicum strains in serogroup 110. Appl. Environ. Microbiol. 61, 2378-2383.Google Scholar
  87. Luna R and Planchon C 1995 Genotype × Bradyrhizobium japonicum strain interactions in dinitrogen fixation and agronomic traits of soybean (Glycine max L. Merr.). Euphytica 86, 127-134.Google Scholar
  88. Lupwayi N Z, Haque I and Holl F B 1997 Strain-specific response of Trifolium semipilosum to inoculation with Rhizobium and the significance of waterlogging in Vertisols. J. Agric. Sci. 129, 439-446.Google Scholar
  89. Martin-Laurent F, Van Tuinen D, Dumas-Gaudot E, Gianinazzi-Pearson V, Gianinazzi S and Franken P 1997 Differential display analysis of RNA accumulation in arbuscular mycorrhiza of pea and isolation of a novel symbiosis-regulated plant gene. Mol. Gen. Genet. 256, 37-44.Google Scholar
  90. Maxwell C A, Hartwig U A, Joseph C M and Phillips D A 1989 A chalcone and two related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol. 91, 842-847.Google Scholar
  91. McKay I A and Djordjevic M A 1993 Production and excretion of Nod metabolites by Rhizobium leguminosarum bv. trifolii are disrupted by the same environmental factors that reduce nodulation in the field. Appl. Environ. Microbiol. 59, 3385-3392.Google Scholar
  92. McKhann H I, Paiva N L, Dixon R A and Hirsch A M 1997 Chalcone synthase transcripts are detected in alfalfa root hairs following inoculation with wild-type Rhizobium meliloti. Mol. Plant-Microbe Interact. 10, 50-58.Google Scholar
  93. McLoughlin T J, Alt S G and Merlo P A 1990 Persistence of introduced Bradyrhizobium japonicum strains in forming nodules in subsequent years after inoculation in Wisconsin soils. Can. J. Microbiol. 36, 794-800.Google Scholar
  94. Mergaert P, Van Montagu M and Holsters M 1997 Molecular mechanisms of Nod factor diversity. Mol. Microbiol. 25, 811-817.Google Scholar
  95. Moens S, Bastelaere E V, Broek A V, Lambrecht M, Keijers V, Revers L F, Passaglia L M P, Schrank I S and Vanderleyden J 1997 Azospirillum genes involved in chemotaxis and adhesion to plant roots. In Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture. A Legocki, H Bothe and A Puhler (Eds.). pp. 123-127. NATO Advanced Research Workshop, Poznan, Poland.Google Scholar
  96. Mullen M D, Israel D W and Wollum A G II 1988 Effects of Bradyrhizobium japonicum and soybean (Glycine max (L.) Merr.) phosphorus nutrition on nodulation and dinitrogen fixation. Appl. Environ. Microbiol. 54, 2387-2392.Google Scholar
  97. Munns N D 1970 Nodulation of Medicago sativa in solution culture. V. Calcium and pH requirements during infection. Plant Soil 32, 90-102.Google Scholar
  98. Murphy P J, Wexler W, Grzemski W, Rao J P and Gordon D 1995 Rhizopines-their role in symbiosis and competition. Soil Biol. Biochem. 27, 525-529.Google Scholar
  99. Murphy P J, Langridge P and Smith S 1997 Cloning plant genes differentially expressed during colonisation of Hordeum vulgare (L.) roots by the vesicular arbuscular-mycorrhizal fungus Glomus intraradices Schenck & Smith. New Phytol. 135, 291-301.Google Scholar
  100. Natsvaladze M Y, Nitse L K and Sakharova S N 1992 Free-living and associative diazotrophs in the rhizocoenosis of tea. Izvestiya Timiryazevskoi Sel'skokhozyaistvennoi Akademii 2, 95-102.Google Scholar
  101. Nemec S and Datnoff L 1993 Pepper and tomato cultivar responses to inoculation with Glomus intraradices. Adv. Hortic. Sci. 7, 161-164.Google Scholar
  102. Neo H H, Hunt S and Layzell D B 1996 Can genotypes of soybean (Glycine max) selected for nitrate tolerance provide good 'models' for studying the mechanism of nitrate inhibition of nitrogenase activity? Physiol. Plant. 98, 653-660.Google Scholar
  103. Nour S M, Cleyet-Marel J C, Beck D, Effosse A and Fernandes M P 1994 Genotypic and phenotypic diversity of Rhizobium isolated from chickpea (Cicer arietinum L.). Can. J. Microbiol. 40, 345-354.Google Scholar
  104. O'Connell K P, Goodman R M and Handelsman J 1996 Engineering the rhizosphere: expressing a bias. Trends Biotechnol. 14, 83-88.Google Scholar
  105. Ofosu Budu K G, Fujita K, Gamo T and Akao S 1993 Dinitrogen fixation and nitrogen release from roots of soybean cultivar Bragg and its mutants nts1116 and nts1007. Soil Sci. Plant Nutr. 39, 497-506.Google Scholar
  106. Orgambide G G, Philip-Hollingsworth S, Mateos P F, Hollingsworth R I and Dazzo F B 1996 Subnanomolar concentrations of membrane chitolipooligosaccharides from Rhizobium leguminosarum biovar trifolii are fully capable of eliciting symbiosis-related responses on white clover. Plant Soil 186, 93-98.Google Scholar
  107. Paffetti D, Daguin F, Fancelli S, Gnocchi S, Lippi F, Scotti C and Bazzicalupo M 1998 Influence of plant genotype on the selection of nodulating Sinorhizobium meliloti strains by Medicago sativa. Antonie van Leeuwenhoek 73, 3-8.Google Scholar
  108. Pandya S and Desai A 1998 Localization of nod, nif, and acidic exopolysaccharide determinants on a large plasmid in slow-growing cowpea Rhizobium sp. S2. Curr. Microbiol. 36, 36-40.Google Scholar
  109. Pandya S, Uchil P, Subramanian M and Desai A 1998 Determination of host specificity of cowpea miscellany Rhizobium spp. by nodABC-lacZ fusion. Curr. Microbiol. 36, 361-364.Google Scholar
  110. Pazdernik D L, Graham P H and Orf J H 1997 Variation in the pattern of nitrogen accumulation and distribution in soybean. Crop Sci. 37, 1482-1486.Google Scholar
  111. Phillips D A and Tsai S M 1992 Flavonoids as plant signals to rhizosphere microbes. Mycorrhiza 1, 55-58.Google Scholar
  112. Phillips D A, Wery J, Joseph C M, Jones A D and Teuber L R 1995 Release of flavonoids and betaines from seeds of seven Medicago species. Crop Sci. 35, 805-808.Google Scholar
  113. Poulin M J, Bel-Rhlid R, Piche Y and Chenevert R 1993 Flavonoids released by carrot (Daucus carota) seedlings stimulate hyphal development of vesicular-arbuscular mycorrhizal fungi in the presence of optimal CO2 enrichment. J. Chem. Ecol. 19, 2317-2327.Google Scholar
  114. Prayitno J, Stefaniak J, McIver J, Weinman J J, Dazzo F B, Ladha J K, Barraquio W, Yanni Y G and Rolfe B G 1999 Interactions of rice seedlings with bacteria isolated from rice roots. Aust. J. Plant Physiol. 26, 521-535.Google Scholar
  115. Prevost D and Bromfield E S P 1991 Effect of low root temperature on symbiotic nitrogen fixation and competitive nodulation of Onobrychis viciifolia (sainfoin) by strains of arctic and temperate rhizobia. Biol. Fertil. Soil 12, 161-164.Google Scholar
  116. Pueppke S G, Bolanos-Vasquez M C, Werner D, Bec-Ferte M P, Prome J C and Krishnan H B 1998 Release of flavonoids by the soybean cultivars McCall and Peking and their perception as signals by the nitrogen-fixing symbiont Sinorhizobium fredii. Plant Physiol. 117, 599-608.Google Scholar
  117. Raffin A and Roumet P 1994 Shoot-root control of nitrate tolerance of N2 fixation in spontaneously tolerant soybean lines: reciprocal grafting experiments. Agronomie 14, 473-480.Google Scholar
  118. Raghuwanshi A, Dudeja S S and Khurana A L 1994 Effect of temperature on flavonoid production in pigeonpea (Cajanus cajan (L.) Millsp) in relation to nodulation. Biol. Fertil. Soils 17, 314-316.Google Scholar
  119. Rai R 1991a Strain-specific salt tolerance and chemotaxis of Azospirillum brasilense and their associative N-fixation with finger millet in saline calcareous soil. Plant Soil 137, 55-59.Google Scholar
  120. Rai R 1991b Effects of soil acidity factors on interaction of chickpea (Cicer arietinum L.) genotypes and Rhizobium strains: symbiotic N-fixation, grain quality and grain yield in acid soils. In Plant-Soil Interactions at Low pH. R J Wright, V C Baligar and R P Murrmann (Eds.). pp. 619-631. Kluwer Academic Publishers, Dordrecht.Google Scholar
  121. Rai R 1992 Effect of acidity factors on aspects of symbiotic N2 fixation of Lens culinaris in acid soils. J. Gen. Appl. Microbiol. 38, 391-406.Google Scholar
  122. Ramanathan N, Ramamurthy R and Balasubramanian V 1997 Nitrogenase activity and Azospirillum population in the rhizosphere of rice cultivars. Indian J. Microbiol. 37, 211-212.Google Scholar
  123. Rao V R, Ramakrishnan B, Adhya T K, Kanungo P K and Nayak D N 1998 Review: current status and future prospects of associative nitrogen fixation in rice. World J. Microbiol. Biotechnol. 14, 621-633.Google Scholar
  124. Reddy P M, Aggarwal R K, Ramos M C, Ladha J K, Brar D S and Kouchi H 1999 Widespread occurrence of the homologues of the early nodulin (ENOD) genes in Oryza species and related grasses. Biochem. Biophys. Res. Commun. 258, 148-154.Google Scholar
  125. Reddy P M, Ladha J K, So R B, Hernandez R J, Ramos M C, Angeles O R, Dazzo F B and De Bruijn F J 1997 Rhizobial communication with rice roots: induction of phenotypic changes, mode of invasion and extent of colonization. Plant Soil 194, 81-98.Google Scholar
  126. Reddy P M, Ladha J K, Ramos M C, Maillet F, Hernandez R J, Torrizo L B, Oliva N P, Datta S K and Datta K 1998 Rhizobial lipochitooligosaccharide nodulation factors activate expression of the legume early nodulin gene ENOD12 in rice. Plant J. 14, 693-702.Google Scholar
  127. Rolfe B G, Djordjevic M A, Weinman J J, McIver J, Gärtner E, Chen C, Creaser E H, Britt K, Lawson C G R, De Boer M H, McKay I A, Shoobridge M V, De Majnik J, Pittock C, Broderick K and Delbridge T 1995 Molecular genetic analysis of subterranean clover-microbe interactions. Soil Biol. Biochem. 27, 485-490.Google Scholar
  128. Rolfe B G, Djordjevic M A, Weinman J J, Mathesius U, Pittock C, Gärtner E, Ride K M, Dong Z M, McCully M and McIver J 1997 Root morphogenesis in legumes and cereals and the effect of bacterial inoculation on root development. Plant Soil 194, 131-144.Google Scholar
  129. Rosenblueth M, Hynes M F and Martinez-Romero E 1998 Rhizobium tropici teu genes involved in specific uptake of Phaseolus vulgaris bean-exudate compounds. Mol. Gen. Genet. 258, 587-598.Google Scholar
  130. Rossbach S, Kulpa D A, Rossbach U and De Bruijn F J 1994 Molecular and genetic characterization of the rhizopine catabolism (mocABRC) genes of Rhizobium meliloti L5-30. Mol. Gen. Genet. 245, 11-24.Google Scholar
  131. Sanginga N, Danso S K A and Bowen G D 1992 Variation in growth, sources of nitrogen and N-use efficiency by provenances of Gliricidia sepium. Soil Biol. Biochem. 24, 1021-1026.Google Scholar
  132. Sanjuan J and Olivares J 1991 Nifa-NtrA regulatory system activates transcription of nfe, a gene locus involved in nodulation competitiveness of Rhizobium meliloti. Arch. Microbiol. 155, 543-548.Google Scholar
  133. Sattar M A, Quader M A and Danso S K A 1995 Nodulation, N2 fixation and yield of chickpea as influenced by host cultivar and Bradyrhizobium strain differences. Soil Biol. Biochem. 27, 725-727.Google Scholar
  134. Schloter M and Hartmann A 1998 Endophytic and surface colonization of wheat roots (Triticum aestivum) by different Azospirillum brasilense strains studied with strain-specific monoclonal antibodies. Symbiosis 25, 159-179.Google Scholar
  135. Schmidt P E, Parniske M and Werner D 1992 Production of the phytoalexin glyceollin I by soybean roots in response to symbiotic and pathogenic infection. Bot. Acta 105, 18-25.Google Scholar
  136. Schmidt P E, Broughton W J and Werner D 1994 Nod factors of Bradyrhizobium japonicum and Rhizobium sp. NGR234 induce flavonoid accumulation in soybean root exudate. Mol. Plant-Microbe Interact. 7, 384-390.Google Scholar
  137. Serraj R and Sinclair T R 1998 Soybean cultivar variability for nodule formation and growth under drought. Plant Soil 202, 159-166.Google Scholar
  138. Shelp B J, Kaiser B N and Deschesne A M 1998 Registration of five near-isogenic genetic stocks of 'Juneau' pea with altered nodulation and nitrate reductase deficiency: A317I, nod3I, A317nod3I, E135I, and R25I. Crop Sci. 38, 554.Google Scholar
  139. Shrestha R K and Ladha J K 1996 Genotypic variation in promotion of rice dinitrogen fixation as determined by nitrogen-15 dilution. Soil Sci. Soc. Am. J. 60, 1815-1821.Google Scholar
  140. Smith S E, Gianinazzi-Pearson V, Koide R and Cairney J W G 1994 Nutrient transport in mycorrhizas: structure, physiology and consequences for efficiency of the symbiosis. Plant Soil 159, 103-113.Google Scholar
  141. Soejima H, Sugiyama T and Ishihara K 1992 Changes in cytokinin activities and mass spectrometric analysis of cytokinins in root exudates of rice plants (Oryza sativa L.). Comparison between cultivars Nipponbare and Akenohoshi. Plant Physiol. 100, 1724-1729.Google Scholar
  142. Song L, Carroll B J, Gresshoff P M and Herridge D F 1993 Field assessment of supernodulating genotypes of soybean for yield, N2 fixation and benefit to subsequent crops. Soil Biol. Biochem. 27, 563-569.Google Scholar
  143. Spiller H, Stallings W J, Woods T and Gunasekaran M 1993 Requirement for direct association of ammonia-excreting Anabaena variabilis mutant (SA-1) with roots for maximal growth and yield of wheat. Appl. Microbiol. Biotechnol. 40, 557-566.Google Scholar
  144. Tagu D and Martin F 1996 Molecular analysis of cell wall proteins expressed during the early steps of ectomycorrhiza development. New Phytol. 133, 73-85.Google Scholar
  145. Tawaraya K, Hashimoto K and Wagatsuma T 1998 Effect of root exudate fractions from P-deficient and P-sufficient onion plants on root colonisation by the arbuscular mycorrhizal fungus Gigaspora margarita. Mycorrhiza 8, 67-70.Google Scholar
  146. Tiwari R P, Reeve W G, Glenn A R 1992 Mutations conferring acid sensitivity in the acid-tolerant strains Rhizobium meliloti WSM419 and Rhizobium leguminosarum biovar viciae WSM710. FEMS Microbiol. Lett. 100, 107-112.Google Scholar
  147. Toro M, Azcon R and Barea J M 1997 Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability and nutrient cycling. Appl. Environ. Microbiol. 63, 4408-4412.Google Scholar
  148. Toro M, Azcon R and Barea J M 1998 The use of isotopic dilution techniques to evaluate the interactive effects of Rhizobium genotype, mycorrhizal fungi, phosphate-solubilizing rhizobacteria and rock phosphate on nitrogen and phosphorus acquisition by Medicago sativa. New Phytol. 138, 265-273.Google Scholar
  149. Trese A T 1995 A single dominant gene inMcCall soybean prevents effective nodulation with Rhizobium fredii USDA257. Euphytica 81, 279-282.Google Scholar
  150. Tsyganov V E, Morzhina E V, Stefanov S Y, Borisov A Y, Lebsky V K and Tikhonovich I A 1998 The pea (Pisum sativum L.) genes sym33 and sym40 control infection thread formation and root nodule function. Mol. Gen. Genet. 295, 491-503.Google Scholar
  151. Utrup L J, Cary A J and Norris J H 1993 Five nodulation mutants of white sweetclover (Melilotus alba Desr.) exhibit distinct phenotypes blocked at root hair curling, infection thread development, and nodule organogenesis. Plant Physiol. 103, 925-932.Google Scholar
  152. Van Rhijn P and Vanderleyen J 1995 The Rhizobium-plant symbiosis. Microbiol. Rev. 59, 124-142.Google Scholar
  153. Van Rhijn P, Desair J, Vlassak K and Vanderleyden J 1994 Functional analysis of nodD genes of Rhizobium tropici CIAT899. Mol. Plant-Microbe Interact. 7, 666-677.Google Scholar
  154. Vlassak K M and Vanderleyden J 1997 Factors influencing nodule occupancy by inoculant rhizobia. Crit. Rev. Plant Sci. 16, 163-229.Google Scholar
  155. Waschutza S, Hofmann N, Niemann E G and Fendrik I 1992 Investigations on root exudates of Korean rice. Symbiosis 13, 181-189.Google Scholar
  156. Wood M, Cooper J E and Holding A J 1984 Soil acidity factors and nodulation of Trifolium repens. Plant Soil 78, 367-79.Google Scholar
  157. Wojtaszek P, Stobiecki M and Gulewicz K 1993 Role of nitrogen and plant growth regulators in the exudation and accumulation of isoflavonoids by roots of intact white lupin (Lupinus albus L.) plants. J. Plant Physiol. 142, 689-694.Google Scholar
  158. Wu P, Zhang G, Ladha J K, McCouch S R and Huang N 1995 Molecular-marker-facilitated investigation on the ability to stimulate N2 fixation in the rhizosphere by irrigated rice plants. Theor. Appl. Genet. 91, 1177-1183.Google Scholar
  159. Xavier L J C and Germida J J 1998 Response of spring wheat cultivars to Glomus clarum NT4 in a P-deficient soil containing arbuscular mycorrhizal fungi. Can. J. Soil Sci. 78, 481-484.Google Scholar
  160. Yanni Y G, Rizk R Y, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, De Bruijn F, Stoltzfus J, Buckley D, Schmidt T M, Mateos P F, Ladha J K and Dazzo F B 1997 Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194, 99-114.Google Scholar
  161. Zhang X-K and Rengel Z 1999 Gradients of pH and ammonium and phosphorus concentration between the banded fertilizer and wheat roots. Aust. J. Agric. Res. 50, 365-373.Google Scholar
  162. Zhang F, Dijak M, Smith D L, Lin J, Walsh K, Voldeng H, Macdowell F and Layzell D B 1997 Nitrogen fixation and nitrate metabolism for growth of six diverse soybean (Glycine max (L.) Merr.) genotypes under low temperature stress. Environ. Exp. Bot. 38, 49-60.Google Scholar
  163. Zuanazzi J A S, Clergeot P H, Quirion J C, Husson H P, Kondorosi A and Ratet P 1998 Production of Sinorhizobium meliloti nod gene activator and repressor flavonoids from Medicago sativa roots. Mol. Plant-Microbe Interact. 11, 784-794.Google Scholar
  164. Zurayk R, Adlan M, Baalbaki R and Saxena M C 1998 Interactive effects of salinity and biological nitrogen fixation on chickpea (Cicer arietinum L.) growth. J. Agron. Crop Sci. 180, 249-258.Google Scholar

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© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Z. Rengel
    • 1
  1. 1.Soil Science and Plant Nutrition, Faculty of AgricultureThe University of Western AustraliaCrawleyAustralia

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