Signals exchanged between legumes and Rhizobium: Agricultural uses and perspectives

Plant and Soil

Volumn 252, Issue 1, 2003, Pages 129-137

  Broughton, William J ^a   Zhang, Feng ^b   Perret, Xavier ^a   Staehelin, Christian ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b BIOS Agriculture Inc   (Canada)

Author keywords

Carbohydrates; Flavonoids; Low temperatures; Nod factors; Nodulation; Secreted proteins; Soybeans

Indexed keywords

HOST-SYMBIONT INTERACTION; LEGUME; LOW TEMPERATURE; NITROGEN FIXATION; NODULATION; PHENOLIC COMPOUND; RHIZOBACTERIUM;

BACTERIA (MICROORGANISMS); GLYCINE MAX; RHIZOBIACEAE; RHIZOBIUM;

EID: 0037704516     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1024179717780     Document Type: Conference Paper

References (76)

1. Alami Y, Achouak W, Marol C and Heulin T 2000 Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl. Environ. Microbiol. 66, 3393-3398.
2. de Billy F, Grosjean C, May S, Bennett, M and Cullimore J V 2001 Expression studies on aux1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol. Plant Microbe Interact. 14, 267-277.
3. Boot K J M, van Brussel A A N, Tak T, Spaink H P and Kijne J W 1999 Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp. nigra roots. Mol. Plant Microbe Interact. 12, 839-844.
4. Broughton W J, Jabbouri S and Perret X 2000 Keys to symbiotic harmony. J. Bacteriol. 182, 5641-5652.
5. Buchanan B B, Gruissem W and Jones R L, Eds. 2000 Biochemistry and Molecular Biology of Plants. Am. Soc. Plant Physiol., Rockville, MD, USA.
6. Charon C, Sousa C, Crespi M and Kondorosi, A 1999 Alteration of enod40 expression modifies Medicago truncatula root nodule development induced by Sinorhizobium meliloti. Plant Cell 11, 1953-1965.
7. Caetano-Anollés G and Gresshoff P M 1991 Plant genetic control of nodulation. Annu. Rev. Microbiol. 45, 345-382.
8. Cullimore J V, Ranjeva R. and Bono J J 2001 Perception of lipochitooligosaccharidic Nod factors in legumes. Trends Plant Sci. 6, 24-30.
9. Dakora F D, Joseph C M and Phillips D A 1993 Alfalfa (Medicago sativa L.) root exudates contain isoflavonoids in the presence of Rhizobium meliloti. Plant Physiol. 101, 819-824.
10. De Jong A J, Heidstra R, Spaink H P, Hartog M V, Meijer E A, Hendriks T, Lo Schiavo F, Terzi M, Bisseling T, van Kammen A and De Vries S C 1993 Rhizobium lipooligosaccharides rescue a carrot somatic embryo mutant. Plant Cell 5, 615-620.
11. D'Haeze W, Gao M, De Rycke R, van Montagu M, Engler G and Holsters M 1998 Roles for azorhizobial Nod factors and surface polysaccharides in intercellular invasion and nodule penetration, respectively. Mol. Plant Microbe Interact. 11, 999-1008.
12. Dowling D N and Broughton W J 1986 Competition for nodulation of legumes. Annu. Rev. Microbiol. 40, 131-157.
13. Harrison M J 1999 Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 361-389.
14. Hartwig, U A and Phillips D A 1991 Release and modification of nod-gene-inducing flavonoids from alfalfa seeds. Plant Physiol. 95, 804-807.
15. Heidstra R, Geurts R, Franssen H, Spaink H P, van Kammen A and Bisseling T 1994 Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol. 105, 787-797.
16. Herridge D and Rose I 2000 Breeding for enhanced nitrogen fixation in crop legumes. Field Crops Res. 65, 229-248.
17. Hirsch A M, Fang Y, Assad S, and Kapulnik Y 1997 The role of phytohormones in plant-microbe symbiosis. Plant Soil 194, 171-184.
18. Hogg B, Davies A. E, Wilson K E, Bisseling T and Downie J A 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 Microbe Interact. 15, 60-68.
19. 2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res. 65, 151-164.
20. Firmin J L, Wilson K E, Rossen L and Johnston A W B 1986 Flavonoid activation of nodulation genes in Rhizobium reversed by other compounds present in plants. Nature 324, 90-92.
21. Firmin J L, Wilson K E, Carlson R W, Davies A E and Downie, J A 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.
22. Freiberg C, Fellay R, Bairoch A, Broughton W J, Rosenthal A and Perret X 1997 Molecular basis of symbiosis between Rhizobium and legumes. Nature 387, 394-401.
23. Irving H R, Boukli N M, Kelly M N and Broughton W J 2000 Nod-factors in symbiotic development of root hairs. In Root Hairs: Cell and Molecular Biology. Eds. R W Ridge and A M C Emons. pp. 241-265. Springer, Tokyo, Japan.
24. Jacobs M and Rubery P H 1988 Naturally occurring auxin transport regulators. Science 241, 346-349.
25. Kawai Y and Yamamoto Y 1986 Increase in the formation and nitrogen fixation of soybean nodules by vesicular-arbuscular mycorrhiza. Plant Cell Physiol. 27, 399-405.
26. Kozik A, Heidstra R, Horvath B, Kulikova O, Tikhonovich I, Ellis T H N, van Kammen A, Lie T A and Bisseling T 1995 Pea lines carrying sym1 or sym2 can be nodulated by Rhizobium strains containing nodX; sym1 and sym2 are allelic. Plant Sci. 108, 41-49.
27. Lie T A 1984 Host genes in Pisum sativum L. conferring resistance to European Rhizobium leguminosarum strains. Plant Soil 82, 415-425.
28. 2 fixation as affected by period of exposure to a low root zone temperature. Physiol. Plant. 88, 212-223.
29. 2-fixing symbiotic activity of two soybean [Glycine max (L.) Merr.] cultivars inoculated with Bradyrhizobium strains of diverse origin. Plant Soil 157, 289-303.
30. Lynch D H and Smith D L 1994 The effect of low root zone temperature stress on two soybean (Glycine max) genotypes when combined with Bradyrhizobium strains of varying geographic origin. Physiol. Plant. 90, 105-113.
31. Marie C, Broughton W J and Deakin W J 2001 Rhizobium type III secretion systems: legume charmers or alarmers? Curr. Opin. Plant Biol. 4, 336-342.
32. Mathesius U, Schlaman H R M, Spaink, H P, Sautter C, Rolfe B G and Djordjevic M A 1998 Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J. 14, 23-34.
33. Matthews D J and Hayes P 1982 Effect of root zone temperature on early growth, nodulation and nitrogen fixation in soybeans. J. Agric. Sci. Cambridge 98, 371-376.
34. McDermott T R and Graham P H 1990 Competitive ability and efficiency in nodule formation of strains of Bradyrhizobium japonicum. Appl. Environ. Microbiol. 56, 3035-3039.
35. Miklashevichs E, Röhrig H, Schell J and Schmidt J 2001 Perception and signal transduction of rhizobial Nod factors. Crit. Rev. Plant Sci. 20, 373-394.
36. Minic Z, Brown S, De Kouchkovsky Y, Schultze M and Staehelin C 1998 Purification and characterization of a novel chitinase-lysozyme, of another chitinase, both hydrolysing Rhizobium meliloti Nod factors, and of a pathogenesis-related protein from Medicago sativa roots. Biochem. J. 332, 329-335.
37. O'Hagan D 1991 The Polyketide Metabolites. Ellis Horwood Ltd., Chichester, UK.
38. Olsthoorn M M A, Stokvis E, Haverkamp J, Spaink H P and Thomas-Oates J E 2000 Growth temperature regulation of host-specific modifications of rhizobial lipo-chitin oligosaccharides: the function of nodX is temperature regulated. Mol. Plant Microbe Interact. 13, 808-820.
39. Ovtsyna A O, Rademaker G-J, Esser E, Weinman J, Rolfe B G, Tikhonovich I A, Lugtenberg B J J, Thomas-Oates J E and Spaink H P 1999 Comparison of characteristics of the nodX genes from various Rhizobium leguminosarum strains. Mol. Plant-Microbe Interact. 12: 252-258.
40. Ovtsyna A O, Schultze M, Tikhonovich I A, Spaink H P, Kondorosi E, Kondorosi A and Staehelin C 2000 Nod factors of Rhizobium leguminosarum bv. viciae and their fucosylated derivatives stimulate a Nod factor cleaving activity in pea roots and are hydrolyzed in vitro by plant chitinases at different rates. Mol. Plant Microbe Interact. 13, 799-807.
41. Paau A S, Bennett M L, Kurtenbach C J and Graham L L 1990 Improvement of inoculant efficiency by strain improvement and formulation manipulation. In Nitrogen Fixation: Achievements and Objectives. Eds. P G Gresshoff, L E Roth, G. Stacey and W E Newton. pp. 617-624. Chapman and Hall, New York.
42. Pan B and Smith D L 2000 Genistein preincubation of Bradyrhizobium japonicum cells improves strain competitiveness under greenhouse, but not field conditions. Plant Soil 223, 229-234.
43. del Papa M F, Balagué L J, Sowinski S C, Wegener C, Segundo E, Abarca F M, Toro N, Niehaus K, Pühler A, Aguilar O M, Martinez-Drets G and Lagares A 1999 Isolation and characterization of alfalfa-nodulating rhizobia present in acidic soils of central Argentina and Uruguay. Appl. Environ. Microbiol. 65, 1420-1427.
44. Peters N K, Frost J W and Long S R 1986 A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233, 977-980.
45. Perret X, Staehelin C and Broughton W J 2000 Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180-201.
46. Pueppke S G and Broughton W J 1999 Rhizobium sp. NGR234 and R. fredii USDA257 share exceptionally broad, nested host-ranges. Mol. Plant Microbe Interact. 12, 293-318.
47. Recourt K, van Tunen A J, Mur L A, van Brussel A A N, Lugtenberg B J J and Kijne J W 1992 activation of flavonoid biosynthesis in roots of Vicia sativa subsp. nigra plants by inoculation with Rhizobium leguminosarum biovar viciae. Plant Mol. Biol. 19, 411-420.
48. 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 ENODI2 in rice. Plant J. 14, 693-702.
49. Redmond J W, Batley M, Djordjevic M A, Innes R W, Kuempel P L and Rolfe B G 1986 Flavones induce expression of nodulation genes in Rhizobium. Nature 323, 632-635.
50. Reitz M, Rudolph K, Schröder I, Hoffmann-Hergarten S, Hallmann J and Sikora R A 2000 Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl. Environ. Microbiol. 66, 3515-3518.
51. Relić B, Talmont F, Kopcinska J, Golinowsky W, Promé J-C and Broughton W J 1993 Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol. Plant Microbe Interact. 6, 764-774.
52. Relić B, Perret X, Estrada-Garcia M T, Kopcinska J, Golinowski W, Krishnan H B, Pueppke S G and Broughton W J 1994 Nod factors of Rhizobium are a key to the legume door. Mol. Microbiol. 13, 171-178.
53. 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.
54. Schultze M and Kondorosi A 1998 Regulation of symbiotic root nodule development. Annu. Rev. Genet. 32, 33-57.
55. Smith D L and Zhang F 1999 Composition for enhancing grain yield and protein yield of legumes grown under environmental conditions that inhibit or delay nodulation thereof. US Patent. 5922316.
56. Spaink H P, Okker R J H, Wijffelman C A, Tak T, Goosen-de-Roo L, Pees E, van Brussel A A N and Lugtenberg B J J 1989 Symbiotic properties of rhizobia containing a flavonoid-independent hybrid nodD product. J. Bacteriol. 171, 4045-4053.
57. Staehelin C, Granado J, Müller J, Wiemken A, Mellor R B, Felix G, Regenass M, Broughton W J and Boller T 1994a Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proc. Natl. Acad. Sci. USA 91, 2196-2200.
58. Staehelin C, Schultze M, Kondorosi E, Mellor R B, Boller T and Kondorosi A 1994b Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. Plant J. 5, 319-330.
59. Staehelin C, Schultze M, Kondorosi E and Kondorosi A 1995 Lipochitooligosaccharide nodulation signals from Rhizobium meliloti induce their rapid degradation by the host plant alfalfa. Plant Physiol. 108, 1607-1614.
60. Staehelin C, Schultze M, Tokuyasu K, Poinsot V, Promé J-C, Kondorosi E and Kondorosi A 2000 N-Deacetylation of Sinorhizobium meliloti Nod factors increases their stability in the Medicago sativa rhizosphere and decreases their biological activity. Mol. Plant Microbe Interact. 13, 72-79.
61. Streit W R, Joseph C M and Phillips D A 1996 Biotin and other water-soluble vitamins are key growth factors for alfalfa root colonization by Rhizobium meliloti 1021. Mol. Plant Microbe Interact. 9, 330-338.
62. Toro N 1996 Nodulation competitiveness in the Rhizobium legume symbiosis. World J. Microbiol. Biotech. 12, 157-162.
63. Triplett E W and Sadowsky M J 1992 Genetics of competition for nodulation of legumes. Annu. Rev. Microbiol. 46, 399-428.
64. Vierheilig H, Bago B, Albrecht C, Poulin M J and Piché Y 1998 Flavonoids and arbuscular mycorrhizal fungi. In Flavonoids in the Living System. Eds. J Manthey and B Buslig. pp. 9-33. Plenum Press, New York.
65. Viprey V, Del Greco A, Golinowski W, Broughton W J and Perret X 1998 Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbiol. 28, 1381-1389.
66. Walsh K B and Layzell D B 1986 Carbon and nitrogen assimilation and partitioning in soybeans exposed to low root temperatures. Plant Physiol. 80, 249-255.
67. Xie Z-P, Staehelin 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 soybeans. Plant Physiol. 108, 1519-1525.
68. Xie Z-P, Müller J, Wiemken A, Broughton W J and Boller T 1998 Nod factors and tri-iodobenzoic acid stimulate mycorrhizal colonization and affect carbohydrate partitioning in mycorrhizal roots of Lablab purpureus. New Phytol. 139, 361-366.
69. Zahran H H 1999 Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol. Mol. Biol. Rev. 63, 968-989.
70. Zhang F and Smith D L 1994 Effects of low root zone temperatures on the early stages of symbiosis establishment between soybean [Glycine max (L.) Merr.] and Bradyrhizobium japonicum. J. Exp. Bot. 279, 1467-1473.
71. Zhang F and Smith D L 1995 Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean [Glycine max (L.) Merr.] at suboptimal root zone temperatures. Plant Physiol. 108, 961-968.
72. Zhang F and Smith D L 1996a Genistein accumulation in soybean [Glycine max (L.) Merr.] root systems under suboptimal root zone temperatures. J. Exp. Bot. 47, 785-792.
73. Zhang F and Smith D L 1996b Inoculation of soybean [Glycine max (L.) Merr.] with genistein-preincubated Bradyrhizobium japonicum or genistein directly applied into soil and soybean protein and dry matter yield under short season conditions. Plant Soil 179, 233-241.
74. Zhang F and Smith D L 1997 Application of genistein to inocula and soil to overcome low spring soil temperature inhibition of soybean nodulation and nitrogen fixation. Plant Soil 192, 141-151.
75. Zhang F, Lynch D H and Smith D L 1995a Impact of low root zone temperatures in soybean [Glycine max (L.) Merr.] on nodulation and nitrogen fixation. Environ. Exp. Bot. 35, 279-285.
76. Zhang F, Hamel C, Kianmehr H and Smith D L 1995b Root-zone temperature and soybean [Glycine max (L.) Merr.] vesicular-arbuscular mycorrhizae: development and interactions with the nitrogen fixation symbiosis. Environ. Exp. Bot. 35, 287-298.