Nodule development in legumes

Nitrogen Fixation in Crop Production

Volumn 52, Issue , 2015, Pages 1-24

  Gage, Daniel J ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Cell division patterns; Crop plants; Infection thread development; Legume family; Lotus japonicas; Medicago truncatula; Nodule development; Root hair infection; Soybean

Indexed keywords

EID: 85102915979     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.2134/agronmonogr52.c1     Document Type: Chapter

References (136)

1. Amon, P., E. Haas, and M. Sumper. 1998. The sex-inducing pheromone and wounding trigger the same set of genes in the multicellular green alga Volvox. Plant Cell 10:781-789.
2. Arrighi, J.F., A. Barre, B. Ben Amor, A. Bersoult, L.C. Soriano, R. Mirabella, F. de Carvalho-Niebel, E.P. Journet, M. Gherardi, T. Huguet, R. Geurts, J. Denarie, P. Rouge, and C. Gough. 2006. The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142:265-279.
3. Batt isti, L., J. Lara, and J.A. Leigh. 1992. Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa. Proc. Natl. Acad. Sci. USA 89:5625-5629.
4. Bolanos-Vasquez, M.C., and D. Werner. 1997. Effects of Rhizobium tropici, R. etli and R. leguminosarum bv. phaseoli on nod gene-inducing flavonoids in root extracts of Phaseolus vulgaris. Mol. Plant Microbe In. 10:339-346
5. Bond, L. 1948. Origin and developmental morphology of root nodules of Pisum sativum. Bot. Gaz. 109:411-434.
6. Bradey, J.D., and S.C. Fry. 1997. Formation of di-isodityrosine and loss of isodityrosine in the cell walls of tomato cell-suspension cultures treated with fungal elicitors or H2O2. Plant Physiol. 115:87-92.
7. Brewin, N.J. 2004. Plant cell wall remodeling in the Rhizobium-legume symbiosis. Crit. Rev. Plant Sci. 23:293-316.
8. Broughton, W.J., S. Jabbouri, and X. Perret. 2000. Keys to symbiotic harmony. J. Bacteriol. 182:5641-5652.
9. Caetano-Anolles, G., and P.M. Gresshoff. 1991. Plant genetic control of nodulation. Annu. Rev. Microbiol. 45:345-382.
10. Cardon, Z.G., and D.J. Gage. 2006. Resource exchange in the rhizosphere: Molecular tools and the microbial perspective. Annu. Rev. Ecol. Evol. Syst. 37:459-488.
11. Carrol, B.J., D.L. McNeil, and P.M. Gresshoff. 1985a. A supernodulation and nitrate tolerant symbiotic (nts) soybean mutant. Plant Physiol. 78:34-40.
12. Carrol, B.J., D.L. McNeil, and P.M. Gresshoff. 1985b. Isolation and properties of soybean (Glycine max) mutants that nodulate in the presence of high nitrate concentrations. Proc. Natl. Acad. Sci. USA 82:4164-4166.
13. Cassab, G.I. 1998. Plant cell wall proteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:281-309.
14. Catalano, C.M., K.J. Czymmek, J.G. Gann, and D.J. Sherrier. 2007. Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules. Planta 225:541-550.
15. Catoira, R., C. Galera, F. de Billy, R.V. Penmetsa, E.P. Journet, F. Maillet, C. Rosenberg, D. Cook, C. Gough, and J. Denarie. 2000. Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12:1647-1665.
16. Catoira, R., A.C.J. Timmers, F. Maillet, C. Galera, R.V. Penmetsa, D. Cook, J. Denarie, and C. Gough. 2001. The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling. Development 128:1507-1518.
17. Chen, W.M., E.K. James, A.R. Prescott, M. Kierans, and J.I. Sprent. 2003. Nodulation of Mimosa spp. by the beta-proteobacterium Ralstonia taiwanensis. Mol. Plant Microbe In. 16:1051-1061.
18. Cheng, H.P., and G.C. Walker. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180:5183-5191.
19. Clark, S.E. 2001. Cell signalling at the shoot meristem. Nat. Rev. Mol. Cell Biol. 2:276-284.
20. Cooper, J.B., and S.R. Long. 1994. Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6:215-225.
21. Crespi, M.D., E. Jurkevitch, M. Poiret, Y. d'Aubenton-Carafa, G. Petrovics, E. Kondorosi, and A. Kondorosi. 1994. enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J. 13:5099-5112.
22. De Koninck, P., and H. Schulman. 1998. Sensitivity of CaM kinase II to the frequency of Ca2+oscillations. Science 279:227-230.
23. Demont, N., M. Ardourel, F. Maillet, D. Prome, M. Ferro, J.C. Prome, and J. Denarie. 1994. The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (omega-1)-hydroxylated fatt y acids. EMBO J. 13:2139-2149.
24. de Ruijter, N.C.A., M.B. Rook, T. Bisseling, and A.M.C. Emons. 1998. Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J. 13:341-350.
25. D'Haeze, W., and M. Holsters. 2002. Nod factor structures, responses and perception during initiation of nodule development. Glycobiology 12:79R-105R.
26. Diaz, C.L., T. Logman, H.C. Stam, and J.W. Kijne. 1995. Sugar-binding activity of pea lectin expressed in white clover hairy roots. Plant Physiol. 109:1167-1177.
27. Diaz, C.L., P.C. Van Spronsen, R. Bakhuizen, G.J.J. Logman, E.J.J. Lugtenberg, and J.W. Kijne. 1986. Correlation between infection by Rhizobium leguminosarum and lectin on the surface of Pisum sativum roots. Planta 168:350-359.
28. Djordjevic, S.P., H. Chen, M. Batley, J.W. Redmond, and B.G. Rolfe. 1987. Nitrogen fixation ability of exopolysaccharide synthesis mutants of Rhizobium sp strain NGR234 and Rhizobium trifolii is restored by the addition of homologous exopolysaccharides. J. Bacteriol. 169:53-60.
29. Ehrhardt, D.W., E.M. Atkinson, and S.R. Long. 1992. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256:998-1000.
30. Ehrhardt, D.W., R. Wais, and S.R. Long. 1996. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673-681.
31. Elliott, G.N., W.M. Chen, J.H. Chou, H.C. Wang, S.Y. Sheu, L. Perin, V.M. Reis, L. Moulin, M.F. Simon, C. Bontemps, J.M. Sutherland, R. Bessi, S.M. de Faria, M.J. Trinick, A.R. Prescott, J.I. Sprent, and E.K. James. 2007. Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol. 173:168-180.
32. Emons, A.M.C., and B. Mulder. 2000. Nodulation factors trigger an increase of fine bundles of subapical actin filaments in Vicia root hairs: Implications for root hair curling around bacteria. p. 44-49. In J.G.M. De Wit et al. (ed.) Biology of plant-microbe interaction, Vol. 2. Inter. Society for Molecular Plant-Microbe Interactions, St. Paul, MN. Esseling, J.J., F.G. Lhuissier, and A.M. Emons. 2003. Nod factor-induced root hair curling: Continuous polar growth towards the point of nod factor application. Plant Physiol. 132:1982-1988.
33. Esseling, J.J., F.G.P. Lhuisser, and A.M.C. Emons. 2004. A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: Implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell 16:933-944.
34. Felle, H.H., E. Kondorosi, A. Kondorosi, and M. Schultze. 1999. Elevation of the cytosolic free [Ca2+] is indispensable for the transduction of the nod factor signal in alfalfa. Plant Physiol. 121:273-279.
35. Finan, T.M., A.M. Hirsch, J.A. Leigh, E. Johansen, G.A. Kuldau, S. Deegan, G.C. Walker, and E.R. Signer. 1985. Symbiotic mutants of Rhizobium meliloti that uncouple plant from bacterial differentiation. Cell 40:869-877.
36. Fletcher, J.C., U. Brand, M.P. Running, R. Simon, and E.M. Meyerowitz. 1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911-1914.
37. Fraysse, N., F. Couderc, and V. Poinsot. 2003. Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur. J. Biochem. 270:1365-1380.
38. Gage, D.J. 2002. Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J. Bacteriol. 184:7042-7046.
39. Gage, D.J. 2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68:280-300.
40. Gage, D.J., T. Bobo, and S.R. Long. 1996. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J. Bacteriol. 178:7159-7166.
41. Gleason, C., S. Chaudhuri, T. Yang, A. Munoz, B.W. Poovaiah, and G.E. Oldroyd. 2006. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441:1149-1152.
42. Gonzalez, J.E., B.L. Reuhs, and G.C. Walker. 1996. Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc. Natl. Acad. Sci. USA 93:8636-8641.
43. Gonzalez, J.E., C.E. Semino, L.X. Wang, L.E. Castellano-Torres, and G.C. Walker. 1998. Biosynthetic control of molecular weight in the polymerization of the octasaccharide subunits of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 95:13477-13482.
44. Gremaud, M.F., and J.E. Harper. 1989. Selection and initial characterization of partially nitrate tolerant nodulation mutants of soybean. Plant Physiol. 89:169-173.
45. Heidstra, R., R. Geurts, H. Franssen, H. Spaink, A. van Kammen, and T. Bisseling. 1994. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol. 105:787-797.
46. Hepler, P.K., L. Vidali, and A.Y. Cheung. 2001. Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17:159-187.
47. Herouart, D., E. Baudouin, P. Frendo, J. Harrison, R. Santos, A. Jamet, G. Van de Sype, D. Touati, and A. Puppo. 2002. Reactive oxygen species, nitric oxide and glutathione: A key role in the establishment of the legume-Rhizobium symbiosis? Plant Physiol. Biochem. 40:619-624.
48. Hirsch, A.M. 1999. Role of lectins (and rhizobial exopolysaccharides) in legume nodulation. Curr. Opin. Plant Biol. 2:320-326.
49. Hirsch, A.M., T.V. Bhuvaneswari, J.G. Torrey, and T. Bisseling. 1989. Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc. Natl. Acad. Sci. USA 86:1244-1248.
50. Hungria, M., C.M. Joseph, and D.A. Phillips. 1991. Rhizobium nod gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris L.). Plant Physiol. 97:759-764.
51. Jones, K.M., H. Kobayashi, B.W. Davies, M.E. Taga, and G.C. Walker. 2007. How rhizobial symbionts invade plants: The Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5:619-633.
52. Kalo, P., C. Gleason, A. Edwards, J. Marsh, R.M. Mitra, S. Hirsch, J. Jakab, S. Sims, S.R. Long, J. Rogers, G.B. Kiss, J.A. Downie, and G.E.D. Oldroyd. 2005. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786-1789.
53. Krause, A., V.T. Lan, and W.J. Broughton. 1997. Induction of chalcone synthase expression by rhizobia and Nod factors in root hairs and roots. Mol. Plant Microbe In. 10:388-393.
54. Krusell, L., L.H. Madsen, S. Sato, G. Aubert, A. Genua, K. Szczyglowski, G. Duc, T. Kaneko, S. Tabata, F. de Bruijn, E. Pajuelo, N. Sandal, and J. Stougaard. 2002. Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422-426.
55. Lavin, M., P.S. Herendeen, and M.F. Wojciechowski. 2005. Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst. Biol. 54:575-594.
56. Lawson, C.G., M.A. Djordjevic, J.J. Weinman, and B.G. Rolfe. 1994. Rhizobium inoculation and physical wounding result in the rapid induction of the same chalcone synthase copy in Trifolium subterraneum. Mol. Plant Microbe In. 7:498-507.
57. Leigh, J.A., E.R. Signer, and G.C. Walker. 1985. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. USA 82:6231-6235.
58. Lhuisser, F.G.P., N.C.A. De Ruijter, B.J. Sieberer, J.J. Esseling, and A.M.C. Emons. 2001. Time course of cell biological events evoked in legume root hairs by Rhizobium Nod factors: State of the art. Ann. Bot. (London) 87:289-302.
59. Libbenga, K.R., and P.A.A. Harkes. 1973. Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum. Planta 114:17-28.
60. Libbenga, K.R., F. van Iren, R.J. Bogers, and M.F. Schrag-Lamers. 1973. The role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L. Planta 114:29-39.
61. Limpens, E., C. Franken, P. Smit, J. Willemse, T. Bisseling, and R. Geurts. 2003. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630-633.
62. Madsen, E.B., L.H. Madsen, S. Radutoiu, M. Olbryt, M. Rakwalska, K. Szczyglowski, S. Sato, T. Kaneko, S. Tabata, N. Sandal, and J. Stougaard. 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637-640.
63. Marsh, J.F., A. Rakocevic, R.M. Mitra, L. Brocard, J. Sun, A. Eschstruth, S.R. Long, M. Schultze, P. Ratet, and G.E.D. Oldroyd. 2007. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol. 144:324-335.
64. Mathesius, U., C. Charon, B.G. Rolfe, A. Kondorosi, and M. Crespi. 2000. Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv. trifolii inoculation or localized cytokinin addition. Mol. Plant Microbe In. 13:617-628.
65. Mathesius, U., H.R.M. Schlaman, H. Spaink, C. Sautter, B.G. Rolfe, and M.A. Djordjevic. 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.
66. Middleton, P.H., J. Jakab, R.V. Penmetsa, C.G. Starker, J. Doll, P. Kalo, R. Prabhu, J.F. Marsh, R.M. Mitra, A. Kereszt, B. Dudas, K. VandenBosch, S.R. Long, D.R. Cook, G.B. Kiss, and G.E.D. Oldroyd. 2007. An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19:1221-1234.
67. Miller, D.D., H.B. Leferink-ten Klooster, and A.M.C. Emons. 2000. Lipochito-oligosaccharide nodulation factors stimulate cytoplasmic polarity with longitudinal endoplasmic reticulum and vesicles at the tip in vetch root hairs. Mol. Plant Microbe In. 13:1385-1390.
68. Mitra, R.M., C.A. Gleason, A. Edwards, J. Hadfield, J.A. Downie, G.E.D. Oldroyd, and S.R. Long. 2004a. A Ca2+/calmodulin dependent protein kinase required for symbiotic noduledevelopment: Gene identification by transcript-based cloning. Proc. Natl. Acad. Sci. USA 101:4701-4705.
69. Mitra, R.M., S.L. Shaw, and S.R. Long. 2004b. Six non-nodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume-rhizobia symbiosis. Proc. Natl. Acad. Sci. USA 101:10217-10222.
70. Monahan-Giovanelli, H., C. Arango-Pinedo, and D.J. Gage. 2006. Architecture of infection thread networks in developing root nodules induced by the symbiotic bacterium Sinorhizobium meliloti on Medicago truncatula. Plant Physiol. 104:661-670.
71. Moulin, L., A. Munive, B. Dreyfus, and C. Boivin-Masson. 2001. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411:948-950.
72. Murray, J.D., B.J. Karas, S. Sato, S. Tabata, L. Amyot, and K. Szczyglowski. 2007. A cytokinin perception mutant colonized by rhizobium in the absence of nodule organogenesis. Science 315:101-104.
73. Naisbitt, T., E.K. James, and J.I. Sprent. 1992. The evolutionary significance of legume genus Chamaecrista, as determined by nodule structure. New Phytol. 122:487-492.
74. Nguyen, C. 2003. Rhizodeposition of organic C by plants: Mechanisms and controls. Agronomie 23:375-396.
75. Niehaus, K., R. Baier, B. Kohring, E. Flashl, and A. Puhler. 1997. Symbiotic suppression of the Medicago sativa plant defense system by Rhizobium meliloti oligosaccharides. p. 110-114. In A. Legoki et al (ed.) Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture. Springer Verlag, Heidelberg, Germany.
76. Niehaus, K., D. Kapp, and A. Puhler. 1993. Plant defense and delayed infection of alfalfa pseudonodules induced by an exopolysaccharide (EPS-I) deficient Rhizobium meliloti mutant. Planta 190:415-425.
77. Nishimura, R., M. Hayashi, G.J. Wu, H. Kouchi, H. Imaizumi-Anraku, Y. Murakami, S. Kawasaki, S. Akao, M. Ohmori, M. Nagasawa, K. Harada, and M. Kawaguchi. 2002. HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426-429.
78. Oka-Kira, E., and M.M. Kawaguchi. 2006. Long-distance signaling to control root nodule number. Curr. Opin. Plant Biol. 9:496-502.
79. Oldroyd, G.E.D., and J.A. Downie. 2004. Calcium, kinases and nodulation signalling in legumes. Nat. Rev. Mol. Cell Biol. 5:566-576.
80. Peck, M.C., R.F. Fisher, and S.R. Long. 2006. Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J. Bacteriol. 188:5417-5427.
81. Pellock, B.J., H.P. Cheng, and G.C. Walker. 2000. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J. Bacteriol. 182:4310-4318.
82. Penmetsa, R.V., J.A. Frugoli, L.S. Smith, S.R. Long, and D.R. Cook. 2003. Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol. 131:998-1008.
83. Peters, N.K., J.W. Frost, and S.R. Long. 1986. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977-980.
84. Peterson, R.L., and M.L. Farquhar. 1996. Root hairs: Specialized tubular cells extending root surfaces. Bot. Rev. 62:1-40.
85. Phillips, D.A., C.M. Joseph, and C.A. Maxwell. 1992. Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol. 99:1526-1531.
86. Phillips, D.A., and W. Streit. 1996. Legume signals to rhizobial symbionts: A new approach for defining rhizosphere colonization. p. 236-271. In G. Stacey and N.T. Keen (ed.) Plant-microbe interactions. Chapman and Hall, New York.
87. Prayitno, J., B.G. Rolfe, and U. Mathesius. 2006. The ethylene-insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiol. 142:168-180.
88. Pueppke, S.G., and W.J. Broughton. 1999. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested, host ranges. Mol. Plant Microbe In. 12:293-318.
89. Radutoiu, S., L.H. Madsen, E.B. Madsen, H.H. Felle, Y. Umehara, M. Gronlund, S. Sato, Y. Nakamura, S. Tabata, N. Sandal, and J. Stougaard. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585-592.
90. Radutoiu, S., L.H. Madsen, E.B. Madsen, E. Jurkevitch, E. Fukai, E.M.H. Quistgaard, A.S. Albrektsen, E.K. James, S. Thirup, and J. Stougaard. 2007. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 26:3923-3935.
91. Rae, A.L., P. Bonfante-Fasolo, and N.J. Brewin. 1992. Structure and growth of infection threads in the legume symbiosis with Rhizobium leguminosarum. Plant J. 2:385-395.
92. Rathbun, E.A., M.J. Naldrett, and N.J. Brewin. 2002. Identification of a family of extensinlike glycoproteins in the lumen of Rhizobium-induced infection threads in pea root nodules. Mol. Plant Microbe In. 15:350-359.
93. Ridge, R.W. 1992. A model of legume root hair growth and Rhizobium infection. Symbiosis 14:349-373.
94. Riely, B.K., G. Lougnon, J.M. Ane, and D.R. Cook. 2007. The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J. 49:208-216.
95. Rivas, R., E. Velazquez, A. Willems, N. Vizcaino, N.S. Subba-Rao, P.F. Mateos, M. Gillis, F.B. Dazzo, and E. Martinez-Molina. 2002. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl. Environ. Microbiol. 68:5217-5222.
96. Rivas, R., A. Willems, N.S. Subba-Rao, P.F. Mateos, F.B. Dazzo, R.M. Kroppenstedt, E. Martinez-Molina, M. Gillis, and E. Velazquez. 2003. Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst. Appl. Microbiol. 26:47-53.
97. Rojo, E., V.K. Sharma, V. Kovaleva, N.V. Raikhel, and J.C. Fletcher. 2002. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14:969-977.
98. Samba, R.T., P. De Lajudie, M. Gillis, M. Neyra, M.M.S. Barreto, and B. Dreyfus. 1999. Diversity of rhizobia nodulating Crotalaria spp. from Senegal. Symbiosis 27:259-268.
99. Santos, R., D. Herouart, S. Sigaud, D. Touati, and A. Puppo. 2001. Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol. Plant Microbe In. 14:86-89.
100. Schlaman, H.R.M., B. Horvath, E. Vijgenboom, R.J.H. Okker, and B.J.J. Lugtengerg. 1991. Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. J. Bacteriol. 173:4277-4287.
101. Schmidt, P.E., W.J. Broughton, and D. Werner. 1994. Nod Factors of Bradyrhizobium japonicum and Rhizobium Sp NGR234 induce flavonoid accumulation in soybean root exudate. Mol. Plant Microbe In. 7:384-390.
102. Schnabel, E., E.P. Journet, F. de Carvalho-Niebel, G. Duc, and J. Frugoli. 2005. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol. Biol. 58:809-822.
103. Schultze, M., B. Quiclet-Sire, E. Kondorosi, H. Virelizer, J.N. Glushka, G. Endre, S.D. Gero, and A. Kondorosi. 1992. Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc. Natl. Acad. Sci. USA 89:192-196.
104. Schwedock, J.S., C. Liu, T.S. Leyh, and S.R. Long. 1994. Rhizobium meliloti NodP and NodQ form a multifunctional sulfate-activating complex requiring GTP for activity. J. Bacteriol. 176:7055-7064.
105. Searle, I.R., A.E. Men, T.S. Laniya, D.M. Buzas, I. Iturbe-Ormaetxe, B.J. Carroll, and P.M. Gresshoff. 2003. Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109-112.
106. Sharma, S.B., and E.R. Signer. 1990. Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Genes Dev. 4:344-356.
107. Shaw, L.J., P. Morris, and J.E. Hooker. 2006. Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ. Microbiol. 8:1867-1880.
108. Sieberer, B., and A.M.C. Emons. 2000. Cytoarchitecture and patt ern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors. Protoplasma 214:118-127.
109. Smit, P., E. Limpens, R. Geurts, E. Fedorova, E. Dolgikh, C. Gough, and T. Bisseling. 2007. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol. 145:183-191.
110. Smit, P., J. Raedts, V. Portyanko, F. Debelle, C. Gough, T. Bisseling, and R. Geurts. 2005. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789-1791.
111. Sprent, J.I. 1995. Legume trees and shrubs in the tropics: N2 fixation in prespective. Soil Biol. Biochem. 27:401-407.
112. Sprent, J.I. 2007. Evolving ideas of legume evolution and diversity: A taxnomic perspective on the occurence of nodulation. New Phytol. 174:11-25.
113. Sprent, J.I., and E.K. James. 2007. Legume evolution: Where do nodules and mycorrhizas fit in? Plant Physiol. 144:575-581.
114. Stacey, G., M. Libault, L. Brechenmacher, J. Wan, and G.D. May. 2006. Genetics and functional genomics of legume nodulation. Curr. Opin. Plant Biol. 9:110-121.
115. Steen, A., G. Buist, K.J. Leenhouts, M. El Khatt abi, F. Grijpstra, A.L. Zomer, G. Venema, O.P. Kuipers, and J. Kok. 2003. Cell wall att achment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J. Biol. Chem. 278:23874-23881.
116. Sy, A., E. Giraud, P. Jourand, N. Garcia, A. Willems, P. de Lajudie, Y. Prin, M. Neyra, M. Gillis, C. Boivin-Masson, and B. Dreyfus. 2001. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183:214-220.
117. Szczyglowski, K., R.S. Shaw, J. Wopereis, S. Copeland, D. Hamburger, B. Kasiborski, F.B. Dazzo, and F.J. de Bruijn. 1998. Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant Microbe In. 11:684-697.
118. Timmers, A.C., M.C. Auriac, and G. Truchet. 1999. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126:3617-3628.
119. Tirichine, L., H. Imaizumi-Anraku, S. Yoshida, Y. Murakami, L.H. Madsen, H. Miwa, T. Nakagawa, N. Sandal, A.S. Albrektsen, M. Kawaguchi, A. Downie, S. Sato, S. Tabata, H. Kouchi, M. Parniske, S. Kawasaki, and J. Stougaard. 2006. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:1153-1156.
120. Tirichine, L., N. Sandal, L.H. Madsen, S. Radutoiu, A.S. Albrektsen, S. Sato, E. Asamizu, S. Tabata, and J. Stougaard. 2007. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104-107.
121. Urzainqui, A., and G.C. Walker. 1992. Exogenous suppression of the symbiotic deficiencies of Rhizobium meliloti exo mutants. J. Bacteriol. 174:3404-3406.
122. Van Batenburg, F.D.H., R. Jonker, and J.W. Kijne. 1986. Rhizobium induces marked root hair curling by redirection of tip growth, a computer simulation. Physiol. Plant. 66:476-480.
123. van Brussel, A.A.N., R. Bakhuizen, P.C. van Spronsen, H.P. Spaink, T. Tak, B.J.J. Lugtenberg, and J.W. Kijne. 1992. Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharidess of Rhizobium. Science 257:70-72.
124. van Rhijn, P., N.A. Fujishige, P.O. Lim, and A.M. Hirsch. 2001. Sugar-binding activity of pea lectin enhances heterologous infection of transgenic alfalfa plants by Rhizobium leguminosarum biovar viciae. Plant Physiol. 126:133-144.
125. van Spronsen, P.C., M. Gronlund, C.P. Bras, H.P. Spaink, and J.W. Kijne. 2001. Cell biological changes of outer cortical root cells in early determinate nodulation. Mol. Plant Microbe In. 14:839-847.
126. van Workum, W.A.T., A.A.N. van Brussel, T. Tak, C.A. Wijffelman, and J.W. Kijne. 1995. Ethylene prevents nodulation of Vicia sativa ssp. nigra by exopolysaccharide-deficient mutants of Rhizobium-Leguminosarum bv. viciae. Mol. Plant Microbe In. 8:278-285.
127. van Workum, W.A.T., S. van Slageren, A.A.N. van Brussel, and J.W. Kijne. 1998. Role of exopolysaccharides of Rhizobium leguminosarum bv. viciae as host plant-specific molecules required for infection thread formation during nodulation of Vicia sativa. Mol. Plant Microbe In. 11:1233-1241.
128. Veereshlingam, H., J.G. Haynes, R.V. Penmetsa, D.R. Cook, D.J. Sherrier, and R. Dickstein. 2004. nip, a symbiotic Medicago truncatula mutant that forms root nodules with aberrant infection threads and plant defense-like response. Plant Physiol. 136:3692-3702.
129. Wais, R.J., C. Galera, G. Oldroyd, R. Catoira, R.V. Penmetsa, D. Cook, C. Gough, J. Denarie, and S.R. Long. 2000. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc. Natl. Acad. Sci. USA 97:13407-13412.
130. Wasson, A.P., F.I. Pellerone, and U. Mathesius. 2006. Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell 18:1617-1629.
131. Willems, A. 2006. The taxonomy of rhizobia: An overview. Plant Soil 287:3-14.
132. Wisniewski, J.P., E.A. Rathbun, J.P. Knox, and N.J. Brewin. 2000. Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: Implications for pea nodule initiation by Rhizobium leguminosarum. Mol. Plant Microbe In. 13:413-420.
133. Wopereis, J., E. Pajuelo, F.B. Dazzo, Q. Jiang, P.M. Gresshoff, F.J. De Bruijn, J. Stougaard, and K. Szczyglowski. 2000. Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J. 23:97-114.
134. Xi, C., G. Dirix, J. Hofk ens, F.C. Schryver, J. Vanderleyden, and J. Michiels. 2001. Use of dual marker transposons to identify new symbiosis genes in Rhizobium. Microb. Ecol. 41:325-332.
135. Yang, C., E.R. Signer, and A.M. Hirsch. 1992. Nodules initiated by Rhizobium meliloti exopolysaccharide mutants lack a discrete, persistent nodule meristem. Plant Physiol. 98:143-151.
136. Yang, W.C., P. Katinakis, P. Hendriks, A. Smolders, F. de Vries, J. Spee, A. van Kammen, T. Bisseling, and H. Franssen. 1993. Characterisation of GmENOD40, a gene showing novel patt erns of cell-specific expression during soybean nodule development. Plant J. 3:573-585.