Root Hairs pp 249-276 | Cite as

Nod Factor Signal Transduction in the Rhizobium–Legume Symbiosis

  • E. Limpens
  • T. BisselingEmail author
Part of the Plant Cell Monographs book series (CELLMONO, volume 12)


The symbiotic interaction between Rhizobium bacteria and most legume plants is initiated by the perception of bacterial signal molecules, the nodulation (Nod) factors, at the root hairs of the plant. This induces responses both in the root hairs, leading to infection by the bacteria, as well as at a distance in the root cortex, leading to nodule organ formation. Molecular genetic approaches have been very successful in elucidating the key components essential for this Nod factor signal transduction. Cloning of these key regulators has been possible because of the establishment of two model legumes, Lotus japonicus and Medicago truncatula, for which extensive molecular genetic tools are available. We discuss the characteristics of the identified epidermal Nod-factor-signaling components from these two legumes and position them in a genetically based signal transduction cascade. To allow a successful rhizobial symbiosis, the responses in the root hairs need to be tightly coordinated with responses in the inner root cells. This is likely achieved through secondary signals that are generated upon Nod factor perception in the epidermis and are transported to the pericycle/cortex. The recent identification of a cytokinin receptor that is essential for the cortical responses supports the involvement of secondary signals, and the possible role of cytokinin as intercellular signal is discussed.


Root Hair Infection Thread Calcium Spike Rhizobial Symbiosis LysM Domain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Erik Limpens is supported by The Netherlands Organization of Scientific Research (NWO) VENI grant 86305023.


  1. Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602PubMedGoogle Scholar
  2. Amor BB, Shaw SL, Oldroyd GE, Maillet F, Penmetsa RV, Cook D, Long SR, Dénarié J, Gough C (2003) The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J 34:495–506PubMedGoogle Scholar
  3. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Carvalho-Niebel F (2007) AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19:2866–2885PubMedGoogle Scholar
  4. Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Levy J, Debellé F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1347PubMedGoogle Scholar
  5. Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, Promé JC, Dénarié J, Truchet G (1994) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6:1357–1374PubMedGoogle Scholar
  6. Arrighi JF, Barre A, Amor BB, Bersoult A, Campos Soriano L, Mirabella R, De Carvalho-Niebel F, Journet EP, Ghérardi M, Huguet T, Geurts R, Dénarié J, Rougé P, Gough C (2006) The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142:265–279PubMedGoogle Scholar
  7. Bateman A, Bycroft M (2000) The structure of a LysM domain from E coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol 299:1113–1119PubMedGoogle Scholar
  8. Bauer P, Ratet P, Crespi MD, Schultze M, Kondorosi A (1996) Nod factors and cytokinins induce similar cortical cell division, amyloplast deposition and Msenod12A expression in alfalfa roots. Plant J 10:91–105Google Scholar
  9. Bender GL, Goydych W, Rolfe BG, Nayudu M (1987) The role of Rhizobium conserved and host specific nodulation genes in the infection of the non-legume Parasponia andersonii. Mol Gen Genet 210:299–306Google Scholar
  10. Benhizia Y, Benhizia H, Benguedouar A, Muresu R, Giacomini A, Squartini A (2004) Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol 27:462–468PubMedGoogle Scholar
  11. Brewin NJ (2004) Cell wall remodeling in the Rhizobium-legume symbiosis. Crit Rev Plant Sci 23:1–24Google Scholar
  12. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12:1647–1666PubMedGoogle Scholar
  13. Catoira R, Timmers AC, Maillet F, Galera C, Penmetsa RV, Cook D, Dénarié J, Gough C (2001) The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling. Development 128:1507–1518PubMedGoogle Scholar
  14. Charron D, Pingret J, Chabaud M, Journet E, Barker DG (2004) Pharmacological evidence that multiple phospholipid signaling pathways link rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses, indicating Ca2+ spiking and specific ENOD gene expression. Plant Physiol 136:3582–3593PubMedGoogle Scholar
  15. Chen XC, Feng J, Hou BH, Li FQ, Li Q, Hong GF (2005) Modulating DNA bending affects NodD-mediated transcriptional control in Rhizobium leguminosarum. Nucl Acids Res 33:2540–2548PubMedGoogle Scholar
  16. Compaan B, Yang WC, Bisseling T, Franssen H (2001) ENOD40 expression in the pericycle precedes cortical cell division in Rhizobium-legume interaction and the highly conserved internal region of the gene does not encode a peptide. Plant Soil 230:1–8Google Scholar
  17. Cooper JB, Long SR (1994) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6:215–225PubMedGoogle Scholar
  18. Cullimore J, Dénarié J (2003) Plant sciences. How legumes select their sweet talking symbionts. Science 302:575–578PubMedGoogle Scholar
  19. D'Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–-105RPubMedGoogle Scholar
  20. Debellé F, Rosenberg C, Vasse J, Maillet F, Martinez E, Dénarié J, Truchet G (1986) Assignment of symbiotic developmental phenotypes to common and specific nodulation (nod) genetic loci of Rhizobium meliloti. J Bacteriol 168:1075–1086PubMedGoogle Scholar
  21. Demont-Caulet N, Maillet F, Tailler D, Jacquinet JC, Promé JC, Nicolaou KC, Truchet G, Beau JM, Dénarié J (1999) Nodule-inducing activity of synthetic Sinorhizobium meliloti nodulation factors and related lipo-chitooligosaccharides on alfalfa Importance of the Acyl Chain Structure. Plant Physiol 120:83–92PubMedGoogle Scholar
  22. Den Hartog M, Verhoef N, Munnik T (2003) Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol 132:311–317PubMedGoogle Scholar
  23. Dudley ME, Long SR (1989) A non-nodulating alfalfa mutant displays neither root hair curling nor early cell division in response to Rhizobium meliloti. Plant Cell 1:65–72PubMedGoogle Scholar
  24. Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681PubMedGoogle Scholar
  25. Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966PubMedGoogle Scholar
  26. Esseling JJ, Lhuissier FGP, Emons AMC (2003) Nod factor-induced root hair curling: continuous polar growth towards the point of Nod factor application. Plant Physiol 132:1982–1988PubMedGoogle Scholar
  27. Esseling JJ, Lhuissier FGP, Emons AMC (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 16:933–944PubMedGoogle Scholar
  28. Fang Y, Hirsch AM (1998) Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol 116:53–68PubMedGoogle Scholar
  29. Felle HH, Kondorosi E, Kondorosi A, Schultze M (1998) The role of ion fluxes in Nod factor signaling in Medicago sativa. Plant J 13:455–463Google Scholar
  30. Feng J, Li Q, Hu HL, Chen XC, Hong GF (2003) Inactivation of the nod box distal half-site allows tetrameric NodD to activate nodA transcription in an inducer-independent manner. Nucl Acids Res 31:3143–3156PubMedGoogle Scholar
  31. Firmin JL, Wilson KE, Carlson RW, Davies AE, Downie JA (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 10:351–360PubMedGoogle Scholar
  32. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing, rhizobia during nodulation of temperate legumes, Microbiol. Mol Biol Rev 68:280–300Google Scholar
  33. Geurts R, Fedorova E, Bisseling T (2005) Nod factor signalling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol 8:346–352PubMedGoogle Scholar
  34. Gleason C, Chaudhuri S, Yang T, Muñoz A, Poovaiah BW, Oldroyd GE (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441:1149–1152PubMedGoogle Scholar
  35. Goedhart J, Hink MA, Visser AJ, Bisseling T, Gadella TW Jr (2000) In vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls. Plant J 21:109–119PubMedGoogle Scholar
  36. Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693PubMedGoogle Scholar
  37. Gupta RS (2005) Protein signatures distinctive of alpha proteobacteria and its subgroups and a model for alpha-proteobacterial evolution. Crit Rev Microbiol 31:101–135PubMedGoogle Scholar
  38. Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, Wang TL, Downie JA (2006) Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142:1739–1750PubMedGoogle Scholar
  39. Heidstra R, Geurts R, Franssen H, Spaink HP, van Kammen A, Bisseling T (1994) Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol 105:787–797PubMedGoogle Scholar
  40. Hirsch AM, Bhuvaneswari TV, Torrey JG, Bisseling T (1989) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci USA 86:1244–1248PubMedGoogle Scholar
  41. Honma MA, Asomaning M, Ausubel FM (1990) Rhizobium meliloti nodD genes mediate host-specific activation of nodABC. J Bacteriol 172:901–911PubMedGoogle Scholar
  42. Horvath B, Heidstra R, Miklos L, Moerman M, Spaink HP, Promé J, van Kammen A, Bisseling T (1993) Lipo-oligosaccharides of Rhizobium induce infection related early nodulin gene expression in pea root hairs. Plant J 4:727–733PubMedGoogle Scholar
  43. Hutchison CE, Kieber JJ (2002) Cytokinin signaling in Arabidopsis. Plant Cell 14 (Suppl):S47–S59PubMedGoogle Scholar
  44. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531PubMedGoogle Scholar
  45. Ito T, Matsui Y, Ago T, Ota K, Sumimoto H (2001) Novel modular domain PB1 recognizes PC motif to mediate functional protein-protein interactions. EMBO J 20:3938–3946PubMedGoogle Scholar
  46. Johnson KL, Ingram GC (2005) Sending the right signals: regulating receptor kinase activity. Curr Opin Plant Biol 8:648–656PubMedGoogle Scholar
  47. Journet EP, Pichon M, Dedieu A, de Billy F, Truchet G, Barker DG (1994) Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J 6:241–249PubMedGoogle Scholar
  48. Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant Microbe Interact 14:737–748PubMedGoogle Scholar
  49. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091PubMedGoogle Scholar
  50. Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786–1789PubMedGoogle Scholar
  51. Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364PubMedGoogle Scholar
  52. Kevei Z, Lougnon G, Mergaert P, Horváth GV, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss GB, Kondorosi A, Endre G, Kondorosi E, Ané JM (2007) 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase1 interacts with NORK and is crucial for nodulation in medicago truncatula. Plant Cell 19:3974–3989PubMedGoogle Scholar
  53. Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker DG, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962PubMedGoogle Scholar
  54. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, De Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426PubMedGoogle Scholar
  55. Lafay B, Bullier E, Burdon JJ (2006) Bradyrhizobia isolated from root nodules of Parasponia (Ulmaceae) do not constitute a separate coherent lineage. Int J Syst Evol Microbiol 56:1013–1018PubMedGoogle Scholar
  56. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784PubMedGoogle Scholar
  57. Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364PubMedGoogle Scholar
  58. Limpens E, Bisseling T (2003) Signaling in symbiosis. Curr Opin Plant Biol 6:343–350PubMedGoogle Scholar
  59. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain recetor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–633PubMedGoogle Scholar
  60. Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, Bisseling T, Geurts R (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102:10375–10380PubMedGoogle Scholar
  61. Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J 38:203–214PubMedGoogle Scholar
  62. Lohar DP, Sharopova N, Endre G, Peñuela S, Samac D, Town C, Silverstein KA, VandenBosch KA (2006) Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol 140:221–234PubMedGoogle Scholar
  63. López-Lara IM, van den Berg JD, Thomas-Oates JE, Glushka J, Lugtenberg BJ, Spaink HP (1995) Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol Microbiol 15:627–638PubMedGoogle Scholar
  64. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640PubMedGoogle Scholar
  65. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335PubMedGoogle Scholar
  66. Mathesius U, Schlaman HR, Spaink HP, Of Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34PubMedGoogle Scholar
  67. Mathesius U, Charon C, Rolfe BG, Kondorosi A, Crespi M (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 Interact 13:617–628PubMedGoogle Scholar
  68. Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kaló P, Prabhu R, Marsh JF, Mitra RM, Kereszt A, Dudas B, VandenBosch K, Long SR, Cook DR, Kiss GB, Oldroyd GE (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19:1221–1234PubMedGoogle Scholar
  69. Mitra RM, Long SR (2004) Plant and bacterial symbiotic mutants define three transcriptionally distinct stages in the development of the Medicago truncatula/Sinorhizobium meliloti symbiosis. Plant Physiol 134:595–604PubMedGoogle Scholar
  70. Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development Gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705PubMedGoogle Scholar
  71. Miwa H, Sun J, Oldroyd GE, Downie JA (2006a) Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48:883–894PubMedGoogle Scholar
  72. Miwa H, Sun J, Oldroyd GE, Downie JA (2006b) Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact 19:914–923PubMedGoogle Scholar
  73. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618PubMedGoogle Scholar
  74. Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the β-subclass of proteobacteria. Nature 411:948–950PubMedGoogle Scholar
  75. Mulligan JT, Long SR (1989) A family of activator genes regulates expression of Rhizobium meliloti nodulation genes. Genetics 122:7–18PubMedGoogle Scholar
  76. Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104PubMedGoogle Scholar
  77. Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Masayoshi K (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429PubMedGoogle Scholar
  78. Ogawa J, Long SR (1995) The Rhizobium meliloti groELc locus is required for regulation of early nod genes by the transcription activator NodD. Genes Dev 9:714–729PubMedGoogle Scholar
  79. Oka-Kira E, Kawaguchi M (2006) Long-distance signlaing to control root nodule number. Curr Opin Plant Biol 9:496–502PubMedGoogle Scholar
  80. Oldroyd GE, Geurts R (2001) Medicago truncatula, going where no plant has gone before. Trends Plant Sci 6:552–554PubMedGoogle Scholar
  81. Oldroyd GE, Long SR (2003) Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod factor signaling. Plant Physiol 131:1027–1032PubMedGoogle Scholar
  82. Oldroyd ED, Downie JA (2004) Calcium, kinases and nodulation signaling in legumes. Nat Rev 5:566–576Google Scholar
  83. Oldroyd GE, Mitra RM, Wais RJ, Long SR (2001) Evidence for structurally specific negative feedback in the Nod factor signal transduction pathway. Plant J 28:191–199PubMedGoogle Scholar
  84. Peiter E, Sun J, Heckmann AB, Venkateshwaran M, Riely BK, Otegui MS, Edwards A, Freshour G, Hahn MG, Cook DR, Sanders D, Oldroyd GE, Downie JA, Ané JM (2007) The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol 145:192–203PubMedGoogle Scholar
  85. Pichon M, Journet EP, Dedieu A, de Billy F, Truchet G, Barker DG (1992) Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 4:1199–1211PubMedGoogle Scholar
  86. Pingret JL, Journet EP, Barker DG (1998) Rhizobium Nod factor signaling: evidence for a G protein-mediated transduction mechanism. Plant Cell 10:659–671PubMedGoogle Scholar
  87. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Grønland M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592PubMedGoogle Scholar
  88. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, Albrektsen AS, James EK, Thirup S, Stougaard J (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26:3923–3935PubMedGoogle Scholar
  89. Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc Natl Acad Sci USA 103:11081–11085PubMedGoogle Scholar
  90. Riely BK, Lougnon G, Ané JM, Cook DR (2007) The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49:208–216PubMedGoogle Scholar
  91. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624PubMedGoogle Scholar
  92. Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11:440–448PubMedGoogle Scholar
  93. Sawada H, Kuykendall LD, Young JM (2003) Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49:155–179PubMedGoogle Scholar
  94. Schauser L, Handberg K, Sandal N, Stiller J, Thykjær T, Nielsen A, Stougaard J (1998) Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus. Mol Gen Genet 259:414–423PubMedGoogle Scholar
  95. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195PubMedGoogle Scholar
  96. Schauser L, Wieloch W, Stougaard J (2005) Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J Mol Evol 60:229–237PubMedGoogle Scholar
  97. Scheres B, McKhann HI, Zalensky A, Löbler M, Bisseling T, Hirsch AM (1992) The PsENOD12 gene is expressed at two different sites in Afghanistan pea pseudonodules induced by auxin transport inhibitors. Plant Physiol 100:1649–1655PubMedGoogle Scholar
  98. Schnabel E, Journet PE, De Carvalho-Niebel F, Duc G, Frugoli J (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 58:809–822PubMedGoogle Scholar
  99. Schultze M, Quiclet-Sire B, Kondorosi E, Virelizier H, Glushka JN, Endre G, Géro SD, Kondorosi A (1992) Rhizobium meliloti produces a family of sulfated lipo-oligosaccharides exhibiting different degrees of plant host specificity. Proc Natl Acad Sci USA 89:192–196PubMedGoogle Scholar
  100. Scott KF (1986) Conserved nodulation genes from the non-legume symbiont Bradyrhizobium sp. (Parasponia). Nucl Acid Res 14:2905–2919Google Scholar
  101. Shaw SL, Long SR (2003) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol 131:976–984PubMedGoogle Scholar
  102. Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791PubMedGoogle Scholar
  103. Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E, Gough C, Bisseling T (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145:183–191PubMedGoogle Scholar
  104. Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92:2647–2651PubMedGoogle Scholar
  105. Sprent I (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174:11–25PubMedGoogle Scholar
  106. Steen A, Buist G, Horsburgh GJ, Venema G, Kuipers OP, Foster SJ, Kok J (2005) AcmA of Lactococcus lactis is an N-acetylglucosaminidase with an optimal number of LysM domains for proper functioning. FEBS J 272:2854–2868PubMedGoogle Scholar
  107. Stougaard J (2001) Genetics and genomics of root symbiosis. Curr Opin Plant Biol 4:328–335PubMedGoogle Scholar
  108. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962PubMedGoogle Scholar
  109. Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273PubMedGoogle Scholar
  110. Subramanian S, Stacey G, Yu O (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends Plant Sci 12:282–285PubMedGoogle Scholar
  111. Sun J, Miwa H, Downie JA, Oldroyd GE (2007) Mastoparan activates calcium spiking analogous to Nod factor-induced responses in Medicago truncatula root hair cells. Plant Physiol 144:695–702PubMedGoogle Scholar
  112. Surin BP, Downie JA (1988) Characterization of the Rhizobium leguminosarum genes nodLMN involved in efficient host-specific nodulation. Mol Microbiol 2:173–183PubMedGoogle Scholar
  113. Szczyglowski K, Shaw SS, Wopereis J, Copeland S, Hamburger D, Kasiborski B, Dazzo FB, de Bruijn FJ (1998) Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol Plant Microbe Interact 11:684–697Google Scholar
  114. Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53:971–977PubMedGoogle Scholar
  115. Timmers ACJ, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126:3617–3628PubMedGoogle Scholar
  116. Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107PubMedGoogle Scholar
  117. Trinick MJ (1973) Symbiosis between Rhizobium and the non-legume, Trema aspera. Nature 244:459–468Google Scholar
  118. Tsyganov VE, Voroshilova VA, Priefer UB, Borisov AY, Tikhonovich IA (2002) Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobium-pea (Pisum sativum L) symbiosis. Ann Bot (Lond) 89:357–366Google Scholar
  119. Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus Japonicus: legume research in the fast lane. Trends Plant Sci 10: 222–228PubMedGoogle Scholar
  120. van Brussel AA, Tak T, Boot KJ, Kijne JW (2002) Autoregulation of root nodule formation: signals of both symbiotic partners studied in a split-root system of Vicia sativa subsp Nigra. Mol Plant Microbe Interact 15:341–349PubMedGoogle Scholar
  121. Velazquez E, Peix A, Zurdo-Pineiro JL, Palomo JL, Mateos PF, Rivas R, Munoz-Adelantado E, Toro N, Garcia-Benavides P, Martinez-Molina E (2005) The coexistence of symbiosis and pathogenicity-determining genes in Rhizobium rhizogenes strains enables them to induce nodules and tumors or hairy roots in plants. Mol Plant-Microbe Interact 12:1325–1332Google Scholar
  122. Vijn I, Martinez-Abarca F, Yang WC, das Neves L, van Brussel A, van Kammen A, Bisseling T (1995) Early nodulin gene expression during Nod factor-induced processes in Vicia sativa. Plant J 8:111–119PubMedGoogle Scholar
  123. Wais RJ, Galera C, Oldroyd G, Catoira R, Penmetsa RV, Cook D, Gough C, Dénarié J, Long SR (2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc Natl Acad Sci USA 97:13407–13412PubMedGoogle Scholar
  124. Wais RJ, Keating DH, Long SR (2002) Structure-function analysis of nod factor-induced root hair calcium spiking in Rhizobium-legume symbiosis. Plant Physiol 129:211–224PubMedGoogle Scholar
  125. Walther TC, Alves A, Pickersgill H, Loïodice I, Hetzer M, Galy V, Hülsmann BB, Köcher T, Wilm M, Allen T, Mattaj IW, Doye V (2003) The conserved Nup107–160 complex is critical for nuclear pore complex assembly. Cell 113:195–206PubMedGoogle Scholar
  126. Wasson AP, Pellerone FI, Mathesius U (2006) Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell 18:1617–1629PubMedGoogle Scholar
  127. Wopereis J, Pajuelo E, Dazzo FB, Jiang Q, Gresshoff PM, De Bruijn FJ, Stougaard J Szczyglowski K (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 23:97–114PubMedGoogle Scholar
  128. Yang WC, de Blank C, Meskiene I, Hirt H, Bakker J, van Kammen A, Franssen H, Bisseling T (1994) Rhizobium nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell 6:1415–1426PubMedGoogle Scholar
  129. Yang Z, Fu Y (2007) ROP/RAC GTPase signaling. Curr Opin Plant Biol 10:490–494PubMedGoogle Scholar
  130. Zhang Y, Li X (2005) A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1–1,constitutive 1. Plant Cell 17:1306–1316PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.Laboratory of Molecular Biology, Graduate School of Experimental Plant Sciences (EPS)Wageningen University and Research CenterWageningenThe Netherlands

Personalised recommendations