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Journal of Plant Growth Regulation

, Volume 22, Issue 1, pp 47–72 | Cite as

Signaling Interactions During Nodule Development

  • Brett James FergusonEmail author
  • Ulrike Mathesius
Thematic Article

Abstract

Nitrogen fixing bacteria, collectively referred to as rhizobia, are able to trigger the organogenesis of a new organ on legumes, the nodule. The morphogenetic trigger is a Rhizobium-produced lipochitin-oligosaccharide called the Nod factor, which is necessary, and in some legumes sufficient, for triggering nodule development in the absence of the bacterium. Because plant development is substantially influenced by plant hormones, it has been hypothesized that plant hormones (mainly the classical hormones abscisic acid, auxin, cytokinins, ethylene and gibberellic acid) regulate nodule development. In recent years, evidence has shown that Nod factors might act in legumes by changing the internal plant hormone balance, thereby orchestrating the nodule developmental program. In addition, many nonclassical hormonal signals have been found to play a role in nodule development, some of them similar to signals involved in animal development. These compounds include peptide hormones, nitric oxide, reactive oxygen species, jasmonic acid, salicylic acid, uridine, flavonoids and Nod factors themselves. Environmental factors, in particular nitrate, also influence nodule development by affecting the plant hormone status. This review summarizes recent findings on the involvement of classical and nonclassical signals during nodule development with the aim of illustrating the multiple interactions existing between these compounds that have made this area so complicated to analyze.

Keywords

Cell division Defence response Meristem Nod factors Nodulation Organogenesis Peptide signals Plant hormones Receptor kinase Systemic acquired resistance 

Notes

Acknowledgements

Due to the vast size of the topic, the authors have undoubtedly omitted some researchers’ work, for which we apologize. Financial support was provided to BJF by the Tasmanian International Research Scholarship and the Thomas Crawford Memorial Research Scholarship, both of the University of Tasmania, and to UM by the Australian Research Council.

References

  1. 1.
    Arora, N, Skoog, F, Alien, ON 1959Kinetin-induced pseudonodules on tobacco roots.Am J Bot46610613Google Scholar
  2. 2.
    Asad, S, Fang, Y, Wykoff, KL, Hirsch, AM 1994Isolation and characterisation of cDNA and genomic clones of MsENOD40: transcripts are detected in meristematic cells of alfalfa.Protoplasma1831023Google Scholar
  3. 3.
    Atzorn, R, Crozier, A, Wheeler, CT, Sandberg, G 1988Production of gibberellins and indole-3-acetic acid by Rhizobium phaseoli in relation to nodulation of Phaseolus vulgaris roots.Planta175532538Google Scholar
  4. 4.
    Badenoch-Jones, J, Parker, CW, Letham, DS 1987Phytohormones, Rhizobium mutants, and nodulation in legumes. VII. Identification and quantification of cytokinins in effective and ineffective pea root nodules using radioimmunoassay.J Plant Growth Regul697111Google Scholar
  5. 5.
    Badenoch-Jones, J, Summons, RE, Rolfe, BG, Letham, DS 1984Phytohormones, Rhizobium mutants, and nodulation in legumes. IV. Auxin metabolites in pea root nodules.J Plant Growth Regul32339Google Scholar
  6. 6.
    Bano, A, Harper, JE, Auge, RM, Neuman, DS 2002Changes in phytohormone levels following inoculation of two soybean lines differing in nodulation.Funct Plant Biol29965974Google Scholar
  7. 7.
    Bano, A, Harper, JE 2002Plant growth regulators and phloem exudates modulate root nodulation of soybean.Funct Plant Biol2912991307Google Scholar
  8. 8.
    Bano, A, Hillman, JR 1986Effect of abscisic acid on nodule morphology, nitrogenase activity and H2 evolution in Faba vulgaris.Ann Bot58281283Google Scholar
  9. 9.
    Bauer, P, Ratet, P, Crespi, MD, Schultze, M, Kondorosi, A 1996Nod-factors and cytokinins induce similar cortical cell divisions, amyloplast deposition and MsENOD12A expression patterns in alfalfa roots.Plant J1091105Google Scholar
  10. 10.
    Benhamou, N, Asselin, A 1989Attempted localisation for a substrate for chitinases in plant cells reveals abundant N-acetyl-D-glucosamine residues in secondary walls.Biol Cell67341350Google Scholar
  11. 11.
    Bhalerao, RP, Eklof, J, Ljung, K, Marchant, A, Bennett, M, Sandberg, G 2002Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings.Plant J29325332PubMedGoogle Scholar
  12. 12.
    Billington, DC, Golding, BT, Primrose, SB 1979Biosynthesis of ethylene from methionine. Isolation of the putative intermediate 4-methylthio-2-oxobutanoate from culture fluids of bacteria and fungi.Biochem J182827836PubMedGoogle Scholar
  13. 13.
    Blilou, I, Ocampo, JA, Garcia-Garrido, JM 1999Resistance of pea roots to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid.J Exp Bot5016631668Google Scholar
  14. 14.
    Boot, KJM, van Brussel, AAN, Tak, T, Spaink, HP, Kijne, JW 1999Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viclae reduce auxin transport capacity in Vicia sativa subsp. nigra roots.Mol Plant-Microbe Interact12839844Google Scholar
  15. 15.
    Brown, DE, Rashotte, AM, Murphy, AS, Normanly, J, Tague, BW, Peer, WA, Taiz, L, Muday, GK 2001Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis.Plant Physiol126524535PubMedGoogle Scholar
  16. 16.
    Bueno, P, Soto, MJ, Rodríguez-Rosales, MP, Sanjuan, J, Olivares, J, Donaire, JP 2001Time-course of lipoxygenase, antioxidant enzyme activities and H2O2 accumulation during the early stages of Rhizobium-legume symbiosis.New Phytol1529196Google Scholar
  17. 17.
    Burg, SP, Burg, EA 1966The interaction between auxin and ethylene and its role in plant growth.Proc Natl Acad Sci USA55262269PubMedGoogle Scholar
  18. 18.
    Caba, JM, Centeno, ML, Fernandez, B, Gresshoff, PM, Ligero, F 2000Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type.Planta21198104PubMedGoogle Scholar
  19. 19.
    Caba, JM, Poveda, L, Gresshoff, PM, Ligero, F 1999Differential sensitivity of nodulation to ethylene in soybean cv. Bragg and a supernodulating mutant.New Phytol142233242Google Scholar
  20. 20.
    Caba, JM, Recalde, L, Ligero, F 1998Nitrate-induced ethylene biosynthesis and the control of nodulation in alfalfa.Plant Cell Env218793Google Scholar
  21. 21.
    Camas, A, Cardenas, L, Quinto, C, Lara, M 2002Expression of different calmodulin genes in bean (Phaseolus vulgaris L.): role of Nod factor on calmodulin gene regulation.Mol Plant-Microbe Interact15428436PubMedGoogle Scholar
  22. 22.
    Carroll, BJ, McNeil, DL, Gresshoff, PM 1985Isolation and properties of soybean (Glycine max) mutants that nodulate in the presence of high nitrate concentrations.Proc Natl Acad Sci USA8241644166Google Scholar
  23. 23.
    Charbonneau, GA, Newcomb, W 1985Growth regulators in developing effective root nodules of the garden pea (Pisum sativum L.).Biochem Physiol Pflanzen180667681Google Scholar
  24. 24.
    Charon, C, Johansson, C, Kondorosi, E, Kondorosi, A, Crespi, M 1997 enod40 induces dedifferentiation and division of root cortical cells in legumes.Proc Natl Acad Sci USA9489018906PubMedGoogle Scholar
  25. 25.
    Charon, C, Sousa, C, Crespi, M, Kondorosi, A 1999Alteration of enod40 expression modifies Medicago truncatula root nodule development induced by Sinorhizobium meliloti.Plant Cell1119531965PubMedGoogle Scholar
  26. 26.
    Chattopadhyay, KK, Basu, PS 1989Studies on root nodules of leguminous trees: II. The bioproduction of different phytohormones in root nodules of Samanea saman (Jacq.) Merril and by its rhizobial symbiont.Biochem Physiol Pflanzen184387394Google Scholar
  27. 27.
    Cho, MJ, Harper, JE 1993Effect of abscisic acid application on root isoflavonoid concentration and nodulation of wild type and nodulation-mutant soybean plants.Plant Soil152145149Google Scholar
  28. 28.
    Collinge, DB, Kragh, KM, Mikkelsen, JD, Nielsen, KK, Rasmussen, U, Vad, K 1993Plant chitinases.Plant J33140PubMedGoogle Scholar
  29. 29.
    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 Soil23018Google Scholar
  30. 30.
    Cook, D, Dreyer, D, Bonnet, D, Howell, M, Nony, E, VandenBosch, K 1995Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti.Plant Cell74355PubMedGoogle Scholar
  31. 31.
    Cooper, JB, Long, SR 1994Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion.Plant Cell6215225PubMedGoogle Scholar
  32. 32.
    Cooper, JE, Rao, R 1992Localised changes in flavonoid biosynthesis in roots of Lotus pendiculatus after infection by Rhizobium loti.Plant Physiol100444450PubMedGoogle Scholar
  33. 33.
    Corich, V, Goormachtig, S, Lievens, S, Van Montagu, M, Holsters, M 1998Patterns of ENOD40 gene expression in stem-borne nodules of Sesbania rostrata.Plant Mol Biol376776PubMedGoogle Scholar
  34. 34.
    Coronado, C, Zuanazzi, JAS, Sallaud, C, Quirion, JC, Esnault, R, Husson, HP, Kondorosi, A, Ratet, P 1995Alfalfa root flavonoid production is nitrogen regulated.Plant Physiol108533542PubMedGoogle Scholar
  35. 35.
    Costacurta, A, Vanderleyden, J 1995Synthesis of phytohormones by plant-associated bacteria.Crit Rev Microbiol21118PubMedGoogle Scholar
  36. 36.
    Crespi, M, Galvez, S 2000Molecular mechanisms in root nodule development.J Plant Growth Regul19155166PubMedGoogle Scholar
  37. 37.
    Crespi, MD, Jurkevitch, E, Poiret, M, d’Aubenton-Carafa, Y, Petrovics, G, Kondorosi, E, Kondorosi, A 1994 enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth.EMBO J1350995112PubMedGoogle Scholar
  38. 38.
    Cueto, M, Hernández-Perera, O, Martín, R, Bentura, ML, Rodrigo, J, Lamas, S, Golvano, MP 1996Presence of nitric oxide synthase activity in roots and root nodules of Lupinus albus.FEBS Lett398159164PubMedGoogle Scholar
  39. 39.
    Cullimore, JV, Ranjeva, R, Bono, JJ 2001Perception of lipo-chitooligosaccharidic Nod factors in legumes.Trends Plant Sci62430PubMedGoogle Scholar
  40. 40.
    D’Agostino, IB, Kieber, JJ 1999Molecular mechanisms of cytokinin action.Curr Opin Plant Biol2359364PubMedGoogle Scholar
  41. 41.
    Dakora, FD 1995Plant flavonoids - biological molecules for useful exploitation.Aust J Plant Physiol228799Google Scholar
  42. 42.
    Dangar, TK, Basu, PS 1984Seasonal changes and metabolism of plant hormones in root nodules of Lens sp.Biol Plant26253259Google Scholar
  43. 43.
    Dangar, TK, Basu, PS 1987Studies on plant growth substances, IAA metabolism and nitrogenase activity in root nodules of Phaseolus aureus Roxb. var. mungo.Biol Plant29350354Google Scholar
  44. 44.
    Dangar, TK, Basu, PS 1991Abscisic acid production in culture by some rhizobium spp. of leguminous trees and pulses.Folia Microbiol36527532Google Scholar
  45. 45.
    Dantán-González, E, Rosenstein, Y, Quinto, C, Sánchez, F 2001Actin monoubiquitylation is induced in plants in response to pathogens and symbionts.Mol Plant-Microbe Interac1412671273Google Scholar
  46. 46.
    Davies, J, Zhang, J 1991Root signals and the regulation of growth and development of plants in drying soil.Annu Rev Plant Physiol Plant Mol Biol425576Google Scholar
  47. 47.
    de Billy, F, Grosjean, C, May, S, Bennett, M, Cullimore, JV 2001Expression studies on AUX1-like gens in Medicago truncatula suggest that auxin is required at two steps in early nodule development.Mol Plant-Microbe Interact14267277PubMedGoogle Scholar
  48. 48.
    Dehio, C, de Bruijn, FJ 1992The early nodulin gene SrEnod2 from Sesbania rostrata is 10 inducible by cytokinin.Plant J2117128PubMedGoogle Scholar
  49. 49.
    DeJong, AJ, Cordewener, J, Lo Schiavo, F, Terzi, M, Vanderkerckove, J, van Kammen, A, de Vries, S 1992A carrot somatic embryo mutant is rescued by chitinase.Plant Cell4425433Google Scholar
  50. 50.
    Delves, AC, Mathews, A, Day, DA, Carter, AS, Carroll, BJ, Gresshoff, PM 1986Regulation of soybean-Rhizobium nodule symbiosis by shoot and root factors.Plant Physiol82588590PubMedGoogle Scholar
  51. 51.
    D’Haeze, W, Holsters, M 2002Nod factor structures, responses, and perception during initiation of nodule development.Glycobiol1279R105RGoogle Scholar
  52. 52.
    Djordjevic, MA, Mathesius, U, Arioli, T, Weinman, JJ, Gärtner, E 1997Chalcone synthase gene expression in transgenic subterranean clover correlates with localised accumulation of flavonoids.Aust J Plant Physiol24119132Google Scholar
  53. 53.
    Dobert, RC, Rood, SB, Blevins, DG 1992aGibberellins and the legume-Rhizobium symbiosis I. Endogenous gibberellins of Lima Bean (Phaseolus lunatus L.) stems and nodules.Plant Physiol98221224Google Scholar
  54. 54.
    Dobert, RC, Rood, SB, Blevins, DG 1992bRhizobial-induced increase in internode length and identification of endogenous GAs of cowpea (Vigna unguiculata [L.] Walp) stems and nodules.J Plant Growth Regul11155164Google Scholar
  55. 55.
    Dobert, RC, Rood, SB, Zanewich, K, Blevins, DG 1992cGibberellins and the legume-Rhizobium symbiosis III. Quantification of gibberellins from stems and nodules of Lima Bean and cowpea.Plant Physiol10019942001Google Scholar
  56. 56.
    Doerner, P, Jorgensen, JE, You, R, Steppuhn, J, Lamb, C 1996Root growth and cyclin control.Trends Plant Sci1211212Google Scholar
  57. 57.
    Drennan, DSH, Norton, C 1972The effect of ethrel on nodulation in Pisum sativum L.Plant Soil365357Google Scholar
  58. 58.
    Dullaart, J, Duba, LI 1970Presence of gibberellin-like substances and their possible role in auxin bioproduction in root nodules and roots of Lupinus luteus L.Acta Bot Neerl19877883Google Scholar
  59. 59.
    Dyachok, JV, Tobin, AE, Price, NPJ, von Arnold, S 2000Rhizobial Nod factors stimulate somatic embryo development in Picea abies.Plant Cell Rep19290297Google Scholar
  60. 60.
    Dyachok, JV, Wiweger, M, Kenne, L, von Arnold, S 2002Endogenous nod-factor-like signal molecules promote early somatic embryo development in Norway spruce.Plant Physiol128523533PubMedGoogle Scholar
  61. 61.
    Endre, G, Kereszt, A, Kevei, Z, Mihacea, S, Kalo, P, Kiss, GB 2002A receptor kinase gene regulating symbiotic nodule development.Nature417962966PubMedGoogle Scholar
  62. 62.
    Estabrook, EM, Sengupta-Gopalan, C 1991Differential expression of phenylalanin ammonia-lyase and chalcone synthase during soybean nodule development.Plant Cell3299308PubMedGoogle Scholar
  63. 63.
    Evensen, KB, Blevins, DG 1981Differences in endogenous levels of gibberellin-like substances in nodules of Phaseolus lunatus L. plants inoculated with two Rhizobial strains.Plant Physiol65195198Google Scholar
  64. 64.
    Fang, Y, Hirsch, AM 1998Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in alfalfa.Plant Physiol1165368PubMedGoogle Scholar
  65. 65.
    Favery, B, Complainville, A, Vinardell, JM, Lecomte, P, Vaubert, D, Mergaert, P, Kondorosi, A, Kondorosi, E, Crespi, M, Abad, P 2002The endosymbiosis-induced genes ENOD40 and CCS52a are involved in endoparasitic-nematode interactions in Medicago truncatula.Mol Plant-Microbe Interact1510081013PubMedGoogle Scholar
  66. 66.
    Fearn, JC, LaRue, TA 1991Ethylene inhibitors restore nodulation to sym5 mutants of Pisum sativum L. cv Sparkle.Plant Physiol96239244PubMedGoogle Scholar
  67. 67.
    Fedorova, EE, Al’zhapparova, ZK, Zhiznevskaya, GY, Artemenko, EN, Izmailov, SF 1992Phytohormones in soybean root nodules.Sov Plant Physiol39135139Google Scholar
  68. 68.
    Fedorova, EE, Zhiznevskaya, GY, Kalibernaya, ZV, Artemenko, EN, Izmailov, SF, Gus’kov, AV 2000IAA metabolism during development of symbiosis between Phaseolus vulgaris and Rhizobium phaseoli.Russ J Plant Physiol47203206Google Scholar
  69. 69.
    Fedorova, M, van der Mortel, J, Matsumoto, PA, Cho, J, Town, CD, VandenBosch, K, Gnatt, S, Vance, CP 2002Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula.Plant Physiol130519537PubMedGoogle Scholar
  70. 71.
    Fernández-López, M, Goormachtig, S, Goa, M, D’Haeze, W, van Montagu, M, Holsters, M 1998Ethylene-mediated phenotypic plasticity in root nodule development on Sesbania rostrate.Proc Natl Acad Sci USA951272412728PubMedGoogle Scholar
  71. 72.
    Fletcher, WW, Alcorn, JWS, Raymond, JC 1959Gibberellic acid and nodulation of legumes.Nature1841576Google Scholar
  72. 73.
    Foucher, F, Kondorosi, E 2000Cell cycle regulation in the course of nodule organogenesis in Medicago.Plant Mol Biol43773786PubMedGoogle Scholar
  73. 74.
    Fu, X, Harberd, NP 2003Auxin promotes Arabidopsis root growth by modulating gibberellin response.Nature421740743PubMedGoogle Scholar
  74. 75.
    Galston, AW 1959Gibberellins and nodulation.Nature183545PubMedGoogle Scholar
  75. 76.
    Gilles-González, MA, González, G, Perutz, MF, Kiger, L, Marden, MC, Poyart, C 1994Heme-based sensors, exemplified by the kinase FixL, are a new class of heme protein with distinctive ligand binding and autoxidation.Biochem3380678073Google Scholar
  76. 77.
    Goicoechea, N, Antolín, MC, Sánchez-Díaz, M 1997Gas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought.Physiol Plant100989997Google Scholar
  77. 78.
    González, EM, Gálvez, L, Arrese-Igor, C 2001aAbscisic acid induces a decline in nitrogen fixation that involves leghaemoglobin, but is independent of sucrose synthase activity.J Exp Bot52285293Google Scholar
  78. 79.
    González, EM, Gálvez, L, Royuela, M, Aparicio-Tejo, PM, Arrese-Igor, C 2001bInsights into the regulation of nitrogen fixation in pea nodules: lessons from drought, abscisic acid and increased photoassimilate availability.Agronomic21607613Google Scholar
  79. 80.
    González-Pasayo, R, Martinez-Romero, E 2000Multiresistance genes of Rhizobium etli CFN42.Mol Plant-Microbe Interact13572577PubMedGoogle Scholar
  80. 81.
    Goodlass, G, Smith, KA 1979Effects of ethylene on root extension and nodulation of pea (Pisum sativum L.) and white clover (Trifolium repens L.).Plant Soil51387395Google Scholar
  81. 82.
    Goormachtig, S, Alves-Ferreira, M, van Montague, M, Engler, G, Holsters, M 1997Expression of cell cycle genes during Sesbania rostrata stem nodule development.Mol Plant-Microbe Interact10316325PubMedGoogle Scholar
  82. 83.
    Goverse, A, Overmars, H, Engelbertink, J, Schots, A, Bakker, J, Helder, J 2000Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin.Mol Plant-Microbe Interact1311211129PubMedGoogle Scholar
  83. 84.
    Gresshoff, PM, Mathews, A, Krotzky, A, Olsson, JE, Carroll, BJ, Delves, AC, Kosslak, R, Applebaum, ER, Day, DA 1988Supernodulating and non-nodulating mutants of soybean.Palacio, RVerma, DPS eds. Molecular Genetics Of Plant-Microbe Interactions.APS PressSt Paul MN364369Google Scholar
  84. 85.
    Gresshoff, PM 1993Molecular-genetic analysis of nodulation genes in soybean.Plant Breed Rev11275318Google Scholar
  85. 86.
    Grobbelaar, N, Clarke, B, Hough, MC 1971The nodulation and nitrogen fixation of isolated roots of Phaseolus vulgaris L. III. The effect of carbon dioxide and ethylene.Plant Soil(Spec Vol)215223Google Scholar
  86. 87.
    Gubler, F, Kalla, R, Roberts, JK, Jacobsen, JV 1995Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactions of a high-pl α-amylase gene promoter.Plant Cell718791891PubMedGoogle Scholar
  87. 88.
    Guinel, FC, Geil, RD 2002A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment in these two symbioses.Can J Bot80695720Google Scholar
  88. 89.
    Guinel, FC, LaRue, TA 1992Ethylene inhibitors partly restore nodulation to pea mutant E107 (brz).Plant Physiol99515518PubMedGoogle Scholar
  89. 90.
    Guinel, FC, Sloetjes, LL 2000Ethylene is involved in the nodulation phenotype of Pisum sativum R50 (sym16), a pleiotropic mutant that nodulates poorly and has pale green leaves.J Exp Bot51885894PubMedGoogle Scholar
  90. 91.
    Gundlach, H, Müller, MJ, Kutchan, TM, Zenk, MH 1992Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures.Proc Natl Acad Sci USA8923892393PubMedGoogle Scholar
  91. 92.
    Hause, B, Maier, W, Miersch, O, Kramell, R, Strack, D 2002Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots.Plant Physiol13012131220PubMedGoogle Scholar
  92. 93.
    Heidstra, R, Yang, YC, Yalcin, Y, Peck, S, Emons, AM, van Kammen, A, Bisseling, T 1997Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium legume interaction.Development12417811787PubMedGoogle Scholar
  93. 94.
    Henson, IE, Wheeler, CT 1976Hormones in plants bearing nitrogen-fixing root nodules: the distribution of cytokinins in Vicia faba L.New Phytol76433439Google Scholar
  94. 95.
    Henson, IE, Wheeler, CT 1977Hormones in plants bearing nitrogen-fixing root nodules: gibberellin-like substances in Alnus glutinosa (L.) gaertn.New Phytol78373381Google Scholar
  95. 96.
    Himanen, K, Boucheron, E, Vanneste, S, Engler, JD, Inzé, D, Beeckman, T 2002Auxin-mediated cell cycle activation during early lateral root initiation.Plant Cell1423392351PubMedGoogle Scholar
  96. 97.
    Hirsch, AM, Bhuvaneswari, TV, Torrey, JG, Bisseling, T 1989Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors.Proc Natl Acad Sci USA8612441248PubMedGoogle Scholar
  97. 98.
    Hirsch, AM, Fang, Y, Asad, S, Kapulnik, Y 1997The role of phytohormones in plant-microbe symbioses.Plant Soil194171184Google Scholar
  98. 99.
    Hirsch, AM, Fang, Y 1994Plant hormones and nodulation: What’s the connection?Plant Mol Biol2659PubMedGoogle Scholar
  99. 100.
    Hirsch, AM 1992Developmental biology of legume nodulation.New Phytol122211237Google Scholar
  100. 101.
    Hunter, WJ 2001Influence of root-applied epibrassinolide and carbenoxolone on the nodulation and growth of soybean (Glycine max L.) seedlings.J Agron Crop Sci186217221Google Scholar
  101. 102.
    Hutangura, P, Mathesius, U, Rolfe, BG, Jones, MEK 1999Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway.Aust J Plant Physiol26221231Google Scholar
  102. 103.
    Jacobs, M, Rubery, PH 1988Naturally occurring auxin transport regulators.Science241346349PubMedGoogle Scholar
  103. 104.
    Jaiswal, V, Rizvi, SJH, Mukerji, D, Mature, SN 1981Cytokinins in root nodules of Phaseolus mungo.Ann Bot48301305Google Scholar
  104. 105.
    Jelenska, J, Deckert, J, Kondorosi, E, Legocki, AB 2000Mitotic B-type cyclins are differentially regulated by phytohormones and during yellow lupine nodule development.Plant Sci1502939Google Scholar
  105. 106.
    Jiang, M, Zhang, J 2001Effect of abscisic acid and active oxygen species, antioxidant defence system and oxidative damage in leaves of maize seedlings.Plant Cell Physiol4212651273PubMedGoogle Scholar
  106. 107.
    Jimenez-Zurdo, JI, Frugier, F, Crespi, MD, Kondorosi, A 2000Expression profiles of 22 novel molecular markers for organogenetic pathways acting in alfalfa nodule development.Mol Plant-Microbe Interact1396106PubMedGoogle Scholar
  107. 108.
    Jinsart, W, Ternai, B, Polya, GM 1991Inhibition of wheat embryo calcium-dependent protein kinase and avian light chanin kinase by flavonoids and related compounds.Biol Chem Hoppe-Seyler372819827PubMedGoogle Scholar
  108. 109.
    John, PCL, Zhang, K, Cong, C, Diederich, L, Wightman, F 1993p34cdc2 related proteins in control of cell cycle progression, the switch between division and differentiation in tissue development, and stimulation of division by auxin and cytokinin.Aust J Plant Physiol20503526Google Scholar
  109. 110.
    Kanayama, Y, Yamamoto, Y 1990Inhibition of nitrogen fixation in soybean plants supplied with nitrate II. Accumulation and properties of nitrosylleghemoglobin in nodules.Plant Cell Physiol31207214Google Scholar
  110. 111.
    Katznelson, H, Cole, SE 1965Production of gibberellin-like substances by bacteria and actinomycetes.Can J Microbiol11733741PubMedGoogle Scholar
  111. 112.
    Kawaguchi, M, Imaizumi-Anraku, H, Fukai, S, Syono, K 1996Unusual branching in the seedlings of Lotus japonicus - gibberellins reveal the nitrogen-sensitive cell divisions within the pericycle on roots.Plant Cell Physiol37461470Google Scholar
  112. 113.
    Ke, D, Saltveit, ME 1988Plant hormone interaction and phenolic metabolism in the regulation of russet spotting in iceberg lettuce.Plant Physiol8811361140PubMedGoogle Scholar
  113. 114.
    Kistner, C, Parniske, M 2002Evolution of signal transduction in intracellular symbiosis.Trends Plant Sci7511518PubMedGoogle Scholar
  114. 115.
    Kneer, R, Poulev, AA, Olesinski, A, Raskin, I 1999Characterization of the elicitor-induced biosynthesis and secretion of genestein from roots of Lupinus luteus L.J Exp Bot5015531559Google Scholar
  115. 116.
    Koltai, H, Dhandaydham, M, Opperman, C, Thomas, J, Bird, D 2001Overlapping plant signal transduction pathways induced by a parasitic nematode and a rhizobial endosymbiont.Mol Plant-Microbe Interact1411681177PubMedGoogle Scholar
  116. 117.
    Kondorosi, E, Hoffmann, B, Endre, G, Börge, L, Koncz, C, Dudits, D, Szecsi, J, Kiss, G, Kondorosi, A 1993Involvement of hormones in nodule initiation: auxin sensitivity and hormone balance affect nodulation of Medicago.Palacios, RMora, JNewton, E eds. New Horizons in Nitrogen FixationKluwer Academic PublishersDordrecht, The Netherlands357Google Scholar
  117. 118.
    Kouchi, H, Hata, S 1993Isolation and characterisation of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development.Mol Gen Gent238106119Google Scholar
  118. 119.
    Kouchi, H, Takane, K, So, RB, Ladha, JK, Reddy, PM 1999Rice ENOD40: isolation and expression analysis in rice and transgenic soybean root nodules.Plant J18121129PubMedGoogle Scholar
  119. 120.
    Krusell, L, Madsen, LH, Sato, S, Aubert, G, Genua, A, Szczyglowski, K, Due, G, Kaneko, T, Tabata, S, de Bruijn, F, Pajuelo, E, Sandals, N, Stougaard, J 2002Shoot control of root development and nodulation is mediated by a receptor kinase.Nature420422426PubMedGoogle Scholar
  120. 121.
    Lawson, CGR, Rolfe, BG, Djordjevic, MA 1996 Rhizobium inoculation induces condition-dependent changes in the flavonoid composition of root exudates from Trifolium subterraneum.Aust J Plant Physiol2393101Google Scholar
  121. 122.
    Lee, KH, LaRue, TA 1992aPleiotropic effects of sym-17: a mutation in Pisum sativum L. cv Sparkle causes decreased nodulation, altered root and shoot growth, and increased ethylene production.Plant Physiol10013261333Google Scholar
  122. 123.
    Lee, KH, LaRue, TA 1992bEthylene as a possible mediator of light- and nitrate-induced inhibition of nodulation of Pisum sativum L. cv Sparkle.Plant Physiol10013341338Google Scholar
  123. 124.
    Lee, KH, LaRue, TA 1992cExogenous ethylene inhibits nodulation of Pisum sativum L. cv 7 Sparkle.Plant Physiol10017591763Google Scholar
  124. 125.
    Lee, TT 1971Cytokinin-controlled indoleacetic acid oxidase isoenzymes in tobacco callus cultures.Plant Physiol47181185PubMedGoogle Scholar
  125. 126.
    Lhuissier, FGP, De Ruijter, NCA, Sieberer, BJ, Esseling, JJ, Emons, AMC 2001Time course of cell biological events evoked in legume root hairs by Rhizobium Nod factors: state of the art.Ann Bot87289302Google Scholar
  126. 127.
    Lian, B, Zhou, X, Miransari, M, Smith, DL 2000Effects of salicylic acid on the development and root nodulation of soybean seedlings.J Agron Crop Sci185187192Google Scholar
  127. 128.
    Libbenga, KR, Harkes, PAA 1973Initial proliferation of cortical cells in the formation of root nodules in Pisum sativum L.Planta1141728Google Scholar
  128. 129.
    Libbenga, KR, van Iren, F, Bogers, RJ, Schraag-Lamers, MF 1973The role of hormones and gradients in the initiation of cortex proliferation and nodule formation in Pisum sativum L.Planta1142939Google Scholar
  129. 130.
    Ligero, F, Caba, JM, Lluch, C, Olivares, J 1991Nitrate inhibition of nodulation can be overcome in the presence of the ethylene inhibitor, aminoethoxyvinylglycine.Plant Physiol9712211225PubMedGoogle Scholar
  130. 131.
    Ligero, F, Lluch, C, Olivares, J 1986Evolution of ethylene from roots of Medicago sativa plants inoculated with Rhizobium meliloti.J Plant Physiol125361365Google Scholar
  131. 132.
    Logemann, E, Wu, SC, Schroder, J, Schmelzer, E, Somssich, IE, Hahlbrock, K 1995Gene activation by UV light, fungal elicitor or fungal infection in Petroselinum crispum is correlated with repression of cell cycle-related genes.Plant J8865876PubMedGoogle Scholar
  132. 133.
    Lorteau, M-A, Ferguson, BJ, Guinel, FC 2001Effects of cytokinin on ethylene production and nodulation in pea (Pisum sativum) cv. Sparkle.Physiol Plant112421428PubMedGoogle Scholar
  133. 134.
    Markwei, CM, LaRue, TA 1997Phenotypic characterization of sym 21, a gene conditioning shoot-controlled inhibition of nodulation in Pisum sativum cv Sparkle.Physiol Plant100927932Google Scholar
  134. 135.
    Martinez-Abarca, F, Herrera-Cervara, JA, Bueno, P, Sanjuan, J, Bisseling, T, Olivares, J 1998Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis.Mol Plant-Microbe Interact11153155Google Scholar
  135. 136.
    Maskell, CS, Gibson, JF, Dart, PJ 1977Electron-paramagnetic-resonance studies of leghaemoglobins from soya-beans and cowpea root nodules.Biochem J167435445Google Scholar
  136. 137.
    Mathesius, U 2001Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase.J Exp Bot52419426PubMedGoogle Scholar
  137. 138.
    Mathesius, U, Bayliss, C, Weinman, JJ, Schlaman, HRM, Spaink, HP, Rolfe, BG, McCully, ME, Djordjevic, MA 1998bFlavonoids synthesised in cortical cells during nodule initiation are early developmental markers in white clover.Mol Plant-Microbe Interac1112231232Google Scholar
  138. 139.
    Mathesius, U, Charon, C, Rolfe, BG, Kondorosi, A, Crespi, M 2000Temporal 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 Interact13617628PubMedGoogle Scholar
  139. 140.
    Mathesius, U, Keijzers, G, Natera, SHA, Weinman, JJ, Djordjevic, MA, Rolfe, BG 2001Establishment of a root proteome reference map for the model legume Medicago truncatula using the EST database for peptide mass fingerprinting.Proteomics114241440PubMedGoogle Scholar
  140. 141.
    Mathesius, U, Schlaman, HRM, Spaink, HP, Sautter, C, Rolfe, BG, Djordjevic, MA 1998aAuxin transport inhibition precedes nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides.Plant J142334Google Scholar
  141. 142.
    Mathieu, C, Moreau, S, Frendo, P, Puppo, A, Davies, MJ 1998Direct detection of radicals in intact soybean nodules: presence of nitric oxide-leghemoglobin complexes.Free Radic Biol Med2412421249PubMedGoogle Scholar
  142. 143.
    McKhann, HI, Frugier, F, Petrovics, G, Coba de la Peña, T, Jurkevitch, E, Brown, S, Kondorosi, E, Kondorosi, A, Crespi, M 1997Cloning of a WD-repeat-containing gene from alfalfa (Medicago saliva): a role in hormone-mediated cell division?Plant Mol Biol34771780PubMedGoogle Scholar
  143. 144.
    Mellor, RB, Collinge, DB 1995A simple model based on known plant defence reactions is sufficient to explain most aspects of nodulation.J Exp Bot46118Google Scholar
  144. 145.
    Mes, MG 1959Influence of gibberellic acid and photoperiod on the growth, flowering nodulation and nitrogen assimilation of Vicia villosa.Nature18420352036Google Scholar
  145. 146.
    Miklashevichs, E, Rohrig, H, Schell, J, Schmidt, J 2001Perception and signal transduction of rhizobial NOD factors.Crit Rev Plant Sci20373394Google Scholar
  146. 147.
    Minami, E, Kouchi, H, Cohn, JR, Ogawa, T, Stacey, G 1996Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules.Plant J102332PubMedGoogle Scholar
  147. 148.
    Muday, GK, DeLong, A 2001Polar auxin transport: controlling where and how much.Trends Plant Sci6535542PubMedGoogle Scholar
  148. 149.
    Murakami-Mizukami, Y, Yamamoto, Y, Yamaki, S 1991Analysis of indole acetic acid and abscisic acid contents in nodules of soybean plants bearing VA Mycorrhizas.Soil Sci Plant Nutr37291298Google Scholar
  149. 150.
    Murphy, A, Peer, WA, Taiz, L 2000Regulation of auxin transport by aminopeptidases and endogenous flavonoids.Planta211315324PubMedGoogle Scholar
  150. 151.
    Newcomb, W, Syono, K, Torrey, JG 1976Development of an ineffective pea root nodule: morphogenesis, fine structure, and cytokinin biosynthesis.Can J Bot5518911907Google Scholar
  151. 152.
    Nishimura, R, Hayashi, M, Wu, GJ, Kouchi, H, Imaizumi-Anraku, H, Murakami, Y, Kawasaki, S, Akao, S, Ohmori, M, Nagasawa, N, Harada, K, Kawaguchi, M 2002aHAR1 mediates systemic regulation of symbiotic organ development.Nature420426429Google Scholar
  152. 153.
    Nishimura, R, Ohmori, M, Fujita, H, Kawaguchi, M 2002bA lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation.Proc Natl Acad Sci USA991520615210Google Scholar
  153. 154.
    Nishimura, R, Ohmori, M, Kawaguchi, M 2002cThe novel symbiotic phenotype of enhanced-nodulating mutant of Lotus japonicus: astray mutant is an early nodulating mutant with wider nodulation zone.Plant Cell Physiol43853859Google Scholar
  154. 155.
    Nukui, N, Ezura, H, Yuhashi, K-I, Yasuta, T, Minamisawa, K 2000Effects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum.Plant Cell Physiol41893897PubMedGoogle Scholar
  155. 156.
    Nutman, PS 1952Studies on the physiology of nodule formation III. Experiments on the excision of root-tips and nodules.Ann Bot1679101Google Scholar
  156. 157.
    Oke, V, Long, SR 1999Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis.Mol Microbiol32837849PubMedGoogle Scholar
  157. 158.
    Oldroyd, GED, Engstrom, EM, Long, SR 2001Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula.Plant Cell1318351849PubMedGoogle Scholar
  158. 159.
    Penmetsa, RV, Cook, DR 1997A legume ethylene-insensitive mutant hyperinfected by its Rhizobium symbiont.Science275527530PubMedGoogle Scholar
  159. 160.
    Peters, NK, Chris-Estes, DK 1989Nodule formation is stimulated by the ethylene inhibitor, aminoethoxyvinylglycine.Plant Physiol91690693PubMedGoogle Scholar
  160. 161.
    Phillips, DA, Torrey, JG 1970Cytokinin production by Rhizobium japonicum.Physiol Plant2310571063Google Scholar
  161. 162.
    Phillips, DA, Torrey, JG 1972Studies on cytokinin production by Rhizobium.Plant Physiol491115PubMedGoogle Scholar
  162. 163.
    Phillips, DA 1971Abscisic acid inhibition of root nodule initiation in Pisum sativum.Planta100181190Google Scholar
  163. 164.
    Porta, H, Rueda-Benitez, P, Campos, F, Colmenaro-Flores, JM, Colorado, JM, Carmona, MJ, Covarrubias, AA, Rocha-Sosa, M 1999Analysis of lipoxygenase mRNA accumulation in the common bean (Phaseolus vulgaris L.) during development and under stress conditions.Plant Cell Physiol40850858PubMedGoogle Scholar
  164. 165.
    Puppo, A, Halliwell, B 1988Generation of hydroxyl radicals by soybean nodule leghaemoglobin.Planta173405410Google Scholar
  165. 166.
    Rademacher, W 1994Gibberellin formation in microorganisms.Plant Growth Regul15303314Google Scholar
  166. 167.
    Radley, M 1961Gibberellin-like substances in plants.Nature191684685PubMedGoogle Scholar
  167. 168.
    Ramu, SK, Peng, HM, Cook, DR 2002Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula.Mol Plant-Microbe Interac15522528Google Scholar
  168. 169.
    Ramanujam, MP, Abdul Jaleel, V, Kumaravelu, G 1998Effect of salicylic acid on nodulation, nitrogenous compounds and related enzymes of Vigna mungo.Biol Plant41307311Google Scholar
  169. 170.
    Recourt, K, van Tunen, AJ, Mur, LA, van Brussel, AAN, Lugtenberg, BJJ, Kijne, JW 1992Activation of flavonoid biosynthesis in roots of Vicia sativa subsp. nigra plants by inoculation with Rhizobium leguminosarum biovar viciae.Plant Mol Biol19211220Google Scholar
  170. 171.
    Redmond, JR, Batley, M, Djordjevic, MA, Innes, RW, Keumpel, PL, Rolfe, BG 1986Flavones induce expression of nod genes in Rhizobium.Nature323632635Google Scholar
  171. 172.
    Regvar, M, Gogala, N, Zalar, P 1996Effects of jasmonic acid on mycorrhizal Allium sativum.New Phytol134703707Google Scholar
  172. 173.
    Relic, B, Perret, X, Estrada-Garcia, MT, Kopcinska, J, Golinowski, W, Krishnan, H, Pueppke, SG, Broughton, WJ 1994Nod factors of Rhizobium are the key to the legume door.Mol Microbiol13171178PubMedGoogle Scholar
  173. 174.
    Rice-Evans, C 2001Flavonoid antioxidants.Curr Med Chem8797807PubMedGoogle Scholar
  174. 175.
    Ridge, RW, Bender, GL, Rolfe, BG 1992Nodule-like structures induced on roots of wheat seedlings by addition of the synthetic auxin 2,4-dichlorophenoxyacetic acid and the effects of microorganisms.Aust J Plant Physiol19481492Google Scholar
  175. 176.
    Roddam, LF, Lewis-Henderson, WR, Djordjevic, MA 2002Two novel chromosomal loci influence cultivar-specific nodulation failure in the interaction between strain ANU794 and subterranean clover cv.Woogenellup. Funct Plant Biol29473483Google Scholar
  176. 177.
    Rodrigez-Barrueco, C, Bermudez de Castro, F 1973Cytokinin-induced pseudonodules on Alnus glutinosa.Physiol Plant29277280Google Scholar
  177. 178.
    Rodriguez-Barrueco, C, Miguel, C, Palni, LMS 1979Cytokinins in root nodules of the nitrogen-fixing non-legume Myrica gale L.Z Pflanzenphysiol95275278Google Scholar
  178. 179.
    Röhrig, H, Schmidt, J, Miklashevichs, E, Schell, J, John, M 2002Soybean ENOD40 encodes two peptides that bind to sucrose synthase.Proc Natl Acad Sci USA9919151920PubMedGoogle Scholar
  179. 180.
    Rojo, E, Solano, R, Sánchez-Serrano, JJ 2003Interactions between signalling compounds involved in plant defence.J Plant Growth Regul222222Google Scholar
  180. 181.
    Ross, JJ, O’Neil, DP, Smith, JJ, Kerckhoffs, HJ, Elliot, RC 2000Evidence that auxin promotes gibberellin A1 biosynthesis in pea.Plant J21547552PubMedGoogle Scholar
  181. 182.
    Ross, JJ 1998Effects of auxin transport inhibitors on gibberellin in pea.J Plant Growth Regul17141146Google Scholar
  182. 183.
    Ryals, JA, Neuenschwander, UH, Willits, MG, Molina, A, Steiner, H-Y, Hunt, MD 1996Systemic acquired resistance.Plant Cell818091819PubMedGoogle Scholar
  183. 184.
    Salzer, P, Corbiere, H, Boller, T 1999Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradicies.Planta208319325Google Scholar
  184. 185.
    Salzwedel, JL, Dazzo, FB 1993pSym nod gene influence on elicitation of peroxidase activity from white clover and pea roots by rhizobia and their cell-free supernatants.Mol Plant-Microbe Interect6127134Google Scholar
  185. 186.
    Santos, R, Hérouart, D, Puppo, A, Touati, D 2000Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis.Mol Microbiol38750759PubMedGoogle Scholar
  186. 187.
    Santos, R, Hérouart, D, Sigaud, S, Touati, D, Puppo, A 2001Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction.Mol Plant-Microbe Interact148689PubMedGoogle Scholar
  187. 188.
    Sato, T, Fujikaki, H, Ohtake, N, Sueyoshi, K, Takahashi, T, Sato, A, Ohyama, T 2002Effect of exogenous salicylic acid on nodule formation of hypernodulating mutant and wild type of soybean.Soil Sci Plant Nutr48413420Google Scholar
  188. 189.
    Scheres, B, McKhann, HI, Zalensky, A, Lobler, M, Bisseling, T, Hirsch, AM 1992The PsENOD12 gene is expressed at two different sites in Afghanistan pea pseudonodules induced by auxin transport inhibitors.Plant Physiol10016491655PubMedGoogle Scholar
  189. 190.
    Schlaman, HRM, Gisel, AA, Quaedvlieg, NEM, Bloemberg, GV, Lugtenberg, BJJ, Kijne, JW, Potrykus, I, Spaink, HP, Sautter, C 1997Chitin oligosaccharides can induce cortical cell division in roots of Vicia sativa when delivered by ballistic microtargeting.Development12448874895PubMedGoogle Scholar
  190. 191.
    Schmid, J, Röhrig, H, John, M, Wienecke, U, Stacey, G, Koncz, C, Schell, J 1993Alteration of plant growth and development by Rhizobium nodA and nodB genes involved in the synthesis of oligosaccharide signal molecules.Plant J4651658Google Scholar
  191. 192.
    Schmidt, JS, Harper, JE, Hoffman, TK, Bent, AF 1999Regulation of soybean nodulation independent of ethylene signalling.Plant Physiol119951959PubMedGoogle Scholar
  192. 193.
    Schmidt, PE, Broughton, WJ, Werner, D 1994Nod-factors of Bradyrhizobium japonicum and Rhizobium sp. NGR234 induce flavonoid accumulation in soybean root exudate.Mol Plant-Microbe Interact7384390Google Scholar
  193. 194.
    Searle, IR, Men, AE, Laniya, T, Buzas, DM, Iturbe-Ormaetxe, I, Carroll, BJ, Gresshoff, PM 2003Long-distance signalling in nodulation directed by a CLAVATA1-like receptor kinase.Science299109112PubMedGoogle Scholar
  194. 195.
    Sinvany, G, Kapulnik, Y, Wininger, S, Badani, H, Jurkevitch, E 2002The early nodulin enod40 is induced by, and also promotes arbuscular mycorrhizal root colonization.Physiol Mol Plant Pathol60103109Google Scholar
  195. 196.
    Smit, G, de Koster, CC, Schripsema, J, Spaink, HP, van Brussel, AA, Kijne, JW 1995Uridine, a 5 cell division factor in pea roots.Plant Mol Biol29869873PubMedGoogle Scholar
  196. 197.
    Sousa, C, Johansson, C, Charon, C, Manyani, H, Sautter, C, Kondorosi, A, Crespi, M 2001Translational and structural requirements of the early nodulin gene enod40, a short-open reading frame-containing RNA, for elicitation of a cell-specific growth response in the alfalfa root cortex.Mol Cell Biol21354366PubMedGoogle Scholar
  197. 198.
    Spaink, HP, Wijfjes, AHM, Vanvliet, TB, Kijne, JW, Lugtenberg, BJJ 1993Rhizobial lipo-oligosaccharide signals and their role in plant morphogenesis. Are analogous lipophilic chitin derivatives produced by the plant?Aust J Plant Physiol20381392Google Scholar
  198. 199.
    Spaink, HP 1999Flavonoids as regulators of plant development: new insights from studies of plant-rhizobia interactions.Verpoorte, RDownum, KRomeo, J eds. Recent Advances in PhytochemistryInteractions of Plants and Microorganismsvol. 32167178Google Scholar
  199. 200.
    Stacey, G, Shibuya, N 1997Chitin recognition in rice and legumes.Plant Soil194161169Google Scholar
  200. 201.
    Staehelin, C, Charon, C, Boller, T, Crespi, M, Kondorosi, A 2001 Medicago truncatula plants overexpressing the early nodulin gene enod40 exhibit accelerated mycorrhizal colonization and enhanced formation of arbuscules.Proc Natl Acad Sci USA981536615371PubMedGoogle Scholar
  201. 202.
    Staehelin, C, Granado, J, Muller, J, Wiemken, A, Mellor, RB, Felix, G, Regenaas, M, Broughton, WJ, Boller, T 1994Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases.Proc Natl Acad Sci USA9121962200PubMedGoogle Scholar
  202. 203.
    Stafford, HA 1997Roles of flavonoids in symbiotic and defence functions in legume roots.Bot Rev632739Google Scholar
  203. 204.
    Stenlid, G 1976Effects of flavonoids on the polar transport of auxins.Physiol Plant38262266Google Scholar
  204. 205.
    Stephenson, LC, Bunker, TW, Dubbs, WE, Grimes, HD 1998Specific soybean lipoxygenases localize to discrete subcellular compartments and their mRNAs are differentially regulated by source-sink status.Plant Physiol116923933PubMedGoogle Scholar
  205. 206.
    Stougaard, J 2001Genetics and genomics of root symbiosis.Curr Opin Plant Biol4328335PubMedGoogle Scholar
  206. 207.
    Stracke, S, Kistner, C, Yoshida, S, Mulder, L, Sato, S, Kaneko, T, Tabata, S, Sandal, N, Stougaard, J, Szczyglowski, K, Parniske, M 2002A plant receptor-like kinase required for both bacterial and fungal symbiosis.Nature417959962PubMedGoogle Scholar
  207. 208.
    Streeter, JG 1988Inhibition of legume nodule formation and N2 fixation by nitrate.Crit Rev Plant Sci7123Google Scholar
  208. 209.
    Suganuma, N, Yamauchi, H, Yamamoto, K 1995Enhanced production of ethylene by soybean roots after inoculation with Bradyrhizobium japonicum.Plant Sci111163168Google Scholar
  209. 210.
    Suttle, JC 1988Effect of ethylene treatment on polar IAA transport, net IAA uptake and specific binding of N-1-naphthylphthalamic acid in tissues and microsomes isolated from etiolated pea epicotyls.Plant Physiol88795799PubMedGoogle Scholar
  210. 211.
    Syono, K, Newcomb, W, Torrey, JG 1976Cytokinin production in relation to the development of pea root nodules.Can J Bot5421552162Google Scholar
  211. 212.
    Thimann, KV 1936On the physiology of the formation of nodules on legumes roots.Proc Natl Acad Sci USA22511513PubMedGoogle Scholar
  212. 213.
    Thurber, GA, Douglas, JR, Galston, AW 1958Inhibitory effects of gibberellins on nodulation in dwarf beans, Phaseolous vulgaris.Nature18110821083Google Scholar
  213. 214.
    Trinchant, JC, Rigaud, J 1982Nitrite and nitric oxide as inhibitors of nitrogenase from soybean bacteroids.Appl Environ Microbiol4413851388PubMedGoogle Scholar
  214. 215.
    Triplett, EW, Heitholt, JJ, Evensen, KB, Blevins, DG 1981Increase in internode length in Paseolus lunatus L. caused by inoculation with a nitrate reductase-deficient strain of Rhizobium sp.Plant Physiol6714PubMedGoogle Scholar
  215. 216.
    Truchet, G, Barker, DG, Camut, S, de Billy, F, Vasse, J, Huguet, T 1989Alfalfa nodulation in the absence of Rhizobium.Mol Gen Genet2196568Google Scholar
  216. 217.
    Truchet, G, Roche, P, Lerouge, P, Vasse, J, Camut, S, de Billy, F, Promé, J-C, Dénarié, J 1991Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa.Nature351670673Google Scholar
  217. 218.
    Tully, RE, van Berkum, P, Lovins, KW, Keister, DL 1998Identification and sequencing of a cytochrome P450 gene cluster from Bradyrhizobium japonicum.Biochim Biophys Acta1398243255PubMedGoogle Scholar
  218. 219.
    van Brussel, AAN, Tak, T, Boot, KJM, Kijne, JW 2002Autoregulation of root nodule formation: signals of both symbiotic partners studied in a split-root system of Vicia sativa subsp. nigra.Mol Plant-Microbe Interact15341349PubMedGoogle Scholar
  219. 220.
    van der Holst, PPG, Schlaman, HRM, Spaink, HP 2001Proteins involved in the production and perception of oligosaccharides in relation to plant and animal development.Curr Opin Struct Biol11608616PubMedGoogle Scholar
  220. 221.
    van Spronsen, PC, van Brussel, AAN, Kijne, JW 1995Nod-factors produced by Rhizobium leguminosarum biovar. viciae induce ethylene-related changes in root cortical cells of Vicia sativa subsp. nigra.Eur J Cell Biol68463469PubMedGoogle Scholar
  221. 222.
    van Spronsen, PC, Tak, T, Rood, AMM, van Brussel, AAN, Kijne, JW, Boot, KJM 2003Salicylic acid inhibits indeterminant-type nodulation but not determinant-type nodulation.Mol Plant Microbe Interact168391PubMedGoogle Scholar
  222. 223.
    van Workum, WAT, van Brussel, AAN, Tak, T, Wijffelman, CA, Kijne, JW 1995Ethylene prevents nodulation of Vicia sativa ssp. nigra by exopolysaccharide-deficient mutants of Rhizobium leguminosarum bv. viciae.Mol Plant Microbe Interact8278285Google Scholar
  223. 224.
    Vardhini, BV, Rao, SSR 1999Effect of brassinosteroids on nodulation and nitrogenase activity in groundnut (Arachis hypogaea L.).Plant Growth Regul28165167Google Scholar
  224. 225.
    Vasse, J, de Billy, F, Truchet, G 1993Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction.Plant J4555566Google Scholar
  225. 226.
    Wang, KL-C, Li, H, Ecker, JR 2002Ethylene biosynthesis and signalling networks.Plant CellS131S131S151Google Scholar
  226. 227.
    Watts, SH, Wheeler, CT, Hillman, JR, Berrie, AMM, Crozier, A, Math, VB 1983Abscisic acid in the nodulated root system of Alnus glutinosa.New Phytol95203208Google Scholar
  227. 228.
    Wheeler, CT, Henson, IE, McLaughlin, ME 1979Hormones in plants bearing actinomycete root nodules.Bot Gaz140S5257Google Scholar
  228. 229.
    Williams, PM, Sicardi De Mallorca, M 1982Abscisic acid and gibberellin-like substances in roots and root nodules of Glycine max.Plant Soil651926Google Scholar
  229. 230.
    Wisniewski, JP, Gardner, CD, Brewin, NJ 1999Isolation of lipoxygenase cDNA clones from pea nodule mRNA.Plant Mol Biol39775783PubMedGoogle Scholar
  230. 231.
    Wisniewski, JP, Rathbun, EA, Knox, JP, Brewin, NJ 2000Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum.Mol Plant Microbe Interact13413420PubMedGoogle Scholar
  231. 232.
    Wopereis, J, Pajuelo, E, Dazzo, FB, Jiang, Q, Gresshoff, PM, de Bruijn, FJ, Stougaard, J, Szczyglowski, K 2000Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype.Plant J2397114PubMedGoogle Scholar
  232. 233.
    Wu, C, Dickstein, R, Cary, AJ, Norris, JH 1996The auxin transport inhibitor N-(1-naphthyl)phthalamic acid elicits pseudonodules on non-nodulating mutants of white sweetclover.Plant Physiol110501510PubMedGoogle Scholar
  233. 234.
    Yang, WC, de Blank, C, Maskiene, 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 cell cycle is only completed in primordium formation.Plant Cell614151426PubMedGoogle Scholar
  234. 235.
    Yang, WC, Katinakis, P, Hendriks, P, Smolders, A, de Vries, F, Spee, J, van Kammen, A, Bisseling, T, Franssen, H 1993Characterisation of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development.Plant J3573585PubMedGoogle Scholar
  235. 236.
    Yuhashi, K-I, Ichikawa, N, Ezura, H, Akao, S, Minakawa, Y, Nukui, N, Yasuta, T, Minamisawa, K 2000Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum.Appl Environ Microbiol6626582663PubMedGoogle Scholar
  236. 237.
    Zaat, SAJ, van Brussel, AAN, Tak, T, Lugtenberg, BJJ, Kijne, JW 1989The ethylene-inhibitor aminoethoxyvinylglycine restores normal nodulation by Rhizobium leguminosarum biovar. viciae on Vicia saliva subsp. nigra by suppressing the ‘Thick and short roots’ phenotype.Planta177141150Google Scholar
  237. 238.
    Zhang, H, Jennings, A, Barlow, PW, Forde, BG 1999Dual pathways for regulation of root branching by nitrate.Proc Natl Acad Sci USA9665296534PubMedGoogle Scholar
  238. 239.
    Zuanazzi, JAS, Clergeot, PH, Quirion, J-C, Husson, HP, Kondorosi, A, Ratet, P 1998Production of Sinorhizobium meliloti nod gene activation and repressor flavonoids from Medicago sativa roots.Mol Plant Microbe Interact11784794Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.School of Plant ScienceUniversity of Tasmania, Private Bag 55, Hobart, Tasmania 7001Australia
  2. 2.School of Biochemistry and Molecular Biology and ARC Centre of Excellence For Integrative Legume ResearchAustralian National University, Linnaeus Way, Canberra ACT 0200Australia

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