Legume Research

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Legume Research, volume 35 issue 2 (june 2012) : 85-103


Surjit Singh Dudeja*, Sunita Sheokand, Swaraj Kumari
1Department of Microbiology CCS Haryana Agricultural University, Hisar 125 004. India
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Cite article:- Dudeja* Singh Surjit, Sheokand Sunita, Kumari Swaraj (2024). LEGUME ROOT NODULE DEVELOPMENT AND FUNCTIONING UNDER TROPICS AND SUBTROPICS: PERSPECTIVES AND CHALLENGES. Legume Research. 35(2): 85-103. doi: .
The article has been written in view of the importance attached to symbiotic N2-fixation taking place in unique organs called legume root nodules under tropics and subtropics. Nodules on legume roots are formed in interaction with soil bacteria a and b rhizobia. Symbiotic interactions between compatible legume host plant and rhizobia involve a fine tuned, molecular communication between the two partners. Calcium has been reported to play a crucial role in symbiotic signaling. Nod factors are central to the initial establishment of legume - rhizobial symbiosis. Production of these signaling molecules is activated by the release of plant phenolics, mainly flavonoids, in the rhizosphere, where they induce a set of nod genes in the appropriate rhizobial strain, leading to synthesis of Nod factors. The nature of both flavonoid signal from plant and Nod factor from the microbial partner are central to the maintenance of specificity in this symbiosis, ensuring that plant accommodates only the useful bacterium. Generally the invasion of plant root occurs through an invagination of root hair cell, called infection thread, at the primary site of interaction. The infection thread spans through the entire root cortex allowing rhizobial invasion into dividing cells of nodule primordium. Rhizobia are released from infection thread into membrane enclosed compartments, where they convert from free living form to N2-fixing form named the bacteroids. Development of functional nodules requires differentiation of both plant and microbial cells. Transcriptomics and proteomics reveal truly great extent of plant and microbial differentiation. Symbiotic N2-fixation is a finely regulated process that involves carbon and energy metabolism of the host plant significantly. The process is also under regulation by N-feedback and O2 supply within the nodules. Redox balance and antioxidant defense system play important roles in establishment of legume-rhizobial symbiosis as well as nodule functioning. Longevity and N2-fixing efficiency of nodules are hugely dependent on environmental conditions prevailing in tropical and subtropical conditions.
  1. Amor, B.B., Shaw, S.L., Oldroyd, G. E., Maillet, F., Penmetsa, R.V., Cook, D., Long, S.R., Denarie, J. and 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. 34:495-506.
  2. Becker, A., Berges, H., Krol, E., Bruand, C., Ruberg, S., Capela, D., Lauber, E., Meilhoc, E., Ampe, F. and de Bruijn, F.J. (2004). Global changes in gene expression in Sinorhizobium meliloti 1021 under microxic and symbiotic conditions. Molecular Plant Microbe Interactions. 17:292-303.
  3. Brewin, N.J. and Dahiya, P. (1997). Carbon-nitrogen metabolism in symbiotic systems: Integration and overall metabolism. In "Biological Nitrogen for Ecology and Sustainable Agriculture" (Legocki, A., Bothe, H., Pühler, A. eds.) Springer-Verlag Berlin Heidelberg, pp. 201-204.
  4. Capoen, W., Den Herder, J., Sun, J., Verplancke, C., De Keyser, A., De Rycke, R., Goormachtig, S., Oldroyd, G., and Holsters, M. (2009). Calcium spiking patterns and the role of the calcium/calmodulin-dependent Kinase CCaMK in lateral root base nodulation of Sesbania rostrata. Plant Cell. 2009 May 26. [Epub ahead of print].
  5. Cardenas, L., Holdawa-Clarke, T.L., Sanchez, F., Quinto, C., Feijo, J.A., Kunkel, J.G. and Hepler, P.K. (2000). Ion changes in legume root hairs responding to Nod-factors. Plant Physiol. 123:443-451.
  6. Catalano, C.M., Lane, W.S. and Sherrier, D.J. (2004). Biochemical characterization of symbiosome membrane proteins from Medicago trunctula root nodules. Electrophoresis 25:519-531.
  7. Chang, C., Damiani, I., Puppo, A. and Frendo, P. (2008). Redox changes during legume- Rhizobium symbiosis.
  8. Molecular Plant. (pubished by Molecular Plant Shinghai Editorial Office in association with Oxford University Press) pp. 1-8.
  9. Christians, M.J., Gingerich, D.J., Hansen, M., Binder, B.M., Kieber, J.J., and Vierstra, R.D. (2009). The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J. 57:332-345.
  10. Colebatch, G., Desbrosses, G., Ott, T., Krussell, L., Montanari, O., Kloska, S., Kopka, J. and Udvardi, M.K. (2004). Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39:443-451.
  11. Colebatch, G., Kloska, S., Trevaskis, B., Freund, S., Altmann, T. and Udvardi, M.K. (2002). Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mole.Plant Microbe Interac. 15:411-420.
  12. Cooper, J.E. (2007). Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue J. Appl. Microbiol. 103(5):1355-1365.
  13. Desbrosses, G.J. and Stougaard, J. (2011). Root nodulation: A paradigm for how plant-microbe symbiosis influences host development pathways. Cell Host Microbe 10:348-358.
  14. Dewitte, W. and Murray, J.A.H. (2003). The plant cell cycle. Ann. Rev. Plant Biol. 54:235-264.
  15. Djordjevic, M.A. (2004). Sinorhizobium meliloti metabolism in the root nodule: a proteomic perspective. Proteomics 44:1859-1872.
  16. Djordjevic, M.A., Chen, H.C., Natera, S., Van, Noorden, G., Menzel, C., Taylor, S., Renard, C., Geiger, O. and Weiller, G.F. (2003). A global analysis of protein expression profiles in Sinorhizobium meliloti discovery of new genes for nodule occupancy and stress adaptation. Mol. Plant Microbe Interac. 16:564-524.
  17. Dudeja S.S and Narula, N. (2008). Molecular diversity of root nodule forming bacteria (Review) In: Agriculturally important microorganisms Vol II (Eds George G. Khachatourians; Dilip K. Arora ; T. P. Rajendran and Alok K. Srivastava) Academic World International. II. pp1-24.
  18. El Yahyaoui, F., Kuster, H. Ben Amor, B. Hohnjec, N., Puhler, A., Becker, A., Gouzy J., Vernie, T., Gough, C., Nibel, A. (2004). Expression profiling Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of symbiotic program. Plant Physiol. 136:3159-3176.
  19. Fischinger, S.A., Drevon J.J., Claassan, N. and Schulze J. (2006). Nitrogen from senescing lower leaves of common bean is retranslocated to nodules and might be involved in an N-feedback regulation of nitrogen fixation. J. Plant Physiol. 163:987-995.
  20. Flemetakis, E., Efrose, R.C., Ott. T., Stedel, C., Aivalakis, G., Udvardi, M.K. and Katanikas, P. (2006). Spatial and temporal organization of sucrose metabolism in Lotus japonicus in nitrogen fixing nodules suggests a role for elusive alkaline/neutral invertase. Plant Mol. Biol. 62:53-69.
  21. Foucher, F. and Kondorosi, E. (2000). Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol. Biol. 43:773-786.
  22. Fujishige, N.A., Lum, M.R., De Hoff, P. L., Whitelegge, J.P., Faull, K.F. and Hirsch, A.M. (2008). Rhizobium common nod genes are required for biofilm formation. Mol. Microbiol. 67(3):504-515.
  23. García, N.A. Tejera, Iribrane, C., Lopez, M., Herrera-Cervera, J.A., and Lluch, C. (2005). Physiological implications of trehelase from Phaseolus vulgaris root nodules: partial purification and characterization. Plant Physiol.Biochem. 43:355-361.
  24. Gherbi, H., Markmann, K., Svistoonoff, S., Estevan, J., Autran, D., Giczey, G., Auguy, F., Pe´ ret, B., Laplaze, L., Franche, C., (2008). SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria. Proc. Natl. Acad. Sci. USA 105:4928-4932.
  25. Gleason, C., Chaudhuri, S., Yang, T., Munoz, A., Poovaiah, B.W. and Oldroyd, G. E. (2006). Nodulation independent of rhizobia induced by a calcium-activated kinase lacking auto inhibition. Nature 441:1149-1152.
  26. Gogorcena, Y., Gordon, A.J., Escurodo, P. R., Minchin, F.R., Witty, J.F., Moran and Becana, M. (1997). N2 fixation and C metabolism and oxidative damage of dark stressed common bean plants. Plant Physiol. 113:1193-1201.
  27. Gogorcena, Y., Iturbe-Ormaetxe, I., Escuredo, P. R. and Becana, M. (1995). Antioxidant defences against activated oxygen in pea subjected to water stress. Plant Physiol. 108:753-759.
  28. Gordon, A.J., Skøt, L. and James, C.L. (2002). Short-term metabolite response of soybean nodules to nitrate. J. Exp. Bot. 53:423-428.
  29. Gresshoff, P. and Catalno-Annoles, G. (1992). Systemic regulators of nodulation in legumes. In Current topics in Plant Molecular Biology: Plant Biotechnology and Development. (Gresshoff, P.M. ed.) CRC Press, Boca Raton Fl, pp. 87-89.
  30. Gresshoff, P. M., Lohar, D., Chan, P.K., Biswas, B., Jiang, Q., Reid, D., Ferguson, B., and Stacey, G. (2009). Genetic analysis of ethylene regulation of legume nodulation. Plant Signal. Behav. 4:818-823.
  31. Heckmann, A.B., Lombardo, F., Miwa, H., Perry, J.A., Bunnewell, S., Parniske, M., Wang, T.L., and Downie, J.A. (2006). Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol. 142:1739-1750.
  32. Heckmann, A.B., Sandal, N., Bek, A.S., Madsen, L.H., Jurkiewicz, A., Nielsen, M.W., Tirichine, L., and Stougaard, J. (2011). Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol. Plant Microbe Interact., in press. Published online July 19, 2011.
  33. Héouart, D., Baudouin, E., Frendo, P., Harrisson, J., Santos, R., Jamet, A. Van de Sype G., Touati and Puppo, A. (2002). Reactive oxygen species, nitric oxide and glutathione: a key role in establishment of the legume: Rhizobium symbiosis. Plant Physiol. Biochem. 40:619-614.
  34. Herald, S. and Puppo, A. (2005). Oxyleghemoglobin scavengers nitrogen monoxide and gluta thione: a possible in functioning nodules. J. Biol. Inorg. Chem. 10:935-945.
  35. Hernández-Jimenez, M.J., Lucas, M.M. and Rosario de Felipe, M. (2002). Antioxidant defence and damage in senescing lupin nodules. Plant Physiol.Biochem. 40:645-657.
  36. Høgslund, N., Radutoiu, S., Krusell, L., Voroshilova, V., Hannah, M.A., Goffard, N., Sanchez, D.H., Lippold, F., Ott, T., Sato, S., (2009). Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS ONE 4, e6556.
  37. Horst, I., Welham, T., Kelly, S., Kaneko, T., Sato, S., Tabata, S., Parniske, M. and Wang, T.L. (2007). TILLING mutants of Lotus japonicus. Plant Physiol. 144:806-820.
  38. King, C.A., and Purcell, L.C. (2005). Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol. 137:1389-1396.
  39. Kondorosi, E., Redondo-Nieto and Kondorosi, A. (2005). Ubiquitin-mediated proteolysis. To be in the right place at right moment during nodule development. Plant Physiol. 137:1197-1204.
  40. Kouchi, H., Shimomura, K., Hata, S., Hirota, A., Wu, G.J., Kumagai, H., Tajima, S., Suganuma, N., Suzuki, A., Aoki, T., (2004). Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume Lotus japonicus. DNA Res. 11:263-274.
  41. Kuster, H., Hohnjevc, N., Krazinski, F., El Yahyaoui, F., Manthey, K., Gouzy, J., Dondrup, M., Meyer, F., Kainowski, J., Brechenmacher, L., (2004). Construction and validation of cDNA based Mt6k-RIT macro and microarray to explore root endosymbioses in the model legume Medicago truncatula. J. Biotechnol. 108:95-113.
  42. Lee, H., Hur, C.J., Kim, H.B., Park, S.Y. and An, C.S. (2004). An analysis of the root nodule-enhanced transcriptome in soybean. Molecules Cells 18:53-62.
  43. Limpens, E., Franken, C., Smit, P., Willmesse, J., Bissling, T. and Guerts, R. (2003). LysM domain receptor kinase regulating Nod Factor- induced infection. Science 303:630-633.
  44. Lohar, D., Stiller, J., Kam, J., Stacey, G., and Gresshoff, P. M. (2009). Ethylene insensitivity conferred by a mutated Arabidopsis ethylene receptor gene alters nodulation in transgenic Lotus japonicus. Ann. Bot. (Lond.) 104:277-285.
  45. Lohar, D.P. and Vanden Bossch, K.A. (2005). Grafting between model legumes demonstrates roles for roots and shoots in determining nodule type and host/ rhizobia specificity. J. Expl. Bot. 56:1643-1650.
  46. Lohar, D.P., Schaff, J.E., Laskey, J.G., Keiber, J.J., Bilyeu, K.D. and Bird, D.M.. (2004). Cytokinins play opposite roles in lateral root formation and nematode and rhizobial symbioses. Plant J. 38:203-214.
  47. Madsen E.B., Madsen, L.H., Radutoui., S., Olbryt, M., Rakwalska, M.,Szczyglowski, K., Sato, S., Kaneko, T., Tabata, S. and Sandal, N. (2003). A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637-640.
  48. Madsen, E.B., Antol1´n-Llovera, M., Grossmann, C., Ye, J., Vieweg, S., Broghammer, A., Krusell, L., Radutoiu, S., Jensen, O.N., Stougaard, J., and Parniske, M. (2011). Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signaling in cooperation with Nod factor receptor 5. Plant J. 65:404-417.
  49. Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A.B., Bek, A.S., Ronson, C.W., James, E.K., and Stougaard, J. (2010). The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1:10.
  50. Maekawa-Yoshikawa, M., Muller, J., Takeda, N., Maekawa, T., Sato, S., Tabata, S., Perry, J., Wang, T. L., Groth, M., Brachmann, A., and Parniske, M. (2009). The temperature-sensitive brush mutant of the legume Lotus japonicus reveals a link between root development and nodule infection by rhizobia. Plant Physiol. 149:1785-1796.
  51. Magori, S., Oka-Kira, E., Shibata, S., Umehara, Y., Kouchi, H., Hase, Y., Tanaka, A., Sato, S., Tabata, S., and Kawaguchi, M. (2009). Too much love, a root regulator associated with the long-distance control of nodulation in Lotus japonicus. Mol. Plant Microbe Interact. 22:259-268.
  52. Marino, D., Frendo, P., Ladrera, R., Zabaza, A., Puppo, A., Arrse-Igor, C., and González E. (2007). Nitrogen fixation control under drought stress. Localized or systemic. Plant Physiol. 143:1968-1979.
  53. Markmann, K., and Parniske, M. (2009). Evolution of root endosymbiosis with bacteria: How novel are nodules? Trends Plant Sci. 14:77-86.
  54. Matamoros, M.A., Baird, L.M., Escuredo P. R., Dalton, D.A., Minchin, F.R., Iturbe-Ormaetxe, I. Rubio M.C., Moran, J.F., Gordon, A.J. and Becana, M. (1999). Stress induced legume nodule senescence. Physiological, biochemical and structural alterations. Plant Physiol. 121:97-111.
  55. Matamoros, M.A., Dalton, D.A., Ramos, J., Clemente, M.R., Rubio, M.C. and Becana M. (2003). Biochemistry and molecular biology of antioxidants in Rhizobia-legume symbiosis. Plant Physiol. 133:499-509.
  56. Matzke, M., Weiger, T.M., Papp, I. and Matzke, A.J. (2009) Nuclear membrane ion channels mediate root nodule development. Trends Plant Sci.. May 15. [Epub ahead of print].
  57. Miller, S.H., Elliot, R.M., Sullivan, J.T. and Ronson, C.W. (2007). Host-specific regulation of symbiotic nitrogen fixation in Rhizobium leguminosarum biovar trifolii Microbiol. 153:3184-3195.
  58. Moran, J.F., James, E.K., Rubio, M.C., Sarath, G., Klucas, R.V. and Becana, M. (2003). Functional characterization and expression of a cytosolic iron-superoxide dismutase. Plant Physiol. 133:773-782.
  59. Nakagawa, T. and Kawaguchi M. (2005). Shoot applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol. 47:176-180.
  60. Nakagawa, T., Kaku, H., Shimoda, Y., Sugiyama, A., Shimamura, M., Takanashi, K., Yazaki, K., Aoki, T., Shibuya, N., and Kouchi, H. (2011). From defense to symbiosis: limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume-Rhizobium symbiosis. Plant J. 65:169-180.
  61. Naya , L., Ladera, R., Ramos, J., González, E.M., Arrese-Igor, C., Minchin, F. R. and Becana, M. (2007). The response of carbon metabolism and antioxidant defenses of alfalfa nodules to drought stress and to subsequent recovery of plants. Plant Physiol. 144:1104-1114.
  62. Oka-Kira, E. and Kawaguchi, M. (2006). Long distance signaling to control nodule number. Curr. Opin.Plant Biol. 9:496 -502.
  63. Oldroyd, C.E.D., Harrison, M.J. and Udvardi, M. (2005). Peace talks and trade deals. Keys to long term harmony in legume- microbe symbiosis. Plant Physiol. 137:1205-1210.
  64. Oldroyd, G.E. and Downie, J.A. (2004). Calcium kinases and nodulation signaling in legumes. Nat. Rev. Mole. Cell Biol. 5:566-576.
  65. Oldroyd, G.E., and Downie, J.A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Ann. Rev. Plant Biol. 59:519-546.
  66. Oldroyd, G.E., Harrison, M.J. and Paszkowski, U. (2009). Reprogramming plant cells for endosymbiosis Science. 324(5928):753-754.
  67. Overvoorde, P., Fukaki, H., and Beeckman, T. (2010). Auxin control of root development. Cold Spring Harb Perspect Biol 2:a001537.
  68. Pacios-Bras, C., Schlaman, H.R.M., Boot, K., Admiraal, P., Langerak, J.M., Stougard, J., and Spaink, H.P. (2003). Auxin distribution in Lotus japonicus during root nodule development. Plant Mole. Biol. 52:1169-1180.
  69. Pauly, N., Pucciariello, C., Mandon, K., Innocente, G., Jamet, A., Harrisson, J., Santos, R., Baudouin, E., Héouart, D., Frendo, P. and Puppo A. (2006). Reactive oxygen and nitrogen species and glutathione: key players in legume -Rhizobium symbiosis. J. Expl. Bot. 57:1769-1776.
  70. Perret, X., Stahelin, C. and Broughton, W.J. (2000). Molecular basis of symbiotic promiscuity. Microbiol. Mole. Biol. Rev. 64:180-201.
  71. Perrine-Walker, F., Gherbi, H., Imanishi, L., Hocher, V., Ghodhbane-Gtari, F., Lavenus, J., Benabdoun, F. M., Nambiar-Veeti, M., Svistoonoff, S., and Laplaze, L. (2011). Symbiotic signaling in actinorhizal symbioses. Curr. Protein Pept. Sci. 12:156-164.
  72. Plet, J., Wasson, A., Ariel, F., Le Signor, C., Baker, D., Mathesius, U., Crespi, M., and Frugier, F. (2011). MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J. 65:622-633.
  73. Prasad, M.E., Schofield, A., Lyzenga, W., Liu, H., and Stone, S.L. (2010). Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis. Plant Physiol. 153:1587-1596.
  74. Puppo, A., Gorten, K., Bastian, F., Carzaniga, F., Soussi, M., Lucas, M.M., de Felipe, M.R. Harrison, J., Vanacker, H. and Foyer, C.H. (2005). Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol. 165:683-701.
  75. Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Gronlund, M., Sato, S., Naamura,Y., Tabata, S. and Sandal (2003). Plant recognition of symbiotic bacteria requires two LysM receptor like kinases. Nature 425:585-592.
  76. Roudier, F., Federova, E., Lebris, M., Lecomte, P., Gyorgyey, J., Vaubert, D., Horvath, G., Abad, P., Kondorosi, A., and Kondorosi, E. (2003). The Medicago species A2-cyclin is auxin regulated and is involved in meristem formation but dispensable for endoreduplication- associated developmental programs. Plant Physiol. 131:1091-1103.
  77. Schauser, L., Roussis, A., Stiller, A. and Stougaard, J. (1999). A plant regulator controlling development of symbiotic root nodules. Nature 402:191-195.
  78. Schulze, J. (2003). Source sink relationship suggest an N-feedback mechanism for the drop in N2 fixation during pod filling in pea and broad bean. J. Plant Physiol. 160:531-537.
  79. Schulze, J. (2004). How are rates of nitrogen fixation regulated in legumes. Plant Nutr. Soil Sci. 167:125-137.
  80. Searle, I.R., Men, A.E., Laniya, T.S., Buzas, D.M., Iturbe-Ormaetxa., I.,Caroll, B.J. and Gresshoff, P. M. (2003). Long distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109-112.
  81. Sheng, C.X. and Harper, J.E. (1997). Shoot versus root signal involvement in nodulation and vegetative growth in wild type and hyper nodulating soybean genotypes. Plant Physiol. 113:825-831.
  82. Sheokand, S., Dhandi, S. and Swaraj, K. (1995). Studies on nodule functioning and hydrogen peroxide scavenging enzymes under salt stress. Plant Physiol. Biochem. 33:561-566.
  83. Shimoda, Y., Nagata, M., Suzuki, A., Abe, M., Sato, S., Kato, T., Tabata, S., Higashi, S. and Uchiumi, T. (2005). Symbiotic Rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol. 46:99-107.
  84. Soltis, D.E., Soltis, P.S., Morgan, D.R., Swensen, S.M., Mullin, B.C., Dowd, J.M., and Martin, P. G. (1995). Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl. Acad. Sci. USA 92:2647-2651.
  85. Sprent, J.I. (2007). Evolving ideas of legume evolution and diversity: a taxanomic perspective on the occurrence of nodulation. New Phytol. 174:11-25.
  86. Sulieman, S., Fischinger, S. and Schulze J. (2008). N- feedback regulation of N2-fixation in Medicago truncatula under P deficiency. Gen. Applied Plant Physiol. Special Issue 34:33-54.
  87. Suzuki, T., Sato, M., Ashikari, M., Miyoshi, M., Nagata, Y. and Hirano, H. (2004). The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131:5649-5657.
  88. Swaraj K., Laura, J. and Bishnoi N.R. (1993). Nitrate induced nodule senescence and activities of enzymes scavenging hydrogen peroxide in clusterbean. J. Plant Physiol. 136:202-203.
  89. Swaraj K., Shishchenko, S.V., Zhiznevskaya G.Ya. and Kozlove, G.I. (1984). Effect of water stress on symbiotic nitrogen fixation in soybean. Physiologia Rastinii 31:833-840.
  90. Swaraj, K., and Garg, O.P. (1970). The effect of ascorbic acid when applied to the rooting medium on nodulation and nitrogen fixation in gram (Cicer arietinum L.). Physiol Plantarum 23:889-897.
  91. Swaraj, K. and Bishnoi N.R. (1996). Physiological and biochemical basis of legume nodule senescence in legumes-A Review. Plant Physiol. Biochem. 23:105-116.
  92. Swaraj, K. and Garg, O.P. (1977).The effect of ageing on the leghemoglobin of cowpea nodules. Physio. Plantarum 39:185-189.
  93. Swaraj, K. and Garg, O.P. (1978). Interrelationship between ascorbic acid and structural stability in leghemoglobin in root nodules of Vigna sinensis L. and Cicer arietinum L. Proceedings National Symposium on "Nitrogen assimilation and crop productivity." (Sen S.P., Abrol, Y.P. and Sinha, S.K. eds) Associate Publication Company, New Dehli, pp.164-170.
  94. Swaraj, K., Dhandi, S. and Sheokand, S. (1995b). Relationship between defense mechanism against activated oxygen species and nodule functioning in plant and nodule development in Cajanus cajan L. Plant Sci. 112:65-74.
  95. Swaraj, K., Kuhad, M.S. and Garg, O.P. (1986b). Effect of dark treatments on symbiotic nitrogen fixation in Cicer arietinum L. (chickpea). Environ. Expl. Bot. 26:31-38.
  96. Swaraj, K., Nandwal, A.S., Babber, S., Ahlawat, S. and Nainawati, H.S. (1995a). Effect of water stress on functioning and structure of Cicer arietinum L. nodules. Biol. Plantarum 37:613-619.
  97. Swaraj, K., Topunov, A.F., Golubeva, L.I. and Kretovich, W.L. (1986a). Influence of water stress on enzymatic reduction of leghemoglobin in soybean nodules. Fiziologia Rastini 33:87-92.
  98. Swaraj. K., Sheoran, I.S. and Garg, O.P. (1988). Dark induced changes in the functioning of root nodules of Vigna unguiculata. Plant Physiol. Biochem. 26:79-84.
  99. Talukdar, T., Gorecka, K.M., de Carvalho-Niebel, F., Downie, J.A., Cullimore J. and Pikula, S. (2009). Annexins - calcium and membrane-binding proteins in the plant kingdom potential role in nodulation and mycorrhization in Medicago truncatula Acta Biochimica Polonica. May 6. [Epub ahead of print].
  100. Terakado, J., Yoneama, T. and Fujihara, S. (2006). Shoot applied polyamine suppress nodule formation in soybean (Glycine max). J. Plant Physiol. 163:497-505.
  101. Tirichine L., Imaizumi-Anraku H., Yoshida S., Murakami Y., Madsen L. H., Miwa H., Nakagawa T., Sandal N., Albrektsen A.S., Kawaguchi M., Downie A., Sato S., Kouchi H., Parniske M., Kawasaki S. and Stougaard J. (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:1153-1156.
  102. Truchet, G., Roche, P., Vasse, J., Camut, S., de Billy, F., Prome, J.C. and Denarie J. (1991). Sulphated lipooligosaccharide signals from Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351:670-673.
  103. Vadez, V., Sinclair, T.R., Serraj, R. and Purcell, L.C. (2000). Manganese application can alleviate water deficit induced decline of N2-fixation Plant Cell Environ. 23:497-505.
  104. Van Brussel, A.A.N., Tak,T., Boot, K.J.M. and Kijne, J.W. (2002). Autoregulation of root nodule formation: signals of both symbiotic partners studied in a split root system of Vicia sativa subsp. Nigra. Mole. Plant microbe Intreac.15:341-349.
  105. Vernoux, T., Wilson, R.C., Seeley, K.A. (2000). The Root Meristemless/Cadmium Sensitive2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during post-embryonic root development. The Plant Cell, 12:97-110.
  106. Vinardell, J.M., Federova, E., Cebolla, A., Kevei, Z., Horvath, G., Kelemen, Z., Tarayre, S., Roudier, F., Mergaert, P. and Kondorosi, A. (2003). Endo reduplication mediated by the anaphase promoting complex activator ccs52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15:2093-2105.
  107. Wais, R.J., Galera C., Oldroyd G., Catoria R., Penmetsa, R.V., Cook, D., Gough, C., Denarie, J. and Long S.R. (2000). Genetic analysis of calcium spiking responses in nodulation mutants of Medicgo truncatula. Proc. Natl. Acad. Sci. U.S.A. 97:13407-13412.
  108. Wasson, A.P., Ramsay, K., Jones, M.G., Mathesius, U. (2009). Differing requirements for flavonoids during the formation of lateral roots, nodules and root knot nematode galls in Medicago truncatula. New Phytologist. 2009 Apr. 27. [Epub ahead of print].
  109. Wei, H. and Layzell, D.B. (2006). Adenylate coupled ion movement. A mechanism for the control of nodule permeability. Plant Physiol. 141:280-287.
  110. Weinkoop, S. and Saalbach, G. (2003). Proteome analysis. Novel proteins identified at peribacteroid membrane from Lotus japonicus root nodules. Plant Physiol. Vol 1080-1090.
  111. Weir, B.S. (2011). The current taxonomy of rhizobia New Zealand rhizobia website. (http://www.rhizobia.co.nz/taxonomy/rhizobia.html.). Last updated: 14 September, 2011.
  112. Yang,W.C., de Blank C., Meskiene, I., Hirt, H., Bakker, J., van Kammen, A., Franssen, H. and 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 6:1415-1426.

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