Legumes and Nitrogen Fixation: Physiological, Molecular, Evolutionary Perspectives, and Applications

The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops

Volumn , Issue , 2011, Pages 457-489

  Venkateshwaran, Muthusubramanian ^a   Ané, Jean Michel ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Auxins and cytokinins, and auxin transport auxin cytokinin ratio, nodule formation; Biological nitrogen fixation, and nitrogenase biology BNF, reduction of inert atmospheric nitrogen into ammonia; Genetic and genomic approaches, deciphering symbiotic signaling mechanisms; Jasmonic acid (JA), or methyl jasmonate negative regulator of nodulation, affecting signaling; Lectin ecto apyrases (LNPs), proteins binding to Nod factors, high affinity; Legumes and nitrogen fixation evolutionary perspectives and applications; Nodule organogenesis, and Nod factors rhizobial infection and invasion; Nonsustainable practices, and soil quality deterioration and nitrogen fertilizers; Rhizobia bioinoculants and Nod factor application; Soil fertility, major limiting factor for crop production, in countries

Indexed keywords

EID: 84881175686     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470960707.ch20     Document Type: Chapter

References (237)

1. Abendroth , L.J. & Elmore , R.W. ( 2006 ) Soybean Inoculation: Applying the facts to Your Fields , G1622 ed. University of Nebraska - Lincoln Ext. , Lincoln .
2. Allen , E.K. & Allen , O.N. ( 1961 ) The scope of Nodulation in the Leguminosae . In: Recent Advances in Botany . Vol I, Proceedings of the Ninth International Botanical Congress, pp. 585 - 588 , University of Toronto Press , Toronto .
3. Al - Mallah , M.K. , Davey , M.R. , & Cocking , E.C. ( 1989 ) Formation of nodular structures on rice seedlings by rhizobia . Journal of Experimental Botany 40 , 473 - 478 .
4. Al - Mallah , M.K. , Davey , M.R. , & Cocking , E.C. ( 1990 ) Nodulation of oilseed rape ( Brassica napus ) by rhizobia . Journal of Experimental Botany 41 , 1567 - 1572 .
5. Amadou, C. , Pascal, G. , Mangenot, S. , et al. ( 2008) Genome sequence of the beta - rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia . Genome Research 18 ( 9), 1472 - 1483.
6. Amor , B.B. , Shaw , S.L. , Oldroyd , G.E.D. , et al. ( 2003 ) The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium fl ux and root hair deformation . The Plant Journal 34 ( 4 ), 495 - 506 .
7. Andriankaja , A. , Boisson - Dernier , A. , Frances , L. , et al. ( 2007 ) AP2 - ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis - regulatory motif . Plant Cell 19 ( 9 ), 2866 - 2885 .
8. Ané, J.M. , Kiss , G.B. , Riely , B.K. , et al. ( 2004 ) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes . Science 303 ( 5662 ), 1364 - 1367 .
9. Appleby , C.A. , Tjepkema , J.D. , & Trinick , M.J. ( 1983 ) Haemoglobin in a Non - leguminous plant, Parasponia: possible genetic origin and function in nitrogen fi xation . Science (New York, N.Y.) 220 ( 4600 ), 951 - 953 .
10. Ardourel , M. , Demont , N. , Debelle , F. , et al. ( 1994 ) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses . The Plant Cell 6 ( 10 ), 1357 - 1374 .
11. Arrighi , J.F. , Barre , A. , Ben Amor , B. , et al. ( 2006 ) The Medicago truncatula lysin [corrected] motif - receptor - like kinase gene family includes NFP and new nodule - expressed genes . Plant Physiology 142 ( 1 ), 265 - 279 .
12. Arrighi , J.F. , Godfroy , O. , de Billy , F. , Saurat , O. , Jauneau , A. , & Gough , C. ( 2008 ) The RPG gene of Medicago truncatula controls Rhizobium - directed polar growth during infection . Proceedings of The National Academy of Sciences of The United States of America 105 ( 28 ), 9817 - 9822 .
13. Banba , M. , Gutjahr , C. , Miyao , A. , et al. ( 2008 ) Divergence of evolutionary ways among common sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signalling pathway . Plant and Cell Physiology 49 ( 11 ), 1659 - 1671 .
14. Barcellos , F.G. , Menna , P. , Batista , J.S. , & Hungria , M. ( 2007 ) Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer ) fredii and Bradyrhizobium elkanii in a Brazilian Savannah soil . Applied and Environmental Microbiology 73 ( 8 ), 2635 - 2643 .
15. Barney , B.M. , Yurth , M.G. , Dos Santos , P.C. , Dean , D.R. , & Seefeldt , L.C. ( 2009 ) A substrate channel in the nitrogenase MoFe protein . Journal of Biological Inorganic Chemistry: JBIC: A Publication of the Society of Biological Inorganic Chemistry 14 ( 7 ), 1015 - 1022 .
16. Barron , E.J. , Pasini , R.J. , Davis , D.W. , Stuthman , D.D. , & Graham , P.H. ( 1999 ) Response to selection for seed yield and nitrogen (N 2 ) fi xation in common bean . Field Crops Research 62 ( 119 ), 128 .
17. Bliss , F.A. & Hardarson , G. ( 1993 ) Enhancement of biological nitrogen fi xation of common bean in Latin America . Plant Soil 152 , 1 - 160 .
18. Boot , K.J.M. , van Brussel , A.A.N. , Tak , T. , Spaink , H.P. , & Kijne , J.W. ( 1999 ) Lipochitinoligosaccharides from Rhizobium leguminosarum bv. vicia e reduce auxin transport capacity in Vicia sativa subsp. nigra roots . Molecular Plant - Microbe Interactions 12 , 839 - 844 .
19. Bright , L.J. , Liang , Y. , Mitchell , D. , & Harris , J. ( 2005 ) The LATD gene of Medicago truncatula is required for both nodule and root development . Molecular Plant - Microbe Interactions 18 , 521 - 532 .
20. Brom , S. , Girard , L. , Tun - Garrido , C. , et al. ( 2004 ) Transfer of the symbiotic plasmid of Rhizobium etli CFN42 requires cointegration with p42a, which may be mediated by site - specifi c recombination . Journal of Bacteriology 186 ( 22 ), 7538 - 7548 .
21. Bryan , J.A. , Berlyn , G.P. , & Gordon , J.C. ( 1996 ) Towards a new concept of the evolution of symbiotic nitrogen fi xation in the Leguminosae . Plant and Soil 186 , 151 - 159 .
22. Burgess , B.K. & Lowe , D.J. ( 1996 ) Mechanism of molybdenum nitrogenase . Chemical Reviews 96 ( 7 ), 2983 - 3012 .
23. Capoen , W. , Goormachtig , S. , De Rycke , R. , Schroeyers , K. , & Holsters , M. ( 2005 ) SrSymRK, a plant receptor essential for symbiosome formation . Proceedings of the National Academy of Sciences of the United States of America 102 ( 29 ), 10369 - 10374 .
24. Capoen , W. , Oldroyd , G.E. , Goormachtig , S. , & Holsters , M. ( 2009 ) Sesbania rostrata: a case study of natural variation in legume nodulation . The New Phytologist 186 , 340 - 345 .
25. Catoira , R. , Timmers , A.C.J. , Maillet , F. , et al. ( 2001 ) The HCL gene of Medicago truncatula controls Rhizobium - induced root hair curling . Development 128 ( 9 ), 1507 - 1518 .
26. Cebolla , A. , Vinardell , J.M. , Kiss , E. , et al. ( 1999 ) The mitotic inhibitor ccs52 is required for endoreduplication and ploidy - dependent cell enlargement in plants . The EMBO Journal 18 , 4476 - 4484 .
27. Cevallos , M.A. , Encarnacion , S. , Leija , A. , Mora , Y. , & Mora , J. ( 1996 ) Genetic and physiological characterization of a Rhizobium etli mutant strain unable to synthesize poly - beta - hydroxybutyrate . Journal of Bacteriology 178 ( 6 ), 1646 - 1654 .
28. Chaintreuil , C. , Boivin , C. , Dreyfus , B. , & Giraud , E. ( 2001 ) Characterization of the common nodulation genes of the photosynthetic Bradyrhizobium sp. ORS285 reveals the presence of a new insertion sequence upstream of nodA . FEMS Microbiology Letters 194 ( 1 ), 83 - 86 .
29. Chan , M.K. , Kim , J. , & Rees , D.C. ( 1993 ) The nitrogenase FeMo - cofactor and P - cluster pair: 2.2 A resolution structures . Science (New York, N.Y.) 260 ( 5109 ), 792 - 794 .
30. Charon , C. , Sousa , C. , Crespi , M. , & Kondorosi , A. ( 1999 ) Alteration of enod40 expression modifi es Medicago truncatula root nodule development induced by Sinorhizobium meliloti . The Plant Cell 11 , 1953 - 1965 .
31. Charpentier , M. , Bredemeier , R. , Wanner , G. , Takeda , N. , Schleiff , E. , & Parniske , M. ( 2008 ) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis . The Plant Cell 20 ( 12 ), 3467 - 3479 .
32. Chen , W.M. , Moulin , L. , Bontemps , C. , Vandamme , P. , Béna , G. , & Boivin - Masson , C. ( 2003 ) Legume symbiotic nitrogen fi xation by beta - proteobacteria is widespread in nature . Journal of Bacteriology 185 ( 24 ), 7266 - 7272 .
33. Chen , C. , Ané, J.M. , & Zhu , H. ( 2008 ) OsIPD3, an orthologue of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice . The New Phytologist 180 , 311 - 315 .
34. Chen , C. , Fan , C. , Gao , M. , & Zhu , H. ( 2009 ) Antiquity and function of CASTOR and POLLUX , the twin ion channel - encoding genes key to the evolution of root symbioses in plants . Plant Physiology 149 , 306 - 317.
35. Chi , F. , Shen , S.H. , Cheng , H.P. , Jing , Y.X. , Yanni , Y.G. , & Dazzo , F.B. ( 2005 ) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefi ts to rice growth physiology . Applied and Environmental Microbiology 71 ( 11 ), 7271 - 7278 .
36. Cho , M.J. & Harper , J.E. ( 1993 ) Effect of abscisic acid application on root isofl avonoid concentration and nodulation of wild - type and nodulation mutant soybean plants . Plant Soil 153 , 145 - 149 .
37. Cocking , E.C. ( 2003 ) Endophytic colonization of plant roots by nitrogen - fi xing bacteria . Plant and Soil 252 ( 169 ), 175 .
38. Cohn , J.R. , Uhm , T. , Ramu , S. , et al. ( 2001 ) Differential regulation of a family of apyrase genes from Medicago truncatula . Plant Physiology 125 ( 4 ), 2104 - 2119 .
39. Combier , J.P. , Frugier , F. , de Billy , F. , et al. ( 2006 ) MtHAP2 - 1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula . Genes and Development 20 ( 22 ), 3084 - 3088 .
40. Cooper , J.B. & Long , S.R. ( 1994 ) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans - zeatin secretion . Plant Cell 6 , 215 - 225 .
41. Crespi , M. , Jurkevitch , E. , Poiret , M. , et al. ( 1994 ) Enod40 , a gene expressed during nodule organogenesis, codes for a non - translatable RNA involved in plant growth . The EMBO Journal 13 , 5099 - 5112.
42. Dart , P. ( 1988 ) Nitrogen fi xation in tropical forestry and the use of Rhizobium . In: Tropical Forest Ecology and Management in the Asia - Pacifi c Region (eds. P. Kapoor - Vijay , S. Appanah & S.M. Saulei ), Proceedings of Regional Workshop held at Lae, Papua New Guinea, Commonwealth Science Council. U.K., pp. 142 - 154 .
43. Day , R.B. , McAlvin , C.B. , Loh , J.T. , et al. ( 2000 ) Differential expression of two soybean apyrases, one of which is an early nodulin . Molecular Plant - Microbe Interactions 13 , 1053 - 1070 .
44. De Bruin , J.L. , Pedersen , P. , Conley , S.P. , et al. ( 2010 ) Probability of yield response to inoculants in fi elds with a history of soybean . Crop Science 50 , 265 - 272 .
45. Degenhart , N.R. , Barnes , D.K. , & Vance , C. ( 1992 ) Divergent selection for nodule aspartate aminotransferase and asparagine synthetase activities in alfalfa. Crop Science 32 , 313 - 317 .
46. Den Herder , G. & Parniske , M. ( 2009 ) The unbearable naivety of legumes in symbiosis . Current Opinion in Plant Biology 12 ( 4 ), 491 - 499 .
47. Dénarié, J. , Debellé, F. , & Promé, J.C. ( 1996 ) Rhizobium lipo - chitooligosaccharide nodulation factors: signalling molecules mediating recognition and morphogenesis . Annual Review of Biochemistry 65 , 503 - 535 .
48. D'Haeze , W. & Holsters , M. ( 2002 ) Nod factor structures, responses, and perception during initiation of nodule development . Glycobiology 12 ( 6 ), 79 . D'Haeze , W. & Holsters , M. ( 2004 ) Surface polysaccharides enable bacteria to evade plant immunity . Trends in in Microbiology 12 ( 12 ), 555 - 561 .
49. D'Haeze , W. & Holsters , M. ( 2004 ) Surface polysaccharides enable bacteria to evade plant immunity . Trends in in Microbiology 12 ( 12 ), 555 - 561
50. Ding , Y. , Kaló, P. , Yendrek , C. , et al. ( 2008 ) Abscisic acid coordinates nod factor and cytokinin signalling during the regulation of nodulation in Medicago truncatula . The Plant Cell 20 ( 10 ), 2681 - 2695 .
51. Dixon , R. & Kahn , D. ( 2004 ) Genetic regulation of biological nitrogen fi xation . Nature Reviews Microbiology 2 ( 8 ), 621 - 631 .
52. Ehrhardt , D.W. , Wais , R. , & Long , S.R. ( 1996 ) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals . Cell 85 ( 5 ), 673 - 681 .
53. Einsle , O. , Tezcan , F.A. , Andrade , S.L. , et al. ( 2002 ) Nitrogenase MoFe - protein at 1.16 A resolution: a central ligand in the FeMo - cofactor . Science (New York, N.Y.) 297 ( 5587 ), 1696 - 1700 .
54. Elliott , G.N. , Chen , W.M. , Chou , J.H. , et al. ( 2007 ) Burkholderia phymatum is a highly effective nitrogen - fi xing symbiont of Mimosa spp. and fi xes nitrogen ex planta . The New Phytologist 173 ( 1 ), 168 - 180 .
55. Endre , G. , Kereszt , A. , Kevei , Z. , Mihacea , S. , Kaló, P. , & Kiss , G.B. ( 2002 ) A receptor kinase gene regulating symbiotic nodule development . Nature 417 ( 6892 ), 962 - 966 .
56. Etzler , M.E. , Kalsi , G. , Ewing , N.N. , Roberts , N.J. , Day , R.B. , & Murphy , J.B. ( 1999 ) A Nod Factor binding lectin with apyrase activity from legume roots . Proceedings of the National Academy of Sciences of the United States of America 96 ( 10 ), 5856 - 5861 .
57. Fang, Y. & Hirsch, A.M. ( 1998) Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in alfalfa . Plant Physiology 116 , 53 - 68 .
58. FAOSTAT ( 2010 ) Food and Agricultural Organization Statistical Year Book 2010 . FAO Statistical Division, Rome, Italy.
59. Felle , H.H. , Kondorosi , E. , Kondorosi , A. , & Schultze , M. ( 1999 ) Elevation of the cytosolic free [Ca 2+ ] is indispensable for the transduction of the Nod factor signal in alfalfa . Plant Physiology 121 ( 1 ), 273 - 280 .
60. Ferguson , B.J. , Ross , J.J. , & Reid , J.B. ( 2005 ) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea . Plant Physiology 138 ( 4 ), 2396 - 2405 .
61. Fleming , A.I. , Wittenberg , J.B. , Wittenberg , B.A. , Dudman , W.F. , & Appleby , C.A. ( 1987 ) The purifi - cation, characterization and ligand - binding kinetics of haemoglobin from root nodules of the non - leguminous Casuarina glauca - Frankia symbiosis . Biochim Biophys Acta 911 , 209 - 220 .
62. Freiberg , C. , Fellay , R. , Bairoch , A. , Broughton , W.J. , Rosenthal , A. , & Perret , X. ( 1997 ) Molecular basis of symbiosis between Rhizobium and legumes . Nature 387 ( 6631 ), 394 - 401 .
63. Garrocho - Villegas , V. , Gopalasubramaniam , S.K. , & Arredondo - Peter , R. ( 2007 ) Plant haemoglobins: what we know six decades after their discovery . Gene 398 ( 1 - 2 ), 78 - 85 .
64. Genre , A. , Chabaud , M. , Facio , A. , Barker , D.G. , & Bonfante , P. ( 2008 ) Prepenetration assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within root cortex of both Medicago truncatula and Daucus carota . The Plant Cell 20 , 1407 - 1420 .
65. Genre , A. , Chabaud , M. , Timmers , T. , Bonfante , P. , & Baker , G.D. ( 2005 ) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection . The Plant Cell 17 , 3489 - 3499 .
66. Gherbi , H. , Markmann , K. , Svistoonoff , S. , et al. ( 2008 ) SymRK defi nes a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria . Proceedings of the National Academy of Sciences of the United States of America 105 ( 12 ), 4928 - 4932 .
67. Gibson , Q.H. , Wittenberg , J.B. , Wittenberg , B.A. , Bogusz , D. , & Appleby , C.A. ( 1989 ) The kinetics of ligand binding to plant haemoglobins. Structural implications . T he Journal of Biological Chemistry 264 ( 1 ), 100 - 107 .
68. Giraud, E. , Moulin, L. , Vallenet, D. , et al. ( 2007) Legume symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316 , 1307 - 1312.
69. Gleason , C. , Chaudhuri , S. , Yang , T. , Muñoz , A. , Poovaiah , B.W. , & Oldroyd , G.E. ( 2006 ) Nodulation independent of rhizobia induced by a calcium - activated kinase lacking autoinhibition . Nature 441 ( 7097 ), 1149 - 1152 .
70. Godfroy , O. , Debelle, F. , Timmers, T. , & Rosenberg, C. ( 2006 ) A rice calcium - and calmodulin - dependent protein kinase restores nodulation to a legume mutant . Molecular Plant - Microbe Interactions 19 ( 5 ), 495 - 501 .
71. 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 . The Plant Cell 18 , 2680 - 2693 .
72. Gonzalez - Sama , A. , Pena , T.C. , Kevei , Z. , et al. ( 2006 ) Nuclear DNA endoreduplication and expression of the mitotic inhibitor Ccs52 associated to determinate and lupinoid nodule organogenesis . Molecular Plant - Microbe Interactions 19 ( 2 ), 173 - 180 .
73. Goormachtig , S. , Capoen , W. , & Holsters , M. ( 2004 ) Rhizobium infection: lessons from the versatile nodulation behaviour of water - tolerant legumes . Trends in in Plant Science 9 ( 11 ), 518 - 522 .
74. Gottfert , M. , Rothlisberger , S. , Kundig , C. , Beck , C. , Marty , R. , & Hennecke , H. ( 2001 ) Potential symbiosis - specifi c genes uncovered by sequencing a 410 - kilobase DNA region of the Bradyrhizobium japonicum chromosome . Journal of Bacteriology 183 ( 4 ), 1405 - 1412 .
75. Govindarajulu , M. , Kim , S.Y. , Libault , M. , et al. ( 2009 ) GS52 ecto - apyrase plays a critical role during soybean nodulation . Plant Physiology 149 , 994 - 1004 .
76. Graham , P.H. , Hungria , M. , & Tlusty , B. ( 2004 ) Breeding for better nitrogen fi xation in grain legumes: where do the rhizobia fi t in? Crop Management doi: 10.1094/CM - 2004 - 0301 - 02 - RV.
77. Guinel , F.C. ( 2009 ) Getting around the legume nodule: I. The structure of the peripheral zone in four nodule types . Botany 87 , 1117 - 1138 .
78. Guinel , F.C. & Geil , R.D. ( 2002 ) A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use ito understand the roles of ethylene in the establishment in these two symbioses . C anadian Journal of Botany 80 , 695 - 720 .
79. Gutierrez - Zamora , M.L. & Martinez - Romero , E. ( 2001 ) Natural endophytic association between Rhizobium etli and maize ( Zea mays L.) . Journal of Biotechnology 91 ( 2 - 3 ), 117 - 126 .
80. Haney , C.H. & Long , S.R. ( 2010 ) Plant fl otillins are required for infection by nitrogen - fi xing bacteria . Proceedings of the National Academy of Sciences of the United States of America 107 ( 1 ), 478 - 483 .
81. Hardy , R.W.F. , Burns , R.C. , & Holsten , R.D. ( 1973 ) Applications of the acetylene - ethylene assay for measurement of nitrogen fi xation . Soil Biology & Biochemistry 5 , 47 - 81 .
82. Hartwig , U.A. , Maxwell , C.A. , Joseph , C.M. , & Phillips , D.A. ( 1990a ) Chrysoeriol and luteolin released from alfalfa seeds induce nod genes in Rhizobium meliloti . Plant Physiology 92 ( 1 ), 116 - 122 .
83. Hartwig , U.A. , Maxwell , C.A. , Joseph , C.M. , & Phillips , D.A. ( 1990b ) Effect of alfalfa nod gene - inducing fl avonoids on nodABC transcription in Rhizobium meliloti s trains containing different nodD genes . Journal of Bacteriology 172 ( 5 ), 2769 - 2773 .
84. Heckmann , A.B. , Lombardo , F. , Miwa , H. , et al. ( 2006 ) Lotus japonicus requires two GRAS domain regulators, one of which is functionally conserved in a non - legume . Plant Physiology 142 , 1739 - 1750 .
85. Heidstra , R. , Geurts , R. , Franssen , H. , Spaink , H.P. , Van Kammen , A. , & Bisseling , T. ( 1994 ) Root hair deformation activity of nodulation factors and their fate on Vicia sativa . Plant Physiology 105 ( 3 ), 787 - 797 .
86. Herridge , D. & Rose , I. ( 2000 ) Breeding for enhanced nitrogen fi xation in crop legumes . Field Crops Research 65 ( 229 ), 248
87. Herridge , D. , Gemell , G. , & Hartley , E. ( 2002 ) Legume inoculants and quality control . In: Inoculants and Nitrogen Fixation of Legumes in Vietnam (ed. D. Herridge ), pp. 105 - 115 . ACIAR Proceedings .
88. Hiltbold , A.E. , Thurlow , D.L. , & Skipper , H.D. ( 1980 ) Evaluation of commercial soybean inoculants by various techniques . Agronomy Journal 72 , 675 - 681 .
89. Hirsch , A.M. ( 1992 ) Developmental biology of legume nodulation . T he New Phytologist 122 , 211 - 237 .
90. Hirsch , A.M. & Fang , Y. ( 1994 ) Plant hormones and nodulation: what's the connection? Plant Molecular Biology 26 , 5 - 9 .
91. Hirsch , A.M. , Bhuvaneswari , T.V. , Torrey , J.G. , & Bisseling , T. ( 1989 ) Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors . P roceedings of the National Academy of Sciences of the United States of America 86 , 1246 - 1248 .
92. Hirsch , S. , Kim , J. , Muñoz , A. , Heckmann , A.B. , Downie , J.A. , & Oldroyd , G.E. ( 2009 ) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signalling in Medicago truncatula . The Plant Cell 21 , 545 - 557 .
93. Hubber , A. , Vergunst , A.C. , Sullivan , J.T. , Hooykaas , P.J. , & Ronson , C.W. ( 2004 ) Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system . Molecular Microbiology 54 ( 2 ), 561 - 574 .
94. Imaizumi - Anraku , H. , Takeda , N. , Charpentier , M. , et al. ( 2005 ) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots . Nature 433 ( 7025 ), 527 - 531 .
95. James , E.K. , Sprent , J.I. , Sutherland , J.M. , McInroy , S.G. , & Minchin , F.R. ( 1992 ) The structure of nitrogen - fi xing root nodules in the aquatic mimosoid legume Neptunia plena . Annals of Botany 14 , 173 - 180 .
96. Jessen , D.L. , Barnes , D.K. , & Vance , C.P. ( 1988 ) Bidirectional selection in alfalfa for activity of nodule nitrogen and carbon assimilating enzymes . Crop Science 28 , 18 - 22 .
97. Jha , P.K. , Nair , S. , & Babu , C.R. ( 1994 ) Development of an inexpensive legume - Rhizobium i noculation technology which may be used in aerial seeding . Journal of Basic Microbiology 34 ( 4 ), 231 - 243 .
98. Jones , K.M. , Kobayashi , H. , Davies , B.W. , Taga , M.E. , & Walker , G.C. ( 2007 ) How rhizobial symbionts invade plants: the Sinorhizobium - Medicago model . Nature Reviews in Microbiology 5 ( 8 ), 619 - 633 .
99. Jones , K.M. , Sharopova , N. , Lohar , D.P. , Zhang , J.Q. , VandenBosch , K.A. , & Walker , G.C. ( 2008 ) Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide - defi cient mutant . Proceedings of the National Academy of Sciences of the United States of America 105 ( 2 ), 704 - 709 .
100. Jourand , P. , Renier , A. , Rapior , S. , et al. ( 2005 ) Role of methylotrophy during symbiosis between Methylobacterium nodulans and Crotalaria podo carpa . Molecular Plant - Microbe Interactions 18 ( 10 ), 1061 - 1068 .
101. Journet , E.P. , Pichon , M. , Dedieu , A. , de Billy , F. , Truchet , G. , & Barker , D.G. ( 1994 ) Rhizobium meliloti Nod factors elicit cell - specifi c transcription of the ENOD12 g ene in transgenic alfalfa . Plant Journal 6 , 241 - 249 .
102. Journet , E.P. , El - Gachtouli , N. , Vernoud , V. , et al. ( 2001 ) Medicago truncatula ENOD11: a novel RPRP - encoding early nodulin gene expressed during mycorrhization in arbuscule - containing cells . Molecular Plant - Microbe Interactions 14 ( 6 ), 737 - 748 .
103. Kaló, P. , Gleason , C. , Edwards , A. , et al. ( 2005 ) Nodulation signalling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators . S cience 308 ( 5729 ), 1786 - 1789 .
104. Kanamori , N. , Madsen , L.H. , Radutoiu , S. , et al. ( 2006 ) A nucleoporin is required for induction of Ca 2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis . Proceedings of the National Academy of Sciences of the United States of America 103 ( 2 ), 359 - 364 .
105. Kaneko , T. , Nakamura , Y. , Sato , S. , et al. ( 2000 ) Complete genome structure of the nitrogen - fi xing symbiotic bacterium Mesorhizobium loti . DNA Research 7 ( 6 ), 331 - 338 .
106. Kawaguchi , M. , Imaizumi - Anraku , H. , Fukai , S. , & Syono , K. ( 1996 ) Unusual branching in the seedlings of Lotus japonicus - Gibberellins reveal the nitrogen sensitive cell divisions within the pericycle on roots . Plant Cell Physiology 37 , 461 - 470 .
107. Kevei , Z. , Lougnon , G. , Mergaert , P. , et al. ( 2007 ) 3 - hydroxy - 3 - methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula . The Plant Cell 19 ( 12 ), 3974 - 3989 .
108. Kim , S.A. & Copeland , L. ( 1996 ) Enzymes of Poly - (beta) - Hydroxybutyrate metabolism in soybean and chickpea bacteroids . Applied and Environmental Microbiology 62 ( 11 ), 4186 - 4190 .
109. Kiss , E. , Olah , B. , Kalo , P. , et al. ( 2009 ) LIN, a novel type of U - box/WD40 protein, controls early infection by rhizobia in legumes . Plant Physiology 151 ( 3 ), 1239 - 1249 .
110. Kistner , C. & Parniske , M. ( 2002 ) Evolution of signal transduction in intracellular symbiosis . Trends in in Plant Science 7 ( 11 ), 511 - 518 .
111. Kosslak , R.M. , Bookland , R. , Barkei , J. , Paaren , H.E. , & Appelbaum , E.R. ( 1987 ) Induction of Bradyrhizobium japonicum c ommon nod genes by isofl avones isolated from Glycine max . Proceedings of the National Academy of Sciences of the United States of America 84 ( 21 ), 7428 - 7432 .
112. Kuppusamy , K.T. , Endre , G. , Prabhu , R. , et al. ( 2004 ) LIN, a Medicago truncatula gene required for nodule differentiation and persistence of rhizobial infections . P lant Physiology 136 , 3682 - 3691 .
113. Kuppusamy , K.T. , Ivashuta , S. , Bucciarelli , B. , Vance , C.P. , Gantt , J.S. , & Vandenbosch , K.A. ( 2009 ) Knockdown of CELL DIVISION CYCLE16 r eveals an inverse relationship between lateral root and nodule numbers and a link to auxin in Medicago truncatula . Plant Physiology 151 ( 3 ), 1155 - 1166 .
114. Laguerre , G. , Nour , S.M. , Macheret , V. , Sanjuan , J. , Drouin , P. , & Amarger , N. ( 2001 ) Classifi cation of rhizobia based on nodC a nd nifH g ene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris s ymbionts . Microbiology (Reading, England) 147 ( Pt 4 ), 981 - 993 .
115. Lanzilotta , W.N. , Christiansen , J. , Dean , D.R. , & Seefeldt , L.C. ( 1998 ) Evidence for coupled electron and proton transfer in the [8Fe - 7S] cluster of nitrogenase . Biochemistry 37 ( 32 ), 11376 - 11384 .
116. Larson , J.L. & Siemann , E. ( 1998 ) Legumes may be symbiont - limited during old - fi eld succession . The American Midland Naturalist 140 , 90 - 95 .
117. Lefebvre , B. , Timmers , T. , Mbengue , M. , et al. ( 2010 ) A remorin protein interacts with symbiotic receptors and regulates bacterial infection . Proceedings of the National Academy of Sciences of the United States of America 107 ( 5 ), 2343 - 2348 .
118. Leigh , J.A. & Coplin , D.L. ( 1992 ) Exopolysaccharides in plant - bacterial interactions . Annual Review of Microbiology 46 , 307 - 346 .
119. Leigh , J.A. , Signer , E.R. , & Walker , G.C. ( 1985 ) Exopolysaccharide - defi cient mutants of Rhizobium meliloti t hat form ineffective nodules . Proceedings of the National Academy of Sciences of the United States of America 82 ( 18 ), 6231 - 6235 .
120. Lévy , J. , Bres , C. , Geurts , R. , et al. ( 2004 ) A putative Ca2+ and calmodulin - dependent protein kinase required for bacterial and fungal symbioses . Science 303 ( 5662 ), 1361 - 1364 .
121. Liang , Y. , Mitchell , D.M. , & Harris , J.M. ( 2007 ) Abscisic acid rescues the root meristem defects of the Medicago truncatula latd mutant . Developmental biology 304 , 297 - 307 .
122. Limpens , E. , Franken , C. , Smit , P. , Willemse , J. , Bisseling , T. , & Geurts , R. ( 2003 ) LysM domain receptor kinases regulating rhizobial Nod factor - induced infection . Science 302 ( 5645 ), 630 - 633 .
123. Limpens , E. , Mirabella , R. , Fedorova , E. , et al. ( 2005 ) Formation of organelle - like N2 - f ixing symbiosomes in legume root nodules is controlled by DMI2 . Proceedings of The National Academy of Sciences of The United States of America 102 ( 29 ), 10375 - 10380 .
124. Lohar , D.P. , Schaff , J.E. , Laskey , J.G. , Kieber , J.J. , Bilyeu , K.D. , & Bird , D.M. ( 2004 ) Cytokinins play opposite roles in lateral root formation, and nema tode and Rhizobial symbioses . Plant Journal 38 , 203 - 214 .
125. Lombardo , F. , Heckmann , A.B. , Miwa , H. , et al. ( 2006 ) Identifi cation of symbiotically defective mutants of Lotus japonicus affected in infection thread growth . Molecular Plant - Microbe Interactions 19 ( 12 ), 1444 - 1450 .
126. Mabood , F. , Souleimanov , A. , Khan , W. , & Smith , D.L. ( 2006 ) Jasmonates induce Nod factor production by Bradyrhizobium japonicum . Plant Physiology and Biochemistry 44 , 759 - 765 .
127. Macchiavelli , R.E. & Brelles - Mariño , G. ( 2004 ) Nod factor - treated Medicago truncatula roots and seeds show an increased number of nodules when inoculated with a limiting population of Sinorhizobium meliloti . Journal of Experimental Botany 55 ( 408 ), 2635 - 2640 .
128. Madsen , E.B. , Madsen , L.H. , Radutoiu , S. , et al. ( 2003 ) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals . Nature 425 ( 6958 ), 637 - 640 .
129. Maekawa , T. , Maekawa - Yoshikawa , M. , Takeda , N. , Imaizumi - Anraku , H. , Murooka , Y. , & Hayashi , M. ( 2009 ) Gibberellin controls the nodulation signalling pathway in Lotus japonicus . Plant Journal 58 , 183 - 194 .
130. Marie , C. , Broughton , W.J. , & Deakin , W.J. ( 2001 ) Rhizobium type III secretion systems: legume charmers or alarmers? Current opinion in plant biology 4 ( 4 ), 336 - 342 .
131. Markmann , K. & Parniske , M. ( 2009 ) Evolution of root endosymbiosis with bacteria: how novel are nodules? T rends in Plant Science 14 ( 2 ), 77 - 86 .
132. Markmann , K. , Giczey , G. , & Parniske , M. ( 2008 ) Functional adaptation of a plant receptor - kinase paved the way for the evolution of intracellular root symbioses with bacteria . PLoS Biology 6 ( 3 ), e68 .
133. Marsh , J.F. , Rakocevic , A. , Mitra , R.M. , et al. ( 2007 ) Medicago truncatula NIN i s essential for rhizobial - independent nodule organogenesis induced by autoactive calcium/calmodulin - dependent protein kinase . Plant Physiology 144 ( 1 ), 324 - 335 .
134. Martinez - Romero , E. ( 2009 ) Coevolution in Rhizobium - legume symbiosis? DNA and cell biology 28 ( 8 ), 361 - 370 .
135. Masson - Boivin , C. , Giraud , E. , Perret , X. , & Batut , J. ( 2009 ) Establishing nitrogen - fi xing symbiosis with legumes: how many rhizobium recipes? Trends in in Microbiology 17 ( 10 ), 458 - 466 .
136. Mathesius , U. ( 2008 ) Auxin: at the root of nodule development? F unctional Plant Biology 35 , 651 - 668 .
137. Mathesius , U. , Schlaman , H.R. , Spaink , H. , Sautter , C. , Rolfe , B. , & Djordjevic , M.A. ( 1998 ) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by fl avanoids and derivatives of chitin oligosaccharides . Plant Journal 14 , 23 - 34 .
138. Maxwell , C.A. , Hartwig , U.A. , Joseph , C.M. , & Phillips , D.A. ( 1989 ) A chalcone and two related fl avonoids released from alfalfa roots induce nod genes of Rhizobium meliloti . Plant Physiology 91 ( 3 ), 842 - 847 .
139. Mazur , A. , Krol , J.E. , Wielbo , J. , Urbanik - Sypniewska , T. , & Skorupska , A. ( 2002 ) Rhizobium leguminosarum bv. trifolii PssP protein is required for exopolysaccharide biosynthesis and polymerization . Molecular Plant - Microbe Interactions 15 ( 4 ), 388 - 397 .
140. McAlvin , C.B. & Stacey , G. ( 2005 ) Transgenic expression of the soybean apyrase in Lotus japonicus e nhances nodulation . Plant Physiology 137 ( 4 ), 1456 - 1462 .
141. Mergaert , P. , Uchiumi , T. , Alunni , B. , et al. ( 2006 ) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium - legume symbiosis . Proceedings of the National Academy of Sciences of the United States of America 103 ( 13 ), 5230 - 5235 .
142. Messinese , E. , Mun , J.H. , Yeun , L.H. , et al. ( 2007 ) A novel nuclear protein interacts with the symbiotic DMI3 calcium - and calmodulin - dependent protein kinase of Medicago truncatula . Molecular Plant - Microbe Interactions 20 ( 8 ), 912 - 921 .
143. Middleton , P.H. , Jakab , J. , Penmetsa , R.V. , et al. ( 2007 ) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction . Plant Cell 19 , 1221 - 1234 .
144. Mitra , R.M. , Gleason , C.A. , Edwards , A. , et al. ( 2004 ) A Ca 2+ /calmodulin - dependent protein kinase required for symbiotic nodule development: gene identifi cation by transcript - based cloning . Proceedings of the National Academy of Sciences of The United States of America 101 ( 13 ), 4701 - 4705 .
145. Morgante , C. , Angelini , J. , Castro , S. , & Fabra , A. ( 2005 ) Role of rhizobial exopolysacharides in crack entry/ intercellular infection of peanut . Soil Biology & Biochemistry 37 , 1436 - 1444 .
146. Morgante , C. , Castro , S. , & Fabra , A. ( 2007 ) Role of rhizobial EPS in the evasion of peanut defence response during the crack - entry infection process . Soil Biology & Biochemistry 39 , 1222 - 1225 .
147. Mukherjee , A. & Ané, J.M. ( 2011 ) Plant hormones and initiation of legume nodulation and arbuscular mycorrhization . In: Environmental Aspects of Plant Nitrogen Metabolism (eds. J. Polacco & C. Todd ) John Wiley & Sons , Hoboken, NJ , pp. 354 - 396 .
148. Muller , J. , Wiemken , A. , & Boller , T. ( 2001 ) Redifferentiation of bacteria isolated from Lotus japonicus r oot nodules colonized by Rhizobium sp. NGR234 . J ournal of Experimental Botany 52 ( 364 ), 2181 - 2186 .
149. Murakami , Y. , Miwa , H. , Imaizumi - Anraku , H. , et al. ( 2006 ) Positional cloning identifi es Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 g ene expression in nodule initiation . DNA Research 13 , 255 - 265 .
150. Murray , J.D. , Karas , B.J. , Sato , S. , Tabata , S. , Amyot , L. , & Szczyglowski , K. ( 2007 ) A cytokinin perception mutant colonized by rhizobium in the absence of nodule organogenesis . Science 315 ( 5808 ), 101 - 104 .
151. Mytton , L.R. ( 1984 ) Developing a breeding strategy to exploit quantitative variation in symbiotic nitrogen fi xation . Plant Soil 82 , 329 - 335 .
152. Nelson , D.W. , Swearingin , M.L. , & Beckham , L.S. ( 1978 ) Response of soybeans to commercial soil - applied inoculants . Agronomy Journal 70 , 517 - 518 .
153. Nukui , N. , Ezura , H. , & Minamisawa , K. ( 2004 ) Transgenic Lotus japonicus with an ethylene receptor gene Cm - ERS1/H70A enhances formation of infection threads and nodule primordia . Plant and Cell Physiology 45 , 427 - 435 .
154. Nutman , P.S. ( 1984 ) Improving nitrogen fi xation in legumes by plant breeding: the relevance of host selection experiments in red clover ( Trifolium pratense L.) and subterranean clover ( T. subterraneum L.) . Plant Soil 82 , 285 - 301 .
155. Oláh , B. , Brière , C. , Bécard , G. , Dénarié, J. , & Gough , C. ( 2005 ) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/ DMI2 signalling pathway . The Plant Journal 44 ( 2 ), 195 - 207 .
156. Oldroyd , G.E. & Downie , J.A. ( 2004 ) Calcium, kinases and nodulation signalling in legumes . Nature Reviews Molecular Cell Biology 5 ( 7 ), 566 - 576 .
157. Oldroyd , G.E. & Downie , J.A. ( 2008 ) Coordinating nodule morphogenesis with rhizobial infection in legumes . Annual Review of Plant Biology 59 , 519 - 546 .
158. Oldroyd , G.E. , Engstrom , E.M. , & Long , S.R. ( 2001b ) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula . The Plant Cell 13 , 1835 - 1849 .
159. Oldroyd , G.E. , Mitra , R.M. , Wais , R.J. , & Long , S.R. ( 2001a ) Evidence for structurally specifi c negative feedback in the Nod factor signal transduction pathway . The Plant Journal 28 ( 2 ), 191 - 199 .
160. Ooki , Y. , Banba , M. , Yano , K. , et al. ( 2005 ) Characterization of the Lotus japonicus symbiotic mutant lot1 that shows a reduced nodule number and distorted trichomes . Plant Physiology 137 , 1261 - 1271 .
161. Ott , T. , van Dongen , J.T. , Gunther , C. , et al. ( 2005 ) Symbiotic leghaemoglobins are crucial for nitrogen fi xation in legume root nodules but not for general plant growth and development . Current Biology 15 , 531 - 535 .
162. Ott , T. , Sullivan , J. , James , E.K. , et al. ( 2009 ) Absence of symbiotic leghaemoglobins alters bacteroid and plant cell differentiation during development of Lotus japonicus root nodules . Molecular Plant - Microbe Interactions 22 ( 7 ), 800 - 808 .
163. Pacios - Bras , C. , Schlaman , H.R. , Boot , K. , et al. ( 2003 ) Auxin distribution in Lotus japonicus during root nodule development . Plant Molecular Biology 52 ( 6 ), 1169 - 1180 .
164. Parniske , M. , Schmidt , P. , Kosch , K. , & Müller , P. ( 1994 ) Plant defence responses of host plants with determinate nodules induced by exopolysaccharide - defective exoB mutants of Bradyrhizobium japonicum . Molecular Plant - Microbe Interaction 7 , 631 - 638 .
165. Parveen , N. , Webb , D. , & Borthakur , D. ( 1997 ) The symbiotic phenotypes of exopolysaccharide - defective mutants of Rhizobium sp. strain TAL1145 do not differ on determinate and indeterminate nodulating tree legumes . Microbiology 143 , 1959 - 1967 .
166. Pathirana , S.M. & Tjepkema , J.D. ( 1995 ) Purifi cation of haemoglobin from the actinorhizal root nodules of Myrica gale L . Plant Physiology 107 ( 3 ), 827 - 831 .
167. Pazdernik , D.L. , Graham , P.H. , Vance , C.P. , & Orf , J.H. ( 1996 ) Host genetic variation in the early nodulation and dinitrogen fi xation of soybeans . Crop Science 36 , 1102 - 1107 .
168. Peiter , E. , Sun , J. , Heckmann , A.B. , et al. ( 2007 ) The Medicago truncatula DMI1 protein modulates cytosolic calcium signalling . Plant Physiology 145 ( 1 ), 192 - 203 .
169. Pellock , B.J. , Cheng , H.P. , & Walker , G.C. ( 2000 ) Alfalfa root nodule invasion effi ciency is dependent on Sinorhizobium meliloti polysaccharides . Journal of Bacteriology 182 ( 15 ), 4310 - 4318 .
170. Penmetsa , R.V. & Cook , D. ( 1997 ) A legume ethylene - insensitive mutant hyperinfected by its rhizobial symbiont . S cience 275 , 527 - 530 .
171. Penmetsa , R.V. , Uribe , P. , Anderson , J. , et al. ( 2008 ) The Medicago truncatula orthologue of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations . Plant Journal 55 , 580 - 595 .
172. Perlick , A.M. , Albus , U. , Stavridis , T. , Fruhling , M. , Kuster , H. , & Puhler , A. ( 1996 ) The Vicia faba lipoxygenase gene VfLOX1 is expressed in the root nodule parenchyma . Molecular Plant - Microbe Interactions 9 ( 9 ), 860 - 863 .
173. Perret , X. , Staehelin , C. , & Broughton , W.J. ( 2000 ) Molecular basis of symbiotic promiscuity . Microbiology and Molecular Biology Reviews 64 ( 1 ), 180 - 201 .
174. Peters , N.K. , Frost , J.W. , & Long , S.R. ( 1986 ) A plant fl avone, luteolin, induces expression of Rhizobium meliloti nodulation genes . Science 233 ( 4767 ), 977 - 980 .
175. Phillips , D.A. , Torrey , J.G. , & Burris , R.H. ( 1971 ) Extending symbiotic nitrogen fi xation to increase man's food supply . Science (New York, N.Y.) 174 ( 4005 ), 169 - 170 .
176. Povolo , S. , Tombolini , R. , Morea , A. , Anderson , A.J. , Casella , S. , & Nuti , M.P. ( 1994 ) Isolation and characterization of mutants of Rhizobium meliloti unable to synthesize poly - b - hydroxybutyrate . Canadian Journal of Microbiology 40 , 823 - 829 .
177. Prayitno , J. , Rolfe , B.G. , & Mathesius , U. ( 2006 ) The ethylene - insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation . Plant Physiology 142 ( 1 ), 168 - 180 .
178. Pueppke , S.G. & Broughton , W.J. ( 1999 ) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges . Molecular Plant - Microbe Interactions 12 ( 4 ), 293 - 318 .
179. Radutoiu , S. , Madsen , L.H. , Madsen , E.B. , et al. ( 2003 ) Plant recognition of symbiotic bacteria requires two LysM receptor - like kinases . Nature 425 ( 6958 ), 585 - 592 .
180. Radutoiu , S. , Madsen , L.H. , Madsen , E.B. , et al. ( 2007 ) LysM domains mediate lipochitin - oligosaccharide recognition and Nfr genes extend the symbiotic host range . The EMBO Journal 26 ( 17 ), 3923 - 3935 .
181. Rasolomampianina , R. , Bailly , X. , Fetiarison , R. , et al. ( 2005 ) Nitrogen - fi xing nodules from rose wood legume trees ( Dalbergia spp. ) e ndemic to Madagascar host seven different genera belonging to alpha - and beta - Proteobacteria . Molecular Ecology 14 ( 13 ), 4135 - 4146 .
182. Renier , A. , Jourand , P. , Rapior , S. , et al. ( 2008 ) Symbiotic properties of Methylobacterium nodulans ORS2060: a classic process for an atypical symbiont . S oil Biology & Biochemistry 4 0 , 1404 - 1412 .
183. Rennie , R.J. & Kemp , G.A. ( 1983 ) Nitrogen fi xation in fi eld beans quantifi ed by 15 N isotope dilution.2. Effect of cultivars of beans . Agronomy Journal 75 , 645 - 649 .
184. Ridge , R.W. , Ride , K.M. , & Rolfe , B.G. ( 1993 ) Nodule - like structures induced on the roots of rice seedlings by addition of the synthetic auxin 2,4 - dichlorophenoxyacetic acid . Australian Journal of Plant Physiology 20 , 705 - 717 .
185. Riely , B.K. , Lougnon , G. , Ané, J.M. , & Cook , D.R. ( 2007 ) The symbiotic ion channel homologue DMI1 is localized in the nuclear membrane of Medicago truncatula roots . The Plant Journal 49 ( 2 ), 208 - 216 .
186. Robledo , M. , Jimenez - Zurdo , J.I. , Velazquez , E. , et al. ( 2008 ) Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots . Proceedings of the National Academy of Sciences of the United States of America 105 ( 19 ), 7064 - 7069 .
187. Rogel , M.A. , Hernandez - Lucas , I. , Kuykendall , L.D. , Balkwill , D.L. , & Martinez - Romero , E. ( 2001 ) Nitrogen - fi xing nodules with En s ifer adhaerens harboring Rhizobium tropici symbiotic plasmids . Applied and Environmental Microbiology 67 ( 7 ), 3264 - 3268 .
188. Rosas , S. , Soria , R. , Correa , N. , & Abdala , G. ( 1998 ) Jasmonic acid stimulates the expression of nod genes in Rhizobium . Plant Molecular Biology 38 , 1161 - 1168 .
189. Ruiz Diaz , D.A. , Pedersen , P. , & Sawyer , J.E. ( 2009 ) Soybean response to inoculation and nitrogen application following long - term grass pasture . Crop Science 49 , 1058 - 1062 .
190. Saito , K. , Yoshikawa , M. , Yano , K. , et al. ( 2007 ) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus . The Plant Cell 19 ( 2 ), 610 - 624 .
191. Schauser , L. , Roussi , A. , Stiller , J. , & Stougaard , J. ( 1999 ) A plant regulator controlling development of symbiotic root nodules . Nature 402 , 191 - 195 .
192. Schauser , L. , Wieloch , W. , & Stougaard , J. ( 2005 ) Evolution of NIN - like proteins in Arabidopsis, rice and Lotus japonicus . Journal of Molecular Evolution 60 , 229 - 237 .
193. Schmidt , J.S. , Harper , J.E. , Hoffman , T.K. , & Bent , A.F. ( 1999 ) Regulation of soybean nodulation independent of ethylene signalling . Plant Physiology 119 , 951 - 959 .
194. Schulz , T.J. & Thelen , K.D. ( 2008 ) Soybean seed inoculant and fungicidal seed treatment effects on soybean . Crop Science 48 , 1975 - 1983 .
195. Shaw , S.L. & Long , S.R. ( 2003 ) Nod factor inhibition of reactive oxygen effl ux in a host legume . Plant Physiology 132 ( 4 ), 2196 - 2204 .
196. Sieberer , B.J. , Chabaud , M. , Timmers , A.C. , Monin , A. , Fournier , J. , & Barker , D.G. ( 2009 ) A nuclear - targeted cameleon demonstrates intranuclear Ca 2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors . Plant Physiology 151 , 1197 - 1206 .
197. Singh , M.K. , Kushwaha , C. , & Singh , R.K. ( 2009 ) Studies on endophytic colonization ability of two upland rice endophytes, Rhizobium sp. and Burkholderia sp. , using green fl uorescent protein reporter . Current Microbiology 59 ( 3 ), 240 - 243 .
198. Singleton , P.W. , Boonkerd , N. , Carr , T.J. , & Thompson , J.A. ( 1997 ) Technical and market constraints limiting legume inoculant use in Asia . In: Extending Nitrogen Fixation Research to Farmers'Fields (eds. O.P. Rupela , C. Johansen & D.F. Herridge ), pp. 17 - 38 . ICRISAT , Patancheru, AP, India .
199. Smit , P. , Raedts , J. , Portyanko , V. , et al. ( 2005 ) NSP1 of the GRAS protein family is essential for rhizobial Nod factor - induced transcription . Science 308 ( 5729 ), 1789 - 1791 .
200. Smit , P. , Limpens , E. , Geurts , R. , et al. ( 2007 ) Medicago LYK3, an entry receptor in rhizobial nodulation factor signalling . Plant Physiology 145 ( 1 ), 183 - 191 .
201. Spaink , H.P. ( 1995 ) The molecular basis of infection and nodulation by rhizobia - the ins and outs of sympathogenesis . A nnual Review of Phytopathology 33 , 345 - 368 .
202. Spaink , H.P. ( 1996 ) Regulation of plant morphogenesis by lipo - chitin oligosaccharides . Critical Review of Plant Science 15 , 559 - 582 .
203. Spencer , D. , James , E.K. , Ellis , G.J. , Shaw , J.E. , & Sprent , J.I. ( 1994 ) Interaction between rhizobia and potato tissue . Journal of Experimental Botany 45 , 1475 - 1482 .
204. Sprent , J.I. ( 2007 ) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation . The New Phytologist 174 ( 1 ), 11 - 25 .
205. Sprent , J.I. ( 2008 ) 60Ma of legume nodulation. What's new? What's changing? Journal of Experimental Botany 59 ( 5 ), 1081 - 1084 .
206. Sprent , J.I. & James , E.K. ( 2007 ) Legume evolution: where do nodules and mycorrhizas fi t in? Plant Physiology 144 ( 2 ), 575 - 581 .
207. Starker , C.G. , Parra - Cohnenares , A.L. , Smith , L. , Mitra , R.M. , & Long , S.R. ( 2006 ) Nitrogen - fi xing mutants of Medicago truncatula fail to support plant and bacterial symbiotic gene expression . Plant Physiology 140 , 671 - 680 .
208. Stougaard , J. ( 2000 ) Regulators and regulation of legume root nodule development . Plant Physiology 124 , 531 - 540 .
209. Stracke , S. , Kistner , C. , Yoshida , S. , et al. ( 2002 ) A plant receptor - like kinase required for both bacterial and fungal symbiosis . Nature 417 ( 6892 ), 959 - 962 .
210. Subramanian , S. , Stacey , G. , & Yu , O. ( 2006 ) Endogenous isofl avones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum . Plant Journal 48 , 261 - 273 .
211. Subramanian , S. , Stacey , G. , & Yu , O. ( 2007 ) Distinct, crucial roles of fl avonoids during legume nodulation . Trends in Plant Science 12 , 282 - 285 .
212. Suharjo , U.K.J. & Tjepkema , J.D. ( 1995 ) Occurrence of haemoglobin in the nitrogen - fi xing root nodules of Alnus glutinosa . Physiologia Plantarum 95 ( 247 ), 252 .
213. Sullivan , J.T. , Patrick , H.N. , Lowther , W.L. , Scott , D.B. , & Ronson , C.W. ( 1995 ) Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment . Proceedings of the National Academy of Sciences of the United States of America 92 ( 19 ), 8985 - 8989 .
214. Sun , J. , Cardoza , V. , Mitchell , D.M. , Bright , L. , Oldroyd , G.E. , & Harris , J.M. ( 2006 ) Crosstalk between jasmonic acid, ethylene and Nod factor signalling allows integration of diverse inputs for regulation of nodulation . Plant Journal 46 , 961 - 970 .
215. Suzuki , A. , Akune , M. , Kogiso , M. , et al. ( 2004 ) Control of nodule number by the phytohormone abscisic Acid in the roots of two leguminous species . Plant & Cell Physiology 45 ( 7 ), 914 - 922 .
216. Teillet , A. , Garcia , J. , de Billy , F. , et al. ( 2008 ) api , A novel Medicago truncatula symbiotic mutant impaired in nodule primordium invasion . Molecular Plant - Microbe Interactions 21 ( 5 ), 535 - 546 .
217. Timmers , A.C.J. , Auriac , M.C. , & Truchet , G. ( 1999 ) Refi ned analysis of early symbiotic steps of the Rhizobium - Medicago interaction in relationship with microtubular cytoskeleton rearrangements . Development 126 , 3617 - 3628 .
218. Timmers , A.C. , Soupene , E. , Auriac , M.C. , et al. ( 2000 ) Saprophytic intracellular rhizobia in alfalfa nodules . Molecular Plant - Microbe Interactions 13 ( 11 ), 1204 - 1213 .
219. Tirichine , L. , Imaizumi - Anraku , H. , Yoshida , S. , et al. ( 2006a ) Deregulation of Ca 2+ /calmodulin - dependent kinase leads to the spontaneous nodule development . Nature 441 , 1153 - 1156 .
220. Tirichine , L. , James , E.K. , Sandal , N. , & Stougaard , J. ( 2006b) Spontaneous root- nodule formation in the model legume Lotus japonicus: a novel class of mutants nodulates in the absence of rhizobia . Molecular Plant- Microbe Interactions 19 , 373 - 382.
221. Tirichine , L. , Sandal , N. , Madsen , L.H. , et al. ( 2007 ) A gain - of - function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis . Science 315 ( 5808 ), 104 - 107 .
222. Tominaga , A. , Nagata , M. , Futsuki , K. , et al. ( 2009 ) Enhanced nodulation and nitrogen fi xation in the abscisic acid low - sensitive mutant enhanced nitrogen fi xation1 of Lotus japonicus . Plant Physiology 151 ( 4 ), 1965 - 1976 .
223. Trinick , M.J. ( 1979 ) Structure of nitrogen - fi xing nodules formed by Rhizobium on roots of Parasponia andersonii Planch . Canadian Journal of Microbiology 25 , 565 - 578 .
224. Van de Velde , W. , Zehirov , G. , Szatmari , A. , et al. ( 2010 ) Plant peptides govern terminal differentiation of bacteria in symbiosis . Science (New York, N.Y.) 327 ( 5969 ), 1122 - 1126 .
225. Vasse , J. , de Billy , F. , Camut , S. , & Truchet , G. ( 1990 ) Correlation between ultrastructural differentiation of bacteroids and nitrogen fi xation in alfalfa nodules . Journal of Bacteriology 172 ( 8), 4295 - 4306.
226. Veereshlingam , H. , Haynes , J.G. , Penmetsa , R.V. , Cook , D.R. , Sherrier , D.J. , & Dickstein , R. ( 2004 ) nip , A symbiotic Medicago truncatula mutant that forms root nodules with aberrant infection threads and plant defence - like response . Plant Physiology 136 , 3692 - 3702 .
227. Viprey , V. , Del Greco , A. , Golinowski , W. , Broughton , W.J. , & Perret , X. ( 1998 ) Symbiotic implications of type III protein secretion machinery in Rhizobium . Molecular Microbiology 28 ( 6 ), 1381 - 1389 .
228. Wais , R.J. , Galera , C. , Oldroyd , G.E. , et al. ( 2000 ) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula . Proceedings of the National Academy of Sciences of the United States of America 97 ( 24 ), 13407 - 13412 .
229. Wang , B. , Yeun , L.H. , Xue , J.Y. , Liu , Y. , Ané, J.M. , & Qiu , Y.L. ( 2010a ) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants . The New Phytologist 186 , 514 - 525 .
230. Wang , D. , Griffi tts , J. , Starker , C. , et al. ( 2010b ) A nodule - specifi c protein secretory pathway required for nitrogen - fi xing symbiosis . Science (New York, N.Y.) 327 ( 5969 ), 1126 - 1129 .
231. Wasson , A.P. , Pellerone , F.I. , & Mathesius , U. ( 2006 ) Silencing the fl avonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia . Plant Cell 18 , 1617 - 1629 .
232. Yano , K. , Yoshida , S. , Muller , J. , et al. ( 2008 ) CYCLOPS , a mediator of symbiotic intracellular accommodation . Proceedings of the National Academy of Sciences of the United States of America 105 , 20540 - 20545 .
233. Zehner , S. , Schober , G. , Wenzel , M. , Lang , K. , & Göttfert, M. ( 2008) Expression of the Bradyrhizobium japonicum type III secretion system in legume nodules and analysis of the associated tts box promoter . Molecular Plant - Microbe Interactions 21 ( 8 ), 1087 - 1093 .
234. Zhang , F. & Smith , D.L. ( 1995 ) Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean at suboptimal root zone temperatures . Plant Physiology 108 ( 3 ), 961 - 968 .
235. Zhang , J.X. , Wang , Y.P. , Shen , S.H. , et al. ( 2001 ) Transformation of pea lectin gene and Parasponia ha emoglobin gene into rice and their expressions . Acta Botanica Sinica 43 ( 3 ), 267 - 274 .
236. Zhu , H. , Riely , B.K. , Burns , N.J. , & Ané, J.M. ( 2006 ) Tracing nonlegume orthologues of legume genes required for nodulation and arbuscular mycorrhizal symbioses . G enetics 172 ( 4 ), 2491 - 2499 .
237. Zhu , H. , Chen , T. , Zhu , M. , et al. ( 2008 ) A novel ARID DNA - binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus . Plant Physiology 148 ( 1), 337 - 347.