On the efficiency of legume supernodulating mutants

Annals of Applied Biology

Volumn 157, Issue 3, 2010, Pages 321-342

  Novak K ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

Breeding; modifiers; nitrogen fixation; nodulation; pleiotropy; Rhizobium

Indexed keywords

BIOMASS ALLOCATION; INHIBITION; LEGUME; NITROGEN FIXATION; NODULATION; PLEIOTROPY; REPRODUCTIVE STRATEGY; RHIZOBACTERIUM; SYMBIONT;

BACTERIA (MICROORGANISMS); RHIZOBIUM;

EID: 78449301994     PISSN: 00034746     EISSN: 17447348     Source Type: Journal    
DOI: 10.1111/j.1744-7348.2010.00431.x     Document Type: Review

References (130)

1. Andrews M., Lea P.J., Raven J.A., Azevedo R.A., (2009) Nitrogen use efficiency. 3. Nitrogen fixation: genes and costs. Annals of Applied Biology, 155, 1 - 13.
2. Ané J.M., Kiss G.B., Riely B.K., Penmetsa R.V., Oldroyd G.E.D., Ayax C., Lévy J., Debellé F., Baek J.M., Kaló P., Rosenberg C., Roe B.A., Long S.R., Dénarié J., Cook D.R., (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science, 303, 1364 - 1367.
3. Arai M., Hayashi M., Takahashi M., Shimada S., Harada K., (2005) Expression and sequence analysis of systemic regulation gene for symbiosis, NTS1/GmNARK in supernodulating soybean cultivar, Sakukei 4. Breeding Science, 55, 147 - 152.
4. Arrighi J.F., Barré A., Ben Amor B., Bersoult A., Soriano L.C., Mirabella R., De Carvalho-Niebel F., Journet E.-P., Gherardi M., Huguet T., Geurts R., Dénarié J., Rougé P., Gough C., (2006) The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiology, 142, 265 - 279.
5. Atkins C.A., Smith P.M.C., (2007) Translocation in legumes: assimilates, nutrients, and signaling molecules. Plant Physiology, 144, 550 - 561.
6. Bhatia R., (2001) Global impact of induced mutations in plant breeding. In Serving Human Needs: Nuclear Technology for Sustainable Development. Vienna, Austria: International Atomic Energy Agency.
7. Biedermannová E., Novák K., Vondrys J., (2002) Pea mutant Risnod27 as reference line for field assessment of impact of symbiotic nitrogen fixation. Journal of Plant Nutrition, 25, 2051 - 2066.
8. Bohlool B.B., Ladha J.K., Garrity D.P., George T., (1992) Biological nitrogen fixation for sustainable agriculture: a perspective. Plant and Soil, 141, 1 - 11.
9. Borisov A.Y., Danilova T.N., Koroleva T.A., Kuznetsova E.V., Madsen L., Mofett M., Naumkina T.S., Nemankin T.A., Ovchinnikova E.S., Pavlova Z.B., Petrova N.E., Pinaev A.G., Radutoiu S., Rozov S.M., Rychagova T.S., Shtark O.Y., Solovov I.I., Stougaard J., Tikhonovich I.A., Topunov A.F., Tsyganov V.E., Vasilchikov A.G., Voroshilova V.A., Weeden N.F., Zhernakov A.I., Zhukov V.A., (2007) Regulatory genes of garden pea (Pisum sativum L.) controlling the development of nitrogen-fixing nodules and arbuscular mycorrhiza: a review of basic and applied aspects. Applied Biochemistry and Microbiology, 43, 237 - 243.
10. Buzas D.M., Gresshoff P.M., (2007) Short- and long-distance control of root development by LjHAR1 during the juvenile stage of Lotus japonicus. Journal of Plant Physiology, 164, 452 - 459.
11. Caetano-Anollés G., Gresshoff P.M., (1991a) Alfalfa controls nodulation during the onset of Rhizobium-induced cortical cell division. Plant Physiology, 95, 366 - 373.
12. Caetano-Anollés G., Gresshoff P.M., (1991b) Excision of nodules induced by Rhizobium meliloti exopolysaccharide mutants releases autoregulation in alfalfa. Journal of Plant Physiology, 138, 765 - 767.
13. Caetano-Anollés G., Joshi P.A., Gresshoff P.M., (1991a) Spontaneous nodules induce feedback suppression of nodulation in alfalfa. Planta, 183, 77 - 82.
14. Caetano-Anollés G., Paparozzi E.T., Gresshoff P.M., (1991b) Mature nodules and root tips control nodulation in soybean. Journal of Plant Physiology, 137, 389 - 396.
15. Carroll B.J., McNeil D.L., Gresshoff P.M., (1985) Isolation and properties of soybean (Glycine max (L.) Merr.) mutants that nodulate in the presence of high nitrate concentrations. Proceedings of the National Academy of Sciences of the United States of America, 82, 4162 - 4166.
16. Castaings L., Camargo A., Pocholle D., Gaudon V., Texier Y., Boutet-Mercey S., Taconnat L., Renou J.-P., Daniel-Vedele F., Fernandez E., Meyer C., Krapp A., (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. The Plant Journal, 57, 426 - 435.
17. Cebolla A., Vinardell E., Kiss G., Olláh B., Roudier F., Kondorosi A., Kondorosi E., (1999) The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO Journal, 18, 4476 - 4484.
18. Chen C.Y., Fan C., Gao M.Q., Zhu H.Y., (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.
19. Cherr C.M., Scholberg J.M.S., McSorley R., (2006) Green manure approaches to crop production. Agronomy Journal, 98, 302 - 319.
20. Day D.A., Carroll B.J., Delves A.C., Gresshoff P.M., (1989) Relationship between autoregulation and nitrate inhibition of nodulation in soybeans. Physiologia Plantarum, 75, 37 - 42.
21. Delves A.C., Higgins A.V., Gresshoff P.M., (1987) Shoot control of supernodulation in a number of mutant soybeans, Glycine max (L.) Merr. Australian Journal of Plant Physiology, 14, 689 - 694.
22. Delves A.C., Carroll B.J., Gresshoff P.M., (1988) Genetic analysis and complementation studies on a number of mutant supernodulating soybean lines. Journal of Genetics, 67, 1 - 8.
23. Duc G., Messager A., (1989) Mutagenesis of pea (Pisum sativum L.) and the isolation of mutants for nodulation and nitrogen fixation. Plant Science, 60, 207 - 214.
24. Ellis T.H.N., Poyser S.J., Knox M.R., Vershinin A.V., Ambrose M.J., (1998) Polymorphism of insertion sites of Ty1-copia class retrotransposons and its use for linkage and diversity analysis in pea. Molecular and General Genetics, 260, 9 - 19.
25. Engvild K.C., (1987) Nodulation and nitrogen fixation mutants of pea Pisum sativum. Theoretical and Applied Genetics, 74, 711 - 713.
26. Ferguson B.J., Ross J.J., Reid J.B., (2005) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiology, 138, 2396 - 2405.
27. Franssen H.J., Vijn I., Yang W.C., Bisseling T., (1992) Developmental aspects of the Rhizobium-legume symbiosis. Plant Molecular Biology, 19, 89 - 107.
28. Frugoli J., Smith L., Schnabel E., Mukherjee A., Long S., (2008) Regulation of nodule number by multiple genes in Medicago truncatula. In 4th International Congress on Legume Genomics and Genetics, Book of Abstracts, p. 42. Cuernavaca, Mexico: UNAM.
29. Fujikake H., Tamura Y., Ohtake N., Sueyoshi K., Ohyama T., (2003) Photoassimilate partitioning in hypernodulation mutant of soybean (Glycine max (L.) Merr.) NOD1-3 and its parent Williams in relation to nitrate inhibition of nodule growth. Soil Science and Plant Nutrition, 49, 583 - 590.
30. Gelin O., Blixt S., (1964) Root nodulation in peas. Agri Hortique Genetica, 22, 149 - 159.
31. Gleason C., Chaudhuri S., Yang T.B., Munoz A., Poovaiah B.W., Oldroyd G.E.D., (2006) Nodulation independent of rhizobia is induced by a calcium activated kinase lacking autoinhibition. Nature, 441, 1149 - 1152.
32. Gremaud M.F., Harper J.E., (1989) Selection and initial characterization of partially nitrate tolerant nodulation mutants of soybean. Plant Physiology, 89, 169 - 173.
33. Gresshoff P.M., Krotzky A., Mathews A., Day D.A., Schuller K.A., Olsson J., Delves A.C., Carroll B.J., (1988) Suppression of the symbiotic supernodulation symptoms of soybean. Journal of Plant Physiology, 132, 417 - 423.
34. Gualtieri G., Kulikova O., Limpens E., Kim D.J., Cook D.R., Bisseling T., Geurts R., (2002) Microsynteny between pea and Medicago truncatula in the SYM2 region. Plant Molecular Biology, 50, 225 - 235.
35. Guinel F.C., Geil R.D., (2002) A 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 of these two symbioses. Canadian Journal of Botany, 80, 695 - 720.
36. Handberg K., Stougaard J., (1992) Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant Journal, 2, 487 - 496.
37. Hansen A.P., Peoples M.B., Brown P.H., Carroll B.J., Gresshoff P.M., (1990) Nitrogen partitioning during early development of supernodulating soybean (Glycine max [L.] Merrill) mutants and their wild-type parent. Journal of Experimental Botany, 41, 1239 - 1244.
38. 2 fixation in Phaseolus vulgaris L. cv. OAC Rico and a supernodulating mutant. New Phytologist, 122, 611 - 615.
39. Häser A., Robinson D.L., Duc G., Vance C.P., (1992) A mutation in Vicia faba results in ineffective nodules with impaired bacteroid differentiation and reduced synthesis of late nodulins. Journal of Experimental Botamy, 43, 1397 - 1407.
40. 1 hybrids: their different response to, and recovery from rapid or gradual onset of low-temperature stress. Photosynthetica, 41, 429 - 442.
41. Inzé D., De Veylder L., (2006) Cell cycle regulation in plant development. Annual Review of Genetics, 40, 77 - 105.
42. Ishikawa K., Yokota K., Li Y.Y., Wang Y.X., Liu C.-T., Suzuki S., Aono T., Oyaizu H., (2008) Isolation of a novel root-determined hypernodulation mutant rdh1 of Lotus japonicus. Soil Science and Plant Nutrition, 54, 259 - 263.
43. Jacobsen E., Feenstra W.J., (1984) A new pea mutant with efficient nodulation in the presence of nitrate. Plant Science Letters, 33, 337 - 344.
44. Jing R., Johnson R., Seres A., Kiss G., Ambrose M.J., Knox M.R., Ellis T.H.N., Flavell A.J., (2007) Gene-based sequence diversity analysis of field pea (Pisum). Genetics, 177, 2263 - 2275.
45. Kévei Z., Lougnon G., Mergaert P., Horvath G.V., Keresszt A., Jayaraman D., Zaman N., Marcel F., Regulski K., Kiss G.B., Kondorosi A., Endre G., Kondorosi E., Ané J.-M., (2007) 3-Hydroxy-3-methylglutaryl coenzyme A reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. The Plant Cell, 19, 3974 - 3989.
46. Kiers E.T., Rousseau R.A., West S.A., Denison R.F., (2003) Host sanctions and the legume-rhizobium mutualism. Nature, 425, 78 - 81.
47. Kinkema M., Scott P.T., Gresshoff P.M., (2006) Legume nodulation: successful symbiosis through short- and long-distance signalling. Functional Plant Biology, 33, 707 - 721.
48. Kneen B.E., LaRue T.A., Hirsch A.M., Smith C.A., Weeden N.F., (1990) sym-13- a gene conditioning ineffective nodulation in Pisum sativum. Plant Physiology, 94, 899 - 905.
49. Kokubun M., Akao S., (1994) Inheritance of supernodulation in soybean mutant En6500. Soil Science and Plant Nutrition, 40, 715 - 718.
50. Krusell L., Madsen L.H., Sato S., Aubert G., Genua A., Szczyglowski K., Duc G., Kaneko T., Tabata S., De Bruijn F., Pajuelo E., Sandal N., Stougaard J., (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature, 420, 422 - 426.
51. Kuppusamy K.T., Endre G., Prabhu R., Penmetsa R.V., Veereshlingam H., Cook D.R., Dickstein R., VandenBosch K.A., (2004) LIN, a Medicago truncatula gene required for nodule differentiation and persistence of rhizobial infections. Plant Physiology, 136, 3682 - 3691.
52. Kwak S.-H., Shen R., Schiefelbein J., (2005) Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science, 307, 1111 - 1113.
53. Lee H.S., Chae Y.A., Park E.H., Kim Y.W., Yun K.I., Lee S.H., (1997) Introduction, development, and characterization of supernodulating soybean mutant. I. Mutagenesis of soybean and selection of supernodulating mutant. Korean Journal of Crop Science, 42, 247 - 253.
54. Lejeune-Henaut I., Hanocq E., Bethencourt L., Fontaine V., Delbreil B., Morin J., Petit A., Devaux R., Boilleau M., Stempniak J.J., Thomas M., Laine A.L., Foucher F., Baranger A., Burstin J., Rameau C., Giauffret C., (2008) The flowering locus Hr colocalizes with a major QTL affecting winter frost tolerance in Pisum sativum L. Theoretical and Applied Genetics, 116, 1105 - 1116.
55. Lestari P., Van K., Kim M.Y., Lee S.-H., (2006) Nodulation and growth of a supernodulating soybean mutant SS2-2 symbiotically associated with Bradyrhizobium japonicum. Jurnal AgroBiogen, 2, 8 - 15.
56. Li D.X., Kinkema M., Gresshoff P.M., (2009) Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation. Journal of Plant Physiology, 166, 955 - 967.
57. 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, 630 - 633.
58. Magori S., Oka-Kira E., Shibata S., Umehara Y., Kouchi H., Hase Y., Tanaka A., Sato S., Tabata S., Kawaguchi M., (2009) TOO MUCH LOVE, a root regulator associated with the long-distance control of nodulation in Lotus japonicus. Molecular Plant-Microbe Interactions, 22, 259 - 268.
59. 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, 497 - 506.
60. Matsunami T., Kaihatsu A., Maekawa T., Takahashi M., Kokubun M., (2004) Characterization of vegetative growth of a supernodulating soybean genotype, Sakukei 4. Plant Production Science, 7, 165 - 171.
61. McPhee K.E., Muehlbauer F.J., (2001) Biomass production and related characters in the core collection of Pisum germplasm. Genetical Resources and Crop Evolution, 48, 195 - 203.
62. Meixner C., Ludwig-Müller J., Miersch O., Gresshoff P., Staehelin C., Vierheilig H., (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta, 222, 709 - 715.
63. Mirza N.A., Bohlool B.B., Somasegaran P., (1990) Non-destructive chlorophyll assay for screening of strains of Bradyrhizobium japonicum. Soil Biology and Biochemistry, 22, 203 - 207.
64. Morandi D., Sagan M., Prado-Vivant E., Duc G., (2000) Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants. Mycorrhiza, 10, 37 - 42.
65. Murray J., Karas B., Ross L., Brachmann A., Wagg C., Geil R., Perry J., Nowakowski K., MacGillivary M., Held M., Stougaard J., Peterson L., Parniske M., Szczyglowski K., (2006) Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype. Molecular Plant-Microbe Interactions, 19, 1082 - 1091.
66. 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, 101 - 104.
67. Nazaryuk V.M., Sidorova K.K., Shumny V.K., Kalimullina F.R., Klenova M.I., (2006) Physiological and agrochemical properties of different symbiotic genotypes of pea (Pisum sativum L.). Izvestiya Akademii Nauk, Seria Biologicheskaya, 2006, 688 - 697.
68. Nishimura R., Hayashi M., Wu G.-J., Kouchi H., Imaizumi-Anraku H., Murakami Y., Kawasaki S., Akao S., Ohmori M., Nagasawa M., Harada K., Kawaguchi M., (2002a) HAR1 mediates systemic regulation of symbiotic organ development. Nature, 420, 426 - 429.
69. Nishimura R., Ohmori M., Fujita H., Kawaguchi M., (2002b) A Lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation. Proceedings of the National Academy of Sciences of the United States of America, 99, 15206 - 15210.
70. Nishimura R., Ohmori M., Kawaguchi M., (2002c) The novel symbiotic phenotype of enhanced-nodulating mutant of Lotus japonicus: astray mutant is an early nodulating mutant with wider nodulation zone. Plant and Cell Physiology, 43, 853 - 859.
71. Nontachalyapoom S., Scott P.T., Men A.E., Kinkema M., Schenk P.M., Gresshoff P.M., (2007) Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants. Molecular Plant-Microbe Interactions, 20, 769 - 780.
72. Novák K., Škrdleta V., Němcová M., Lisá L., (1993a) Symbiotic traits, growth, and classification of pea nodulation mutants. Rostlinná Výroba, 39, 157 - 170.
73. Novák K., Škrdleta V., Němcová M., Lisá L., (1993b) Behavior of pea nodulation mutants as affected by increasing nitrate level. Symbiosis, 15, 195 - 206.
74. Novák K., Pešina K., Nebesářová J., Škrdleta V., Lisá L., Našinec V., (1995) Symbiotic tissue degradation pattern in the ineffective nodules of three nodulation mutants of pea (Pisum sativum L.). Annals of Botany, 76, 303 - 313.
75. Novák K., Škrdleta V., Kropáčová M., Lisá L., Němcová M., (1997) Interaction of two genes controlling symbiotic nodule number in pea (Pisum sativum L.). Symbiosis, 23, 43 - 62.
76. Novák K., Lisá L., Škrdleta V., (2004) Rhizobial nod gene-inducing activity in pea nodulation mutants: dissociation of nodulation and flavonoid response. Physiologia Plantarum, 120, 546 - 555.
77. Novák K., Biedermannová E., Vondrys J., (2009) Symbiotic and growth performance of supernodulating forage pea lines. Crop Science, 49, 1227 - 1234.
78. Oka-Kira E., Kawaguchi M., (2006) Long-distance signaling to control root nodule number. Current Opinion in Plant Biology, 9, 496 - 502.
79. Oka-Kira E., Tateno K., Miura K., Haga T., Hayashi M., Harada K., Sato S., Tabata S., Shikazono N., Tanaka A., Watanabe Y., Fukuhara I., Nagata T., Kawaguchi M., (2005) klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. Plant Journal, 44, 505 - 515.
80. Okamoto S., Ohnishi E., Sato S., Takahashi H., Nakazono M., Tabata S., Kawaguchi M., (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant and Cell Physiology, 50, 67 - 77.
81. Oldroyd G.E.D., Downie J.A., (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology, 59, 519 - 546.
82. Paau A.S., Leps W.T., Brill W.J., (1985) Regulation of nodulation by Rhizobium meliloti 102F15 on its mutant which forms an unusually high number of nodules on alfalfa. Applied and Environmental Microbiology, 50, 1118 - 1122.
83. Park S.J., Buttery B.R., (1988) Nodulation mutants of white bean (Phaseolus vulgaris L.) induced by ethyl-methane sulphonate. Canadian Journal of Plant Science, 68, 199 - 202.
84. Penmetsa R.V., Cook D.R., (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science, 275, 527 - 530.
85. Penmetsa R.V., Frugoli J.A., Smith L.S., Long S.R., Cook D.R., (2003) Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiology, 131, 998 - 1008.
86. Penmetsa R.V., Uribe P., Anderson J., Lichtenzveig J., Gish J.C., Nam Y.W., Engstrom E., Xu K., Sckisel G., Pereira M., Baek J.M., Lopez-Meyer M., Long S.R., Harrison M.J., Singh K.B., Kiss G.B., Cook D.R., (2008) The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant Journal, 55, 580 - 595.
87. Phillips D.A., (1980) Efficiency of symbiotic nitrogen fixation in legumes. Annual Review of Plant Physiology, 31, 29 - 49.
88. Postma J.G., Jacobsen E., Feenstra W.J., (1988) Three pea mutants with an altered nodulation studied by genetic analysis and grafting. Journal of Plant Physiology, 132, 424 - 430.
89. Provorov N.A., Borisov A.Y., Tikhonovich I.A., (2002) Developmental genetics and evolution of symbiotic structures in nitrogen-fixing nodules and arbuscular mycorrhiza. Journal of Theoretical Biology, 214, 215 - 232.
90. Pyke K.A., Hedley C.L., (1983) Growth and photosynthesis of mutant pea seedlings. Annals of Botany, 52, 719 - 724.
91. Radutoiu S., Madsen L.H., Madsen E.B., Felle H.H., Umehara Y., Gronlund M., Sato S., Nakamura Y., Tabata S., Sandal N., Stougaard J., (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature, 425, 585 - 592.
92. Reid J.B., Murfet I.C., Potts W.C., (1983) Internode length in Pisum. II. Additional information on the relationship and action of loci Le, La, Cry, Na and Lm. Journal of Experimental Botany, 34, 349 - 364.
93. Roché P., Maillet F., Plazanet C., Debellé F., Ferro M., Truchet G., Promé J.-C., Dénarié J., (1996) The common nodABC genes of Rhizobium meliloti are host-range determinants. Proceedings of the National Academy of Sciences of the United States of America, 93, 15305 - 15310.
94. Rosendahl L., Vance C.P., Miller S.S., Jacobsen E., (1989) Nodule physiology of a supernodulating pea mutant. Physiologia Plantarum, 77, 606 - 612.
95. Ruffel S., Freixes S., Balzergue S., Tillard P., Jeudy C., Martin-Magniette M.L., Van der Merwe M.J., Kakar K., Gouzy J., Fernie A.R., Udvardi M., Salon C., Gojon A., Lepetit M., (2008) Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiology, 146, 2020 - 2035.
96. Sagan M., Duc G., (1996) Sym28 and Sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L). Symbiosis, 20, 229 - 245.
97. Sagan M., Gresshoff P.M., (1996) Developmental mapping of nodulation events in pea (Pisum sativum L.) using supernodulating plant genotypes and bacterial variability reveals both plant and Rhizobium control of nodulation regulation. Plant Science, 117, 167 - 179.
98. Sagan M., Ney B., Duc G., (1993) Plant symbiotic mutants as a tool to analyze nitrogen nutrition and yield relationship in field-grown peas (Pisum sativum L.). Plant and Soil, 153, 33 - 45.
99. Sagan M., Huguet T., Duc G., (1994) Phenotypic characterization and classification of nodulation mutants of pea (Pisum sativum L.). Plant Science, 100, 59 - 70.
100. Sagan M., Morandi D., Tarenghi E., Duc G., (1995) Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after gamma-ray mutagenesis. Plant Science, 111, 63 - 71.
101. Schnabel E., Journet E.P., De Carvalho-Niebel F., Duc G., Frugoli J., (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Molecular Biology, 58, 809 - 822.
102. Schneider A., Walker S.A., Sagan M., Duc G., Ellis T.H.N., Downie J.A., (2002) Mapping of the nodulation loci sym9 and sym10 of pea (Pisum sativum L.). Theoretical and Applied Genetics, 104, 1312 - 1316.
103. Searle I.R., Men A.E., Laniya T.S., Buzas D.M., Iturbe-Ormaetxe I., Carroll B.J., Gresshoff P.M., (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science, 299, 109 - 112.
104. Sidorova K.K., Shumnyi V.K., (1998) Analysis of pea (Pisum sativum L.) supernodulating mutants. Genetika, 34, 1452 - 1454.
105. Sidorova K.K., Shumnyi V.K., (2003) A collection of symbiotic mutants in pea Pisum sativum L.: creation and genetic study. Russian Journal of Genetics, 39, 406 - 413.
106. Sidorova K.K., Shumnyi V.K., Glianenko M.N., Mischenko T.M., Vlasova E.Y., Gaeva T.A., (2005) Expression of the symbiotic nod4 pea gene against various genotypic backgrounds. Russian Journal of Genetics, 41, 533 - 538.
107. Škrdleta V., Novák K., Lisá L., (1994) Comparison of two Pisum sativum nodulation mutants with their parental cultivar. Biologia Plantarum, 36, 435 - 441.
108. Spaink H.P., (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annual Review of Microbiology, 54, 257 - 288.
109. Sprent J.I., (2008) Evolution and diversity of legume symbiosis. In Nitrogen-Fixing Leguminous Symbioses, pp. 1 - 21. Eds, M.J. Dilworth, E.K. James, J.I. Sprent, and, W.E. Newton,. Dordrecht, The Netherlands: Springer.
110. Sprent J.I., James E.K., (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiology, 144, 575 - 581.
111. Stracke S., Kistner C., Yoshida S., Mulder L., Sato S., Kaneko T., Tabata S., Sandal N., Stougaard J., Szczyglowski K., Parniske M., (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature, 417, 959 - 962.
112. 2 fixation by nitrate. CRC Critical Reviews in Plant Sciences, 7, 1 - 23.
113. Studer D., Gloudemans T., Franssen H.J., Fischer H.-M., Bisseling T., Hennecke H., (1987) Involvement of the bacterial nitrogen fixation regulatory gene (nifA) in control of nodule-specific host-plant gene expression. European Journal of Cell Biology, 45, 177 - 184.
114. Takahashi M., Arihara J., Nakayama N., Kokubun M., (2003) Characteristics of growth and yield formation in the improved genotype of supernodulating soybean (Glycine max L. Merr.). Plant Production Science, 6, 112 - 118.
115. Teillet A., Garcia J., De Billy F., Gherardi M., Huguet T., Barker D.G., De Carvalho-Niebel F., Journet E.-P., (2008) api, a novel Medicago truncatula symbiotic mutant impaired in nodule primordium invasion. Molecular Plant-Microbe Interactions, 21, 535 - 546.
116. Tirichine L., Sandal N., Madsen L.H., Radutoiu S., Albrektsen A.S., Sato S., Asamizu E., Tabata S., Stougaard J., (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science, 315, 104 - 107.
117. Tsyganov V.E., Voroshilova V.A., Priefer U.B., Borisov A.Y., Tikhonovich I.A., (2002) Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobium-pea (Pisum sativum L.) symbiosis. Annals of Botany, 89, 357 - 366.
118. Untergasser A., Hartly M., Bisseling T., Geurts R., (2008) Transferring eight key regulators required for Nod factor signalling to non-legumes. In 8th European Nitrogen Fixation Conference, Abstract Book, p. 48. Ghent, Belgium: University of Ghent.
119. Van de Velde W., Guerra J.C.P., De Keyser A., De Rycke R., Rombauts S., Maunoury N., Mergaert P., Kondorosi E., Holsters M., Goormachtig S., (2006) Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiology, 141, 711 - 720.
120. Van de Wiel C., Scheres B., Franssen H., Van Lierop M.-J., Van Lammeren A., Van Kammen A., Bisseling T., (1990) The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO Journal, 9, 1 - 7.
121. 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 defense-like response. Plant Physiology, 136, 3692 - 3702.
122. Vernié T., Moreau S., De Billy F., Plet J., Combier J.-P., Rogers C., Oldroyd G., Frugier F., Niebel A., Gamas P., (2008) EFD is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. The Plant Cell, 20, 2696 - 2713.
123. Voisin A.S., Bourion B., Duc G., Salon C., (2007) Using an ecophysiological analysis to dissect genetic variability and to propose an ideotype for nitrogen nutrition in pea. Annals of Botany, 100, 1525 - 1536.
124. Voroshilova V.A., Demchenko K.N., Brewin N.J., Borisov A.Y., Tikhonovich I.A., (2009) Initiation of a legume nodule with an indeterminate meristem involves proliferating host cells that harbour infection threads. New Phytologist, 181, 913 - 923.
125. Weeden N.F., Kneen B.E., LaRue T.A., (1990) Genetic analysis of sym genes and other nodule related genes in Pisum sativum. In Nitrogen Fixation: Achievements and Objectives, pp. 323 - 330. Eds, P.M. Gresshoff, L.E. Roth, G. Stacey, and, W.E. Newton,. New York: Chapman and Hall.
126. Willems A., (2006) The taxonomy of rhizobia: an overview. Plant and Soil, 287, 3 - 14.
127. Wopereis J., Pajuelo E., Dazzo F.B., Jiang Q.Y., Gresshoff P.M., De Bruijn F.J., Stougaard J., Szczyglowski K., (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant Journal, 23, 97 - 114.
128. Wu S.C., Harper J.E., (1990) Nitrogen fixation of nodulation mutants of soybean as affected by nitrate. Plant Physiology, 92, 1142 - 1147.
129. Yokota K., Li Y.Y., Hisatomi M., Wang Y.X., Ishikawa K., Liu C.T., Suzuki S., Aonuma K., Aono T., Nakamoto T., Oyaizu H., (2009) Root-determined hypernodulation mutant of Lotus japonicus shows high-yielding characteristics. Bioscience, Biotechnology and Biochemistry, 73, 1690 - 1692.
130. Zhang C., Taran B., Warkentin T.D., Tullu A., Bett K.E., Vandenberg A., Somers D.J., (2006) Selection for lodging resistance in early generations of field pea by molecular markers. Crop Science, 46, 321 - 329.