Agronomy for Sustainable Development

, Volume 32, Issue 1, pp 65–91 | Cite as

Legumes in the reclamation of marginal soils, from cultivar and inoculant selection to transgenic approaches

  • Teodoro Coba de la Peña
  • José J. PueyoEmail author
Review Paper


Mineral nitrogen deficiency is a frequent characteristic of arid and semi-arid soils. Biological nitrogen fixation by legumes is a sustainable and environmental-friendly alternative to chemical fertilization. Therefore, legumes have a high potential for the reclamation of marginal soils. Such issue is becoming more urgent due to the ever-rising requirement for food and feed, and the increasing extension of salinized and degraded lands, both as a consequence of global change and irrigation practices. This manuscript reviews current research on physiological and molecular mechanisms involved in the response and tolerance to environmental stresses of the Rhizobium–legume symbiosis. We report in particular recent advances on the isolation, characterization, and selection of tolerant rhizobial strains and legume varieties, both by traditional methods and through biotechnological approaches. The major points are the following. (1) Understanding mechanisms involved in stress tolerance is advancing fast, thus providing a solid basis for the selection and engineering of rhizobia and legumes with enhanced tolerance to environmental constraints. (2) The considerable efforts to select locally adapted legume varieties and rhizobial inocula that can fix nitrogen under conditions of drought or salinity are generating competitive crop yields in affected soils. (3) Biotechnological approaches are used to obtain improved legumes and rhizobia with enhanced tolerance to abiotic stresses, paying particular attention to the sensitive nitrogen-fixing activity. Those biotechnologies are yielding transgenic crops and inocula with unquestionable potential. In conclusion, the role of legumes in sustainable agriculture, and particularly, their use in the reclamation of marginal lands, certainly has a very promising future.


Legume Rhizobium Soil Nitrogen fixation Nodule Stress Salinity Drought 



This work was supported by grants from the Spanish Ministry of Science and Innovation, the Comunidad de Madrid, the Junta de Comunidades de Castilla-La Mancha and the Fundación Ramón Areces.


  1. Acuna H, Inostroza L, Sanchez MP, Tapia G (2010) Drought-tolerant naturalized populations of Lotus tenuis for constrained environments. Acta Agric Scand B Soil Plant Sci 60:174–181. doi: 10.1080/09064710902800224 Google Scholar
  2. Adjei-Nsiah S, Kuyper TW, Leeuwis C, Abekoe MK, Giller KE (2007) Evaluating sustainable and profitable cropping sequences with cassava and four legume crops: effects on soil fertility and maize yields in the forest/savannah transitional agro-ecological zone of Ghana. Field Crop Res 103:87–97. doi: 10.1016/j.fcr.2007.05.001 CrossRefGoogle Scholar
  3. Ahmad P, Jhon R (2005) Effect of salt stress on growth and biochemical parameters of Pisum sativum L. Arch Agron Soil Sci 51:665–672. doi: 10.1080/03650340500274151 CrossRefGoogle Scholar
  4. Albareda M, Rodríguez-Navarro DN, Temprano FJ (2009) Use of Sinorhizobium (Ensifer) fredii for soybean inoculants in South Spain. Eur J Agron 30:205–211. doi: 10.1016/j.eja.2008.10.002 CrossRefGoogle Scholar
  5. Alegre J, Alonso-Blazquez N, de Andrés EF, Tenorio JL, Eyerbe L (2004) Revegetation and reclamation of soils using wild leguminous shrubs in cold semiarid Mediterranean conditions: litterfall and carbon and nitrogen returns under two aridity regimes. Plant Soil 263:203–212. doi: 10.1023/B:PLSO.0000047735.73030.41 CrossRefGoogle Scholar
  6. Allen ON, Allen EK (1991) The leguminosae: a source book of characteristics, uses and nodulation. University of Wisconsin Press, MadisonGoogle Scholar
  7. Alloing G, Travers I, Sagot B, Le Rudulier D, Dupont L (2006) Proline betaine uptake in Sinorhizobium meliloti: characterization of Prb, an Opp-like ABC transporter regulated by both proline betaine and salinity stress. J Bacteriol 188:6308–6317. doi: 10.1128/JB.00585-06 PubMedCrossRefGoogle Scholar
  8. Annicchiarico P, Iannucci A (2007) Winter survival of pea, faba bean and white lupin cultivars in contrasting Italian locations and sowing times, and implications for selection. J Agric Sci 145:611–622. doi: 10.1017/S0021859607007289 CrossRefGoogle Scholar
  9. Aouani ME, Mhamdi R, Mars M, Elayeb M, Ghrir R (1997) Potential for inoculation of common bean by effective rhizobia in Tunisian soils. Agronomie 17:445–454. doi: 10.1051/agro:19970902 CrossRefGoogle Scholar
  10. Arenas-Huertero C, Perez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sánchez F, Covarrubias AA, Reyes JL (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401. doi: 10.1007/s11103-009-9480-3 PubMedCrossRefGoogle Scholar
  11. Arrese-Igor C, González EM, Gordon AJ, Minchin FR, Galvez L, Royuela M, Cabrerizo PM, Aparicio-Tejo PM (1999) Sucrose synthase and nodule nitrogen fixation under drought and other environmental stresses. Symbiosis 27:189–212Google Scholar
  12. Ashraf M (1994) Organic-substances responsible for salt tolerance in Eruca sativa. Biol Plant 36:255–259. doi: 10.1007/BF02921095 CrossRefGoogle Scholar
  13. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93. doi: 10.1016/j.biotechadv.2008.09.003 PubMedCrossRefGoogle Scholar
  14. Ashraf M, Waheed A (1993) Responses of some genetically diverse lines of chick pea (Cicer arietinum L.) to salt. Plant Soil 154:257–266. doi: 10.1007/BF00012531 CrossRefGoogle Scholar
  15. Aydi S, Drevon JJ, Abdelly C (2004) Effect of salinity on root-nodule conductance to the oxygen diffusion in the Medicago truncatulaSinorhizobium meliloti symbiosis. Plant Physiol Biochem 42:833–840. doi: 10.1016/j.plaphy.2004.10.003 PubMedCrossRefGoogle Scholar
  16. Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soils 45:405–413. doi: 10.1007/s00374-008-0344-9 CrossRefGoogle Scholar
  17. Bao AKB, Wang S-M, Wu G-Q, Xi J-J, Zhang J-L, Wang CM (2009) Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant Sci 176:232–240. doi: 10.1016/j.plantsci.2008.10.009 CrossRefGoogle Scholar
  18. Báscones E, Imperial J, Ruiz-Argüeso T, Palacios JM (2000) Generation of new hydrogen-recycling Rhizobiaceae strains by introduction of a novel hup minitransposon. Appl Environ Microbiol 66:4292–4299PubMedCrossRefGoogle Scholar
  19. Bastiat B, Sauviac L, Bruand C (2010) Dual control of Sinorhizobium meliloti RpoE Sigma factor activity by two PhyR-type two-component response regulators. J Bacteriol 192:2255–2265. doi: 10.1128/JB.01666-09 PubMedCrossRefGoogle Scholar
  20. Bayuelo-Jimenez JS, Debouck DG, Lynch JP (2003) Growth, gas exchange, water relations, and ion composition of Phaseolus species grown under saline conditions. Field Crop Res 80:207–222. doi: 10.1016/S0378-4290(02)00179-X CrossRefGoogle Scholar
  21. Becana M, Moran JF, Iturbe-Ormaetxe I (1998) Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection. Plant Soil 201:137–147. doi: 10.1023/A:1004375732137 CrossRefGoogle Scholar
  22. Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC (2000) Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381. doi: 10.1034/j.1399-3054.2000.100402.x CrossRefGoogle Scholar
  23. Ben Rebah F, Prevost D, Yezza A, Tyagi RD (2007) Agro-industrial waste materials and wastewater sludge for rhizobial inoculant production: a review. Bioresour Technol 98:3535–3546. doi: 10.1016/j.biortech.2006.11.066 PubMedCrossRefGoogle Scholar
  24. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao PX, Tang Y, Udvardi MK (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55:504–513. doi: 10.1111/j.1365-313X.2008.03519.x PubMedCrossRefGoogle Scholar
  25. Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209. doi: 10.1007/s00253-008-1567-2 PubMedCrossRefGoogle Scholar
  26. Bhattacharya I, Das HR (2003) Cell surface characteristics of two halotolerant strains of Sinorhizobium meliloti. Microbiol Res 158:187–194. doi: 10.1078/0944-5013-00195 PubMedCrossRefGoogle Scholar
  27. Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107. doi: 10.1093/jxb/erp140 PubMedCrossRefGoogle Scholar
  28. Binde DR, Menna P, Bangel EV, Barcellos FG, Hungria M (2009) rep-PCR fingerprinting and taxonomy based on the sequencing of the 16S RNA gene of 54 elite commercial rhizobial strains. Appl Microbiol Biotechnol 83:897–908. doi: 10.1007/s00253-009-1927-6 PubMedCrossRefGoogle Scholar
  29. Biswas JC, Ladha JK, Dazzo FB (2000a) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650CrossRefGoogle Scholar
  30. Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolfe BG (2000b) Rhizobial inoculation influences seedling vigor and yield of rice. Agron J 92:880–886CrossRefGoogle Scholar
  31. Blanco AR, Sicardi M, Frioni L (2010) Competition for nodule occupancy between introduced and native strains of Rhizobium leguminoarum biovar trifolii. Biol Fertil Soils 46:419–425. doi: 10.1007/s00374-010-0439-y CrossRefGoogle Scholar
  32. Boddey RM, Döbereiner J (1982) Association of Azospirillum and other diazotrophs with tropical gramineae. In: Non symbiotic nitrogen fixation and organic matter in the tropics. Transactions of the 12th International Congress of Soil Science. New Delhi, India, Symposia Papers 1, pp 28–47Google Scholar
  33. Boddey RM, Polidoro JC, Resende AS, Alves BJR, Urquiaga S (2001) Use of the 15N natural abundance technique for the quantification of the contribution of N2 fixation to sugar cane and other grasses. Aust J Plant Physiol 28:889–895. doi: 10.1071/PP01058 Google Scholar
  34. Boddey RM, Urquiaga S, Alves BJR, Reis V (2003) Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252:139–149. doi: 10.1023/A:1024152126541 CrossRefGoogle Scholar
  35. Bohlool BB, Ladha JK, Garrity DP, George T (1992) Biological nitrogen fixation for sustainable agriculture: a perspective. Plant Soil 141:1–11. doi: 10.1007/BF00011307 CrossRefGoogle Scholar
  36. Boiero L, Perrig D, Masciarelli O, Penna C, Cassan F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880. doi: 10.1007/s00253-006-0731-9 PubMedCrossRefGoogle Scholar
  37. Boncompagni E, Osteras M, Poggi MC, Le Rudulier D (1999) Occurrence of choline and glycine betaine uptake and metabolism in the family Rhizobiaceae and their roles in osmoprotection. Appl Environ Microbiol 65:2072–2077PubMedGoogle Scholar
  38. Borucki W, Sujkowska M (2008) The effects of sodium chloride-salinity upon growth, nodulation, and root nodule structure of pea (Pisum sativum L.) plants. Acta Physiol Plant 30:293–301. doi: 10.1007/s11738-007-0120-8 CrossRefGoogle Scholar
  39. Boscari A, Van de Sype G, Le Rudulier D, Mandon K (2006) Overexpression of BetS, a Sinorhizobium meliloti high-affinity betaine transporter, in bacteroids from Medicago sativa nodules sustains nitrogen fixation during early salt stress adaptation. Mol Plant-Microbe Interact 19:896–903. doi: 10.1094/MPMI-19-0896 PubMedCrossRefGoogle Scholar
  40. Bosworth AH, Williams MK, Albrecht KA, Kwiatkowski R, Beynon J, Hankinson TR, Ronson CW, Cannon F, Wacek TJ, Triplett EW (1994) Alfalfa yield response to inoculation with recombinant strains of Rhizobium meliloti with an extra copy of dctABD and/or modified nifA expression. Appl Environ Microbiol 60:3815–3832PubMedGoogle Scholar
  41. Botsford JL, Lewis TA (1990) Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress. Appl Environ Microbiol 56:488–494PubMedGoogle Scholar
  42. Bouhmouch I, Brhada F, Filali-Maltouf A, Aurag J (2001) Selection of osmotolerant and effective strains of Rhizobiaceae for inoculation of common bean (Phaseolus vulgaris) in Moroccan saline soils. Agronomie 21:591–599. doi: 10.1051/agro:2001149 CrossRefGoogle Scholar
  43. Breedveld MW, Zevenhuizen LPTM, Zehnder AJB (1991) Osmotically induced oligo and polysaccharide synthesis by Rhizobium meliloti SU-47. J Gen Microbiol 136:2511–2519Google Scholar
  44. Breedveld MW, Dijkema C, Zevenhuizen PTM, Zehnder AJB (1993) Response of intracellular carbohydrates to a NaCl shock in Rhizobium leguminosarum bv. trifolii TA-1 and Rhizobium meliloti SU-47. J Gen Microbiol 139:3157–3163Google Scholar
  45. Brewin NJ (1991) Development of legume root nodules. Annu Rev Cell Biol 7:191–226. doi: 10.1146/annurev.cb.07.110191.001203 PubMedCrossRefGoogle Scholar
  46. Brigido C, Alexandre A, Laranjo M, Oliveira S (2007) Moderately acidophilic mesorhizobia isolated from chickpea. Lett Appl Microbiol 44:168–174. doi: 10.1111/j.1472-765X.2006.02061.x PubMedCrossRefGoogle Scholar
  47. Brockwell J, Bottomley PJ (1995) Recent advances in inoculant technology and prospects for the future. Soil Biol Biochem 27:683–697. doi: 10.1016/0038-0717(95)98649-9 CrossRefGoogle Scholar
  48. Brophy LS, Heichel GH (1989) Nitrogen release from roots of alfalfa and soybean grown in sand culture. Plant Soil 116:77–84. doi: 10.1007/BF02327259 CrossRefGoogle Scholar
  49. Busse MD, Bottomley PJ (1989) Growth and nodulation responses of Rhizobium meliloti to water stress induced by permeating and nonpermeating solutes. Appl Environ Microbiol 55:2431–2436PubMedGoogle Scholar
  50. Cabot C, Sibole JV, Barceló J, Poschenrieder C (2009) Abscisic acid decreases leaf Na+ exclusion in salt-treated Phaseolus vulgaris L. J Plant Growth Regul 28:187–192. doi: 10.1007/s00344-009-9088-5 CrossRefGoogle Scholar
  51. Camerini S, Senatore B, Lonardo E, Imperlini E, Bianco C, Moschetti G, Rotino GL, Campion B, Defez R (2008) Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development. Arch Microbiol 190:67–77. doi: 10.1007/s00203-008-0365-7 PubMedCrossRefGoogle Scholar
  52. Campbell GR, Sharypova LA, Scheidle H, Jones KM, Niehaus K, Becker A, Walker GC (2003) Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants. J Bacteriol 185:3853–3862. doi: 10.1128/JB.185.13.3853-3862.2003 PubMedCrossRefGoogle Scholar
  53. Caravaca F, Alguacil MM, Figueroa D, Barea JM, Roldán A (2003) Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semi-arid Mediterranean area. For Ecol Manage 182:49–58. doi: 10.1016/S0378-1127(03)00067-7 CrossRefGoogle Scholar
  54. Castillo M, Flores M, Mavingui P, Martínez-Romero E, Palacios R, Hernández G (1999) Increase in the alfalfa nodulation, nitrogen fixation and plant growth by specific DNA amplification in Sinorhizobium meliloti. Appl Environ Microbiol 65:2716–2722PubMedGoogle Scholar
  55. Chandra A (2009) Diversity among Stylosanthes species: habitat, edaphic and agro-climatic affinities leading to cultivar development. J Environ Biol 30:471–478PubMedGoogle Scholar
  56. Chang C, Damiani I, Puppo A, Frendo P (2009) Redox changes during the legume–Rhizobium symbiosis. Mol Plant 2:370–377. doi: 10.1093/mp/ssn090 PubMedCrossRefGoogle Scholar
  57. Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257. doi: 10.1016/S1369-5266(02)00255-8 PubMedCrossRefGoogle Scholar
  58. Chen H, Richardson AE, Gartner E, Djordjevic MA, Roughley RJ, Rolfe BG (1991) Construction of an acid-tolerant Rhizobium leguminosarum biovar trifolii strain with enhanced capacity for nitrogen fixation. Appl Environ Microbiol 57:2005–2011PubMedGoogle Scholar
  59. Chen D, Liang MX, DeWald D, Weimer B, Peel MD, Bugbee B, Michaelson J, Davis E, Wu Y (2008) Identification of dehydration responsive genes from two non-nodulated alfalfa cultivars using Medicago truncatula microarrays. Acta Physiol Plant 30:183–199. doi: 10.1007/s11738-007-0107-5 CrossRefGoogle Scholar
  60. Chernyad’ev II (2009) The protective action of cytokinins on the photosynthetic machinery and productivity of plants under stress. Appl Biochem Microbiol 45:351–362. doi: 10.1134/S0003683809040012 CrossRefGoogle Scholar
  61. Chianu JN, Nkonya EM, Mairura FS, Chianu JN, Akinnifesi FK (2010) Biological nitrogen fixation and socioeconomic factors for legume production in sub-Saharan Africa: a review. Agron Sustain Dev. doi: 10.1051/agro/2010004, in pressGoogle Scholar
  62. Clark IM, Mendum TA, Hirsch PR (2002) The influence of the symbiotic plasmid pRL1JI on the distribution of GM rhizobia in soil and crop rhizospheres, and implications for gene flow. Antonie Leeuwenhoek 81:607–616. doi: 10.1023/A:1020574009445 PubMedCrossRefGoogle Scholar
  63. Coba de la Peña T, Verdoy D, Redondo FJ, Pueyo JJ (2003) Salt tolerance in the Rhizobium–legume symbiosis: an overview. In: Pandalai SG (ed) Recent research developments in plant molecular biology 1. Research Signpost, Trivandrum, pp 187–205Google Scholar
  64. Coba de la Peña T, Cárcamo CB, Almonacid L, Zaballos A, Lucas MM, Balomenos D, Pueyo JJ (2008a) A salt stress-responsive cytokinin receptor homologue isolated from Medicago sativa nodules. Planta 227:769–779. doi: 10.1007/s00425-007-0655-3 PubMedCrossRefGoogle Scholar
  65. Coba de la Peña T, Cárcamo CB, Almonacid L, Zaballos A, Lucas MM, Balomenos D, Pueyo JJ (2008b) A cytokinin receptor homologue is induced during root nodule organogenesis and senescence in Lupinus albus L. Plant Physiol Biochem 46:219–225. doi: 10.1016/j.plaphy.2007.10.021 CrossRefGoogle Scholar
  66. Coba de la Peña T, Cárcamo CB, Lucas MM, Pueyo JJ (2008c) Multiple roles for cytokinin receptors and cross-talk of signalling pathways. Plant Signal Behav 3:791–794PubMedCrossRefGoogle Scholar
  67. Coba de la Peña T, Redondo FJ, Manrique E, Lucas MM, Pueyo JJ (2010) Nitrogen fixation persists under conditions of salt stress in transgenic Medicago truncatula plants expressing a cyanobacterial flavodoxin. J Plant Biotechnol 8:954–965. doi: 10.1111/j.1467-7652.2010.00519.x Google Scholar
  68. Cock PS (1992) Plant attributes leading to persistence in grazed annual medics (Medicago spp.) growing in rotation with wheat. Aust J Agric Res 43:1559–1570. doi: 10.1071/AR9921559 CrossRefGoogle Scholar
  69. Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365. doi: 10.1111/j.1365-2672.2007.03366.x PubMedCrossRefGoogle Scholar
  70. Cordovilla MP, Ligero F, Lluch C (1999) Effect of salinity on growth, nodulation and nitrogen assimilation in nodules of faba bean (Vicia faba L.). Appl Soil Ecol 11:1–7. doi: 10.1016/S0929-1393(98)00132-2 CrossRefGoogle Scholar
  71. Dakora FD, Keya SO (1997) Contribution of legume nitrogen fixation to sustainable agriculture in Sub-Saharan Africa. Soil Biol Biochem 29:809–817. doi: 10.1016/S0038-0717(96)00225-8 CrossRefGoogle Scholar
  72. Dalton DA, Russel SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci USA 83:3811–3815PubMedCrossRefGoogle Scholar
  73. Dalton DA, Post CJ, Langeberg L (1991) Effects of ambient oxygen and of fixed nitrogen on concentrations of glutathione, ascorbate, and associated enzymes in soybean root-nodules. Plant Physiol 96:812–818. doi: 10.1104/pp.96.3.812 PubMedCrossRefGoogle Scholar
  74. Dalton DA, Langeberg L, Robbins M (1992) Purification and characterization of monodehydroascorbate reductase from soybean root nodules. Arch Biochem Biophys 292:281–286. doi: 10.1016/0003-9861(92)90080-G PubMedCrossRefGoogle Scholar
  75. Dalton DA, Langeberg L, Treneman NC (1993) Correlations between the ascorbate-glutathione pathway and effectiveness in legume root-nodules. Physiol Plant 87:365–370. doi: 10.1111/j.1399-3054.1993.tb01743.x CrossRefGoogle Scholar
  76. Danga BO, Ouma JP, Wakindiki IIC, Bar-Tal A (2009) Legume-wheat rotation effects on residual soil moisture, nitrogen and wheat yield in tropical regions. Adv Agronom 101:315–349. doi: 10.1016/S0065-2113(08)00805-5 CrossRefGoogle Scholar
  77. Davies MJ, Puppo A (1992) Direct detection of a globin-derived radical in lehaemoglobin treated with peroxides. Biochem J 281:197–201PubMedGoogle Scholar
  78. de Andrés F, Walter I, Tenorio JL (2007) Revegetation of abandoned agricultural land amended with biosolids. Sci Total Environ 378:81–83. doi: 10.1016/j.scitotenv.2007.01.017 PubMedCrossRefGoogle Scholar
  79. Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology—a review. Soil Biol Biochem 36:1275–1288. doi: 10.1016/j.soilbio.2004.04.009 CrossRefGoogle Scholar
  80. Delauney A, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223. doi: 10.1046/j.1365-313X.1993.04020215.x CrossRefGoogle Scholar
  81. Delgado MJ, Ligero F, Lluch C (1994) Effects of salt stress on growth and nitrogen-fixation by pea, faba-bean, common bean and soybean plants. Soil Biol Biochem 26:371–376. doi: 10.1016/0038-071(94)90286-0 CrossRefGoogle Scholar
  82. Ding H, Hynes MF (2009) Plasmid transfer system in the rhizobia. Can J Microbiol 55:917–927. doi: 10.1139/W09-056 PubMedCrossRefGoogle Scholar
  83. Dita MA, Rispail N, Prats E, Rubiales D, Singh KB (2006) Biotechnology approaches to overcome biotic and abiotic stress constraints in legumes. Euphytica 147:1–24. doi: 10.1007/s10681-006-6156-9 CrossRefGoogle Scholar
  84. Djekoun A, Planchon C (1991) Water status effect on dinitrogen fixation and photosynthesis in soybean. Agron J 83:316–322CrossRefGoogle Scholar
  85. Dominguez-Ferreras A, Perez-Arnedo R, Becker A, Olivares J, Soto MJ, Sanjuan J (2006) Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti. J Bacteriol 188:7617–7625. doi: 10.1128/JB.00719-06 PubMedCrossRefGoogle Scholar
  86. Duan J, Müller KM, Charles TC, Vesely S, Glick BR (2009) 1-aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from southern Saskatchewan. Microb Ecol 57:423–436. doi: 10.1007/s00248-008-9407-6 PubMedCrossRefGoogle Scholar
  87. Eapen S (2008) Advances in development of transgenic pulse crops. Biotechnol Adv 26:162–168. doi: 10.1016/j.biotechadv.2007.11.001 PubMedCrossRefGoogle Scholar
  88. Egener T, Hurek T, Reinhold-Hurek B (1999) Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots. Mol Plant-Microbe Interact 12:813–819. doi: 10.1094/MPMI.1999.12.9.813 CrossRefGoogle Scholar
  89. El-Akhal MR, Rincón A, Arenal F, Lucas MM, El MN, Barrijal S, Pueyo JJ (2008) Genetic diversity and symbiotic efficiency of rhizobial isolates obtained from nodules of Arachis hypogaea in northwestern Morocco. Soil Biol Biochem 40:2911–2914. doi: 10.1016/j.soilbio.2008.08.005 CrossRefGoogle Scholar
  90. El-Akhal MR, Rincón A, El MN, Pueyo JJ, Barrijal S (2009) Phenotypic and genotypic characterization of rhizobia isolated from root nodules of peanut (Arachis hypogaea L.) grown in Moroccan soils. J Basic Microbiol 49:415–425. doi: 10.1002/jobm.200800359 PubMedCrossRefGoogle Scholar
  91. Elboutahiri N, Thami-alami I, Zaid E, Udupa SM (2009) Genotypic characterization of indigenous Sinorhizobium meliloti and Rhizobium sullae by rep-PCR, RAPD and ARDRA analyses. Afr J Biotechnol 8:979–985Google Scholar
  92. Elboutahiri N, Thami-Alami I, Udupa SM (2010) Phenotypic and genetic diversity in Sinorhizobium meliloti and S. medicae from drought and salt affected regions of Morocco. BMC Microbiol 10:15. doi: 10.1186/1471-2180-10-15 PubMedCrossRefGoogle Scholar
  93. El-Saidi MT, Ali AMM (1993) Towards the rational use of high salinity tolerant plants, vol. 2. In: Leith H, Al-Masoo A (eds). Towards the rational use of high salinity tolerant plants 2. Kluwer Academic, Netherlands, pp 59–65Google Scholar
  94. El-Sheikh EAE, Wood M (1990) Salt effects on survival and multiplication of chickpea and soybean rhizobia. Soil Biol Biochem 22:343–347. doi: 10.1016/0038-0717(90)90111C CrossRefGoogle Scholar
  95. Erdner DL, Price NM, Doucette GJ, Peleato ML, Anderson DM (1999) Characterization of ferredoxin and flavodoxin as markers of iron limitation in marine phytoplankton. Mar Ecol Prog Ser 184:43–53. doi: 10.3354/meps184043 CrossRefGoogle Scholar
  96. Essendoubi M, Brhada F, Elijamali JE, Filali-Maltouf A, Bonnassie S, Georgeault S, Blanco C, Jebbar M (2007) Osmoadaptative responses in the rhizobia nodulating Acacia isolated from Southeastern Moroccan Sahara. Environ Microbiol 9:603–611. doi: 10.1111/j.1462-2920.2006.01176.x PubMedCrossRefGoogle Scholar
  97. Evans J (2005) An evaluation of potential Rhizobium inoculant strains used for pulse production in acidic soils of south-east Australia. Aust J Exp Agric 45:257–268. doi: 10.1071/EA03129 CrossRefGoogle Scholar
  98. Evans PJ, Gallesi D, Mathieu C, Hernández MJ, De Felipe M, Halliwell B, Puppo A (1999) Oxidative stress occurs during soybean nodule senescence. Planta 208:73–79. doi: 10.1007/s004250050536 CrossRefGoogle Scholar
  99. Fedorova E, Redondo FJ, Koshiba T, Pueyo JJ, De Felipe MR, Lucas MM (2005) Aldehyde oxidase (AO) in the root nodules of Lupinus albus and Medicago truncatula: identification of AO in meristematic and infection zones. Mol Plant-Microbe Interact 18:405–413. doi: 10.1094/MPMI-18-0405 PubMedCrossRefGoogle Scholar
  100. Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72. doi: 10.1007/s00344-003-0032-9 CrossRefGoogle Scholar
  101. Fernández-Pascual M, De Lorenzo C, De Felipe MR, Rajalakshmi S, Gordon AJ, Thomas BJ, Minchin FR (1996) Possible reasons for relative salt stress tolerance in nodules of white lupin cv. Multolupa. J Exp Bot 47:1709–1716. doi: 10.1093/jxb/47.11.1709 CrossRefGoogle Scholar
  102. Fougère F, Le Rudulier D (1990) Uptake of glycine betaine and its analogues by bacteroids of Rhizobium meliloti. J Gen Microbiol 136:157–163PubMedGoogle Scholar
  103. Fougère F, Le Rudulier D, Streeter JG (1991) Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol 96:1228–1236. doi: 10.1104/pp.96.4.1228 PubMedCrossRefGoogle Scholar
  104. Foyer CH, Graham N (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905. doi: 10.1089/ars.2008.2177 PubMedCrossRefGoogle Scholar
  105. Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59. doi: 10.1007/s11104-008-9833-8 CrossRefGoogle Scholar
  106. Franco AA, De Faria SM (1997) The contribution of nitrogen-fixing tree legumes to land reclamation and sustainability in the tropics. Soil Biol Biochem 29:897–903. doi: 10.1016/S0038-0717(96)00229-5 CrossRefGoogle Scholar
  107. Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the Rhizobium–legume symbiosis. Eur J Biochem 270:1365–1380. doi: 10.1046/j.1432-1033.2003.03492.x PubMedCrossRefGoogle Scholar
  108. Fustec J, Lesuffleur F, Mahieu S, Cliquet J-B (2010) Nitrogen rhizodeposition of legumes. A review. Agron Sustain Dev 30:57–66. doi: 10.1051/agro/2009003 CrossRefGoogle Scholar
  109. Gan Y, Zentner RP, McDonald CL, Warkentin T, Vandenberg A (2009) Adaptability of chickpea in northern high latitude areas—maturity responses. Agric For Meteorol 149:711–720. doi: 10.1016/j.agrformet.2008.10.026 CrossRefGoogle Scholar
  110. Garau G, Yates RJ, Deiana P, Howieson JG (2009) Novel strains of nodulating Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils. Soil Biol Biochem 41:125–134. doi: 10.1016/j.soilbio.2008.10.011 CrossRefGoogle Scholar
  111. Garg N, Geetanjali (2007) Symbiotic nitrogen fixation in legume nodules: process and signaling. A review. Agron Sustain Dev 27:59–68. doi: 10.1051/agro:2006030 CrossRefGoogle Scholar
  112. Gemmell LG, Roughley RJ (1993) Field evaluation in acid soils of strains of Rhizobium leguminosarum biovar trifolii selected for their tolerance or sensitivity to acid soil factors in agar medium. Soil Biol Biochem 25:1447–1452. doi: 10.1016/0038-0717(93)90060-O CrossRefGoogle Scholar
  113. Ghittoni NE, Bueno MA (1995) Peanut rhizobia under salt stress: role of trehalose accumulation in strain ATCC51466. Can J Microbiol 41:1021–1030. doi: 10.1139/m95-141 CrossRefGoogle Scholar
  114. Gholipoor M, Ghasemi-Golezani K, Khooie FR, Moghaddam M (2000) Effects of salinity on initial seedling growth of chickpea (Cicer arietinum L.). Acta Agron Hung 48:337–343. doi: 10.1556/AAgr.48.2000.4.3 CrossRefGoogle Scholar
  115. Giller KE, Wilson K (1991) Nitrogen fixation in tropical cropping systems. CAB International, WallingfordGoogle Scholar
  116. Glenn AR, Reeve WG, Tiwari RP, Dilworth MJ, Cook GM, Booth IR, Poole RK, Foster JW, Slonczewski JL, Padan E, Epstein W, Skulachev V, Matin A, Fillingame RH (1999) Acid tolerance in root nodule bacteria. In: Chadwick D, Cardew G (eds) Bacterial response to pH. Novartis Foundation Symposium 221, pp 112–130Google Scholar
  117. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7. doi: 10.1016/j.femsle.2005.07.030 PubMedCrossRefGoogle Scholar
  118. Goergen E, Chambers JC, Blank R (2009) Effects of water and nitrogen availability on nitrogen contribution by the legume, Lupinus argenteus Pursh. Appl Soil Ecol 42:200–208. doi: 10.1016/j.apsoil.2009.04.001 CrossRefGoogle Scholar
  119. Gogorcena Y, Iturbe-Ormaetxe I, Escuredo PR, Becana M (1995) Antioxidant defences against activated oxygen in pea nodules subjected to water stress. Plant Physiol 108:753–759. doi: 10.1104/pp.108.2.753 PubMedGoogle Scholar
  120. González-Sama A, Lucas MM, de Felipe MR, Pueyo JJ (2004) An unusual infection mechanism and nodule morphogenesis in white lupin (Lupinus albus). New Phytol 163:371–380. doi: 10.1111/j.1469-8137.2004.01121.x CrossRefGoogle Scholar
  121. Gordon AJ, Minchin FR, Skot L, James CL (1997) Stress-induced declines in soybean nitrogen fixation are related to nodule sucrose synthase activity. Plant Physiol 114:937–946. doi: 10.1104/pp.114.3.937 PubMedGoogle Scholar
  122. Gordon LJ, Finlayson CM, Falkenmark M (2010) Managing water in agriculture for food production and other ecosystem services. Agric Water Manage 97:512–519. doi: 10.1016/j.agwat.2009.03.017 CrossRefGoogle Scholar
  123. Gouffi K, Pica N, Pichereau V, Blanco C (1999) Disaccharides as a new class of nonaccumulated osmoprotectants for Sinorhizobium meliloti. Appl Environ Microbiol 65:1491–1500PubMedGoogle Scholar
  124. Govind G, Vokkaliga H, ThammeGowda V, Kalaiarasi PJ, Iyer DR, Muthappa SK, Nese S, Makarla UK (2009) Identification and functional validation of a unique set of drought induced genes preferentially expressed in response to gradual water stress in peanut. Mol Genet Genomics 281:591–605. doi: 10.1007/s00438-009-0432-z PubMedCrossRefGoogle Scholar
  125. Graham PH, Vance CP (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crop Res 65:93–106. doi: 10.1016/S0378-4290(99)00080-5 CrossRefGoogle Scholar
  126. Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877. doi: 10.1104/pp.017004 PubMedCrossRefGoogle Scholar
  127. Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martínez E, Aarons SR, Quinto C (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Can J Microbiol 40:198–207. doi: 10.1139/m94-033 CrossRefGoogle Scholar
  128. Guan B, Zhou D, Zhang H, Tian Y, Japhet W, Wang P (2009) Germination responses of Medicago ruthenica seeds to salinity, alkalinity and temperature. J Arid Environ 73:135–138. doi: 10.1016/j.jaridenv.2008.08.009 CrossRefGoogle Scholar
  129. Hellweg C, Puhler A, Weidner S (2009) The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. BMC Microbiol 9:37. doi: 10.1186/1471-2180-9-37 PubMedCrossRefGoogle Scholar
  130. Hernández-Jiménez MJ, Lucas MM, de Felipe MR (2002) Antioxidant defense and damage in senescing lupin nodules. Plant Physiol Biochem 40:645–657. doi: 10.1016/S0981-9428(02)01422-5 CrossRefGoogle Scholar
  131. Herridge DF, Danso SKA (1995) Enhancing crop legume nitrogen fixation through selection and breeding. Plant Soil 174:51–82. doi: 10.1007/BF00032241 CrossRefGoogle Scholar
  132. Herridge DF, Turpin JE, Robertson MJ (2001) Improving nitrogen fixation of crop legumes through breeding and agronomic management analysis with simulation modelling. Aust J Exp Agric 41:391–401. doi: 10.1071/EA00041 CrossRefGoogle Scholar
  133. Hinde R, Trautman DA (2002) Symbiosomes. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer Academic, Netherlands, pp 207–220Google Scholar
  134. Hirsch PR (1996) Population dynamics of indigenous and genetically modified rhizobia in field. New Phytol 133:159–171. doi: 10.1111/j.1469-8137.1996.tb04351.x CrossRefGoogle Scholar
  135. Hirsch PR, Spokes JD (1994) Survival and dispersion of genetically-modified rhizobia in the field and genetic interactions with native strains. FEMS Microbiol Ecol 15:147–159. doi: 10.1111/j.1574-6941.1994.tb00239.x CrossRefGoogle Scholar
  136. Hossain MS, Martensson A (2008) Potential use of Rhizobium spp. to improve fitness of non-nitrogen-fixing plants. Acta Agric Scand B Soil Plant Sci 58:352–358. doi: 10.1080/09064710701788810 Google Scholar
  137. Howieson J, Ballard R (2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia—some contemporary thoughts. Soil Biol Biochem 36:1261–1273. doi: 10.1016/j.soilbio.2004.04.008 CrossRefGoogle Scholar
  138. Howieson JG, Loi A, Carr SJ (1995) Biserrula pelecinus L.—a legume pasture species with potential for acid, duplex soils which is nodulated by unique root-nodule bacteria. Aust J Agric Res 46:997–1009. doi: 10.1071/AR9950997 CrossRefGoogle Scholar
  139. Hua ST, Tsai VY, Lichens GM, Noma AT (1982) Accumulation of amino acids in Rhizobium sp. strain WR1001 in response to sodium chloride salinity. Appl Environ Microbiol 44:135–140PubMedGoogle Scholar
  140. Hungria M (1995) Efeito das temperaturas elevadas na exsudaçaõ de indutores dos genes nod pelo feijoeiro e soja. In: Hungria M, Balota EL, Colozzi-Filho A, Andrade DS (eds) Microbiologia do Solo: Desafios para o Século XXI. IAPAR/EMBRAPA-CNPSo, Londrina, pp 368–373Google Scholar
  141. Hungria M, Stacey G (1997) Molecular signals exchanged between host plants and rhizobia: basic aspects and potential application in agriculture. Soil Biol Biochem 29:819–830. doi: 10.1016/S0038-0717(96)00239-8 CrossRefGoogle Scholar
  142. Hungria M, Vargas MAT (2000) Environmental factors affecting nitrogen fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res 65:151–164. doi: 10.1016/S0378-4290(99)00084-2 CrossRefGoogle Scholar
  143. Hungria M, Franco AA, Sprent JI (1993) New sources of high-temperature tolerant rhizobia for Phaseolus vulgaris L. Plant Soil 149:103–109. doi: 10.1007/BF00010767 CrossRefGoogle Scholar
  144. Hungria M, Campo RJ, Mendes IC (2003) Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biol Fertil Soils 39:88–93. doi: 10.1007/s00374-003-0682-6 CrossRefGoogle Scholar
  145. Hunt S, Layzell DB (1993) Gas-exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44:483–511. doi: 10.1146/annurev.pp.44.060193.002411 CrossRefGoogle Scholar
  146. Iannetta PPM, James EK, Sprent MI, Minchin FR (1995) Time-course of changes involved in the operation of the oxygen diffusion barrier in white lupin nodules. J Exp Bot 46:565–575. doi: 10.1093/jxb/46.5.565 CrossRefGoogle Scholar
  147. Ikeda J (1994) The effect of short term withdrawal of NaCl stress on nodulation of white clover. Plant Soil 158:23–27. doi: 10.1007/BF00007913 CrossRefGoogle Scholar
  148. Imperlini E, Bianco C, Lonardo E, Camerini S, Cermola M, Moschetti G, Defez R (2009) Effects of indole-3-acetic acid on Sinorhizobium meliloti survival and on symbiotic nitrogen fixation and stem dry weight production. Appl Microbiol Biotechnol 83:727–738. doi: 10.1007/s00253-009-1974-z PubMedCrossRefGoogle Scholar
  149. Iniguez AL, Robleto EA, Kent AD, Triplett EW (2004) Significant yield increase in Phaseolus vulgaris obtained by inoculation with a trifolitoxin-producing, Hup+ strain of Rhizobium leguminosarum bv. phaseoli, Crop Management. Available at doi:10.1094/CM-2004-0301-07-RV
  150. Israel DW, Jackson WA (1978) The influence of nitrogen nutrition on ion uptake and translocation by leguminous plants. In: Andrew CS, Kamprath EJ (eds) Mineral nutrition of legumes in tropical and subtropical soils. Commonwealth Scientific and Industrial Research Organization, Melbourne, pp 113–129Google Scholar
  151. Iturbe-Ormaetxe I, Escuredo FR, Arrese-Igor C, Becana M (1998) Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol 116:173–181. doi: 10.1104/pp.116.1.173 CrossRefGoogle Scholar
  152. Jain D, Chattopadhyay D (2010) Analysis of gene expression in response to water deficit of chickpea (Cicer arietinum L.) varieties differing in drought tolerance. BMC Plant Biol 10:24. doi: 10.1186/1471-2229-10-24 PubMedCrossRefGoogle Scholar
  153. Jensen ES, Hauggaard-Nielsen H (2003) How can increased use of biological nitrogen fixation in agriculture benefit the environment? Plant Soil 252:177–186. doi: 10.1023/A:1024189029226 CrossRefGoogle Scholar
  154. Jeschke WD, Wolf O, Hartung W (1992) Effect of NaCl salinity on flows and partitioning of C, N, and mineral ions in whole plants of white lupin (Lupinus albus L.). J Exp Bot 43:777–788. doi: 10.1093/jxb/43.6.777 CrossRefGoogle Scholar
  155. Jiang QZ, Zhang JY, Guo X, Bedair M, Sumner L, Bouton J, Wang ZY (2010) Improvement of drought tolerance in white clover (Trifolium repens) by transgenic expression of a transcription factor gene WPX1. Funct Plant Biol 37:157–165. doi: 10.1071/FP09177 CrossRefGoogle Scholar
  156. Jin CW, He YF, Tang CX, Wu P, Zheng SJ (2006) Mechanisms of microbially enhanced Fe acquisition in red clover (Trifolium pratense L.). Plant Cell Environ 29:888–897. doi: 10.1111/j.1365-2005.01468.x PubMedCrossRefGoogle Scholar
  157. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the SinorhizobiumMedicago model. Nat Rev Microbiol 5:619–633. doi: 10.1038/nrmicro1705 PubMedCrossRefGoogle Scholar
  158. Jordan DC (1984) Family III Rhizobiaceae CONN 1938, 321 AL. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology. William and Wilkins, Baltimore, pp 235–244Google Scholar
  159. Kakimoto T (2003) Perception and signal transduction of cytokinins. Annu Rev Plant Physiol Plant Mol Biol 54:605–627. doi: 10.1146/annurev.arplant.54.031902.134802 CrossRefGoogle Scholar
  160. Karlen DL, Varvel GE, Bullock DG, Cruse RM (1994) Crop rotations for the 21st century. Adv Agron 53:1–45. doi: 10.1016/S0065-2113(08)60611-2 CrossRefGoogle Scholar
  161. Keller F, Ludlow MM (1993) Carbohydrate metabolism in drought-stressed leaves of pigeonpea (Cajanus cajan). J Exp Bot 44:1351–1359. doi: 10.1093/jxb/44.8.1351 CrossRefGoogle Scholar
  162. Kerr RB, Snapp S, Chirwa M, Shumba L, Msachi R (2007) Participatory research on legume diversification with Malawian smallholder farmers for improved human nutrition and soil fertility. Expl Agric 43:437–453. doi: 10.1017/S0014479707005339 CrossRefGoogle Scholar
  163. Kishor PBK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438Google Scholar
  164. Kneip C, Lockhart P, Voß C, Maier U-G (2007) Nitrogen fixation in eukaryotes—new models for symbiosis. BMC Evol Biol 7:55–66. doi: 10.1186/1471-2148-7-55 PubMedCrossRefGoogle Scholar
  165. Kostopoulou P, Vrahnakis MS, Merou T, Lazaridou M (2010) Perennial-like adaptation mechanisms of annual legumes to limited irrigation. J Environ Biol 31:311–314PubMedGoogle Scholar
  166. L’taief B, Sifi B, Zarnan-Allah M, Drevon JJ, Lachaal M (2007) Effect of salinity on root-nodule conductance to the oxygen diffusion in the Cicer arietinum Mesorhizobium ciceri symbiosis. J Plant Physiol 164:1028–1036. doi: 10.1016/j.jptph.2006.05.016 PubMedCrossRefGoogle Scholar
  167. Langer H, Nandasena KG, Howieson JG, Jorquera M, Borie F (2008) Genetic diversity of Sinorhizobium meliloti associated with alfalfa in Chilean volcanic soils and their symbiotic effectiveness under acidic conditions. World J Microbiol Biotechnol 24:301–308. doi: 10.1007/s11274-007-9471-y CrossRefGoogle Scholar
  168. Larrainzar E, Wienkoop S, Scherling C, Kempa S, Ladrera R, Arrese-Igor C, Weckwerth W, González EM (2009) Carbon metabolism and bacteroid functioning are involved in the regulation of nitrogen fixation in Medicago truncatula under drought and recovery. Mol Plant-Microbe Interact 22:1565–1576. doi: 10.1094/MPMI-22-12-1565 PubMedCrossRefGoogle Scholar
  169. Läuchli A (1984) Salt exclusion: an adaptation of legumes for crops and pastures under saline conditions. In: Staples RC, Toenniessen GH (eds) Salinity tolerance in plants—strategies for crop improvement. Wiley, New York, pp 171–188Google Scholar
  170. Lauter DJ, Meiri A, Shuali M (1988) Isoosmotic regulation of cotton and peanut at saline concentrations of K and Na. Plant Physiol 87:911–916. doi: 10.1104/pp.87.4.911 PubMedCrossRefGoogle Scholar
  171. Lazrek F, Roussel V, Ronfort J, Cardinet G, Chardon F, Aouani M, Huguet T (2009) The use of neutral and non-neutral SSRs to analyse the genetic structure of a Tunisian collection of Medicago truncatula lines and to reveal associations with eco-environmental variables. Genetica 135:391–402. doi: 10.1007/s10709-008-9285-3 PubMedCrossRefGoogle Scholar
  172. Leslie SB, Israeli B, Lighthart B, Crowe JH, Crowe LM (1995) Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl Environ Microbiol 61:3592–3597PubMedGoogle Scholar
  173. Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Biol 49:199–222. doi: 10.1146/annurev.arplant.49.1.199 CrossRefGoogle Scholar
  174. Li D, Su Z, Dong J, Wang T (2009) An expression database for roots of the model legume Medicago truncatula under salt stress. BMC Genomics 10:517. doi: 10.1186/1471-2164-10-517 PubMedCrossRefGoogle Scholar
  175. Lindström K, Jussila MM, Hintsa H, Kaksonen A, Mokelke L, Makelainen K, Pitkajarvi J, Suominen L (2003) Potential of the Galega Rhizobium galegae system for bioremediation of oil-contaminated soil. Food Technol Biotechnol 41:11–16Google Scholar
  176. Liu Y, Wu L, Baddeley JA, Watson CA (2010) Models of biological nitrogen fixation of legumes. A review. Agron Sustain Dev. doi: 10.1051/agro/2010008, In PressGoogle Scholar
  177. Lloret L, Martínez-Romero E (2005) Evolution and phylogeny of rhizobia. Rev Latinoam Microbiol 47:43–60PubMedGoogle Scholar
  178. Lloret J, Bolanos L, Lucas MM, Peart JM, Brewin NJ, Bonilla I, Rivilla R (1995) Ionic stress and osmotic pressure induce different alterations in the lipopolysaccharide of a Rhizobium meliloti strain. Appl Environ Microbiol 61:3701–3704PubMedGoogle Scholar
  179. Lloret J, Wulff BB, Rubio JM, Downie JA, Bonilla I, Rivilla R (1998) Exopolysaccharide II production is regulated by salt in the halotolerant strain Rhizobium meliloti EFB1. Appl Environ Microbiol 64:1024–1028PubMedGoogle Scholar
  180. Loscos J, Matamoros MA, Becana M (2008) Ascorbate and homoglutathione metabolism in common bean nodules under stress conditions and during natural senescence. Plant Physiol 146:1282–1292. doi: 10.1104/pp.107.114066 PubMedCrossRefGoogle Scholar
  181. Ma XF, Wright E, Ge YX, Bell J, Xi YJ, Bouton JH, Wang ZY (2009) Improving phosphorus acquisition of white clover (Trifolium repens L.) by transgenic expression of plant-derived phytase and acid phosphatase genes. Plant Sci 176:479–488. doi: 10.1016/j.plantsci.2009.01.001 CrossRefGoogle Scholar
  182. Maj D, Wielbo J, Marek-Kozaczuk M, Martyniuk S, Skorupska A (2009) Pretreatment of clover seeds with Nod factors improves growth and nodulation of Trifolium pratense. J Chem Ecol 35:479–487. doi: 10.1007/s10886-009-9672-y PubMedCrossRefGoogle Scholar
  183. Manchada G, Garg N (2008) Salinity and its effects on the functional biology of legumes. Acta Physiol Plant 30:595–618. doi: 10.1007/s11738-008-0173-3 CrossRefGoogle Scholar
  184. Márquez AJ, Betti M, García-Calderón M, Pal’ove-Balang P, Díaz P, Monza J (2005) Nitrate assimilation in Lotus japonicus. J Exp Bot 56:1741–1749. doi: 10.1093/jxb/eri171 PubMedCrossRefGoogle Scholar
  185. Marroquí S, Zorreguieta A, Santamaría C, Temprano F, Soberón M, Megías M, Downie JA (2001) Enhanced symbiotic performance by Rhizobium tropici glycogen synthase mutants. J Bacteriol 183:854–864. doi: 10.1128/JB.183.3.854-864.2001 PubMedCrossRefGoogle Scholar
  186. Martínez-Romero E, Segovia E, Mercante FM, Franco AA, Graham PH, Pardo MA (1991) Rhizobium tropicii, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacteriol 41:417–426. doi: 10.1099/00207713-41-3-417 PubMedCrossRefGoogle Scholar
  187. Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many Rhizobium recipes? Trends Microbiol 17:458–466. doi: 10.1016/j.tim.2009.07.004 PubMedCrossRefGoogle Scholar
  188. Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M (2003) Biochemistry and molecular biology of antioxidants in the rhizobia–legume symbiosis. Plant Physiol 133:499–509. doi: 10.1104/pp.103.025619 PubMedCrossRefGoogle Scholar
  189. Matamoros MA, Loscos J, Coronado MJ, Ramos J, Sato S, Testillano PS, Tabata S, Becana M (2006) Biosynthesis of ascorbic acid in legume root nodules. Plant Physiol 141:1068–1077. doi: 10.1104/pp.106.081463 PubMedCrossRefGoogle Scholar
  190. Matos MC, Campos PS, Ramalho JC, Medeira MC, Maia MI, Semedo JM, Marques NM, Matos A (2002) Photosynthetic activity and cellular integrity of the Andean legume Pachyrhizus ahipa (Wedd.) Parodi under heat and water stress. Photosynthetica 40:493–501. doi: 10.1023/A:1024331414564 CrossRefGoogle Scholar
  191. McKersie BD, Chen Y, de Beus M, Bowley SR, Bowler C, Inzé D, D’Halluin K, Botterman J (1993) Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). Plant Physiol 103:1155–1163. doi: 10.1104/pp.103.4.1155 PubMedCrossRefGoogle Scholar
  192. McKersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111:1177–1181. doi: 10.1104/pp.111.4.1177 PubMedGoogle Scholar
  193. McKersie BD, Bowley SR, Jones KS (1999) Winter survival of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 119:839–848. doi: 10.1104/pp.119.3.839 PubMedCrossRefGoogle Scholar
  194. McKersie BD, Murnaghan J, Jones KS, Bowley SR (2000) Iron-superoxide dismutase expression in transgenic alfalfa increases winter survival without a detectable increase in photosynthetic oxidative stress tolerance. Plant Physiol 122:1427–1437. doi: 10.1104/pp.122.4.1427 PubMedCrossRefGoogle Scholar
  195. McLauchlan K (2006) The nature and longevity of agricultural impacts on soil carbon and nutrients: a review. Ecosystems 9:1364–1382. doi: 10.1007/s10021-005-0135-1 CrossRefGoogle Scholar
  196. Merchan F, de Lorenzo L, Rizzo SG, Niebel A, Manyani H, Frugier F, Sousa C, Crespi M (2007) Identification of regulatory pathways involved in the reacquisition of root growth after salt stress in Medicago truncatula. Plant J 51:1–17. doi: 10.1111/j.1365-313X.2007.03117.x PubMedCrossRefGoogle Scholar
  197. Merou TP, Papanastasis VP (2009) Factors affecting the establishment and growth of annual legumes in semi-arid Mediterranean grasslands. Plant Ecol 201:491–500. doi: 10.1007/s11258-008-9550-7 CrossRefGoogle Scholar
  198. Meyer DW, Badaruddin M (2001) Frost tolerance of ten seedling legume species at four growth stages. Crop Sci 41:1838–1842CrossRefGoogle Scholar
  199. Miethling R, Tebbe CC (2004) Resilience of a soil-established, genetically modified Sinorhizobium meliloti inoculant to soil management practices. Appl Soil Ecol 25:161–167. doi: 10.1016/j.apsoil.2003.08.003 CrossRefGoogle Scholar
  200. Miller KJ, Kennedy EP, Reinhold VN (1986) Osmotic adaptation by gram-negative bacteria: possible role for periplasmic oligosaccharides. Science 231:48–51. doi: 10.1126/science.3941890 PubMedCrossRefGoogle Scholar
  201. Miller-Williams M, Loewen PC, Oresnik IJ (2006) Isolation of salt-sensitive mutants of Sinorhizobium meliloti strain Rm1021. Microbiology 152:2049–2059. doi: 10.1099/mic.0.28937-0 PubMedCrossRefGoogle Scholar
  202. Miransari M, Balakrishnan P, Smith D, Mackenzie AF, Bahrami HA, Malakouti MJ, Rejali F (2006) Overcoming the stressful effect of low pH on soybean root hair curling using lipochitooligosaccharides. Commun Soil Sci Plant Anal 37:1103–1110. doi: 10.1080/00103620600586391 CrossRefGoogle Scholar
  203. Mnasri B, Tajini F, Trabelsi M, Aouani ME, Mhamdi R (2007) Rhizobium gallicum as an efficient symbiont for bean inoculation. Agron Sustain Dev 27:331–336. doi: 10.1051/agro:2007024 CrossRefGoogle Scholar
  204. Moawad H, El-Rahim WMA, El-Aleem DA, Sedera SAA (2005) Persistence of two Rhizobium etli inoculant strains in clay and silty loam soils. J Basic Microbiol 45:438–446. doi: 10.1002/jobm.200510590 PubMedCrossRefGoogle Scholar
  205. Montero E, Cabot C, Barceló J, Poschenrieder C (1997) Endogenous abscisic acid levels are linked to decreased growth of bush bean plants treated with NaCl. Physiol Plant 101:17–22. doi: 10.1111/j.1399-3054.1997.tb01814.x CrossRefGoogle Scholar
  206. Mouhsine B, Prell J, Filali-Maltouf A, Priefer UB, Aurag J (2007) Diversity, phylogeny and distribution of bean rhizobia in salt-affected soils of North-West Morocco. Symbiosis 43:83–96Google Scholar
  207. Muehlbauer FJ, Cho S, Sarker A, McPhee KE, Coyne CJ, Rajesh PN, Ford R (2006) Application of biotechnology in breeding lentil for resistance to biotic and abiotic stress. Euphytica 147:149–165. doi: 10.1007/s10681-006-7108-0 CrossRefGoogle Scholar
  208. Muglia CI, Grasso DH, Aguilar OM (2007) Rhizobium tropici response to acidity involves activation of glutathione synthesis. Microbiol 153:1286–1296. doi: 10.1099/mic.0.2006/003483-0 CrossRefGoogle Scholar
  209. Murphy PJ, Wexler W, Grzemski W, Rao JP, Gordon D (1995) Rhizopines—their role in symbiosis and competition. Soil Biol Biochem 27:525–529. doi: 10.1016/0038-0717(95)98627-Z CrossRefGoogle Scholar
  210. Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104. doi: 10.1126/science.1132514 PubMedCrossRefGoogle Scholar
  211. Nandal K, Sehrawat AR, Yadav AS, Vashishat RK, Boora KS (2005) High temperature-induced changes in exopolysaccharides, lipopolysaccharides and protein profile of heat-resistant mutants of Rhizobium sp. (Cajanus). Microbiol Res 160:367–373. doi: 10.1016/j.micres.2005.02.011 PubMedCrossRefGoogle Scholar
  212. Nichols PGH, Rogers ME, Craig AD, Albertsen TO, Miller SM, McClements DR, Hughes SJ, D’Antuono MF, Dear BS (2008) Production and persistence of temperate perennial grasses and legumes at five saline sites in southern Australia. Aust J Exp Agric 48:536–552. doi: 10.1071/EA07168 CrossRefGoogle Scholar
  213. Nilsen ET (1992) The influence of water-stress on leaf and stem photosynthesis in Spartium junceum L. Plant Cell Environ 15:455–461. doi: 10.1111/j.1365-3040.1992.tb00996.x CrossRefGoogle Scholar
  214. Noctor N, Foyer CH (1998) Ascorbate and gluthatione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279. doi: 10.1146/annurev.arplant.49.1.249 PubMedCrossRefGoogle Scholar
  215. Nogales J, Campos R, BenAbdelkhalek H, Olivares J, Lluch C, Sanjuán J (2002) Rhizobium tropici genes involved in free-living salt tolerance are required for the establishment of efficient nitrogen-fixing symbiosis with Phaseolus vulgaris. Mol Plant-Microbe Interact 15:225–232. doi: 10.1094/MPMI.2002.15.3.225 PubMedCrossRefGoogle Scholar
  216. Nunes C, Araújo SS, Silva JM, Fevereiro P, Silva AB (2009) Photosynthesis light curves: a method for screening water deficit resistance in the model legume Medicago truncatula. Ann Appl Biol 155:321–332. doi: 10.1111/j.1744-7348.2009.00341.x CrossRefGoogle Scholar
  217. Ohashi Y, Saneoka H, Fujita K (2000) Effect of water stress on growth, photosynthesis, and photoassimilate translocation in soybean and tropical pasture legume siratro. Soil Sci Plant Nutr 46:417–425Google Scholar
  218. Oliveira ALM, Urquiaga S, Döbereiner J, Baldani JI (2002) The effect of inoculating endophytic nitrogen-fixing bacteria on micropropagated sugarcane plants. Plant Soil 242:205–215. doi: 10.1023/A:1016249704336 CrossRefGoogle Scholar
  219. Oren A (1999) Bioenergetics aspects of halophilism. Microbiol Mol Biol Rev 63:334–348PubMedGoogle Scholar
  220. Oresnik IJ, Twelker S, Hynes MF (1999) Cloning and characterizaton of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins. Appl Environ Microbiol 65:2833–2840PubMedGoogle Scholar
  221. Ormeño-Orrillo E (2005) Lipopolysaccharides of rhizobiaceae: structure and biosynthesis. Rev Latinoam Microbiol 47:165–175PubMedGoogle Scholar
  222. Orozco-Mosqueda M, del C, Altimirano-Hernández J, Farias-Rodríguez R, Valencia-Cantero F, Santoyo G (2009) Homologous recombination and dynamics of rhizobial genomes. Res Microbiol 160:733–741. doi: 10.1016/j.resmic.2009.09.011 CrossRefGoogle Scholar
  223. Ovalle C, del Pozo A, Fernández F, Chavarria J, Arredondo S (2010) Arrowleaf clover (Trifolium vesiculosum Savi): a new species of annual legumes for high rainfall areas of the Mediterranean climate zone of Chile. Chilean J Agric Res 70:170–177. doi: 10.4067/S0718-58392010000100018 Google Scholar
  224. Pandey RK, Herrera WAT, Villepas AN, Pendelton JW (1984) Drought response of grain legumes under irrigation gradient. III. Plant growth. Agron J 76:557–560CrossRefGoogle Scholar
  225. Pang J, Tibbett M, Denton MD, Lambers H, Siddique KHM, Bolland MDA, Revell CK, Ryan MH (2010) Variation in seedling growth of 11 perennial legumes in response to phosphorus supply. Plant Soil 328:133–143. doi: 10.1007/s11104-009-0088-9 CrossRefGoogle Scholar
  226. Parker CA (1986) Legumes and nitrogen fixation; their importance for farming in the future. Impact Sci Soc 36:153–164Google Scholar
  227. Pedersen AL, Feldner HC, Rosendahl L (1996) Effect of proline on nitrogenase activity in symbiosomes from root nodules of soybean (Glycine max L.) subjected to drought stress. J Exp Bot 47:1533–1539. doi: 10.1093/jxb/47.10.1533 CrossRefGoogle Scholar
  228. Peoples MB, Crasswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39. doi: 10.1007/BF00011308 CrossRefGoogle Scholar
  229. Pimratch S, Jogloy S, Vorassot N, Toomsan B, Kesmala T, Patanothai A, Holbrook CC (2009) Heritability of nitrogen fixation traits, and phenotypic and genotypic correlations between nitrogen fixation traits with drought resistance traits and yield in peanut. Crop Sci 49:791–800. doi: 10.2135/cropsci2008.06.0331 CrossRefGoogle Scholar
  230. Popelka JC, Terryn N, Higgins TJV (2004) Gene technology for grain legumes: can it contribute to the food challenge in developing countries? Plant Sci 167:195–206. doi: 10.1016/j.plantsci.2004.03.027 CrossRefGoogle Scholar
  231. Priefer UB, Aurag J, Boesten B, Bouhmouch I, Defez R, Filali-Maltouf A, Miklis M, Moawad H, Mouhsine B, Prell J, Schlüter A, Senatore B (2001) Characterisation of Phaseolus symbionts isolated from Mediterranean soils and analysis of genetic factors related to pH tolerance. J Biotechnol 91:223–236. doi: 10.1016/S0168-1656(01)00329-7 PubMedCrossRefGoogle Scholar
  232. Priyanka B, Sekhar K, Sunita T, Reddy VD, Rao KV (2010) Characterization of expressed sequence tags (ESTs) of pigeonpea (Cajanus cajan L.) and functional validation of selected genes for abiotic stress tolerance in Arabidopsis thaliana. Mol Genet Genomics 283:273–287. doi: 10.1007/s00438-010-0516-9 PubMedCrossRefGoogle Scholar
  233. Pueyo JJ, Gómez-Moreno C (1991) Characterization of the cross-linked complex formed between ferredoxin-NADP+ reductase and flavodoxin from Anabaena PCC 7119. Biochim Biophys Acta 1059:149–156. doi: 10.1016/S0005-2728(05)80199-9 CrossRefGoogle Scholar
  234. Pueyo JJ, Gómez-Moreno C, Mayhew SG (1991) Oxidation-reduction potentials of ferredoxin NADP+ reductase and flavodoxin from Anabaena PCC7119 and of their electrostatic and covalent complexes. Eur J Biochem 202:1065–1071. doi: 10.1111/j.1432-1033.1991.tb16471.x PubMedCrossRefGoogle Scholar
  235. Pule-Meuelenberg F, Dakora FD (2007) Assessing the biological potential of N2-fixing Leguminosae in Botswana for increased crop yields and commercial exploitation. Afr J Biotechnol 6:325–334Google Scholar
  236. Puppo A, Halliwell B (1988) Generation of hydroxyl radicals by soybean nodule leghaemoglobin. Planta 173:405–410. doi: 10.1007/BF00401028 CrossRefGoogle Scholar
  237. Puppo A, Rigaud J, Job D (1981) Role of superoxide anion in leghemoglobin autoxidation. Plant Sci Lett 22:353–360. doi: 10.1016/0304-4211(81)90081-X CrossRefGoogle Scholar
  238. Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, De Felipe MR, Harrison J, Vanacker H, Foyer CH (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165:683–701. doi: 10.1111/j.1469-8137.2004.01285.x PubMedCrossRefGoogle Scholar
  239. Rahmani HA, Saleh-rastin N, Khavazi K, Asgharzadeh A, Fewer D, Kiani S, Lindström K (2009) Selection of thermotolerant bradyrhizobial strains for nodulation of soybean (Glycine max L.) in semi-arid regions of Iran. World J Microbiol Biotechnol 25:591–600. doi: 10.1007/s11274-008-9927-8 CrossRefGoogle Scholar
  240. Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45:481–487. doi: 10.1023/A:1022308229759 CrossRefGoogle Scholar
  241. Ramírez M, Valderrama B, Arredondo-Peter R, Soberón M, Mora J, Hernández G (1999) Rhizobium etli genetically engineered for the heterologous expresion of Vitreoscilla sp. hemoglobin: effects on free-living and symbiosis. Mol Plant-Microbe Interact 12:1008–1015. doi: 10.1094/MPMI.1999.12.11.1008 CrossRefGoogle Scholar
  242. Rao AV, Tak R (2001) Effect of rhizobial inoculation on Albizia lebbeck and its rhizosphere activity in mine spoils. Arid Land Res Manag 15:157–162. doi: 10.1080/15324980151062805 CrossRefGoogle Scholar
  243. Ratinam M, Abdelmoneim AM, Saxena MC (1994) Variations in sugar content and dry matter distribution in roots and their associations with frost tolerance in certain forage legume species. J Agron Crop Sci 173:345–353. doi: 10.1111/j.1439-037X.1994.tb00582.x CrossRefGoogle Scholar
  244. Raven JA (1986) Biochemical disposal of excess H+ in growing plants? New Phytol 104:175–206. doi: 10.1111/j.1469-8137.1986.tb00644.x CrossRefGoogle Scholar
  245. Reddy TY, Reddu VR, Anbumozhi V (2003) Physiological responses of groundnut (Arachis hypogea L.) to drought stress and its amelioration: a critical review. Plant Growth Regul 41:75–88. doi: 10.1023/A:1027353430164 CrossRefGoogle Scholar
  246. Reddy PCO, Sairanganayakulu G, Thippeswamy M, Reddy PS, Reddy MK, Sudhakar C (2008) Identification of stress-induced genes from the drought tolerant semi-arid legume crop horsegram (Macrotyloma uniflorum (Lam.) Verdc.) through analysis of subtracted expressed sequence tags. Plant Sci 175:372–384. doi: 10.1016/j.plantsci.2008.05.012 CrossRefGoogle Scholar
  247. Redondo FJ, Coba de la Peña T, Morcillo CN, Lucas MM, Pueyo JJ (2009) Overexpression of flavodoxin induces changes in antioxidant metabolism leading to delayed senescence and starch accumulation in alfalfa root nodules. Plant Physiol 149:1166–1178. doi: 10.1104/pp.108.129601 PubMedCrossRefGoogle Scholar
  248. Reis VM, dos Reis FB, Quesada DM, de Oliveira OCA, Alves BJR, Urquiaga S, Boddey RM (2001) Biological nitrogen fixation associated with tropical pasture grasses. Aust J Plant Physiol 28:837–844. doi: 10.1071/PP01079 Google Scholar
  249. Reitz M, Hoffmann-Hergarten S, Hallmann J, Sikora RA (2001) Induction of sytemic resistance in potato by rhizobacterium Rhizobium etli strain G12 is not associated with accumulation of pathogenesis-related proteins and enhanced lignin biosynthesis. J Plant Dis Prot 108:11–20Google Scholar
  250. Rincón A, Arenal F, González I, Manrique E, Lucas MM, Pueyo JJ (2008) Diversity of rhizobial bacteria isolated from nodules of the gypsophyte Ononis tridentata L. growing in Spanish soils. Microb Ecol 56:223–233. doi: 10.1007/s00248-007-9339-6 PubMedCrossRefGoogle Scholar
  251. Robleto EA, Scupham AJ, Triplett EW (1997) Trifolitoxin production in Rhizobium etli strain CE3 increases competitiveness for rhizosphere growth and root nodulation of Phaseolus vulgaris in soil. Mol Plant-Microbe Interact 10:228–233. doi: 10.1094/MPMI.1997.10.2.228 CrossRefGoogle Scholar
  252. Robleto EA, Kmiecik K, Oplinger ES, Nienhuis J, Triplett EW (1998) Trifolitoxin production increases nodulation competitiveness of Rhizobium etli CE3 under agricultural conditions. Appl Environ Microbiol 64:2630–2633PubMedGoogle Scholar
  253. Rodríguez-Echevarría S, Pérez-Fernández MA (2005) Potencial use of Iberian shrubby legumes and rhizobia inoculation in revegetation projects under acidic soil conditions. Appl Soil Ecol 29:203–208. doi: 10.1016/j.apsoil.2004.11.004 CrossRefGoogle Scholar
  254. Rogers ME, Noble CL, Pederick RJ (1997) Identifying suitable temperature forage legume species for saline areas. Aust J Exp Agric 37:639–645. doi: 10.1071/EA96102 CrossRefGoogle Scholar
  255. Romdhane SB, Aouani ME, Trabelsi M, de Lajudie P, Mhamdi R (2008) Selection of high nitrogen-fixing rhizobia nodulating chickpea (Cicer arietinum) for semi-arid Tunisia. J Agron Crop Sci 194:413–420. doi: 10.1111/j.1439-037X.2008.00328.x Google Scholar
  256. Romdhane SB, Trabelsi M, Aouani ME, de Lajudie P, Mhamdi R (2009) The diversity of rhizobia nodulating chickpea (Cicer arietinum) under water deficiency as a source of more efficient inoculants. Soil Biol Biochem 41:2568–2572. doi: 10.1016/j.soilbio.2009.09.020 CrossRefGoogle Scholar
  257. Ross EJ, Kramer SB, Dalton DA (1999) Efectiveness of ascorbate peroxidase in promoting nitrogen fixation in model systems. Phytochemistry 52:1203–1210. doi: 10.1016/S0031-9422(99)00407-0 PubMedCrossRefGoogle Scholar
  258. Ruberg S, Tian ZX, Krol E, Linke B, Meyer F, Wang YP, Puhler A, Weidner S, Becker A (2003) Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptative gene expression. J Biotechnol 106:255–268. doi: 10.1016/j.jbiotec.2003.08.005 PubMedCrossRefGoogle Scholar
  259. Rubio MC, González EM, Minchin FR, Webb KJ, Arrese-Igor C, Ramos J, Becana M (2002) Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. Physiol Plant 115:531–540. doi: 10.1034/j.1399-3054.2002.1150407.x PubMedCrossRefGoogle Scholar
  260. Ruiz-Díez B, Fajardo S, Puertas-Mejías MA, de Felipe MR, Fernández-Pascual M (2009) Stress tolerance, genetic analysis and symbiotic properties of root-nodulating bacteria isolated from Mediterranean leguminous shrubs in Central Spain. Arch Microbiol 191:35–46. doi: 10.1007/s00203-008-0426-y PubMedCrossRefGoogle Scholar
  261. Sadiki M, Rabih K (2001) Selection of chickpea (Cicer arietinum) for yield and symbiotic nitrogen fixation ability under salt stress. Agronomie 21:659–666. doi: 10.1051/agro:2001158 CrossRefGoogle Scholar
  262. Sanchez DH, Lippold F, Redestig H, Hannah MA, Erban A, Krämer U, Kopka J, Udvardi MK (2008) Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant J 53:973–987. doi: 10.1111/j.1365-313X.2007.03381.x PubMedCrossRefGoogle Scholar
  263. Sauvage D, Hamelin J, Larher F (1983) Glycine betaine and other structurally related compounds improve the salt tolerance of Rhizobium meliloti. Plant Sci Lett 31:291–302. doi: 10.1016/0304-4211(83)90068-8 CrossRefGoogle Scholar
  264. Sauviac L, Philippe H, Phok K, Bruand C (2007) An extracytoplasmic function sigma factor acts as a general stress response regulator in Sinorhizobium meliloti. J Bacteriol 189:4204–4216. doi: 10.1128/JB.00175-07 PubMedCrossRefGoogle Scholar
  265. Schubert S, Serraj R, Pliesbalzer E, Mengel K (1995) Effect of drought stress on growth, sugar concentrations and amino acid accumulation in nitrogen-fixing alfalfa (Medicago sativa). J Plant Physiol 146:541–546CrossRefGoogle Scholar
  266. Seena S, Sridhar KR (2006) Nutritional and microbiological features of little known legumes, Canavalia cathartica Thouars and C. maritima Thouars of the southwest coast of India. Curr Sci 90:1638–1650Google Scholar
  267. Serraj R, Fleurat-Lessard P, Jaillard B, Drevon JJ (1995) Structural changes in the inner-cortex cells of soybean root-nodules are induced by short-term exposure to high salt or oxygen concentrations. Plant Cell Environ 18:455–462. doi: 10.1111/j.1365-3040.1995.tb00380.x CrossRefGoogle Scholar
  268. Serraj R, Bona S, Purcell LC, Sinclair TR (1997) Nitrogen accumulation and nodule activity of field-grown “Jackson” soybean in response to water deficits. Field Crops Res 52:109–116. doi: 10.1016/S0378-4290(96)01068-4 CrossRefGoogle Scholar
  269. Serraj R, Vadez VV, Denison RF, Sinclair TR (1999) Involvement of ureides in nitrogen fixation inhibition in soybean. Plant Physiol 119:289–296. doi: 10.1104/pp.119.1.289 PubMedCrossRefGoogle Scholar
  270. Sessitsch A, Howieson JG, Perret X, Antoun H, Martínez-Romero E (2002) Advances in Rhizobium research. Crit Rev Plant Sci 21:323–378. doi: 10.1080/0735-260291044278 CrossRefGoogle Scholar
  271. Sevilla M, Kennedy C (2000) Genetic analysis of nitrogen fixation and plant-growth stimulating properties of Acetobacter diazotrophicus, an endophyte of sugarcane. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for analysis of a biological process. Horizon Scientific, Norwich, pp 737–760Google Scholar
  272. Sheokand S, Dhandi S, Swaraj K (1995) Studies on nodule functioning and hydrogen-peroxide scavenging enzymes under salt stress in chickpea nodules. Plant Physiol Biochem 33:561–566Google Scholar
  273. Shvaleva A, Coba de la Peña T, Rincón A, Morcillo CN, García de la Torre VS, Lucas MM, Pueyo JJ (2010) Flavodoxin overexpression reduces cadmium-induced damage in alfalfa root nodules. Plant Soil 326:109–121. doi: 10.1007/s11104-009-9985-1 CrossRefGoogle Scholar
  274. Simões-Araújo JL, Rodríguez RL, Gerhardt LBD, Mondego JMC, Alves-Ferreira M, Rumjanek NG, Margis-Pinheiro M (2002) Identification of differentially expressed genes by cDNA-AFLP technique during heat stress in cowpea nodules. FEBS Lett 515:44–50. doi: 10.1016/S0014-5793(02)02416-X PubMedCrossRefGoogle Scholar
  275. Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soybean. Plant Physiol 74:72–76. doi: 10.1104/pp.74.1.72 PubMedCrossRefGoogle Scholar
  276. Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysacharides: genetic control and symbiotic functions. Microb Cell Fact 5:7. doi: 10.1186/1475-2859-5-7 PubMedCrossRefGoogle Scholar
  277. Small E (2003) Distribution of perennial Medicago with particular reference to agronomic potential for the semiarid Mediterranean climate. In: Bennett SJ (ed) New perennial legumes for sustainable agriculture. University of Western Australia Press, Perth, pp 57–80Google Scholar
  278. Smith LT, Smith GM (1989) An osmoregulated dipeptide in stressed Rhizobium meliloti. J Bacteriol 171:4714–4717PubMedGoogle Scholar
  279. Soberón M, López O, Morera C, de Lourdes Girard M, Tabche ML, Miranda J (1999) Enhanced nitrogen fixation in a Rhizobium etli ntrC mutant that overproduces the Bradyrhizobium japonicum symbiotic terminal oxidase cbb 3. Appl Environ Microbiol 65:2015–2019PubMedGoogle Scholar
  280. Soberón-Chavez G, Nájera R, Oliveira H, Segovia L (1986) Genetic rearrangements of a Rhizobium phaseoli symbiotic plasmid. J Bacteriol 167:487–491PubMedGoogle Scholar
  281. Soon YK, Lupwayi NZ (2008) Influence of pea cultivar and inoculation on the nitrogen budget of a pea-wheat rotation in northwestern Canada. Can J Plant Sci 88:1–9. doi: 10.4141/CJPS06055 CrossRefGoogle Scholar
  282. Soussi M, Ocaña A, Lluch C (1998) Effects of salt stress on growth, photosynthesis and nitrogen fixation in chickpea (Cicer arietinum L.). J Exp Bot 49:1329–1337. doi: 10.1093/jexbot/49.325.1329 CrossRefGoogle Scholar
  283. Soussi M, Santamaría M, Ocaña A, Lluch C (2001) Effects of salinity on protein and lipopolysaccharide pattern in a salt-tolerant strain of Mesorhizobium ciceri. J Appl Microbiol 90:476–481. doi: 10.1046/j.1365-2672.2001.01269.x PubMedCrossRefGoogle Scholar
  284. Spaink HP, Okker RJH, Wijffelman CA, Tak T, Goosen-de-Roo L, Pees E, van Brussel AAN, Lugtenberg BJJ (1989) Symbiotic properties of rhizobia containing a flavonoid-independent hybrid nodD product. J Bacteriol 171:4045–4053PubMedGoogle Scholar
  285. Spiertz JHJ (2010) Nitrogen, sustainable agriculture and food security. A review. Agron Sustain Dev 30:43–55. doi: 10.1051/agro:2008064 CrossRefGoogle Scholar
  286. Sprent JI, Odee DW, Dakora FD (2010) African legumes: a vital but under-utilized resource. J Exp Bot 61:1257–1265. doi: 10.1093/jxb/erp342 PubMedCrossRefGoogle Scholar
  287. Streeter JG (2003) Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation. J Appl Microbiol 95:484–491. doi: 10.1046/j.1365-2672.2003.02017.x PubMedCrossRefGoogle Scholar
  288. Suzuki A, Yamashita K, Ishihara M, Nakahara KI, Abe M, Kucho KI, Uchiumi T, Higashi S, Arima S (2008) Enhanced symbiotic nitrogen fixation by Lotus japonicus containing an antisense beta-1, 3-glucanase gene. Plant Biotechnol 25:357–360CrossRefGoogle Scholar
  289. Swaraj K, Bishnoi NR (1999) Effect of salt stress on nodulation and nitrogen fixation in legumes. Indian J Exp Bot 37:843–848Google Scholar
  290. Szabolcs I (1994) Soils and salinisation. In: Pessarakali M (ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 3–11Google Scholar
  291. Talibart R, Jebbar M, Gouesbet G, Himdi-Kabbab S, Wroblewski H, Blanco C, Bernard T (1994) Osmoadaptation in rhizobia: ectoine-induced salt tolerance. J Bacteriol 176:5210–5217PubMedGoogle Scholar
  292. Talibart R, Jebbar M, Gouffi K, Pichereau V, Gouesbet G, Blanco C, Bernard T, Pocard J (1997) Transient accumulation of glycine betaine and dynamics of endogenous osmolytes in salt-stressed cultures of Sinorhizobium meliloti. Appl Environ Microbiol 63:4657–4663PubMedGoogle Scholar
  293. Tang R, Li C, Xu K, Du YH, Xia T (2010) Isolation, functional characterization, and expression pattern of a vacuolar Na+/H+ antiporter gene TrNHX1 from Trifolium repens L. Plant Mol Biol Rep 28:102–111. doi: 10.1007/s11105-009-0135-y CrossRefGoogle Scholar
  294. Teakle NL, Real D, Colmer TD (2006) Growth and ion relations in response to combined salinity and waterlogging in the perennial forage legume Lotus corniculatus and Lotus tenuis. Plant Soil 289:369–383. doi: 10.1007/s11104-006-9146-8 CrossRefGoogle Scholar
  295. Teakle NL, Snell A, Real D, Barrett-Lennard EG, Colmer TD (2010) Variation in salinity tolerance, early shoot mass and shoot ion concentration within Lotus tenuis: towards a perennial pasture legume for saline land. Crop Pasture Sci 61:379–388. doi: 10.1071/CP09318 CrossRefGoogle Scholar
  296. Thrall PH, Millsom DA, Jeavons AC, Waayers M, Harvey GR, Bagnall DJ, Brockwell J (2005) Seed inoculation with effective root-nodule bacteria enhances revegetation success. J Appl Ecol 42:740–751. doi: 10.1111/j.1365-2664.2005.01058.x CrossRefGoogle Scholar
  297. Thrall PH, Broadhurst LM, Hoque MS, Bagnall DJ (2009) Diversity and salt tolerance of native Acacia rhizobia isolated from saline and non-saline soils. Austral Ecol 34:950–963. doi: 10.1111/j.1442-9993.2009.01998.x CrossRefGoogle Scholar
  298. Toderich KN, Shuyskaya EV, Ismail S, Gismatullina LG, Radjabov T, Bekchanov BB, Aralova DB (2009) Phytogenetic resources of halophytes of central Asia and their role for rehabilitation of sandy desert degraded rangelands. Land Degrad Dev 20:386–396. doi: 10.1002/ldr.936 CrossRefGoogle Scholar
  299. Tognetti VB, Palatnik JF, Fillat MF, Melzer M, Hajirezael M-R, Valle EM, Carrillo N (2006) Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broad-range stress tolerance. Plant Cell 18:2035–2050. doi: 10.1105/tpc.106.042424 PubMedCrossRefGoogle Scholar
  300. Tognetti VB, Monti MR, Valle EM, Carrillo N, Smania A (2007a) Detoxification of 2, 4-dinitrotoluene by transgenic plants expressing a bacterial flavodoxin. Environ Sci Technol 41:4071–4076. doi: 10.1021/es070015y PubMedCrossRefGoogle Scholar
  301. Tognetti VB, Zurbriggen MD, Morandi EN, Fillat MF, Valle EM, Hajirezael M-R, Carrillo N (2007b) Enhanced plant tolerance to iron starvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin. Proc Natl Acad Sci USA 104:11495–11500. doi: 10.1073/pnas.0704553104 PubMedCrossRefGoogle Scholar
  302. Tran LSPT, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi SK (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623–20628. doi: 10.1073/pnas.0706547105 PubMedCrossRefGoogle Scholar
  303. Trevors JT (1986) Plasmid curing in bacteria. FEMS Microbiol Rev 32:149–157CrossRefGoogle Scholar
  304. Triplett EW, Barta TM (1987) Trifolitoxin production and nodulation are necessary for the expression of superior nodulation competitiveness by Rhizobium leguminosarum bv. trifolii strain T24 on clover. Plant Physiol 85:335–342. doi: 10.1104/pp.85.2.335 PubMedCrossRefGoogle Scholar
  305. Tu JC (1981) Effect of salinity on Rhizobium-root hair interaction, nodulation and growth of soybean. Can J Plant Sci 61:231–239. doi: 10.4141/cjps81-035 CrossRefGoogle Scholar
  306. Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Physiol Plant Mol Biol 48:493–523. doi: 10.1146/annurev.arplant.48.1.493 PubMedCrossRefGoogle Scholar
  307. Van Dillewijn P, Soto MJ, Villadas PJ, Toro N (2001) Construction and environmental release of a Sinorhizobium meliloti strain genetically modified to be more competitive for alfalfa nodulation. Appl Environ Microbiol 67:3860–3865. doi: 10.1128/AEM.67.9.3860-3865.2001 PubMedCrossRefGoogle Scholar
  308. Van Dillewijn P, Soto MJ, Villadas PJ, Toro N (2002) Effect of a Sinorhizobium meliloti strain with a modified putA gene on the rhizosphere microbial community of alfalfa. Appl Environ Microbiol 67:4201–4208. doi: 10.1128/AEM.68.9.4201-4208.2002 CrossRefGoogle Scholar
  309. Van Heerden PDR, Kiddle G, Pellny TK, Mokwala PW, Jordaan A, Strauss AJ, De Beer M, Schlueter U, Kunert KJ, Foyer CH (2008) Regulation of respiration and the oxygen diffusion barrier in soybean protect symbiotic nitrogen fixation from chilling-induced inhibition and shoots from premature senescence. Plant Physiol 148:316–327. doi: 10.1104/pp.108.123422 PubMedCrossRefGoogle Scholar
  310. Vanderlinde EM, Muszynski A, Harrison JJ, Koval SF, Foreman DL, Ceri H, Kannenberg EL, Carlson RW, Yost CK (2009) Rhizobium leguminosarum biovar viciae 3841, deficient en 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired in dessication tolerance, biofilm formation and motility. Microbiol SGM 155:3055–3069. doi: 10.1099/mic.0.025031-0 CrossRefGoogle Scholar
  311. Vanderlinde EM, Harrison JJ, Muszynski A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC transporter required for desicattion tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Ecol 71:327–340. doi: 10.1111/j.1574-6941.2009.00824.x PubMedCrossRefGoogle Scholar
  312. Vargas AAT, Graham PH (1989) Cultivar and pH effects on competition for nodules sites between isolates of Rhizobium in beans. Plant Soil 117:195–200. doi: 10.1007/BF02220712 CrossRefGoogle Scholar
  313. Vargas MAT, Hungria M (1997) Fixação biológica do nitrogen na cultura da soja. In: Vargas MAT, Hungria M (eds) Biologia dos Solos de Cerrados. EMBRAPA-CPAC, Planaltina, pp 297–360Google Scholar
  314. Vargas LK, Lisboa BB, Schlindwein G, Granada CE, Giongo A, Beneduzi A, Passaglia LMP (2009) Occurrence of plant growth-promoting traits in clover-nodulating rhizobia strains isolated from different soils in Rio Grande do Sul State. Rev Bras Ciênc Solo 33:1227–1235. doi: 10.1590/S0100-06832009000500016 CrossRefGoogle Scholar
  315. Varshney RK, Hiremath PJ, Lekha P, Kashiwagi J, Balaji J, Deokar AA, Vadez V, Xiao Y, Srinivasan R, Gaur PM, Siddique KHM, Town CD, Hoisington DA (2009) A comprehensive resource of drought- and salinity-responsive ESTs for gene discovery and marker development in chickpea (Cicer arietinum L.). BMC Genomics 10:523. doi: 10.1186/1471-2164-10-523 PubMedCrossRefGoogle Scholar
  316. Velthof GL, Oudendag D, Witzke HP, Asman WAH, Klimont Z, Oenema O (2009) Integrated assessment of nitrogen emissions form agriculture in EU-27 using MITERRA EUROPE. J Environ Qual 38:402–417. doi: 10.2134/jeq2008.0108 PubMedCrossRefGoogle Scholar
  317. Verdoy D, Lucas MM, Manrique E, Covarrubias AA, De Felipe MR, Pueyo JJ (2004) Differential organ-specific response to salt stress and water deficit in nodulated bean (Phaseolus vulgaris). Plant Cell Environ 27:757–767. doi: 10.1111/j.1365-3040.2004.01179.x CrossRefGoogle Scholar
  318. Verdoy D, Coba de la Peña T, Redondo FJ, Lucas MM, Pueyo JJ (2006) Transgenic Medicago truncatula plants that accumulate proline display nitrogen-fixing activity with enhanced tolerance to osmotic stress. Plant Cell Environ 29:1913–1923. doi: 10.1111/j.1365-3040.2006.01567.x PubMedCrossRefGoogle Scholar
  319. Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91:127–141. doi: 10.1016/S0168-1656(01)00333-9 PubMedCrossRefGoogle Scholar
  320. Vignolio OR, Fernández ON, Maceira NO (1999) Flooding tolerance in five populations of Lotus glaber Mill. (Syn. Lotus tenuis Waldst. et. Kit.). Aust J Agric Res 50:555–559. doi: 10.1071/A98112 CrossRefGoogle Scholar
  321. Villar-Salvador P, Valladares F, Domínguez-Lerena S, Ruíz-Díez B, Fernández-Pascual M, Delgado A, Penuelas JL (2008) Functional traits related to seedling performance in the Mediterranean leguminous shrub Retama sphaerocarpa: insights from a provenance, fertilization, and rhizobial inoculation study. Environ Exp Bot 64:145–154. doi: 10.1016/j.envexpbot.2008.04.005 CrossRefGoogle Scholar
  322. Vriezen JAC, De Bruijn FJ, Nüsslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen and temperature. Appl Environ Microbiol 73:3451–3459. doi: 10.1128/AEM.02991-06 PubMedCrossRefGoogle Scholar
  323. Wang ET, Martínez-Romero E (2000) Phylogeny of root- and stem-nodule bacteria associated with legumes. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for analysis of a biological process. Horizon Scientific, Wymondham, pp 177–186Google Scholar
  324. Watkin ELJ, O’Hara GW, Glenn AR (2003) Physiological responses to acid stress of an acid-soil tolerant and an acid-soil sensitive strain of Rhizobium leguminosarum biovar trifolii. Soil Biol Biochem 35:621–624. doi: 10.1016/S0038-0717(03)00012-9 CrossRefGoogle Scholar
  325. Wei W, Jiang J, Li X, Wang L, Yang SS (2004) Isolation of salt-sensitive mutants from Sinorhizobium meliloti and characterization of genes involved in salt tolerance. Lett Appl Microbiol 39:278–283. doi: 10.1111/j.1472-765X.2004.01577.x PubMedCrossRefGoogle Scholar
  326. Wei GH, Yang XY, Zhang ZX, Yang YZ, Lindström K (2008) Strain Mesorhizobium sp. CCNWGX035: a stress-tolerant isolate from Glycyrrhiza glabra displaying a wide host range for nodulation. Pedosphere 18:102–112. doi: 10.1016/S1002-0160(07)60108-8 CrossRefGoogle Scholar
  327. Weir BS (2009). The current taxonomy of rhizobia. New Zealand rhizobia website. Available at Partially updated 14th September 2009
  328. Weisskopf L, Akello P, Milleret R, Khan ZR, Schulthess F, Gobat J-M, Le Bayon R-C (2009) White lupin leads to increased maize yield through a soil fertility-independent mechanism: a new candidate for fighting Striga hermonthica infestation? Plant Soil 319:101–114. doi: 10.1007/s11104-008-9853-4 CrossRefGoogle Scholar
  329. Winicov I, Bastola DR (1999) Transgenic overexpression of the transcription factor Alfin1 enhances expression of the endogenous MsPRP2 gene in alfalfa and improves salinity tolerance of the plants. Plant Physiol 120:473–480. doi: 10.1104/pp.120.2.473 PubMedCrossRefGoogle Scholar
  330. Winter E, Läuchli A (1982) Salt tolerance of Trifolium alexandrinum L.: I. Comparison of the salt response of Trifolium alexandrinum and T. pratense. Aust J Plant Physiol 9:221–226. doi: 10.1071/PP9820221 Google Scholar
  331. Yajima A, van Brussel AA, Schripsema J, Nukada T, Yabuta G (2008) Synthesis and stereochemistry–activity relationship of small bacteriocin, an autoinducer of the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum. Org Lett 10:2047–2050. doi: 10.1021/ol8005198 PubMedCrossRefGoogle Scholar
  332. Yanni YG, Rizk RY, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114. doi: 10.1023/A:1004269902246 CrossRefGoogle Scholar
  333. Yanni YG, Rizk RY, El-Fattah FKA, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martínez-Molina E, Mateos P, Velazquez E, Wopereis J, Triplett E, Umali-Garcia M, Anarna JA, Rolfe BG, Ladha JK, Hill J, Mujoo R, Ng PK, Dazzo FB (2001) The beneficial plant-growth promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust J Plant Physiol 28:845–870. doi: 10.1071/PP01069 Google Scholar
  334. Yousef N, Pistorius EK, Michel KP (2003) Comparative analysis of idiA and isiA transcription under iron starvation and oxidative stress in Synechococcus elongatus PCC 7942 wild-type and selected mutants. Arch Microbiol 180:471–483. doi: 10.1007/s00203-003-0618-4 PubMedCrossRefGoogle Scholar
  335. Zahran HH (1991) Conditions for successful Rhizobium–legume symbiosis in saline environments. Biol Fertil Soils 12:73–80. doi: 10.1007/BF00369391 CrossRefGoogle Scholar
  336. Zahran HH (1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989PubMedGoogle Scholar
  337. Zahran HH (2001) Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnology. J Biotechnol 91:143–153. doi: 10.1016/S0168-1656(01)00342-X PubMedCrossRefGoogle Scholar
  338. Zahran HH, Sprent JI (1986) Effects of sodium chloride and polyethylene glycol on root-hair infection and nodulation of Vicia faba L. plant by Rhizobium leguminosarum. Planta 167:303–309. doi: 10.1007/BF00391332 CrossRefGoogle Scholar
  339. Zdunek-Zastocka E (2008) Molecular cloning, characterization and expression analysis of three aldehyde oxidase genes from Pisum sativum L. Plant Physiol Biochem 46:19–28. doi: 10.1016/plaphy.2007.09.011 PubMedCrossRefGoogle Scholar
  340. Zengeni R, Giller KE (2007) Effectiveness of indigenous soyabean rhizobial isolates to fix nitrogen under field conditions of Zimbabwe. Symbiosis 43:129–135Google Scholar
  341. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42:689–707. doi: 10.1111/j.1365-313X.2005.02405.x PubMedCrossRefGoogle Scholar
  342. Zheng M, Doan B, Schneider TD, Storz G (1999) OxyR and SoxRS regulation of fur. J Bacteriol 181:4639–4643PubMedGoogle Scholar
  343. Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273. doi: 10.1146/annurev.arplant.53.091401.143329 CrossRefGoogle Scholar

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© INRA and Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Instituto de Ciencias Agrarias, CSICMadridSpain

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