Abstract
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.
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References
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
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
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
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
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
Allen ON, Allen EK (1991) The leguminosae: a source book of characteristics, uses and nodulation. University of Wisconsin Press, Madison
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
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
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
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
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 27:189–212
Ashraf M (1994) Organic-substances responsible for salt tolerance in Eruca sativa. Biol Plant 36:255–259. doi:10.1007/BF02921095
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
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
Aydi S, Drevon JJ, Abdelly C (2004) Effect of salinity on root-nodule conductance to the oxygen diffusion in the Medicago truncatula–Sinorhizobium meliloti symbiosis. Plant Physiol Biochem 42:833–840. doi:10.1016/j.plaphy.2004.10.003
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
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
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 66:4292–4299
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
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
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
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
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
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
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
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
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
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
Biswas JC, Ladha JK, Dazzo FB (2000a) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650
Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolfe BG (2000b) Rhizobial inoculation influences seedling vigor and yield of rice. Agron J 92:880–886
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
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 28–47
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
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
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
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
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 65:2072–2077
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
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
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 60:3815–3832
Botsford JL, Lewis TA (1990) Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress. Appl Environ Microbiol 56:488–494
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
Breedveld MW, Zevenhuizen LPTM, Zehnder AJB (1991) Osmotically induced oligo and polysaccharide synthesis by Rhizobium meliloti SU-47. J Gen Microbiol 136:2511–2519
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 139:3157–3163
Brewin NJ (1991) Development of legume root nodules. Annu Rev Cell Biol 7:191–226. doi:10.1146/annurev.cb.07.110191.001203
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
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
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
Busse MD, Bottomley PJ (1989) Growth and nodulation responses of Rhizobium meliloti to water stress induced by permeating and nonpermeating solutes. Appl Environ Microbiol 55:2431–2436
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
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
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
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
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 65:2716–2722
Chandra A (2009) Diversity among Stylosanthes species: habitat, edaphic and agro-climatic affinities leading to cultivar development. J Environ Biol 30:471–478
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
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
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 57:2005–2011
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
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
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 press
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
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 187–205
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
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
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 3:791–794
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
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
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
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
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
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 83:3811–3815
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
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
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
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
Davies MJ, Puppo A (1992) Direct detection of a globin-derived radical in lehaemoglobin treated with peroxides. Biochem J 281:197–201
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
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
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
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
Ding H, Hynes MF (2009) Plasmid transfer system in the rhizobia. Can J Microbiol 55:917–927. doi:10.1139/W09-056
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
Djekoun A, Planchon C (1991) Water status effect on dinitrogen fixation and photosynthesis in soybean. Agron J 83:316–322
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
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
Eapen S (2008) Advances in development of transgenic pulse crops. Biotechnol Adv 26:162–168. doi:10.1016/j.biotechadv.2007.11.001
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
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
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
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 8:979–985
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
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 59–65
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
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
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
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
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
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
Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72. doi:10.1007/s00344-003-0032-9
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
Fougère F, Le Rudulier D (1990) Uptake of glycine betaine and its analogues by bacteroids of Rhizobium meliloti. J Gen Microbiol 136:157–163
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
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
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
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
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
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
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
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
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
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
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
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
Giller KE, Wilson K (1991) Nitrogen fixation in tropical cropping systems. CAB International, Wallingford
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 112–130
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
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
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
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
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
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
Gouffi K, Pica N, Pichereau V, Blanco C (1999) Disaccharides as a new class of nonaccumulated osmoprotectants for Sinorhizobium meliloti. Appl Environ Microbiol 65:1491–1500
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
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
Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877. doi:10.1104/pp.017004
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
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
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
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
Herridge DF, Danso SKA (1995) Enhancing crop legume nitrogen fixation through selection and breeding. Plant Soil 174:51–82. doi:10.1007/BF00032241
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
Hinde R, Trautman DA (2002) Symbiosomes. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer Academic, Netherlands, pp 207–220
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
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
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
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
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
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 44:135–140
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 368–373
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
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
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
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
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
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
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
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
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 http://www.plantmanagementnetwork.org/sub/cm/review/2004/yield/. doi:10.1094/CM-2004-0301-07-RV
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 113–129
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
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
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
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
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
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
Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nat Rev Microbiol 5:619–633. doi:10.1038/nrmicro1705
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 235–244
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
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
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
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
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 88:424–438
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
Kostopoulou P, Vrahnakis MS, Merou T, Lazaridou M (2010) Perennial-like adaptation mechanisms of annual legumes to limited irrigation. J Environ Biol 31:311–314
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
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
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
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 171–188
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
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
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 61:3592–3597
Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Biol 49:199–222. doi:10.1146/annurev.arplant.49.1.199
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
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 41:11–16
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 Press
Lloret L, Martínez-Romero E (2005) Evolution and phylogeny of rhizobia. Rev Latinoam Microbiol 47:43–60
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 61:3701–3704
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 64:1024–1028
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Meyer DW, Badaruddin M (2001) Frost tolerance of ten seedling legume species at four growth stages. Crop Sci 41:1838–1842
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
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
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
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
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
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
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
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 43:83–96
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
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
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
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
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
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
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
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
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
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
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 46:417–425
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
Oren A (1999) Bioenergetics aspects of halophilism. Microbiol Mol Biol Rev 63:334–348
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 65:2833–2840
Ormeño-Orrillo E (2005) Lipopolysaccharides of rhizobiaceae: structure and biosynthesis. Rev Latinoam Microbiol 47:165–175
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
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
Pandey RK, Herrera WAT, Villepas AN, Pendelton JW (1984) Drought response of grain legumes under irrigation gradient. III. Plant growth. Agron J 76:557–560
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
Parker CA (1986) Legumes and nitrogen fixation; their importance for farming in the future. Impact Sci Soc 36:153–164
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
Peoples MB, Crasswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39. doi:10.1007/BF00011308
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
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
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
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
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
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
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 6:325–334
Puppo A, Halliwell B (1988) Generation of hydroxyl radicals by soybean nodule leghaemoglobin. Planta 173:405–410. doi:10.1007/BF00401028
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
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
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
Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45:481–487. doi:10.1023/A:1022308229759
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
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
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
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
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
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
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
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
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 108:11–20
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
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
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 64:2630–2633
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
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
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
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
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
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
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
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
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
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
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
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
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 146:541–546
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 90:1638–1650
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
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
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
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
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 737–760
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 33:561–566
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
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
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
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
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 57–80
Smith LT, Smith GM (1989) An osmoregulated dipeptide in stressed Rhizobium meliloti. J Bacteriol 171:4714–4717
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 65:2015–2019
Soberón-Chavez G, Nájera R, Oliveira H, Segovia L (1986) Genetic rearrangements of a Rhizobium phaseoli symbiotic plasmid. J Bacteriol 167:487–491
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
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
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
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 171:4045–4053
Spiertz JHJ (2010) Nitrogen, sustainable agriculture and food security. A review. Agron Sustain Dev 30:43–55. doi:10.1051/agro:2008064
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
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
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 25:357–360
Swaraj K, Bishnoi NR (1999) Effect of salt stress on nodulation and nitrogen fixation in legumes. Indian J Exp Bot 37:843–848
Szabolcs I (1994) Soils and salinisation. In: Pessarakali M (ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 3–11
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 176:5210–5217
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 63:4657–4663
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
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
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
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
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
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
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
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
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
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
Trevors JT (1986) Plasmid curing in bacteria. FEMS Microbiol Rev 32:149–157
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
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
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
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
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
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
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
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
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
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 297–360
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
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
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
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
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
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
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
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
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
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 177–186
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
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
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
Weir BS (2009). The current taxonomy of rhizobia. New Zealand rhizobia website. Available at http://www.rhizobia.co.nz/taxonomy/rhizobia.htlm. Partially updated 14th September 2009
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
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
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
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
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
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
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
Zahran HH (1991) Conditions for successful Rhizobium–legume symbiosis in saline environments. Biol Fertil Soils 12:73–80. doi:10.1007/BF00369391
Zahran HH (1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
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
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
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
Zengeni R, Giller KE (2007) Effectiveness of indigenous soyabean rhizobial isolates to fix nitrogen under field conditions of Zimbabwe. Symbiosis 43:129–135
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
Zheng M, Doan B, Schneider TD, Storz G (1999) OxyR and SoxRS regulation of fur. J Bacteriol 181:4639–4643
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
Acknowledgements
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.
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Coba de la Peña, T., Pueyo, J.J. Legumes in the reclamation of marginal soils, from cultivar and inoculant selection to transgenic approaches. Agron. Sustain. Dev. 32, 65–91 (2012). https://doi.org/10.1007/s13593-011-0024-2
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DOI: https://doi.org/10.1007/s13593-011-0024-2