Skip to main content

Legumes–Microbes Interactions Under Stressed Environments

  • Chapter

Abstract

Legumes and their associated microbes are common and exist in different environments. Microbes have evolved many mechanisms, which enable them to cope with changing environment. Resilience to these changes is essential to their survival and depends on rapid and efficient control of genetic expression and metabolic responses. Legumes establish several mutual, antagonistic, and beneficial interactions with microbes, which are occasionally subject to unfavorable (stressed) environmental conditions. Stressed terrestrial environments include, deserts with arid climate (warm and dry), salt-affected soils, alkaline and acidic soils, soils contaminated with toxic metals, and nutrient deficiency. During the course of development, microbes inherit traits that enable them to survive under undesirable conditions. Legumes, however, are stress-sensitive plants, and only few of them can withstand stressed environments. Legume rhizospheres colonized by a consortium of microbes are influenced by nutrient-rich root exudates. Legumes and microbes exhibit mutual relationships such as, association, symbiosis, and parasitism and live together in one habitat for long periods. The associated microorganisms include plant-growth-promoting rhizobacteria (PGPR), which are either nitrogen-fixing or not, and many fungi. Symbiotic organisms include mycorrhiza and the root-nodule bacteria (rhizobia). Recent molecular and genetic tools have assisted in discovering new effective stress-tolerant microbes. This chapter broadens the scope of microbes interfering with growth of legumes – a relationship that has been misunderstood to be restricted to rhizobia. Therefore, future investigations have to consider a consortium of microbes in order to improve productivity of legume crops.

Keywords

  • Salt Stress
  • Arbuscular Mycorrhizal
  • Salt Tolerance
  • Plant Growth Promote Rhizobacteria
  • Glycine Betaine

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-211-99753-6_15
  • Chapter length: 35 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   249.00
Price excludes VAT (USA)
  • ISBN: 978-3-211-99753-6
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout

References

  • Aguirreolea J, Sánchez-Díaz M (1989) CO2 evolution by nodulated roots in Medicago sativa L. under water stress. J Plant Physiol 134:598–602

    CAS  CrossRef  Google Scholar 

  • Al-Sherif EA, Zahran HH, Atteya MA (2004) Nitrogen fixation and chemical composition of wild annual legumes at Beni-Suef Governorate, Egypt. Egypt J Biol 6:32–38

    Google Scholar 

  • Alva AK, Assher CJ, Edwards DG (1990) Effect of solution pH, external calcium concentration, and aluminm activity on nodulation and early growth of cowpea. Aust J Agric Res 41:359–365

    CAS  CrossRef  Google Scholar 

  • Apse MP, Dharon GS, Snedden WA, Bumerold E (1999) Salt tolerance conferred by overexpression of a vascular Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    PubMed  CAS  CrossRef  Google Scholar 

  • Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816

    PubMed  CAS  CrossRef  Google Scholar 

  • Ashraf M (1994) Breeding for salinity tolerance in plants. Crit Rev Plant Sci 13:17–42

    Google Scholar 

  • Ashraf M, Waheed A (1990) Screening of local/exotic accessions of lentil (Lens culinaris) for salt tolerance at two growth stages. Plant Soil 128:167–176

    CAS  CrossRef  Google Scholar 

  • Aydi S, Drevon J-J, 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

    PubMed  CAS  CrossRef  Google Scholar 

  • Barassi C, Ayrault G, Creus C, Sueldo R, Sobrero M (2006) Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci Hortic 109:8–14

    CAS  CrossRef  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. CRC Crit Rev Plant Sci 24:23–58

    CAS  CrossRef  Google Scholar 

  • 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

    CAS  CrossRef  Google Scholar 

  • Beck DP, Munns DN (1985) Effect of calcium on the phosphorous nutrition of Rhizobium meliloti. Soil Sci Soc Am J 49:334–337

    CAS  CrossRef  Google Scholar 

  • Belimov AA, Kojemiakov AP, Chuvarliyeva CV (1995) Interaction between barley and mixed cultures of nitrogen fixing and phosphate-solubilizing bacteria. Plant Soil 173:29–37

    CAS  CrossRef  Google Scholar 

  • Benaroudj N, Lee DH, Al G (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 276:24261–24267

    PubMed  CAS  CrossRef  Google Scholar 

  • Bhatnagar-Mathur P, Devi MJ, Reddy DS, Lavanya M, Vadez V, Serraj R, Yamaguchi-Shinozaki K, Sharma KK (2007) Stress-inducible expression of At DREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions. Plant Cell Rep 26:2071–2082

    PubMed  CAS  CrossRef  Google Scholar 

  • Biró B, Köves-Péchy K, Vörös I, Takács T, Eggenberg P, Strasser RJ (2000) Interrelation between Azospirillum and Rhizobium nitrogen-fixers and arbuscular mycorrhizal fungi in the rhizosphere of alfalfa at sterile, AMF-free or normal soil conditions. Appl Soil Ecol 15:159–168

    CrossRef  Google Scholar 

  • Biró B, Tiricz H, Morvai B (2001) Investigations on the vitality, resistance and diversity of metal-adapted and non-adapted Rhizobium strains. Acta Microbiol Immunol Hung 48:156–157

    CrossRef  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress; a review. Ann Bot 91:179–194

    PubMed  CAS  CrossRef  Google Scholar 

  • Blumwald E, Gelli A (1997) Secondary inorganic ion transport in plant vacuoles. Adv Bot Res 25:401–407

    CAS  CrossRef  Google Scholar 

  • Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151

    PubMed  CAS  CrossRef  Google Scholar 

  • Bohin A, Bouchart F, Richet C, Kol O, Leroy V, Timmerman P, Huet G, Bohin J, Zane J (2005) GC/MS identification and quantification of constituents of bacterial lipids and glycoconjugates obtained after methanolysis as heptafuorobutyrate derivatives. Anal Biochem 340:231–244

    PubMed  CAS  CrossRef  Google Scholar 

  • Boscari A, Mandon K, Dupont L, Poggi M-C, Le Rudulier D (2002) BetS is a major glycine betaine/proline betaine transporter required for early osmotic adjustment in Sinorhizobium meliloti. J Bacteriol 184:2654–2663

    PubMed  CAS  CrossRef  Google Scholar 

  • Boscari A, Mandon K, Poggi M-C, Le Rudulier D (2004) Functional expression of Sinorhizobium meliloti BetS, a high-affinity betaine transporter, in Bradyrhizobium japonicum USDA110. Appl Environ Microbiol 70:5916–5922

    PubMed  CAS  CrossRef  Google Scholar 

  • Boschma SP, Lodge GM, Harden S (2008) Herbage mass and persistence of pasture legumes and grasses at two potentially different saline and waterlogged sites in northern New South Wales. Aust J Exp Agric 48:553–567

    CrossRef  Google Scholar 

  • Bouhmouch I, Souad-Mouhsine B, Brhada F, Aurag J (2005) Influence of host cultivars and Rhizobium species on the growth and symbiotic performance of Phaseolus vulgaris under salt stress. J Plant Physiol 162:1103–1113

    PubMed  CAS  CrossRef  Google Scholar 

  • Boumahdi M, Mary P, Hornez JP (2001) Changes in fatty acid composition and degree of unsaturation of (brady) rhizobia as a response to phases of growth, reduced water activities and mild desiccation. Antonie Van Leeuwenhoek 79:73–79

    PubMed  CAS  CrossRef  Google Scholar 

  • Brockwell J, Pilka A, Holliday RA (1991) Soil pH is the major determinant of the number of naturally-occurring Rhizobium meliloti in non-cultivated soils in New South Wales. Aust J Exp Agric 31:211–219

    CrossRef  Google Scholar 

  • Burd IG, Dixon DG, Glick BR (2000) Plant growth promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245

    PubMed  CAS  CrossRef  Google Scholar 

  • Carrasco JA, Armario P, Pajuelo E, Burgos A, Caviedes MA, Lopez R, Chamber MA, Palomares AJ (2005) Isolation and characterization of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spell at the Aznalocollar pyrite mine. Soil Biol Biochem 37:1131–1140

    CAS  CrossRef  Google Scholar 

  • Cassán F, Maiale S, Masciarelli O, Vidal A (2009) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur J Soil Biol 45:12–19

    CrossRef  CAS  Google Scholar 

  • Castro-Sowiniski S, Herschkovitz Y, Okon Y, Jurkevitch E (2007) Effects of inoculation with plant growth-promoting rhizobacteria on resident rhizosphere microorganisms. FEMS Microbiol Lett 276:1–11

    CrossRef  CAS  Google Scholar 

  • Chang RZ, Chen YW, Shao GH, Wan CW (1994) Effect of salt stress on agronomic characters and chemical quality of seeds in soybean. Soybean Sci 13:101–105

    Google Scholar 

  • Chen W-M, Lee TM, Lan C-C, Cheng C-P (2000) Characterization of halotolerant rhizobia isolated from root nodules of Canavalia rosea from seaside areas. FEMS Microbiol Ecol 34:9–16

    PubMed  CAS  CrossRef  Google Scholar 

  • Chen J-L, Lin S, Lin L-P (2006) Rhizobial surface biopolymers and their interaction with lectin measured by atomic force microscopy. World J Microbiol Biotechnol 22:565–570

    CAS  CrossRef  Google Scholar 

  • Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

    CAS  CrossRef  Google Scholar 

  • Coba De La Peña T, Cárcamo CB, Almonacid L, Zaballos A, Lucas MM, Balomenos D, Pueyo JJ (2008) A salt stress-responsive cytokinin receptor homologue isolated from Medicago sativa nodules. Planta 227:769–779

    PubMed  CrossRef  CAS  Google Scholar 

  • Cooper JE (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365

    PubMed  CAS  CrossRef  Google Scholar 

  • Csonka LN (1991) Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol 45:569–606

    PubMed  CAS  CrossRef  Google Scholar 

  • Dajic Z (2006) Salt stress. In: Madhava Rao VK, Raghavendra AS, Janardhan Reddy K (eds) Physiology and molecular biology of stress tolerance in plants. Springer, Netherlands, pp 41–99

    CrossRef  Google Scholar 

  • Dardanelli MS, Fernández De Córdoba FJ, Espuny MR, Rodríguez Carvajal MA, Soria Díaz ME, Gil Serrano AM (2008) Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and nod factor production under salt stress. Soil Biol Biochem 40:2713–2721

    CAS  CrossRef  Google Scholar 

  • Debelle F, Moulin L, Mangin B, Denarie J, Boivin C (2001) Nod genes and nod signals and the evolution of the Rhizobium–legume symbiosis. Acta Biochim Pol 48:359–365

    PubMed  CAS  Google Scholar 

  • Denison RF, Kiers ET (2004) lifestyle alternatives of rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett 237:187–193

    PubMed  CAS  CrossRef  Google Scholar 

  • D'Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79–105

    CrossRef  Google Scholar 

  • Domínguez-Ferreras A, Pérez-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

    PubMed  CrossRef  CAS  Google Scholar 

  • Echeverria M, Scambato AA, Sannazzaro AI, Maiale S, Ruiz OA, Menéndez AB (2008) Phenotypic plasticity with respect to salt stress response by Lotus glaber: the role of its AM fungal and rhizobial symbionts. Mycorrhiza 18:317–329

    PubMed  CrossRef  Google Scholar 

  • Egamberdiyeva D, Hoflich G (2003) Effect of plant growth promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. J Arid Environ 56:293–301

    CrossRef  Google Scholar 

  • Egamberdiyeva D, Isalm KR (2008) Salt-tolerant rhizobacteria: plant growth promoting traits and physiological characterization within ecologically stressed environments. In: Ahmad I, Pichtel J, Hayat S (eds) Plant-bacteria interactions: strategies and techniques to promote plant growth. WILEY-VCH Verlag Gmbh & Co. KGaA, Weinheim, pp 257–281

    CrossRef  Google Scholar 

  • El-Komy HMA (2005) Coimmobilization of A. lipoferum and B. megaterium for plant nutrition. Food Technol Biotechnol 43:19–27

    Google Scholar 

  • Essendoubi M, Brhada F, Eljamail JE, Filali-Maltouf A, Bonnassie S, Georgeault S, Blanco C, Jebbar M (2007) Osmoadaptive responses in the rhizobia nodulating Acacia isolated from south-eastern Moroccan Sahara. Environ Microbiol 9:603–611

    PubMed  CAS  CrossRef  Google Scholar 

  • Estevéz J, Soria-Díaz ME, De Córdoba FF, Morón B, Manyani H, Gil A, Thomas-Oates J, Van Brussel AAN, Dardanelli MS, Sousa C, Megías M (2009) Different and new Nod factors produced by Rhizobium tropici CIAT899 following Na+ stress. FEMS Microbiol Lett 293:220–231

    PubMed  CrossRef  CAS  Google Scholar 

  • FAO (2005) Global network on integrated soil management for sustainable use of salt-affected soils. FAO Land and Plant Nutrition Management Service, Rome, Italy. http://www.fao.org.ag/agl/agll/spush

  • Galiana A, Gnahoua GM, Chaumont J, Lesueur D, Prin Y, Mallet B (1998) Improvement of nitrogen fixation in Acacia mangium through inoculation with Rhizobium. Agroforest Syst 40:297–307

    CrossRef  Google Scholar 

  • Galibert F, Finan TM, Long SR et al (2001) The composite gnome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672

    PubMed  CAS  CrossRef  Google Scholar 

  • Garg N, Manchanda G (2008) Effect of mycorrhizal inoculation on salt-induced nodule senescence in Cajanus cajan (pigeonpea). J Plant Growth Regul 17:115–124

    CrossRef  CAS  Google Scholar 

  • Garthwaite AJ, Von Bothmer R, Colmer TD (2005) Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl into the shoots. J Exp Bot 56:2365–2378

    PubMed  CAS  CrossRef  Google Scholar 

  • Geurts R, Fedorova E, Bisseling T (2005) Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol 8:346–352

    PubMed  CAS  CrossRef  Google Scholar 

  • Ghorbanli M, Ebrahimzadeh H, Sharifi M (2004) Effect of NaCl and mycorrhizal fungi on antioxidative enzymes in soybean. Biol Plant 48:575–581

    CAS  CrossRef  Google Scholar 

  • Giri B, Mukerji KG (2004) Mycorrhizal inoculation alleviates salt stress in Sesbania aegyptica and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312

    PubMed  CrossRef  Google Scholar 

  • Giri B, Kapoor R, Mukerji KG (2002) Va mycorrhizal techniques/VAM technology in establishment of plants under salinity stress conditions. In: Mukerji KG, Manorahari C, Singh J (eds) Techniques in mycrorrhizal studies. Kluwer, Dordrecht, The Netherland, pp 313–327

    Google Scholar 

  • Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175

    CrossRef  Google Scholar 

  • Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasiculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760

    PubMed  CAS  CrossRef  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    PubMed  CAS  CrossRef  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693

    PubMed  CAS  CrossRef  Google Scholar 

  • Graham PH, Vance CP (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crops Res 65:93–106

    CrossRef  Google Scholar 

  • Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877

    PubMed  CAS  CrossRef  Google Scholar 

  • Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martinez E, Arons SR, Quinto C (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for pH tolerance of Rhizobium tropici UMR 1899. Can J Microbiol 40:198–207

    CAS  CrossRef  Google Scholar 

  • Gualtieri G, Bisseling T (2000) The evolution of nodulation. Plant Mol Biol 42:181–194

    PubMed  CAS  CrossRef  Google Scholar 

  • Hamaoui B, Abbadi JM, Burdman S, Rashid A, Sarig A, Okon Y (2001) Effects of inoculation of Azospirillum brasilense on chickpeas (Cicer arietinum) and faba bean (Vicia faba) under different growth conditions. Agronomie 21:553–560

    CrossRef  Google Scholar 

  • Hamdy A (1990) Management practices under saline water irrigation. Acta Hortic 278:745–754

    Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1997) The involvement of cytokinins in plant responses to environmental stress. J Plant Growth Regul 23:79–103

    CAS  CrossRef  Google Scholar 

  • Hasegawa PM, Bressan R, Zhu J-K, Bohmert H-J (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    PubMed  CAS  CrossRef  Google Scholar 

  • Hatimi A (1999) Effect of salinity on the association between root symbionts and Acacia cyanophyla Lind: growth and nutrition. Plant Soil 216:93–101

    CAS  CrossRef  Google Scholar 

  • Herridge D, Rose I (2000) Breeding for enhanced nitrogen fixation in crop legumes. Field Crops Res 65:229–248

    CrossRef  Google Scholar 

  • Horie T, Schroeder JI (2004) Sodium transporters in plants. Diverse gene and physiological functions. Plant Physiol 136:2457–2462

    PubMed  CAS  CrossRef  Google Scholar 

  • Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris (L.). Plant Soil 149:95–102

    CAS  CrossRef  Google Scholar 

  • Hungria M, Stacey G (1997) Molecular signals exchanged between host plants and rhizobia, basic aspects and potential application in agriculture. Soil Biol Biochem 29:519–530

    CrossRef  Google Scholar 

  • Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with emphasis on Brazil. Field Crops Res 65:151–164

    CrossRef  Google Scholar 

  • Hungria M, Franco AA, Sprent JI (1993) New sources of high-temperature tolerant rhizobia for Phaseolus vulgaris (L.). Plant Soil 149:103–109

    CrossRef  Google Scholar 

  • Ibragimova MV, Rumyantseva ML, Onishchuk OP, Belova VS, Kurchak ON, Andronov EE, Dzyubenko NI, Simarov BV (2006) Symbiosis between the root-nodule bacterium Sinorhizobium meliloti and alfalfa (Medicago sativa) under salinization conditions. Microbiology 75:77–81

    CAS  CrossRef  Google Scholar 

  • Jebara S, Jebara M, Limam F, Aouani ME (2005) Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J Plant Physiol 162:929–936

    PubMed  CAS  CrossRef  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    PubMed  CAS  CrossRef  Google Scholar 

  • Jiang JQ, Wei W, Du BH, Li XH, Wang L, Yang SS (2004) Salt-tolerance genes involved in cation efflux and osmoregulation of Sinorhizobium fredii RT19 detected by isolation of Tn5 mutants. FEMS Microbiol Lett 239:139–146

    PubMed  CAS  CrossRef  Google Scholar 

  • Jimenez-Zurdo JI, Frugier F, Crespi MD, Kondorosi A (2000) Expression profiles of 22 novel molecular markers for organogenetic pathways acting in alfalfa nodule development. Mol Plant Microbe Interact 13:96–106

    PubMed  CAS  CrossRef  Google Scholar 

  • Jin H, Sun Y, Yang Q, Chao Y, Kang J, Jin H, Li Y, Margaret G (2009) Screening of genes induced by salt stress from Alfalfa. Mol Biol Rep. doi:10.1007/s11033-009-9590-7

    Google Scholar 

  • Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13

    PubMed  CAS  CrossRef  Google Scholar 

  • Katerji N, Van Hoorn JW, Hamdi A, Mastrorilli M, Oweis T, Erskine W (2001) Response of two varieties of lentil to soil salinity. Agric Water Managem 47:179–190

    CrossRef  Google Scholar 

  • Khadri M, Tejera NA, Lluch C (2007) Sodium chloride-ABA interaction in two common bean (Phaseolus vulgaris) cultivars differing in salinity tolerance. Environ Exp Bot 60:211–218

    CAS  CrossRef  Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Oves M (2009a) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem lett 7:1–19

    CrossRef  CAS  Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Ahemad M, Oves M (2009b) Functional diversity among plant growth-promoting rhizobacteria: current status. In: Khan MS, Zaidi A, Musarrat J (eds) Microbial strategies for crop improvement. Springer, Germany, pp 105–132

    CrossRef  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kiss E, Huguet T, Poinsot V, Batut J (2004) The typA gene is required for stress adaptation as well as for symbiosis of Sinorhizobium meliloti 1021 with certain Medicago truncatula lines. Mol Plant Microbe Interact 17:235–244

    PubMed  CAS  CrossRef  Google Scholar 

  • Kononowics AK, Nelson DE, Singh NK, Hasegawa PM, Bressan RA (1992) Regulation of the osmotin gene promoter. Plant Cell 4(513):524

    Google Scholar 

  • Kotb THS, Watanabe T, Ogino Y, Tanji KK (2000) Soil salinization in the Nile Delta and related policy issues in Egypt. Agric Water Manage 43:239–261

    CrossRef  Google Scholar 

  • Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg JJ (2004) Rhizo-remediation: a beneficial plant–microbe interaction. Mol Plant Microbe Interact 17:6–15

    PubMed  CAS  CrossRef  Google Scholar 

  • Kulkarni S, Nautiyal CS (1999) Characterization of high-tmperature tolerant rhizobia isolated from Prosopis juliflora grown in alkaline soil. J Gen Appl Microbiol 45:213–220

    PubMed  CAS  CrossRef  Google Scholar 

  • Lindström K, Lipsanen P, Kaijalainen S (1990) Stability of markers used for identification of two Rhizobium galegae inoculation strains after five years in the field. Appl Environ Microbiol 56:444–450

    PubMed  Google Scholar 

  • Liu K, Fu H, Bei K, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1325

    PubMed  CAS  CrossRef  Google Scholar 

  • López M, Herrera-Cervera JA, Iribarne C, Tejera NA, LLuch C (2008) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism. J Plant Physiol 165:641–650

    PubMed  CrossRef  CAS  Google Scholar 

  • Lovato MB, De Lemos Filho JP, Martins PS (1999) Growth responses of Stylosanthes humilis (Fabaceae) populations to saline stress. Environ Exp Bot 41:145–153

    CrossRef  Google Scholar 

  • L'taief B, Sifi B, Zaman-Allah M, Drevon J-J, Lachaâl M (2007) Effect of salinity on root-nodule conductance to the oxygen diffusion in the Cicer arietinumMesorhizobium ciceri symbiosis. J Plant Physiol 164:1028–1036

    PubMed  CrossRef  CAS  Google Scholar 

  • Macur RE, Wheeler JT, McDermott TR, Inskeep WP (2001) Microbial populations associated with the reduction and enhanced mobilization of arsenic in mine tailings. Environ Sci Technol 35:3676–3682

    PubMed  CAS  CrossRef  Google Scholar 

  • Mahdhi M, Mars M (2006) Genotypic diversity of rhizobia isolated from Retama raetam in arid regions of Tunisia. Ann Microbiol 56:305–311

    CAS  CrossRef  Google Scholar 

  • Mahdhi M, Nzoué A, De Lajudie P, Mars M (2008) Characterization of root-nodulating bacteria on Retama raetam in arid Tunisian soils. Prog Nat Sci 18:43–49

    CAS  CrossRef  Google Scholar 

  • Marañón T, Garcia LV, Troncoso A (1989) Salinity and germination of annual Melilotus from the Gauadalquivir delta (SW Spain). Plant Soil 119:223–228

    CrossRef  Google Scholar 

  • Marcar NE, Dart P, Sweeney C (1991) Effect of root zone salinity on growth and chemical composition of Acacia ampliceps B.R. Maslin, A. auriculiformis A. Cunn. Ex. Benth. and A. mangium Wild. at two nitrogen levels. New Phytol 119:567–573

    CAS  CrossRef  Google Scholar 

  • Mathesius U, Charon C, Rolfe BG, Kondorosi A, Crespi M (2000) Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv. trifolii inoculation or localized cytokinin addition. Mol Plant Microbe Interact 13:617–628

    PubMed  CAS  CrossRef  Google Scholar 

  • Mathesius U, Keijzers G, Natera SHA et al (2001) Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting. Proteomics 1:1424–1440

    PubMed  CAS  CrossRef  Google Scholar 

  • McKay IA, Djordjevic MA (1993) Production and excretion of nod metaboloites by Rhizobium leguminosarum bv. trifolii are disrupted by the same environmental factors that reduce nodulation in the field. Appl Environ Microbiol 59:3385–3392

    PubMed  CAS  Google Scholar 

  • Medeot DB, Bueno MA, Dardanelli MS, De Lema MG (2007) Additional changes in lipids of Bradyrhizobium SEMIA 6114 nodulating peanut as a response to growth temperature and salinity. Curr Microbiol 54:31–35

    PubMed  CAS  CrossRef  Google Scholar 

  • Melchior-Marroquin JI, Vargas-Hernandez JJ, Herrera-Cerrato R, Krishnamurthy L (1999) Screening Rhizobium spp. strains associated with Gliricidia sepium along an altidudinal transect in Veracruz, Mexico. Agroforest Syst 46:25–38

    CrossRef  Google Scholar 

  • Mhadhbi H, Jebara M, Zitoun A, Limam F, Aouani E (2008) Symbiotic effectiveness and response to mannitol-mediated osmotic stress of various chickpea–rhizobia associations. World J Microbiol Biotechnol 24:1027–1035

    CrossRef  Google Scholar 

  • Michiels J, Verreth C, Vnderleyden J (1994) Effects of temperature on bean-nodulating Rhizobium strains. Appl Environ Microbiol 60:1206–1212

    PubMed  CAS  Google Scholar 

  • Mills D, Zhang G, Benzioni A (2001) Effect of different salt and of ABA on growth and mineral uptake in jojoba shoots grown in vitro. J Plant Physiol 158:1031–1039

    CAS  CrossRef  Google Scholar 

  • Minchin FR (1997) Regulation of oxygen diffusion in legume nodules. Soil Biol Biochem 29:881–888

    CAS  CrossRef  Google Scholar 

  • Moawad H, Beck D (1991) Some characteristics of Rhizobium leguminosarum isolates from uninoculated field-grown lentil. Soil Biol Biochem 23:917–925

    CrossRef  Google Scholar 

  • Morón B, Soria-Díaz ME, Ault J et al (2005) Low pH changes the profile of nodulation factors produced by Rhizobium tropici CIAT899. Chem Biol 12:1029–1040

    PubMed  CrossRef  CAS  Google Scholar 

  • Mulder L, Hogg B, Bersoult A, Cullimore JV (2005) Integration of signalling pathways in the establishment of the legume-rhizobia symbiosis. Physiol Plant 123:207–218

    CAS  CrossRef  Google Scholar 

  • Müller J, Xie ZP, Staehelin C, Mellor RB, Boller T, Wiemken A (1994) Trehalose and trehalase in root nodules from various legumes. Physiol Plant 90:86–89

    CrossRef  Google Scholar 

  • Munns DN (1986) Acid soils tolerance in legumes and rhizobia. Adv Plant Nutr 2:63–91

    CAS  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    PubMed  CAS  CrossRef  Google Scholar 

  • Nabil M, Coudret A (1995) Effects of sodium chloride on growth, tissue elasticity and solute adjustment in two Acacia nilotica subspecies. Physiol Plant 93:217–224

    CAS  CrossRef  Google Scholar 

  • Nguyen NT, Moghaieb REA, Saneoka H, Fujita K (2004) RAPD markers associated with salt tolerance in Acacia auriculiformis and Acacia mangium. Plant Sci 167:797–805

    CAS  CrossRef  Google Scholar 

  • Nichols PGH, Craig AD, Rogers ME, Albertsen TO, Miller S, McClements DR et al (2008) Production and persistence of annual legumes at five saline sites in southern Australia. Aust J Exp Agric 48:518–535

    CrossRef  Google Scholar 

  • Nichols PGH, Malik AI, Stockdale M, Colmer TD (2009) Salt tolerance and avoidance mechanismss at germination of annual pasture legumes: importance for adaptation to saline environments. Plant Soil 315:241–255

    CAS  CrossRef  Google Scholar 

  • Nijiti CF, Galiana A (1996) Symbiotic properties and Rhizobium requirements for effective nodulation of five tropical dry zone acacias. Agroforest Syst 34:265–275

    CrossRef  Google Scholar 

  • Nogales J, Campos R, Ben Abdelkhalek H, Olivares J, LLuch C, Pandey A, Mann M (2000) Proteomics to study genes and genomes. Nature 405:837–846

    CrossRef  CAS  Google Scholar 

  • Novikova TI, Gordienko NY (1999) Specific features of functioning of the symbiotic system Rhizobium–Glycyrrhiza uralensis under the conditions of chloride salinization. Sibirskii Ekolog Z 3:295–302

    Google Scholar 

  • Onishi M, Tachi H, Kojima T, Shiraiwa M, Takahara H (2006) Molecular cloning and characterization of a novel salt-inducible gene encoding an acidic isoform of PR-5 protein in soybean. Plant Physiol Biochem 44:574–580

    PubMed  CAS  CrossRef  Google Scholar 

  • Pardo JM, Cubero B, Leidi EO, Quintero FJ (2006) Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot 57:1181–1199

    PubMed  CAS  CrossRef  Google Scholar 

  • Patankar AV, González JE (2009) An orphan LuxR homolog of Sinorhizobium meliloti affects stress adaptation and competition for nodulation. Appl Environ Microbiol 75:946–955

    PubMed  CAS  CrossRef  Google Scholar 

  • Peña JI, Sánchez-Diaz M, Aguirreolea J, Becana M (1988) Increased stress tolerance of nodule activity in the Medicago-Rhizobium Glomus symbiosis under drought. J Plant Physiol 133:79–83

    CrossRef  Google Scholar 

  • Perrig D, Boiero L, Masciarelli O, Penna C, Ruíz O, Cassán F, Luna V (2007) Plant growth promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and their implications for inoculant formulation. Appl Microbiol Biotechnol 75:1143–1150

    PubMed  CAS  CrossRef  Google Scholar 

  • Phang T-H, Shao G, Lam H-M (2008) Salt tolerance in soybean. J Integr Plant Biol 50:1196–1212

    PubMed  CAS  CrossRef  Google Scholar 

  • Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143

    CAS  CrossRef  Google Scholar 

  • 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) Characterization of Phaseolus symbionts isolated from Mediterranean soils and analysis of genetic factors related to pH tolerance. J Biotechnol 91:223–236

    PubMed  CAS  CrossRef  Google Scholar 

  • Qadir M, Ghafoor A, Murtaza G (2000) Amelioration strategies for saline soils: a review. Land Degrad Dev 11:501–521

    CrossRef  Google Scholar 

  • Rabie GH (2005) Influence of VA-mycorrhizal fungi and kinetin on the response of mungbean plants to irrigation with seawater. Mycorrhiza 15:225–230

    PubMed  CAS  CrossRef  Google Scholar 

  • Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotechnol 4:210–222

    CAS  Google Scholar 

  • Raghuwanshi R, Upadhyay RS (2004) Performance of vesicular-arbuscular mycorrhizae in saline-alkali soil in relation to various amendments. World J Microbiol Biotechnol 20:1–5

    CrossRef  Google Scholar 

  • Räsänen LA, Lindström K (2003) Effects of biotic and a biotic constraints on the symbiosis between rhizobia and the tropical leguminous trees Acacia and Prosopis. Indian J Exp Biol 41:1142–1159

    PubMed  Google Scholar 

  • Raza S, Jørnsgård B, Abou-Taleb H, Christiansen JL (2001) Tolerance of Bradyrhizobium sp. (Lupini) strains to salinity, pH, CaCO3 and antibiotics. Lett Appl Microbiol 32:379–383

    PubMed  CAS  CrossRef  Google Scholar 

  • Rehman A, Nautiyal CS (2002) Effect of drought on the growth and survival of the stress-tolerant bacterium Rhizobium sp. NBRI2505 sesbania and its drought sensitive trnsposon Tn5 mutant. Curr Microbiol 45:368–377

    PubMed  CAS  CrossRef  Google Scholar 

  • Reichman SM (2007) The potential use of the legume–rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol Biochem 39:2587–2593

    CAS  CrossRef  Google Scholar 

  • Riccillo PM, Muglia CI, De Brujin FJ, Row AJ, Booth IR, Aguilar OM (2000) Glutathione is involved in environmental stress responses in Rhizobium tropici, including acid tolerance. J Bacteriol 182:1748–1753

    PubMed  CAS  CrossRef  Google Scholar 

  • Richardson AE, Simpson RJ, Djordjevic MA, Rolfe BG (1988) Expression of nodulation genes in Rhizobium leguminosarum bv. trifolii is affected by low pH and by Ca2+ and Al ions. Appl Environ Microbiol 54:2541–2548

    PubMed  CAS  Google Scholar 

  • Rodelas B, González-López J, Salmerón V, Pozo C, Martínez-Toledo MV (1996) Enhancement of nodulation, N2 fixation and growth of faba bean (Vicia faba L.) by combined inoculation with Rhizobium leguminosarum bv. viceae and Azospirillm brasilense. Symbiosis 21:175–186

    Google Scholar 

  • Rodelas B, González-López J, Martínez-Toledo MV, Pozo C, Salmerón V (1999) Influence of Rhizobium/Azotobacter and Rhizobium/Azospirillum combined inoculation on mineral composition of faba bean (Vicia faba L.). Biol Fertil Soils 29:165–169

    CAS  CrossRef  Google Scholar 

  • Rodriguez H, Fraga R (1999) Phosphate-solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    PubMed  CAS  CrossRef  Google Scholar 

  • Rogers ME, Noble CL (1991) The effect of NaCl on the establishment and growth of balansa clover (Trifolium michelianum Savi var. balansae Boiss.). Aust J Agric Res 42:847–857

    CrossRef  Google Scholar 

  • Rogers ME, Colmer TD, Frost K, Henry D, Cornwall D, Hulm E et al (2008) Diversity in the genus Melilotus for tolerance to salinity and water logging. Plant Soil 304:89–101

    CAS  CrossRef  Google Scholar 

  • Rolfe BG, Mathesius U, Djordjevic M, Weinman J, Hocart C, Weiller G, Bauer WD (2003) Proteomic analysis of legume–microbe interactions. Comp Funct Genomics 4:225–228

    PubMed  CAS  CrossRef  Google Scholar 

  • Romero C, Bellés JM, Vayá JL, Serrano R, Culiáñez-Macia FA (1997) Expression of the yeast trehalose-6-phosphate synthase in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201:293–297

    PubMed  CAS  CrossRef  Google Scholar 

  • Rosas SB, Andrés JA, Rovera M, Correa NS (2006) Phosphate-solubilizing Pseudomonas putida can influence the rhizobia–legume symbiosis. Soil Biol Biochem 38:3502–3505

    CAS  CrossRef  Google Scholar 

  • Rüberg S, Tian Z-X, Krol E, Linke B, Meyer F, Wang Y, Pühler A, Weidner S, Becker A (2003) Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression. J Biotechnol 106:255–268

    PubMed  CrossRef  CAS  Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317

    PubMed  CrossRef  Google Scholar 

  • Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95:472–478

    CAS  CrossRef  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151:493–502

    CAS  CrossRef  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Aroca R (2006) Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of drought-induced plant genes? New Phytol 171:693–698

    PubMed  CAS  CrossRef  Google Scholar 

  • Sadowsky MJ (2005) Soil stress factors influencing symbiotic nitrogen fixation. In: Werner D, Newton WE (eds) Nitrogen fixation in agriculture, forestry, ecology, and the environment. Springer, The Netherlands, pp 89–112

    CrossRef  Google Scholar 

  • Sadowsky MJ, Graham PH (1998) Soil biology of the Rhizobiaceae. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Kluwer Acadmic Publishers, Dordrecht, pp 155–172

    CrossRef  Google Scholar 

  • Safronova VI, Stepanok VV, Engqvist GL, Yv A, Belimov AA (2006) Root-associated bacteria containing 1-aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol Fertil Soils 42:267–272

    CAS  CrossRef  Google Scholar 

  • Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34:635–648

    PubMed  CAS  CrossRef  Google Scholar 

  • Sampedro JG, Uribe S (2004) Trehalose–enzyme interactions result in structure stabilization and activity inhibition. The role of viscosity. Mol Cell Biochem 256–257:127–319

    Google Scholar 

  • Sánchez-Diaz M (2001) Adaptation of legumes to multiple stresses in Mediterranean-type environments. Options Mediterr 45:145–151

    Google Scholar 

  • Sánchez-Diaz M, Pardo M, Antolin MC, Peña J, Aguirreolea J (1990) Effect of water stress on photosynthetic activity in the Medicago-Rhizobium Glomus symbiosis. Plant Sci 71:215–221

    CrossRef  Google Scholar 

  • Sassi S, Gonzalez EM, Aydi S, Arrese-Igor C, Abdelly C (2008) Tolerance of common bean to long-term osmotic stress is related to nodule carbon flux and antioxidant defenses: evidence from two cultivars with contrasting tolerance. Plant Soil 312:39–48

    CAS  CrossRef  Google Scholar 

  • Saxena AK, Rewari RB (1991) The influence of phosphate and zinc on growth, nodulation and mineral composition of chickpea (Cicer arietinum L.). World J Microbiol Biotechnol 7:202–205

    CAS  CrossRef  Google Scholar 

  • Segovia L, Pinero D, Palacios R, Martinez-Romero E (1991) Genetic structure of a soil population of nonsymbiotic Rhizobium leguminosarum. Appl Environ Microbiol 57:426–430

    PubMed  CAS  Google Scholar 

  • Serraj R, Sinclair T, Purcell L (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155

    CAS  Google Scholar 

  • Shamseldin A, Werner D (2005) High salt and high pH tolerance of new isolated Rhizobium etli strains from Egyptian soils. Curr Microbiol 50:11–16

    PubMed  CAS  CrossRef  Google Scholar 

  • Shamseldin A, Nyalwidhe J, Werner D (2006) A proteomic approach towards the analysis of salt tolerance in Rhizobium etli and Sinorhizobium meliloti strains. Curr Microbiol 52:333–339

    PubMed  CAS  CrossRef  Google Scholar 

  • Sharma MP, Bhatia NP, Adholeya A (2001) Mycorrhizal dependency and growth responses of Acacia nilotica and Albizzia lebbeck to inoculation by indigenous AM fungi as influenced by available soil P levels in a semi-arid Alfisol wasteland. New For 21:89–104

    CrossRef  Google Scholar 

  • Sheng XF (2005) Growth promotion and increased potassium uptake of cotton and rape by a potassium releasing strain of Bacillus edaphicus. Soil Biol Biochem 37:1918–1922

    CAS  CrossRef  Google Scholar 

  • Sibole JV, Cabot C, Poschenrieder C, Barceló J (2003) Efficient leaf ion partitioning, an overriding condition or absicisic acid-controlled stomatal and leaf growth responses to NaCl salinization in two legumes. J Exp Bot 54:2111–2119

    PubMed  CAS  CrossRef  Google Scholar 

  • Smit G, Swart S, Lugtenberg BJJ, Kijne JW (1992) Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol Microbiol 6:2897–2903

    PubMed  CAS  CrossRef  Google Scholar 

  • Smith LT, Smith GM, D'Souza MR, Pocard J-A, Le Rudulier D, Madkour MA (1994) Osmoregulation in Rhizobium meliloti: mechanism and control by other environmental signals. J Exp Zool 268:162–165

    CAS  CrossRef  Google Scholar 

  • Soussi M, Ocaña A, Lluch C (1998) Effect of salt stress on growth, photosynthesis and nitrogen fixation in chick-pea (Cicer arietinum L.). J Exp Bot 49:1329–1337

    CAS  Google Scholar 

  • Soussi M, Lluch C, Ocaña A (1999) Comparative study of nitrogen fixation and carbon metabolism in two-chick-pea (Cicer arietinum L.) cultivars under salt stress. J Exp Bot 50:1701–1708

    CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    PubMed  CAS  CrossRef  Google Scholar 

  • Sprent JI (2006) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25

    CrossRef  CAS  Google Scholar 

  • Sprent JI (2008) 60 Ma of legume nodulation: what’s new? what’s changing? J Exp Bot 59:1081–1084

    PubMed  CAS  CrossRef  Google Scholar 

  • Sprent JI, Zahran HH (1988) Infection, development and functioning of nodules under drought and salinity. In: Beck DP, Materon LA (eds) Mediterranean agriculture. Martinus Nijhoff/Dr. W. Junk, Dordrecht, The Netherlands, pp 145–151

    Google Scholar 

  • Swaine EK, Swaine MD, Killham K (2007) Effect of drought on isolates of Bradyrhizobium elkanii cultured from Albizzia adianthifolia seedlings of different provenances. Agroforest Syst 69:135–145

    CrossRef  Google Scholar 

  • Tachi H, Fukuda-Yamada K, Kojima T, Shiraiwa M, Takahara H (2009) Molecular characterization of a novel soybean gene encoding a neutral PR-5 protein induced by high-salt stress. Plant Physiol Biochem 47:73–79

    PubMed  CAS  CrossRef  Google Scholar 

  • Tain CY, Feng G, Li XL, Zhang PS (2004) Different effects of arbuscular mycorrhizal fungus isolates from saline or non-saline soil on salinity tolerance of plants. Appl Soil Ecol 26:143–148

    CrossRef  Google Scholar 

  • Tejera NA, Campos R, Sanjuan J, Lluch C (2004) Nitrogenase and antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropici isogenic strains with varying tolerance to salt stress. J Plant Physiol 161:329–338

    PubMed  CAS  CrossRef  Google Scholar 

  • Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR (1996) Acid tolerance in Rhizobium meliloti strains WSM419 involved a two-component sensor-regulator system. Microbiology 142:1693–1704

    PubMed  CAS  CrossRef  Google Scholar 

  • Tomar OS, Minhas PS, Sharma VK, Singh YP, Gupta RK (2003) Performance of 31 tree species and soil conditions in a plantation established with saline irrigation. For Ecol Manage 177:333–346

    CrossRef  Google Scholar 

  • Triplett EW, Sadowsky MJ (1992) Genetics of competition for nodulation. Annu Rev Microbiol 46:399–428

    PubMed  CAS  CrossRef  Google Scholar 

  • Valdenegro M, Barea JM, Azcón R (2001) Influence of arbuscular-mycorrhizal fungi, Rhizobium meliloti strains and PGPR inoculation on the growth of Medicago arborea used as model legume for re-vegetation and biological reactivation in a semi-arid mediterranean area. Plant Growth Regul 34:233–240

    CAS  CrossRef  Google Scholar 

  • Vance CP (1998) Legume symbiotic nitrogen fixation: agronomic aspects. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Kluwer Acad. Pub, Dordrecht, pp 509–530

    CrossRef  Google Scholar 

  • Vázquez MM, Azcón R, Barea JM (2001) Compatibility of a wild type and its genetically modified Sinorhizobium strain with two mycorrhizal fungi on Medicago species as affected by drought stress. Plant Sci 161:347–358

    PubMed  CrossRef  Google Scholar 

  • Verdoy D, De La Peña TC, 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

    PubMed  CAS  CrossRef  Google Scholar 

  • Vessey JK, Chemining'wa GN (2006) The genetic diversity of Rhizobium leguminosarum bv. viciae in cultivated soils of the eastern Canadian prairie. Soil Biol Biochem 38:153–163

    CAS  CrossRef  Google Scholar 

  • Vessey JK, Pawlowski K, Bergman B (2005) Root-based N2-fixing symbiosis: legumes, actinorhizal plants, Parasponia sp. and cycads. Plant Soil 274:51–78

    CAS  CrossRef  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    PubMed  CAS  CrossRef  Google Scholar 

  • Vivas A, Biró B, Németh T, Barea JM, Azcón R (2006) Nickel-tolerant Brevibacillus brevis and arbuscular mycorrhizal fungus can reduce metal acquisition and nickel toxicity effects in plant growing in nickel supplemented soil. Soil Biol Biochem 38:2694–2704

    CAS  CrossRef  Google Scholar 

  • Vriezen JAC, De Bruijn FJ, Nüsslein K (2006) Desiccation responses and survival of Sinorhizobium meliloti USDA 1021 in relation to growth phase, temperature, chloride and sulfate availability. Lett Appl Microbiol 42:172–178

    PubMed  CAS  CrossRef  Google Scholar 

  • 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

    PubMed  CAS  CrossRef  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2008a) Effects of heavy metal toxicity on growth, symbiosis, seed yield and metal uptake in pea grown in metal amended soil. Bull Environ Contam Toxicol 81:152–158

    PubMed  CAS  CrossRef  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2008b) Effect of metal-tolerant plant growth-promoting Rhizobium on the performance of pea grown in metal-amended soil. Arch Environ Contam Toxicol 55:33–42

    PubMed  CAS  CrossRef  Google Scholar 

  • Wankhade S, Apte SK, Rao KK (1996) Salinity and osmotic stress regulated proteins in cowpea Rhizobium 4a (peanut isolate). Biochem Mol Biol Int 39:621–628

    PubMed  CAS  Google Scholar 

  • Ward JM, Hirschi KD, Sze H (2003) Plants pass the salt. Trends Plant Sci 8:200–201

    PubMed  CAS  CrossRef  Google Scholar 

  • 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

    PubMed  CAS  CrossRef  Google Scholar 

  • Wei G-H, Yang X-Y, Zhang Z-X, Yang Y-Z, Lindström K (2008) Strain Mesorhizobium sp. CCNWGX035: a stress-tolerant isolate from Glycyrrhiza glabra displaying a wide host range of nodulation. Pedosphere 18:102–112

    CAS  CrossRef  Google Scholar 

  • Wood JM, Bremer E, Csonka IN, Kramer R, Poolman B, Van Der Heide T, Smith IT (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 130:437–460

    PubMed  CAS  CrossRef  Google Scholar 

  • Wu CH, Wood TK, Mulchandani A, Chen W (2006) Engineering plant–microbe symbiosis for rhizoremediation of heavy metals. Appl Environ Microbiol 72:1129–1134

    PubMed  CAS  CrossRef  Google Scholar 

  • Xiong L, Zhu J-K (2001) Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol Plant 112:152–166

    PubMed  CAS  CrossRef  Google Scholar 

  • Yang Q, Wu M, Wang P, Kang J, Zhou X (2005) Cloning and expression analysis of a vacuolar Na+/H+ antiporter gene from alfalfa. DNA Seq 16:352–357

    PubMed  CAS  Google Scholar 

  • Yano-Melo AM, Saggin OJ, Maia LC (2003) Tolerance of mycorrhizal banana (Musa sp. cv. Pacovan) plantlets to saline stress. Agric Ecosyst Environ 95:343–348

    CrossRef  Google Scholar 

  • Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30:529–539

    PubMed  CAS  CrossRef  Google Scholar 

  • Zahran HH (1991) Conditions for successful Rhizobium–legume symbiosis in saline environments. Biol Fertil Soils 12:73–80

    CrossRef  Google Scholar 

  • Zahran HH (1998) Structure of root nodules and nitrogen fixation in Egyptian wild herb legumes. Biol Plant 41:575–585

    CrossRef  Google Scholar 

  • Zahran HH (1999) Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    PubMed  CAS  Google Scholar 

  • Zahran HH (2001) Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnology. J Biotechnol 91:143–153

    PubMed  CAS  CrossRef  Google Scholar 

  • Zahran HH (2005) Rhizobial nitrogen fixation in agriculture: biotechnological perspectives. In: Ray RC (ed) Microbial biotechnology in agriculture and aquaculture, vol 1. Science Publishers, Inc., Enfield, USA, pp 71–100

    Google Scholar 

  • Zahran HH (2006a) Wild legume rhizobia: biodiversity and potential as biofertilizers. In: Rai MK (ed) Handbook of microbial biofertilizers. Haworth Press Inc., New York, pp 203–222

    Google Scholar 

  • Zahran HH (2006b) Nitrogen (N2) fixation in vegetable legumes: biotechnological perspectives. In: Ray RC, Ward OP (eds) Microbial biotechnology in horticulture, vol 1. Science Publishers, Inc., Enfield, USA, pp 49–82

    Google Scholar 

  • Zahran HH (2009) Enhancement of rhizobia–legumes symbioses and nitrogen fixation for crops productivity improvement. In: Khan MS, Zaidi A, Musarrat J (eds) Microbial strategies for crop improvement. Springer, Germany, pp 227–254

    CrossRef  Google Scholar 

  • Zahran HH, Sprent JI (1986) Effects of sodium chloride and polyethylene glycol on root-hair infection and nodulation of Vicia faba L. plants by Rhizobium leguminosarum. Planta 167:303–309

    CAS  CrossRef  Google Scholar 

  • Zahran HH, Räsanen LA, Karsisto M, Lindström K (1994) Alteration of lipopolysaccharide and protein profiles in SDS-PAGE of rhizobia by osmotic and heat stress. World J Microbiol Biotechnol 10:100–105

    CAS  CrossRef  Google Scholar 

  • Zahran HH, Ahmad MS, Afkar E (1995) Isolation and characterization of nitrogen-fixing moderate halophilic bacteria from saline soils of Egypt. J Basic Microbiol 35:269–275

    CrossRef  Google Scholar 

  • Zahran HH, Abdel-Fattah M, Ahmad MS, Zaki AY (2003) Polyphasic taxonomy of symbiotic rhizobia from wild leguminous plants growing in Egypt. Folia Microbiol 48:510–520

    CAS  CrossRef  Google Scholar 

  • Zahran HH, Marin-Mansano MC, Sánchez-Raya AJ, Bedmar EJ, Venema K, Rodríguez-Rosales MP (2007) Effect of salt stress on the expression of NHX-type ion transporters in Medicago intertexta and Melilotus indicus. Physiol Plant 131:122–130

    PubMed  CAS  CrossRef  Google Scholar 

  • Zaidi A, Khan MS, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hung 56:263–284

    PubMed  CAS  CrossRef  Google Scholar 

  • Zerhari K, Aurag J, Khbaya B, Kharchaf D, Filali-Matlouf A (2000) Phenotypic characteristics of rhizobia isolates nodulating Acacia species in the arid and Saharan regions of Morocco. Lett Appl Microbiol 30:351–357

    PubMed  CAS  CrossRef  Google Scholar 

  • Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    PubMed  CAS  CrossRef  Google Scholar 

  • Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    PubMed  CAS  CrossRef  Google Scholar 

  • Zhu J-K, Hasegawa PM, Bressan R (1997) Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci 16:253–277

    CAS  Google Scholar 

  • Zörb C, Noll A, Karl S, Leib K, Yan F, Schubert S (2005) Molecular characterization of Na+/H+ antiporters (ZmNHX) of maize (Zea mays L.) and their expression under salt stress. J Plant Physiol 162:55–66

    PubMed  CrossRef  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hamdi H. Zahran .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2010 Springer-Verlag/Wien

About this chapter

Cite this chapter

Zahran, H.H. (2010). Legumes–Microbes Interactions Under Stressed Environments. In: Khan, M.S., Musarrat, J., Zaidi, A. (eds) Microbes for Legume Improvement. Springer, Vienna. https://doi.org/10.1007/978-3-211-99753-6_15

Download citation