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Conditions for successful Rhizobium-legume symbiosis in saline environments

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Summary

The Rhizobium-legume symbiosis in arid ecosystems is particularly important for locations where the area of saline soils is increasing and becoming a threat to plant productivity. Legumes, which are usually present in arid ecosystems, may be adapted to fix more N2 under saline conditions than legumes grown in other habitats.

Legumes are known to be either sensitive or moderately resistant to salinity. The salt sensitivity can be attributed to toxic ion accumulations in different plant tissues, which disturb some enzyme activities.

Among the basic selection criteria for salt-tolerant legumes and rhizobia are genetic variability within species with respect to salt tolerance, correlation between accumulations of organic solutes (e. g., glycine betaine, proline betaine, and proline) and salt tolerance, and good relationships between ion distribution and compartmentation, and structural adaptations in the legumes.

Salt stress reduces the nodulation of legumes by inhibiting the very early symbiotic events. Levels of salinity that inhibit the symbiosis between legumes and rhizobia are different from those that inhibit the growth of the individual symbionts. The poor symbiotic performance of some legumes under saline conditions is not due to salt limitations on the growth of rhizobia.

Prerequisites for a successful Rhizobium-legume symbiosis in saline environments include rhizobial colonization and invasion of the rhizosphere, root-hair infection, and the formation of effective salt-tolerant nodules.

The possibility of exploring the Rhizobium-legume symbiosis to improve the productivity of saline soils is reviewed in this paper.

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References

  • Abdel-Ghaffar AS (1989) Aspects of microbial activities and dinitrogen fixation in Egyptian desert soils. Arid Soil Res Rehabil 3:281–294

    Google Scholar 

  • Abdel-Wahab AM, Zahran HH (1979a) The effects of water stress on N2 (C2H2)-fixation and growth of four legumes. Agricultura (Heverlee) 28:383–400

    Google Scholar 

  • Abdel-Wahab AM, Zahran HH (1979b) Salt tolerance of Rhizobium species in broth cultures. Z Allg Mikrobiol 19:681–685

    Google Scholar 

  • Abdel-Wahab AM, Zahran HH (1981) Effects of salt stress on nitrogenase activity and growth of four legumes. Biol Plant (Praha) 23:16–23

    Google Scholar 

  • Adams MA, Attiwill PM (1984) Role of Acacia spp. in nutrient balance and cycling in regenerating Eucalyptus regnans F. Muell Forests: II Field studies of acetylene reduction. Aust J Bot 32:217–223

    Google Scholar 

  • Arutyunova NV, Shevyakova NI (1984) Role of nitrogen source in improving the salt resistance of the peanut. Arachis hypogaea L. Biol Bull Acad Sci USSR 10:495–501

    Google Scholar 

  • Ashraf M (1989) The effect of NaCl on water relations, chlorophyll, and protein and proline contents of two cultivars of blackgram (Vigna mungo L.). Plant and Soil 119:205–210

    Google Scholar 

  • Bajpai PD, Gupta BR (1977) Studies on the exploitation of rhizobial potentiality for berseem (Trifolium alexandrinum L.) under saline-alkaline soils. J Indian Soc Soil Sci 25:62–68

    Google Scholar 

  • Bajpai PD, Gupta BR (1979) Effects of salinization, phosphorus fertilization and their interaction on the symbiosis between Rhizobium trifolii and berseem (Trifolium alexandrinum L.). J. Indian Soc Soil Sci 27:462–469

    Google Scholar 

  • Bajpai PD, Gupta BR, Singh C (1974) A note on the effect of salinity on symbiosis between Rhizobium trifolii and berseem (Trifolium alexandrinum) crops. J Indian Soc Soil Sci 22:365–376

    Google Scholar 

  • Barradas CA, Boddey LH, Hungria M (1989) Selection of bean cultivars and Rhizobium strains for early nodulation and late senescence of nodules. Rev Bras Cienc Sol 13:169–179

    Google Scholar 

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

    Google Scholar 

  • Bekki A, Trinchant J-C, Rigaud J (1987) Nitrogen fixation (C2H2 reduction) by Medicago nodules and bacteroids under sodium chloride stress. Physiol Plant 71:61–67

    Google Scholar 

  • Bernard T, Pocard J-A, Perroud B, Le Rudulier D (1986) Variations in the response of salt-stressed Rhizobium strains to betaines. Arch Microbiol 143:359–364

    Google Scholar 

  • Bethenfalway GJ, Brown HS, Aems RN, Thomas RS (1988) Effects of drought on host and endophyte development in mycorrhizal soybeans in relation to water use and phosphate uptake. Physiol Plant 72:565–571

    Google Scholar 

  • Bhardwaj KKR (1975) Survival and symbiotic characteristics of Rhizobium in saline alkaline soils. Plant and Soil 43:377–385

    Google Scholar 

  • Bhuvaneswari TV, Solheim B (1985) Root hair deformation in the white clover/Rhizobium symbiosis. Physiol Plant 63:25–34

    Google Scholar 

  • Bhuvaneswari TV, Bhagwat AA, Bauer WD (1981) Transient susceptibility of root hair cell in four common legumes to nodulation by rhizobia. Plant Physiol 68:1144–1149

    Google Scholar 

  • Botsford JL (1984) Osmoregulation on Rhizobium meliloti: Inhibition of growth by salts. Arch Microbiol 137:124–127

    Google Scholar 

  • Botsford JL, Lewis TA (1990) Osmoregulation in Rhizobium meliloti: Production of glutamic acid in response to osmotic stress. Appl Environ Microbiol 56:488–494

    Google Scholar 

  • Brady CJ, Gibson TS, Barlow EWR, Speirs J, Wyn Jones RG (1984) Salt tolerance in plants: I. Ions, compatible organic solutes and the stability of plant ribosomes. Plant Cell Environ 7:571–578

    Google Scholar 

  • Brockwell J (1981) A strategy for legume nodulation research in developing regions of the world. Plant and Soil 58:367–382

    Google Scholar 

  • Busse MD, Bottomley PJ (1989) Growth and nodulation responses of Rhizobium meliloti to water stress induced by permeating and non-permeating solutes. Appl Environ Microbiol 55:2431–2436

    Google Scholar 

  • Cerda A, Caro M, Franandez FG (1982) Salt tolerance of two pea cultivars. Agron J 74:796–798

    Google Scholar 

  • Chandler MR (1978) Some observations on infection of Arachis hypogaea L. by Rhizobium. J Exp Bot 29:749–755

    Google Scholar 

  • Chandler MR, Data RA, Roughley RJ (1982) Infection and root nodule development in Stylosanthes species by Rhizobium. J Exp Bot 33:47–57

    Google Scholar 

  • Chen H, Gartner E, Djordevic MA, Rolfe BG (1990) Construction of acid tolerant, nitrogen fixing strains of Rhizobium leguminosarum bv trifolii. In: Gresshoff PM, Evan Roth L, Stacey G, Newton WE (eds) Nitrogen Fixation: Achievements and Objectives. Proc 8th Int Congr Nitrogen Fixation, May 20–26, 1990, Knoxville, Tennessee, USA. Chapman and Hall, New York

    Google Scholar 

  • Douka CE, Apostalakis CG, Skarloy VD (1978) Studies of Rhizobium meliloti isolated from salt-affected soils. Ann Appl Biol 88:457–460

    Google Scholar 

  • Dudeja SS, Khurana AI (1989) Persistence of Bradyrhizobium sp. (Cajanus) in a sandy loam. Soil Biol Biochem 21:709–713

    Google Scholar 

  • Duvick DN, Kleese RA, Frey NM (1981) Breeding for tolerance of nutrient imbalances and constraints to growth in acid, alkaline and saline soils. J Plant Nutr 4:111–129

    Google Scholar 

  • El Karouri MOH (1979) Effects of soil salinity on broad bean (Vicia faba) in the Sudan. Exp Agric 15:59–63

    Google Scholar 

  • El Sheikh EAE, Wood M (1989a) Response of chickpea and soybean rhizobia to salt: Influence of carbon source, temperature and pH. Soil Biol Biochem 21:883–887

    Google Scholar 

  • El Sheikh EAE, Wood M (1989b) Response of chickpea and soybean rhizobia to salt: Osmotic and specific ion effects of salt. Soil Biol Biochem 21:889–895

    Google Scholar 

  • El Sheikh EAE, Wood M (1990) Salt effects on survival and multiplication of chickpea and soybean rhizobia. Soil Biol Biochem 22:343–347

    Google Scholar 

  • El Shinnawi MM, El Saify NA, Waly TM (1989) Influence of the ionic form of mineral salts on growth of faba bean and Rhizobium leguminosarum. MIRCEN J Appl Microbiol Biotechnol 5:247–254

    Google Scholar 

  • Engin M, Sprent JI (1973) Effects of water stress on growth and nitrogen-fixing activity of Trifolium repens. New Phytol 72:117–126

    Google Scholar 

  • Epstein E, Norlyn JD, Rush DW, Kingsbury DB, Kelley GA, Cunningham GA, Wrona AF (1980) Saline culture of crops: A genetic approach. Science 210:399–404

    Google Scholar 

  • Ewens M, Leigh RA (1985) The effects of nutrient solution composition on the length of root hairs of wheat (Triticum aestivum L.). J Exp Bot 36:713–724

    Google Scholar 

  • Faria SM de, McInroy SG, Sprent JI (1987) The occurrence of infected cells, with persistent infection threads, in legume root nodules. Can J Bot 65:553–558

    Google Scholar 

  • Felker P, Clark PR, Laag AE, Pratt PF (1981) Salinity tolerance of the tree legumes: Mesquite (Prosopis glandulosa var. Torreyana; P. velutina and P. articulata), algarrobo (P. chilensis), kiawa (P. pallida) and tamarugo (P. tamarugo) grown in sand culture on nitrogen-free media. Plant and Soil 61:311–317

    Google Scholar 

  • Fougere F, Le Rudulier D (1990) Uptake of glycine betaine and its analogues by bacteroids of Rhizobium meliloti. J Gen Microbiol 136:157–163

    Google Scholar 

  • Friedman R, Altman A, Levin N (1989) The effect of salt stress on polyamine biosynthesis and content in mung bean plants and in halophytes. Physiol Plant 76:295–302

    Google Scholar 

  • Garg BK, Venkateswarlu B, Vyas SP, Lahiri AN (1984) Nodulation and N2-ase activity in clusterbean and Mothbean under salt stress. Indian J Exp Biol 22:511–512

    Google Scholar 

  • Gloux K, Le Rudulier D (1989) Transport and catabolism of proline betaine in salt-stressed Rhizobium meliloti. Arch Microbiol 151:143–148

    Google Scholar 

  • Gorham J, McDonnell E, Wyn Jones RG (1984) Pinitol and other solutes in salt-stressed Sesbania aculeata. Z Pflanzenernaehr Physiol 114:143–178

    Google Scholar 

  • Graham PH, Parker CA (1964) Diagnostic features in the characterization of root nodule bacteria of legumes. Plant and Soil 20:383–396

    Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:49–90

    Google Scholar 

  • Greenway H, Munns R (1983) Interaction between growth, uptake of Cl- and Na+, and water relations of plants in saline environments: II. Highly vacuolated cells. Plant Cell Environ 6:575–589

    Google Scholar 

  • Greenway H, Munns R, Wolfe J (1983) Interactions between growth, uptake of Cl- and Na+, and water relations of plants in saline environments: I. Slightly vacuolated cells. Plant Cell Environ 6:567–574

    Google Scholar 

  • Hamdi YA, Al Tai AM (1981) Salt tolerance of strains of Rhizobium meliloti and R. trifolii to the chlorides of sodium, calcium, and magnesium. Egypt J Microbiol 16:1–7

    Google Scholar 

  • Hammouda FMM (1980) Biological nitrogen fixation in the desert ecosystems of Egypt. Ph D thesis Alexandria Univ, Alexandria

  • Harvey DM, Thorpe JR (1986) Some observations on the effect of salinity on ion distribution and cell ultrastructure in wheat leaf mesophyll cells. J Exp Bot 37:1–7

    Google Scholar 

  • Hawkeer JS (1980) Invertases from leaves of Phaseolus vulgaris plants grown on nutrient solutions containing NaCl. Aust J Plant Physiol 7:67–72

    Google Scholar 

  • Helal HM, Mengel K (1981) Interaction between light intensity and sodium chloride salinity and their effects on growth, CO2 assimilation and photosynthate conversions in young broad beans. Plant Physiol 67:999–1002

    Google Scholar 

  • Hoffman GJ, Ayers RS, Doering EJ, McNeal BL (1980) Salinity in irrigated agriculture. In: Design and operation of farm irrigation systems. St. Joseph, Michigan, Am Soc Agric Eng, pp 145–185

    Google Scholar 

  • Hopmanns P, Douglas LA, Chalk PM (1984) Effects of soil salinity and mineral nitrogen on the acetylene reduction activity of Trifolium alexandrinum L. Aust J Agric Res 35:9–15

    Google Scholar 

  • Hua SST, Tsai VY, Lichens GM, Noma AT (1982) Accumulation of amino acids in Rhizobium spp. WR 1001 in response to sodium chloride salinity. Appl Environ Microbiol 44:135–140

    Google Scholar 

  • Imamul-Haq SH, Larher F (1985) Dynamics of Na+, K+ and proline accumulation in salt-treated Vigna sinensis (L): J Plant Physiol 119:133–147

    Google Scholar 

  • Ishaq YZ, Zohdy LI, EI Haddad ME, Moawad H, Abdel-Aziz RA (1989) Population dynamics of introduced R. trifolii strains in the rhizosphere of Egyptian clover in relation to salt stress and pattern of competition. In: Abstracts 5th Int Symp Microbial Ecology (ISME-5), August 27-September 1st, Kyoto, Japan

  • Jasper DA, Abbott LK, Robson AD (1989) Acacias respond to additions of phosphorus and to inoculation with VA mycorrhizal fungi in soils stockpiled during mineral sand mining. Plant and Soil 115:99–108

    Google Scholar 

  • Jefferies RL (1981) Osmotic adjustment and the response of halophytic plants to salinity. Bio Science 31:42–46

    Google Scholar 

  • Johnson DA, Rumbaugh MD, Asay KH (1981) Plant improvement for semi-arid range lands: possibilities for drought resistance and nitrogen fixation. Plant and Soil 58:279–303

    Google Scholar 

  • Joshi SS (1984) Effect of salinity stress on organic and mineral constituents in the leaves of pigeonpea (Cajauns cajan L. var. C-11). Plant and Soil 82:69–76

    Google Scholar 

  • Keck TJ, Wagenet RJ, Campbell WF, Knighton RE (1984) Effects of water and salt stress on growth and acetylene reduction in alfalfa. Soil Sci Soc Am J 48:1310–1316

    Google Scholar 

  • Kohl DH, Bryan BA, Schearer G, Skeeters JL (1981) Natural abundance of 15N of Prosopis as an index of N2 fixation in desert ecosystems. Bull Ecol Soc Am Sci 62:133–134

    Google Scholar 

  • Kramer D (1984) Cytological aspects of salt tolerance in higher plants. In: Staples RC (ed) Salinity tolerance in plants: Strategies for crop improvements. John Wiley, New York, pp 3–15

    Google Scholar 

  • Lakshmi-Kumari M, Singh CS, Subbarao NS (1974) Root hair infection and nodulation in lucerne (Medicago sativa) as influenced by salinity and alkalinity. Plant and Soil 40:261–268

    Google Scholar 

  • La Rue TA, Patterson TG (1981) How much nitrogen do legumes fix? Adv Agron 34:15–38

    Google Scholar 

  • Läuchli A (1984) Salt exclusion: An adaptation of legumes for crops and pastures under saline conditions. In: Staples RC (ed) Salinity tolerance in plants: Strategies for crop improvement. John Wiley, New York, pp 171–187

    Google Scholar 

  • Läuchli A, Wieneke J (1979) Studies on grwoth and distribution of Na+, K+ and Cl- in soybean varieties differing in salt tolerance. Z Pflanzenernaehr Bodenkd 142:3–13

    Google Scholar 

  • Lauter DJ, Munns DN (1982) Salt response of chickpea and cowpea genotypes to different ionic compositions. Agron Abstr p 213

  • Lauter DJ, Munns DN, Clarkin KL (1981) Salt response of chickpea as influenced by N supply. Agron J 73:961–966

    Google Scholar 

  • Le Rudulier D, Valentine RC (1982) Genetic engineering in agriculture: Osmoregulation. Trends Biochem Sci 7:431–433

    Google Scholar 

  • Le Rudulier D, Gloux K, Riou N, Poggi MC (1990) Characterization of a periplasmic glycine betaine binding protein from Rhizobium meliloti. In: Gresshoff PM, Evan Roth L, Stacey G, Newton WE (eds) Nitrogen Fixation: Achievements and objectives. Proc 8th Int Congr Nitrogen fixation, May 20–26, Knoxville, Tennessee. Chapman and Hall, New York

    Google Scholar 

  • Mackay AD, Barber SA (1985) Effect of soil moisture and phosphate level on root hair growth of corn roots. Plant and Soil 86:321–331

    Google Scholar 

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

    Google Scholar 

  • Marcarian V (1982) Management of the cowpea/Rhizobium symbiosis under stress conditions. In: Graham PH, Harris SC (eds) BNF technology for tropical agriculture. Cali colombia, Centro Int, Agric Trop, pp 279–287

    Google Scholar 

  • Melor HY, Glenn AR, Arwas R, Dilworh MJ (1987) Symbiotic and competitive properties of motility of mutants of Rhizobium trifolii TA1. Arch Microbiol 148:34–39

    Google Scholar 

  • Michelsen A, Rosendahl S (1990) The effect of VA mycorrhizal fungi, phosphorus and drought stress on the growth of Acacia nilotica and leucaena leucocephala seedlings. Plant and Soil 124:7–13

    Google Scholar 

  • Mielenz J, Andersen K, Tait R, Valentine RC (1979) Potential for genetic engineering for salt tolerance. In: Hollaender A, Aller JC, Epstein E, San Pietri A, Zaborsky OR (eds) The biosaline concept: An approach to the utilization of underexploited resources. Plenum Press, New York, pp 361–370

    Google Scholar 

  • Mohammad M, Campbell WF, Rumbaugh MD (1989a) Variation in salt tolerance of alfalfa. Arid Soil Rehabil 3:11–20

    Google Scholar 

  • Mohammad M, Campbell WF, Rumbaugh MD (1989b) Acetylene reduction activity in salt-tolerant alfalfa/Rhizobium under drought stress. Arid Soi Res Rehabil 3:431–438

    Google Scholar 

  • Mohammad M, Campbell WF, Rumbaugh MD (1989c) Acetylene reduction in salt-tolerant alfalfa and Rhizobium. Arid Soil Res Rehabil 3:469–476

    Google Scholar 

  • Moore CV (1984) An economic analysis of plant improvement strategies for saline conditions. In: Staples RC (ed) Salinity tolerance in plants: Strategies for crop improvement. John Wiley, New York, pp 381–397

    Google Scholar 

  • Munns DN, Cassman KG, Keyser HH (1981) Selection of naturally occurring stress tolerant Rhizobium. In: Lyons JM, Valentine RC, Phillips DA, Rains DW, Huffaker RC (eds) Genetic engineering of symbiotic nitrogen fixation and conservation of fixed nitrogen. Plenum Press, New York, pp 181–191

    Google Scholar 

  • Nielsen ET, Virginia RA, Jarrel WM (1986) Water relations and growth characteristic of Prosopis glandulosa var. Torreyana in simulated phreatophytic environment. Am J Bot 73:427–433

    Google Scholar 

  • Noble CL, Halloran GM, West DW (1984) Identification and selection for salt tolerance in lucerne (Medicago sativa L.). Agric Res 35:239–252

    Google Scholar 

  • Padmanabhan S, Hirtz RD, Broughton WJ (1990) Rhizobia in tropical legumes: Cultural characteristics of Bradyrhizobium and Rhizobium sp. Soil Biol Biochem 22:23–28

    Google Scholar 

  • Parihar JS, Baijal BD (1982) Effect of salinity on nitrogen metabolism in berseem (Trifolium alexandrinum L.). Acta Bot Indian 10:282–287

    Google Scholar 

  • Pocard J-A, Bernard T, Smith LT, Le Rudulier D (1989) Characterization of three choline transport activities in Rhizobium meliloti: Modulation by choline and osmotic stress. J Bacteriol 171:531–537

    Google Scholar 

  • Rao GG, Rao GR (1982) Anatomical changes in the leaves and their role in adaptation to salinity in pigeon pea (Cajanus indicus Spreng) and Gingelley (Sesamum indicum L.). Proc Indian Natl Sci Acad, 48:774–778

    Google Scholar 

  • Rathert G, Doering HW, Witt J (1981) Influence of extreme K: Na ratios and high substrate salinity on plant metabolism of crops differing in salt tolerance: III. K/Na effects on the carbohydrate pattern of bush bean and sugar beet plants in response to the salt tolerance of the species. J Plant Nutr 4:131–141

    Google Scholar 

  • Ravikovitch S, Yoles D (1971a) The influence of phosphorus and nitrogen on millet and clover growing in soils affected by salinity: I. Plant development. Plant and Soil 35:555–567

    Google Scholar 

  • Ravikovitch S, Yoles D (1971b) The influence of phosphorus and nitrogen on millet and clover growing in soils affected by salinity: II. Plant composition. Plant and Soil 35:569–588

    Google Scholar 

  • Roskoski JP (1981) Nodulation and nitrogen fixation by Inga jinicuil, a woody legume of coffee plantations: I. Measurement of nodule biomass and field C2H2 reduction rates. Plant and Soil 59:201–206

    Google Scholar 

  • Salem SH, Gewaily EM, El Zamik FI (1981) Effect of salinity on the symbiosis of root nodule bacteria and broad bean plant. Agrokem Talajtan 30:83–89

    Google Scholar 

  • Sanchez-Diaz M, Aparicio-Tejo P, Gonzalez-Mura C, Pena JI (1982) The effect of NaCl salinity and water stress with polyethylene glycol on nitrogen fixation, stomatal response and transpiration of Medicago sativa, Trifolium repens and Trifolium brachycalycinum (subclover). Physiol Plant 54:361–366

    Google Scholar 

  • Shaheen AM (1984) Growth analysis and photosynthetic pigments of broad bean (Vicia faba L.) plants in relation to water stress and GA application. Beitr Trop Landwirtsch Veterinaermed 22:263–268

    Google Scholar 

  • Shannon MC (1984) Breeding, selection and the genetics of salt. In: Staples RC (ed) Salinity tolerance in plants: Strategies for crop improvement. John Wiley, New York, pp 231–254

    Google Scholar 

  • Sherrel CG (1983) Sodium and potassium effects on cation concentration and yield of lucerne and phalaris grown separately and together. J Plant Nutr 6:801–816

    Google Scholar 

  • Shoushtari NH, Pepper IL (1985a) Mesquite rhizobia isolated from the Sonoran desert: Physiology and effectiveness. Soil Biol 17:797–802

    Google Scholar 

  • Shoushtari NH, Pepper IL (1985b) Mesquite rhizobia isolated from the Sonoran desert: Competitiveness and survival in soil. Soil Biol Biochem 17:803–806

    Google Scholar 

  • Siddiqui S, Kumar D, Singh MP, Kumar S (1983) Salinization and desalinization impacts on certain mineral contents in plant organs of “Bonneville” pea. Trans Indian Soc Dest Tech and Univ Ced Dest Studies 8:118–122

    Google Scholar 

  • Sinclair MJ, Eaglesham ARJ (1990) Serological diversity of Bradyrhizobium sp. (Vigna) from three West African soils. Soil Biol Biochem 22:69–74

    Google Scholar 

  • Singleton PW (1983) A split-root growth system for evaluating the effect of salinity on components of the soybean Rhizobium japonicum symbiosis. Crop Sci 23:259–262

    Google Scholar 

  • Singleton PW, Bohlool BB (1983) Effect of salinity on the functional components of the soybean — Rhizobium japonicum symbiosis. Crop Sci 23:815–818

    Google Scholar 

  • Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soy bean. Plant Physiol 74:72–76

    Google Scholar 

  • Singleton PW, El Swaify SA, Bohlool BB (1982) Effect of salinity on Rhizobium growth and survival. Appl Environ Microbiol 44:884–890

    Google Scholar 

  • Sirry AB, Salem SH, Gewaily EM, EI Zamic FI (1981) Effect of mineral N-fertilization in reclaimed soils on the nodulation capacities and symbiotic nitrogen fixation of some leguminous plants. Agrokem Talajtan 30:16–24

    Google Scholar 

  • Skujins J (1984) Microbial ecology of desert soils. Adv Microb Ecol 7:49–91

    Google Scholar 

  • Smartt J (1983) Genetic improvement of grain legumes. In: Arora SK (ed) Chemistry and biochemistry of legumes. Edward Arnold, London, pp 329–349

    Google Scholar 

  • Smith LT, Smith GM (1989) An osmoregulated dipeptide in stressed Rhizobium meliloti. J Bacteriol 171:4714–4717

    Google Scholar 

  • Smith D, Dobrenz AK, Schonhorst MH (1981) Response of alfalfa seedling plants to high levels of chloride salts. J Plant Nutr 4:143–174

    Google Scholar 

  • Smith LT, Pocard J-A, Bernard T, Le Rudulier D (1988) Osmotic control of glycine betaine biosynthesis and degradation in Rhizobium meliloti. J Bacteriol 170:3142–3149

    Google Scholar 

  • Smith MK, McComb JA (1981) Use of callus cultures to detect NaCl tolerance in cultivars of three species of pasture legumes. Aust J Plant Physiol 8:437–442

    Google Scholar 

  • Solomon M, Gedalovaitch E, Mayer AM, Poljakoff-Mayber A (1986) Changes induced by salinity to the anatomy and morphology of pea roots in culture. Ann Bot 57:811–818

    Google Scholar 

  • Sprent JI (1976) Water deficits and nitrogen-fixing root nodules. In: Kozloswki TT (ed) Water deficits and plant growth. Academic Press, New York, pp 291–315

    Google Scholar 

  • Sprent JI (1983) Adaptive variations in legume nodule physiology resulting from host rhizobial interactions. In: Lee JA, McNeill S, Rorison IH (eds) Nitrogen as an ecological factor. Blackwell Scientific, London, pp 29–42

    Google Scholar 

  • Sprent JI (1984) Effects of drought and salinity on heterotrophic nitrogen-fixing bacteria and infection of legumes by rhizobia. In: Veeger C, Newton WE (eds) Advances in nitrogen fixation research. Martinus Nijhoff/Dr W Junk, The Hague Boston Lancaster, pp 295–302

    Google Scholar 

  • Sprent JI (1985) Nitrogen fixation in arid environments. In: Plants for arid lands. Royal Botanic Gardens. Kew, London, pp 215–229

    Google Scholar 

  • Sprent JI, McInroy SG (1984) Effects of salinity on growth and nodulation of Arachis hypogaea. In: Veeger C, Newton WE (eds) Advances in nitrogen fixation research. Martinus Nijhoff/Dr W Junk, The Hague Boston Lancaster, pp 546

    Google Scholar 

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

    Google Scholar 

  • Stowers MD (1985) Carbon metabolism in Rhizobium species. Annu Rev Microbiol 39:89–108

    Google Scholar 

  • Subbarao NS, Lakshmi-Kumari M, Singh CS, Magu SP (1972) Nodulation of lucerne (Medicago sativa L.) under the influence of sodium chloride. Indian J Agric Sci 42:384–386

    Google Scholar 

  • Subbarao GV, Johansen C, Kumar Rao JVDK, Jana MK (1990) Response of the pigeonpea — Rhizobium symbiosis to salinity stress: Variation among Rhizobium strains in symbiotic ability. Biol Fertil Soils 9:49–53

    Google Scholar 

  • Tu JC (1981) Effect of salinity on Rhizobium-root hair interaction, nodulation and growth of soybean. Can J Plant Sci 61:231–239

    Google Scholar 

  • Udovenko GV, Mashanskii VF, Sinitskoya IA (1970) Changes of root cell ultrastructure under salinization in plants of different salt resistance. Sov Plant Physiol 17:813–818

    Google Scholar 

  • Velagaleti RR, Marsh S (1989) Influence of host cultivars and Bradyrhizobium strains on the growth and symbiotic performance of soybean under salt stress. Plant and Soil 119:133–138

    Google Scholar 

  • Wadisirisuk P, Danso SKA, Hardarason G, Bowen GD (1989) Influence of Bradyrhizobium japonicum location and movement on nodulation and nitrogen fixation in soybeans. Appl Environ Microbiol 55:1711–1716

    Google Scholar 

  • Wange SS (1989) Response of ground nut (Arachis hypogaea L.) to inoculation with Rhizobium strains isolated from wild arboreal legumes. MIRCEN J Appl Microbiol Biotechnol 5:135–141

    Google Scholar 

  • West DW, Taylor JA (1981) Germination and growth of cultivars of Trifolium subterraneum L. in the presence of sodium chloride salinity. Plant and Soil 62:221–230

    Google Scholar 

  • Wilson JR (1985) Comparative response to salinity of the growth and nodulation of Macroptilium atropurpureum cv. Siratro and Neonotonia wightii cv. Cooper seedlings. Aust J Agric Res 36:589–599

    Google Scholar 

  • Winter E, Läuchli A (1982) Salt tolerance of Trifolium alexandrinum L: 1. Comparison of the salt response of Trifolium alexandrinum and T. pratense. Aust J Plant Physiol 9:221–226

    Google Scholar 

  • Wyn Jones RG (1980) An assessment of Quaternary ammonium and related compounds as osmotic affectors in crop plants. In: Rains DW, Valentine RC, Hollaender A (eds) Genetic engineering and osmoregulation. Plenum Press, New York, pp 155–170

    Google Scholar 

  • Yadav NK, Vyas SR (1971) Response of root-nodule rhizobia to saline, alkaline and acid conditions. Indian J Agric Sci 41:875–881

    Google Scholar 

  • Yap SF, Lim ST (1983) Response of Rhizobium sp. UMKL 20 to sodium chloride stress. Arch Microbiol 135:224–228

    Google Scholar 

  • Zahran HH (1978) Studies on the effect of water stress and salinity on nitrogen fixation by some legumes. M Sc thesis, Assiut University, Assiut, Egypt

  • Zahran HH (1986) Effects of sodium chloride and polyethylene glycol on rhizobial root hair infection, root nodule structure and symbiotic nitrogen fixation in Vicia faba L. plants. Ph D thesis, Dundee University, Dundee, Scotland

  • 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

    Google Scholar 

  • Zhao YT, Kamisaka S, Masuda Y (1985) Quantitative relationships between osmotic potential and epicotyl growth in Vigna radiata as affected by osmotic stress and cotyledon excision. Physiol Plant 64:431–437

    Google Scholar 

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  1. Department of Botany, Faculty of Science, University of Assiut, Quena Branch, Quena, Egypt

    H. H. Zahran

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Zahran, H.H. Conditions for successful Rhizobium-legume symbiosis in saline environments. Biol Fert Soils 12, 73–80 (1991). https://doi.org/10.1007/BF00369391

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  • DOI: https://doi.org/10.1007/BF00369391

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