Abstract
Numerous studies have shown that soil salinity decreases nodulation and dramatically reduces N2 fixation and nitrogenase activity of nodulated legumes. Thus, the development of salt-tolerant symbioses is an absolute necessity to enable cultivation of leguminous crops in salt-affected soils. Dual inoculation of legumes with plant growth-promoting rhizobacteria (PGPR) and rhizobia has been reported to increase the number of nodules compared to those formed by a rhizobial strain alone. The production of IAA by Pseudomonas strains represents a beneficial mechanism that promoted enlargement of root system and thereby further enhanced nutrient uptake, nodulation, and shoot growth of leguminous plants. When PGPR are able to alleviate salt stress experienced by the plant, more nodules might develop into nitrogen-fixing ones, thereby enabling the plant to obtain part of its nitrogen from the atmosphere. Co-inoculation techniques could be a new approach to increase the salt tolerance and yield of legumes used for the food and green manure production in salt-affected soils, providing supply of biologically fixed N at low cost.
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References
Afzal I, Basra S, Iqbal A (2005) The effect of seed soaking with plant growth regulators on seedling vigor of wheat under salinity stress. J Stress Physiol Biochem 1:6–14
Akhtar MS, Siddiqui ZA (2009) Use of plant growth-promoting rhizobacteria for the biocontrol of root-rot disease complex of chickpea. Aust Plant Pathol 38:44–50
Ardakani S, Heydari A, Tayebi L, Mohammadi M (2010) Promotion of cotton seedlings growth characteristics by development and use of new bioformulations. Int J Bot 6(2):95–100
Arora NK, Khare E, Oh JH, Kang SC, Maheshwari DK (2008) Diverse mechanisms adopted by fluorescent Pseudomonas PGC2 during the inhibition of Rhizoctonia solani and Phytophthora capsici. World J Microbiol Biotechnol 24:581–585
Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with plant growth promoting rhizobacteria containing ACC-deaminase partially eliminates the effects of water stress on growth, yield and ripening of Pisum sativum L. Pedosphere 18:611–620
Ashraf M, McNeilly T (2004) Salinity tolerance in Brassica oilseeds. Crit Rev Plant Sci 23:157–174
Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT (2009) Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci Hortic 109:8–14
Barriuso J, Pereyra MT, Lucas García JA, Megías M, Gutierrez Mañero FJ, Ramos B (2005) Screening for putative PGPR to improve establishment of the symbiosis Lactarius deliciosus-pinus sp. Microb Ecol 50(1):82–89
Beltra R, Diaz F, Fraile G (1980) The formation of growth substances by Rhizobium species. Z Bakteriol Parasitenkd Infektionskr Hyg Abt 135:617–622
Bolton HJ, Elliott LF, Turco RF, Kennedy AC (1990) Rhizoplane colonisation of pea seedlings by Rhizobium leguminosarum and a deleterious root colonising Pseudomonas sp. and its effect on plant growth. Plant Soil 123:121–124
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
Burdman S, Kigel J, Okon Y (1997) Effects of Azospirillum brasilense on nodulation and growth of common bean (Phaseolus vulgaris L.). Soil Biol Biochem 29:923–929
Burdman S, Okon Y, Jurkevitch E (2000) Surface characteristics of Azospirillum brasilense in relation to cell aggregation and attachment to plant roots. Crit Rev Microbiol 26:91–110
Cakmakci R, Donmez D, Aydın A, Sahin F (2005) Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol Biochem 38:1482–1487
Carter JM, Gardner WK, Gibson AH (1994) Improved growth and yield of faba beans (Vicia faba cv. fiord) by inoculation with strains of Rhizobium leguminosarum biovar. viciae in acid soils in south-west Victoria. Aust J Agric Res 94:613–623
Cordovilla MP, Ocana A, Ligero F, Lluch C (1995) Salinity effects on growth analysis and nutrient composition in four grain legumes-Rhizobium symbiosis. J Plant Nutr 18:1595–1609
Cordovilla MD, 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
Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant associated bacteria. Crit Rev Microbiol 21:1–18
Creus CM, Sueldo RJ, Barassi CA (2004) Water relations and yield in Azospirillum inoculated wheat exposed to drought in the field. Can J Bot 82:273–281
Dashti N, Zhang F, Hynes R, Smith DL (1998) Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean (Glycine max (L. Merr.) under short season conditions. Plant Soil 200:205–213
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
Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159(4):371–394
Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879
Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864
Egamberdieva D (2011) Survival of Pseudomonas extremorientalis TSAU20 and P. chlororaphis TSAU13 in the rhizosphere of common bean (Phaseolus vulgaris) under saline conditions. Plant Soil Environ 57(3):122–127
Egamberdieva D, Kucharova Z (2009) Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45:563–571
Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, Chebotar V, Tikhonovich I, Kamilova F, Validov S, Lugtenberg B (2010) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fertil Soil 47:197–205
Egamberdieva D, Berg G, Lindström K, Räsänen LA (2013) Alleviation of salt stress of symbiotic Galega officinalis L. (Goat’s Rue) by co-inoculation of Rhizobium with root colonising Pseudomonas. Plant Soil doi: 10.1007/s11104-013-1586-3
Egamberdiyeva D, Hoflich G (2002) Root colonization and growth promotion of winter wheat and pea by Cellulomonas spp. at different temperatures. J Plant Growth Regul 38:219–224
Egamberdiyeva D, Islam KR (2008) Salt tolerant rhizobacteria: Plant growth promoting traits and physiological characterization within ecologically stressed environment. In: Ahmad I, Pichtel J, Hayat S (eds) Plant-bacteria interactions: strategies and techniques to promote plant growth. Wiley-VCH Verlag GmbH & Co., Weinheim, pp 257–281
Egamberdiyeva D, Qarshieva D, Davranov K (2004) The use of Bradyrhizobium japonicum to enhance growth and yield of soybean varieties in Uzbekistan conditions. J Plant Growth Regul 23:54–57
Egamberdiyeva D, Gafurova L, Islam KR (2007) Salinity effects on irrigated soil chemical and biological properties in the Syr Darya basin of Uzbekistan. In: Lal R, Sulaimanov M, Stewart B, Hansen D, Doraiswamy P (eds) Climate change and terrestrial c sequestration in Central Asia. Taylor-Francis, New York, pp 147–162
Elsheikh EAE, Elzidany AA (1997) Effects of Rhizobium inoculation, organic and chemical fertilizers on yield and physical properties of bean seeds. Plant Foods Human Nutr 51:137–144
Elsheikh EAE, Wood M (1995) Nodulation and N2 fixation by soybean inoculated with salt-tolerant Rhizobia or salt-sensitive Bradyrhizobia in saline soil. Soil Biol Biochem 27(4/5):657–661
FAO (2005) Salt-affected soils from sea water intrusion: strategies for rehabilitation and management. Report of the regional workshop, Bangkok, 62p
Frankenberger JWT, Arshad M (1995) Microbial synthesis of auxins. In: Frankenberger WT, Arshad M (eds) Phytohormones in soils. Marcel Dekker Inc, New York, pp 35–71
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117
Glick BR, Liu C, Ghosh S, Dumbrof EB (1997) Early development of canola seedlings in the presence of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Soil Biol Biochem 29:1233–1239
Glick BR, Penrose DM, Li JA (1998) Model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68
Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339
Goel AK, Sindhu SS, Dadarwal KR (2002) Stimulation of nodulation and plant growth of chickpea (Cicer arietinum) by Pseudomonas spp. antagonistic to fungal pathogens. Biol Fertil Soil 36:391–396
Gruodien J, Zvironaite V (1971) Effect of IAA on growth and synthesis of N compounds in Lucerne. Luk TSR Aukstuja Mosklo Darbai Biologia 17:77–87
Gulash M, Ames P, Larosiliere RC, Bergman K (1984) Rhizobia are attracted to localized sites on legume roots. Appl Environ Micobiol 48:149–152
Han H, Lee S (2005) Physiological responses of soybean - inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions. Res J Agric Biol Sci 1(3):216–221
Hashem FM, Swelim DM, Kuykendall LD, Mohamed AI, Abdel-Wahab SM, Hegazi NI (1998) Identification and characterization of salt and thermo-tolerant Leucaena nodulating Rhizobium strains. Biol Fertil Soil 27:335–341
Hasnain S, Sabri AN (1996) Growth stimulation of Triticum aestivum seedlings under Cr-stress by nonrhizospheric Pseudomonas strains. In: Abstract Book of 7th international symposium on nitrogen fixation with non-legumes, Faisalabad, 1996, 36p
Heidari M, Mousavinik SM, Golpayegani A (2011) Plant growth promoting rhizobacteria (PGPR) effect on physiological parameters and mineral uptake in basil (Ociumum basilicm L.) under water stress. ARPN J Agric Biol Sci 6(5):6–11
Hontzeas N, Richardson AO, Belimov A, Safronova V, Abu-Omar MM, Glick BR (2005) Evidence for horizontal transfer of 1-aminocyclopropane-1-carboxylate deaminase genes. Appl Environ Microbiol 71:7556–7558
Hunter WJ (1989) Indole-3-acetic acid production by bacteroids from soybean root nodules. Physiol Plant 76:31–36
Jackson M (1997) Hormones from roots as signals for the shoots of stressed plants. Elsevier Trends J 2:22–28
Joseph B, Patra RR, Lawrence R (2007) Characterization of plant growth promoting Rhizobacteria associated with chickpea (Cicer arietinum L). Int J Plant Prod 1:141–152
Kang SM, Joo GJ, Hamayun M, Na CI, Shin DH, Kim YK, Hong JK, Lee IJ (2009) Gibberellin production and phosphate solubilization by newly isolated strain of Acinetobacter calcoaceticus and its effect on plant growth. Biotechnol Lett 31:277–281
Khosravi H, Yakhchali B, Alikhani HA (2010) Potential evaluation of some native Rhizobia as plant growth promoting bacteria and their role on decreasing of stress ethylene. Iran J Biol 22(4):661–671
Khurana AS, Sharma P (2000) Effect of dual inoculation of phosphate solubilizing bacteria, Bradyrhizobium sp. and phosphorus on nitrogen fixation and yield of chickpea. Indian J Pulses Res 13:66–67
Klassen SP, Bugbee B (2002) Sensitivity of wheat and rice to low levels of atmospheric ethylene. Crop Sci 42:746–753
Lugtenberg B, Kamilova F (2009) Plant growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556
Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490
Ma JH, Yao JL, Cohen D, Morris B (1998) Ethylene inhibitors enhance in vitro root formation from apple shoot cultures. Plant Cell Rep 17:211–214
Mantelin S, Touraine B (2004) Plant growth-promoting bacteria and nitrate availability impacts on root development and nitrate uptake. J Exp Bot 55:27–34
Marcar NE, Dart P, Sweeney C (1991) Effect of root zone salinity on growth and chemical composition of Acacia ampliceps BR, Maslin A., auriculiformis A. Cunn ex Benth, and A. mangium Wild, at two nitrogen levels. New Phytol 119:567–573
Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530
Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51:326–335
Mensah JK, Ihenyen J (2009) Effect of salinity on germination, seedling establishment and yield of three genotypes of mung bean (Vigna Mungo L. Hepper) in Edo State, Nigeria. Niger Ann Nat Sci 8(2):17–24
Mishra PK, Mishra S, Bisht SC, Selvakumar G, Kundu S, Bisht JK, Gupta HS (2009) Isolation, molecular characterization and growth-promotion activities of a cold tolerant bacterium Pseudomonas sp. NARs9 (MTCC9002) from the Indian Himalayas. Biol Res 42:305–313
Mishra RK, Prakash O, Alam M, Dikshit A (2010) Influence of plant growth promoting rhizobacteria (PGPR) on the productivity of Pelargonium Graveolens l. herit. Recent Res Sci Technol 2(5):53–57
Parmar N, Dadarwall KR (1999) Stimulation of nitrogen fixation and induction of flavonoid like compounds by rhizobacteria. J Appl Microbiol 86:36–44
Plazinski J, Rolfe BG (1985) Azospirillum-Rhizobium interaction leading to plant growth stimulation without nodule formation. Can J Microbiol 31:1026–1030
Räsänen LA, Saijets S, Jokinen K, Lindström K (2003) Evaluation of the roles of two compatible solutes, glycine betaine and trehalose, for the Acacia senegal–Sinorhizobium symbiosis exposed to drought stress. Plant Soil 260:237–251
Ratti N, Kumar S, Verma HN, Gautams SP (2001) Improvement in bioavailability of tricalcium phosphate to Cymbopogon martini var. motia by rhizobacteria, AMF and azospirillum inoculation. Microbiol Res 156:145–149
Rekha PD, Lai WA, Arun AB, Young CC (2007) Effect of free and encapsulated Pseudomonas putida CC-FR2-4 and Bacillus subtilis CC-pg104 on plant growth under gnotobiotic condition. Bioresour Technol 98:447–451
Remans R, Beebe S, Blair M, Manrique G, Tovar E, Rao I, Croonenborghs A, Gutierrez RT, El-Howeitym M, Michiels J, Vanderleyden J (2008) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161
Rogers ME, Craig AD, Munns R, Colmer TD, Nichols PGH, Malcolm CV, Barrett-Lennard EG, Brown AJ, Semple WS, Evans PM, Cowley K, Hughes SJ, Snowball R, Bennett SJ, Sweeney GC, Dear BS, Ewing MA (2005) The potential for developing fodder plants for the salt-affected areas of southern and eastern Australia: an overview. Aust J Exp Agric 45:301–329
Rokhzadi A, Asgharzadeh A, Darvish F, Nour-Muhammadi G, Majidi E (2008) Influence of plant growth promoting rhizobacteria on dry matter accumulation and yield of chickpea (Cicer arietinum L.) under field conditions. Am Eur J Agric Environ Sci 3(2):253–257
Rosas SB, Andres JA, Rovera M, Correa N (2006) Phosphate-solubilizing Pseudomonas putida can influence the rhizobia-legume symbiosis. Soil Biol Biochem 38:3502–3505
Serraj RH, Vasquez- Diaz G, Hernandez DJJ (2001) Genotypic difference in response of nitrogenase activity (C2H2 reduction) to salinity and oxygen in common bean. Agronomie 21:645–650
Shahab S, Nuzhat A, Nasreen SK (2009) Indole acetic acid production and enhanced plant growth promotion by indigenous PSBs. Afr J Agric Res 4:1312–1316
Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Lett Appl Microbiol 42(2):155–159
Shannon MC (1997) Adaptation of plants to salinity. Adv Agron 60:75–120
Shirokova Y, Forkutsa I, Sharafutdinova N (2000) Use of electrical conductivity instead of soluble salts for soil salinity monitoring in Central Asia. Irrig Drain Syst 14:199–205
Siddiqui ZA, Iqbal A, Mahmood I (2001) Effects of Pseudomonas fluorescens and fertilizers on the reproduction of Meloidogyne incognita and growth of tomato. Appl Soil Ecol 16:179–185
Sindhu SS, Dadarwal KR (2001) Chitinolytic and cellulolytic Pseudomonas sp. antagonistic to fungal pathogens enhances nodulation by Mesorhizobium sp. Cicer in chickpea. Microbiol Res 156:353–358
Singleton PW, Bohlool B (1984) Effect of salinity on the nodule formation by soybean. Plant Physiol 74:72–76
Spaepen S, Vanderleyden J, Okon Y (2009) Plant growth-promoting actions of rhizobacteria. In: van Loon LC, Ed Kader JC, Delseny M (eds) Adv Bot Res 51:283–320
Srinivasan PS, Gopal KS (1977) Effect of plantofix and NAA formulation on groundnut var TMU-7. Curr Sci 46:119–120
Subbarao GV, Johansen C, Jana MK, Rao DKK (1990) Comparative salinity tolerance of symbiotically dependent at nitrogen fed pigeon pea (Cajanus cajan) and its wild relative Atylosia platycarpa. Biol Fertil Soil 10:11–16
Tanimoto E (2005) Regulation of root growth by plant hormones: roles for auxin and gibberellin. Crit Rev Plant Sci 24:249–265
Tilak KVBR, Ranganayaki N, Manoharachari C (2006) Synergistic effects of plant growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeon pea (Cajanus cajan). Eur J Soil Sci 57(1):67–71
Tsavkelova EA, Cherdyntseva TA, Klimova S, Shestakov AI, Botina SG, Netrusov AI (2007) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188:655–664
Upadhyay SK, Singh JS, Singh DP (2011) Exopolysaccharide-producing plant growth promoting rhizobacteria under salinity condition. Pedosphere 2:214–222
Valverde A, Velazquez E, Santos FF, Vizcaino N, Rivas R, Mateos PF, Molina EM, Igual JM, Willems A (2005) Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol 55:1985–1989
Van Hoorn JW, Katerji N, Hamdy A, Mastororilli M (2001) Effect of salinity on yield and nitrogen uptake of four grain legumes and on biological nitrogen contribution from the soil. Agric Water Manage 51:87–98
Velagaleti RR, Marsh S (1989) Influence of host cultivars and Bradyrhizobium strains on the growth and symbiotic performance of soybean under salt stress. Plant Soil 119:133–138
Vincent B, Marlet S, Vidal A, Bouarfa S, Wu J, Yang J, N’Diaye MK, Kuper M, Zimmer D (2006) Water and soil salinity management and salt redistribution in irrigation systems. In: Combating global soil and land degradation IV. Salinization, sodification and other forms of degradation in agricultural and native ecosystems. Proceedings 18th world congress of soil science, Philadelphia, 2006
Walsh KB (1995) Physiology of the legume nodule and its response to stress. Soil Biol Biochem 27:637–655
Wang TL, Wood EA, Brewin NJ (1982) Growth regulators, Rhizobium and nodulation in peas. Indole-3-acetic acid from the culture medium of nodulating and non-nodulating strains of R. leguminosarum. Planta 155:343–349
Wheeler CT, Henson IE, Mc Laughlin ME (1979) Hormones in plants bearing actinomycete nodules. Bot Gaz 140:52–57
Williams MNV, Singer ER (1990) Metabolism of tryptophan and tryptophan analogs by Rhizobium meliloti. Plant Physiol 92:1009–1013
Yadegari M, Rahmani A (2010) Evaluation of bean (Phaseolus vulgaris) seeds inoculation with Rhizobium phaseoli and plant growth promoting Rhizobacteria (PGPR) on yield and yield components. Afr J Agric Res 5:792–799
Yasmin F, Othman R, Saad MS, Sijam K (2007) Screening for beneficial properties of Rhizobacteria isolated from sweet potato rhizosphere. J Biotechnol 6:49–52
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, Abu-Gharbia MA (1995) Development and structure of bacterial root-nodules of two Egyptian cultivars of Vicia faba L. under salt and water stresses. Bull Fac Sci Assiut Univ 24:1–10
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
Zholkevich VN, Pustovoytova TN (1993) The role of Cucumis sativum L. leaves and content of phytohormones under soil drought. Russ J Plant Physiol 40:676–680
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Egamberdieva, D., Jabborova, D., Wirth, S. (2013). Alleviation of Salt Stress in Legumes by Co-inoculation with Pseudomonas and Rhizobium . In: Arora, N. (eds) Plant Microbe Symbiosis: Fundamentals and Advances. Springer, New Delhi. https://doi.org/10.1007/978-81-322-1287-4_11
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