Abstract
This study was conducted to examine the effects of the combined application of rhizobial strains and plant growth-promoting rhizobacteria at different ratios on growth and salt tolerance of lucerne. Vegetative growth, relative water content, photosynthetic pigments and organic and inorganic solute contents in leaves were measured after 6 weeks of sowing. The results showed that bacterial inoculation significantly increased shoot and root dry weight, leaf number and relative water content whereas salinity reduced the growth of plants mainly in root dry weight and leaf area. However, the obtained results showed a significant improvement in the growth under salt stress of inoculated plants compared to non-inoculated ones. Regarding photosynthetic pigments, inoculation and salt induced significant variations in the total chlorophyll content, whereas changes in carotenoids remained insignificant. The inoculated plants accumulated less sodium and chloride and maintained a constant potassium content compared to non-inoculated plants. This would imply that the bacteria have retained Na+ and Cl− and so have consequently limited their translocation to the leaves and have promoted selectivity of K+ ions relative to Na+. The levels of organic solutes and soluble proteins were not significantly affected in most plants by both salt and bacterial inoculation, suggesting that they are not directly involved in the strategy of salt tolerance of Lucerne. These results indicate that inoculation with these plant growth promoting rhizobacteria could mitigate the adverse effects of soil salinity on growth of lucerne suggesting that these species could be used as bio-inoculants to increase productivity in arid and semi-arid lands.
Similar content being viewed by others
References
Al Khanjari S, Al Khathiri A, Esechie HA (2002) Variation in chlorophyll meter readings, nodulation and dry matter yield of alfalfa (Medicago sativa L.) cultivars differing in salt tolerance. Crop Res 24:350–356
Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Brady-rhizobium species as plant growth promoting rhizobacteria on non legumes: effects of Radishes (Rhaphanus sativus L.). Plant Soil 204:57–67
Apse MP, Blumwald E (2002) Engineering salt tolerance in plants. Curr Opin Biotech 13:146–150
Ashraf M, O’Leary JW (1996) Responses of some newly developed salt-tolerant genotypes of spring wheat to salt stress: II Water relations and photosynthetic capacity. Acta Bot Neerl 45:29–39
Ashraf M, Hasnain S, Berge O, Mahmood T (2004) Inoculating wheat seeds with exopolysaccharides producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol Fert Soils 40:157–162
Awad NM, Turky AS, Abdelhamid MT, Attia M (2012) Ameliorate of environmental salt stress on the growth of Zea mays L. plants by exopolysaccharides producing bacteria. J Appl Sci Res 8:2033–2044
Belkhodja M, Bidai Y (2004) Réponse des graines d’Atriplex halimus L. à la salinité au stade de la germination. Secheresse 15:331–335
Boughalleb F, Hajlaoui H, Mhamdi M, Denden M (2011) Possible involvement of organic compounds and the antioxidant defense system in salt tolerance of Medicago arborea L. Agron J 6:353–365
Boughanmi N, Michonneau P, Daghfous D, Fleurat-Lessard P (2005) Adaptation of Medicago sativa cv. Gabès to long-term NaCl stress. J Plant Nutr Soil Sc 168:262–268
Boutraa T, Sanders FE (2001) Influence of water stress on grain yield and vegetative growth of two cultivars of bean (Phaseolus vulgaris L.). J Agron Crop Sci 187(4):251–257
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein –dye binding. Anal Biochem 72:248–254
Camila D Medeiros, Jose´ R. C Ferreira Neto, Marciel T. Oliveira Rebeca Rivas, Valesca Pandolfi, Ederson A. Kido, Jose´. I. Baldani, Mauro G.Santos (2014) Photosynthesis, antioxidant activities and transcriptional responses in two sugarcane (Saccharum officinarum L.) cultivars under salt stress. Acta Physiol Plant 36(2): 447–459
Cetaldo DA, Haroon M, Schrader LE, Young VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plan 6:71–80
Ciriaco da Silva E, Nogueira RJMC, Pinheiro De Araujo F, Franklin de Melo N, de Azevedo Dias, Neto A (2008) Physiological responses to salt stress in young umbu plants. Environ Exp Bot 63:147–157
Clark JM, Mc Caig TN (1982) Evaluation of techniques for screening for drought resistance in wheat. Crop Sci 22:503–506
De Lacerda CF, Cambraia J, Oliva MA, Ruiz HA, Prisco JT (2003) Solute accumulation and distribution during shoot and leaf devlopment in two sorghum genotypes under salt stress. Environ Exp Bot 49:107–120
Delauney A, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223
Demirevska K, Zasheva D, Dimitrov R, Simova Stoilova L, Stamenova M, Feller U (2009) Drought stress effects on Rubisco in Wheat: changes in the Rubisco large subunit. Acta Physiol Plant 31:1129–1138
Desbrosses GJ, Stougaard J (2011) Root nodulation: A paradigm for how plant- microbe symbiosis influences host developmental pathways. Cell host Microbe 10:348–358
Dimpka C, Weinand T, Ash F (2009) Plant Rhizobacteria interactions alleviate abiotic stress conditions. Plant, Cell Environ 32:1682–1694
Ding Y, Kalo P, Yendrek C, Sun J, Liang Y, Marsh JF, Harris JM, Oldroyd GED (2008) Abscissic acid coordinates Nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20:2681–2695
Djilianov D, Prinsen E, Oden S, Van Onckelen A, Muller J (2003) Nodulation under salt stress of alfalfa lines obtained after in vitro selection for osmotic tolerance. Plant Sci 165:887–894
Dobbelaere S, Croonenborghs A, Thys A, Vanderbroek A, Vanderleyden J (1999) Phytostimulatory effects of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164
Elsheery NI, Cao KF (2008) Gas exchange, chlorophyll fluorescence and osmotic adjustment in two mango cultivars under drought stress. Acta Physiol Plant 30:769–777
Esechie HA, Rodriguez V, Al Asmi MS (2002) Effect of sodium chloride salinity on cation equilibria in alfalfa (Medicago sativa L.). Crop Res 23:253–258
FAO (2002) Crop water management alfalfa. FAO, http://www.fao.Org/AG/aglW/cropwater/alfalfa.stm
FAO (2010) Land and plant nutrition management service, FAO, http://www.fao.org/ag/AGL/agll/prosoil/saline.htm
Farissi M, Bouizgaren A, Faghire M, Bargaz A, Ghoulam C (2011) Agro-physiological responses of Moroccan alfalfa (Medicago sativa L.) populations to salt stress during germination and early seedling stages. Seed Sci Technol 39:389–401
Figueiredo H, Burity C, Martinez C, Chanway C (2008a) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182–188
Figueiredo MVB, Martinez CR, Burity HA, Chanway CP (2008b) Plant growth promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean(Phaseolus vulgaris L.). World J Microbiol Biotechnol 24:1178–1193
Garg N, Shikha C (2011) Effect of mycorhizal inoculation on growth, nitrogen fixation and nutrient uptake in Cicer arietinum under salt stress. Turk. J. Agric. For 35:205–214
Garg N, Singla R (2004) Growth, photosynthesis, nodule nitrogen and carbon fixation in the chickpea cultivars under salinity stress. Braz J Plant Physiol 16:50–74
Ghosh S, Basu PS (2006) Production and metabolism of indole acetic acid in roots and root nodules of Phaseolus mungo. Microbiol Res 161:362–366
Giri B, Mukerji KG (2004) Mycorrhizal inoculants alleviates salt stress in Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312
Guru Devi R, Pandiyarajan V, Gurusaravanan P (2012) Alleviating effect of IAA on salt stressed Phaseolus mungo L. with reference to growth and biochemical characteristics. Rec Res Sci Tech 4:22–24
Hamrouni L, Hanana M, Abdelly C, Ghorbel A (2011) Exclusion du chlorure et inclusion du sodium : deux mécanismes concomitants de tolérance à la salinité chez la vigne sauvage vitis vinifera subsp. sylvestris Biotechnol Agronom Soc Environ 15:387–400
Han HS, Lee KD (2005a) Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res J Agric Biol Sci 1:210–215
Han HS, Lee KD (2005b) Physiological response of soybean- inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions. Res J Agric Biol Sci 1:216–221
Hanana M, Hamrouni L, Cagnac O, Blumwald E (2011) Mécanismes et strategies cellulaires de tolérance à la salinité (NaCl) chez les plantes. Environ Rev 19:121–140
Kaya C, Ashraf M, Dikilitas M, Tuna AL (2013) Alleviation of salt stress induced adverse effects on maize plants by exogenous application of indole acetic acid (IAA) and inorganic nutrients- A field trial. Aust J Crop Sci 7:249–254
Laguerre G, Allard MR, Revoy F, Amarger N (1994) Rapid identification of Rhizobia by restriction fragment length polymorphism analysis of PCR amplified 16S rRNA genes. Appl Environ Microbiol 60:56–63
Lichtenthaler HK (1987) Chlorophylls and caratenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Liu C, Liu Y, Guo K, Fan D, Li G, Zheng Y, Yu L, Yang R (2011) Effect of drought on pigments, osmotic adjustment and antioxydant enzymes in six woody plant species in karst habitats of south western China. Environ Exp Bot 71:174–183
Martinez-Viveros O, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant gowth promotion by Rhizobacteria. J Soil Sci Plant Nutr 10:293–319
Mayak S, Tirosh T, Glick BR (2004) Plant growth promoting bacteria confere resistance in tomato plants to salt stress. Plant Physiol Bioch 42:565–572
McReady RM, Guggoz J, Silver V, Owensh S (1950) Determination of starch and amylase in vegetables. Anal Chem 22:1156–1160
Mezni M, Albouchi A, Bizid E, Hamza M (2010) Mineral uptake, organic osmotic contents and water balance in alfalfa under salt stress. J Phytol 2:01–12
Monirifar H, Barghi M (2009) Identification and selection for salt tolerance in alfalfa (Medicago sativa L.) ecotypes via physiological traits. Not Sci Biol 1:63–66
Munné-Bosch S, Penulas J (2003) Photo and antioxydative protection during summer leaf senescence in Pistacia lentiscus L. grown under mediterranean field conditions. Ann Bot 92:385–391
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Nabizadeh E, Jalilnejad N, Armakani M (2011) Effect of salinity on growth and nitrogen fixation of alfalfa (Medicago sativa L.). World Appl Sci J 13: 1895-1900
Perez –Alfocea F, Estan F, Caro M, Balarin MC (1993) Response of tomato cultivars to salinity. Plant Soil 150:203–211
Pitman MG, Lauchli A (2002) Global impact of salinity and agricultural ecosystem. In: Lauchli A, Luttge U (eds) Salinity: environment –plants-molecules. Kluwer Academic Publishers, Dordrecht, pp 3–20
Platten JD, Egdane JA, Ismail AM (2013) Salinity tolerance, Na + exclusion and allele miing of HKT1:5 in Oryza sativa and O.glaberrima: many source, many genes, one mechanism? BMC Plant Biol 13:32
Saadallah K, Drevon JJ, Abdelly C (2001) Nodulation et croissance nodulaire chez le haricot (Phaseolus vulgaris) sous contrainte saline. Agronomie 21:627–634
Sandhya V, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62:21–30
Sandhya V, Ali SZ, Grover M, Reddy G, Bandi V (2011) Drought tolerant plant growth promoting Bacillus spp: effect on growth, osmolytes and antioxidant status of maize under drought stress. J Plant Interact 6:1–14
Serradj R, Drevon JJ (1998) Effects of salinity and nitrogen source on growth and nitrogen fixation in alfalfa. J Plant Nutr 21:1805–1818
Shannon MC (1997) Adaptation of plants to salinity. Adv Agron 60:75–120
Shukla PP, Agarwal PK, Jha B (2012) Improved salinity tolerance of Arachis hypogeal L. by the interaction of halotolerant plant growth promoting rhizobacteria. J Plant Growth Regul 31:195–206
Talaouizte A, Moyse A, Champigny ML (1989) Bases physiologiques de la nutrition nitrique des végétaux supérieurs. I. Absorption de NO3. Ann. Biol. 28:233–254
Tiwari TN, Singh BB (1991) Stress studies in lentil (Lens esculenta Moench). II. Sodicity induced changes in chlorophyll, nitrate, nitrite reductase, nucleic acids, proline, yield and yield component in lentil. Plant Soil 35:225–250
Troll W, Lindsey J (1954) A photometric method for the determination of proline. J Biol Chem 215:655–660
Upadhyay SK, Singh JS, Saxena AK, Singh DP (2012) Impact of PGPR inoculation on growth and antioxydant status of wheat under saline conditions. Plant Biol 14:605–611
Vincent JN (1970) A manual for the practical study handbook N°15. Blakwell, Oxford, p 164
Wang WB, Kim YH, Lee HS, Kim K, Deng XP, Kwak SS (2009) Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant physiol. Bioch 47:570–577
Wang X, Chen W, Zhou Y, Han J, Zhao J, Shi D, Yang C (2012) Comparison of adaptive strategies of alfalfa (Medicago sativa L.) to salt and alkali stress. Aust J Crop Sci 6:309–315
Wanichananan P, Kirdmanee C, Vutiyano C (2003) Effect of salinity on biochemical and physiological characteristics in correlation to selection of salt tolerance in aromatic rice (Oryza sativa L.). Science Asia 29:333–339
Wu Y, Hu Y, Xu G (2009) Interactive effect of potassium and sodium on root growth and expression of K/Na transporter gene in rice. Plant Growth Regul 57:271–280
Xue Z, Zhao S, Gao H, Sun S (2014) The salt resistance of wild soybean (Glycine soja Sieb. et Zucc. ZYD 03262) under NaCl stress is mainly determined by Na + distribution in the plant. Acta Physiol Plant 36:61–70
Yang P, Zhang P, Li B, Hu T (2013) Effect of nodules on dehydration response in alfalfa (Medicago sativa L.). Environ Exper Bot 86:29–34
Yildirim E, Turan M, Donmez MF (2008) Mitigation of salt stress in radish (Raphanus sativus L.) by plant growth promoting rhizobacteria. Rom Biotech Lett 13:3933–3943
Yildirim E, Turan M, Ekinci M, Dursun A, Cakmakci R (2011) Plant growth promoting rhizobacteria ameliorate deleterious effect of salt stress on lettuce. Sci Res Essays 6:4389–4396
Yousfi N, Slama I, Abdelly C (2012) Phenology, leaf gas exchange, growth and seed yield in contrasting Medicago truncatula and Medicago laciniata populations during prolonged water deficit and recovery. Botany 90:79–91
Zaman B, Niazi BH, Athar M, Ahmad M (2005) Response of wheat plants to sodium and calcium ion interaction under saline environment. Int J Environ Sci Te 2:7–12
Zhang F, Dashti N, Hynes RK, Smith DL (1996) Plant growth promoting rhizobacteria and soybean (Glycine max L. Merr). Nodulation and nitrogen fixation at suboptimal root zone temperatures. Ann Bot 77:453–459
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Baha, N., Bekki, A. An Approach of Improving Plant Salt Tolerance of Lucerne (Medicago sativa) Grown Under Salt Stress: Use of Bio-inoculants. J Plant Growth Regul 34, 169–182 (2015). https://doi.org/10.1007/s00344-014-9455-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-014-9455-8