Applied Microbiology and Biotechnology

, Volume 100, Issue 6, pp 2829–2841 | Cite as

A synergistic interaction between salt-tolerant Pseudomonas and Mesorhizobium strains improves growth and symbiotic performance of liquorice (Glycyrrhiza uralensis Fish.) under salt stress

  • Dilfuza Egamberdieva
  • Li Li
  • Kristina Lindström
  • Leena A. Räsänen
Environmental biotechnology


Chinese liquorice (Glycyrrhiza uralensis Fish.) is a salt-tolerant medicinal legume that could be utilized for bioremediation of salt-affected soils. We studied whether co-inoculation of the symbiotic Mesorhizobium sp. strain NWXJ19 or NWXJ31 with the plant growth-promoting Pseudomonas extremorientalis TSAU20 could restore growth, nodulation, and shoot/root nitrogen contents of salt-stressed G. uralensis, which was grown in potting soil and irrigated with 0, 50, and 75 mM NaCl solutions under greenhouse conditions. Irrigation with NaCl solutions clearly retarded the growth of uninoculated liquorice, and the higher the NaCl concentration (75 and 100 mM NaCl), the more adverse is the effect. The two Mesorhizobium strains, added either alone or in combination with P. extremorientalis TSAU20, responded differently to the salt levels used. The strain NWXJ19 was a good symbiont for plants irrigated with 50 mM NaCl, whereas the strain NWXJ31 was more efficient for plants irrigated with water or 75 mM NaCl solution. P. extremorientalis TSAU20 combined with single Mesorhizobium strains alleviated the salt stress of liquorice plants and improved yield and nodule numbers significantly in comparison with single-strain-inoculated liquorice. Both salt stress and inoculation raised the nitrogen content of shoots and roots. The nitrogen contents were at their highest, i.e., 30 and 35 % greater compared to non-stressed uninoculated plants, when plants were inoculated with P. extremorientalis TSAU20 and Mesorhizobium sp. NWXJ31 as well as irrigated with 75 mM NaCl solution. From this study, we conclude that dual inoculation with plant growth-promoting rhizobacteria could be a new approach to improve the tolerance of G. uralensis to salt stress, thereby improving its suitability for the remediation of saline lands.


Liquorice Glycyrrhiza uralensis Symbiosis Salinity Plant growth Nutrition 


  1. Ahmad P (2013) Oxidative damage to plants, antioxidant networks and signaling. Academic, Elsevier, San DiegoGoogle Scholar
  2. Ahmad M, Zahir ZA, Khalid M, Nazli F, Arshad M (2013) Efficacy of Rhizobium and Pseudomonas strains to improve physiology, ionic balance and quality of mung bean under salt-affected conditions on farmer’s fields. Plant Phys Biochem 63:170–176. doi:10.1016/j.plaphy.2012.11.024 CrossRefGoogle Scholar
  3. Beringer JB (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188–198PubMedGoogle Scholar
  4. Dardanelli MS, Manyani H, González-Barroso S, Rodríquez-Carvajal MA, Gil-Serrano AM, Espuny MR, López-Baena FJ, Bellogin RA, Megías M, Ollero FJ (2010) Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum AUR9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 328:483–493. doi:10.1007/s11104-009-0127-6 CrossRefGoogle Scholar
  5. Dhingra D, Sharma A (2006) Antidepressant-like activity of Glycyrrhiza glabra L. in mouse models of immobility tests. Prog Neuropsychopharmacol Biol Psychiatry 30:449–454CrossRefPubMedGoogle Scholar
  6. 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 Env 57(3):122–127Google Scholar
  7. Egamberdieva D, Kucharova Z (2009) Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol Fert Soils 45:561–573. doi:10.1007/s00374-009-0366-y CrossRefGoogle Scholar
  8. Egamberdieva D, Berg G, Lindström K, Räsänen LA (2010) Root colonizing Pseudomonas spp. improve growth and symbiosis performance of fodder galega (Galega orientalis LAM) grown in potting soil. Eur J Soil Biol 46(3-4):269–272. doi:10.1016/j.ejsobi.2010.01.005 CrossRefGoogle Scholar
  9. Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, Chebotar V, Tikhonovich I, Kamilova F, Validov S, Lugtenberg B (2011) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fert Soils 47:197–205. doi:10.1007/s00374-010-0523-3 CrossRefGoogle Scholar
  10. Egamberdieva D, Berg G, Lindström K, Räsänen LA (2013a) Alleviation of salt stress of symbiotic Galega officinalis L. (goat’s rue) by co-inoculation of Rhizobium with root colonizing Pseudomonas. Plant Soil 369(1):453–465. doi:10.1007/s11104-013-1586-3 CrossRefGoogle Scholar
  11. Egamberdieva D, Jabborova D, Wirth S (2013b) Alleviation of salt stress in legumes by co-inoculation with Pseudomonas and Rhizobium. In: Arora NK (ed) Plant microbe symbiosis—fundamentals and advances. Springer, New Delhi, pp 291–303CrossRefGoogle Scholar
  12. Egamberdieva D, Jabborova D, Mamadalieva N (2013c) Salt tolerant Pseudomonas extremorientalis able to stimulate growth of Silybum marianum under salt stress condition. Med Aromat Plant Sci Biotechnol 7(1):7–10Google Scholar
  13. FAO (2008) Land and plant nutrition management service.
  14. Fukai T, Ali M, Kaitou K, Kanda T, Terada S, Nomura T (2002) Anti-Helicobacter pylori flavonoids from licorice extract. Life Sci 71:1449–1463CrossRefPubMedGoogle Scholar
  15. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scient 2012:963401CrossRefGoogle Scholar
  16. Hayashi H, Sudo H (2009) Economic importance of licorice. Plant Biotechnol 26:101–104CrossRefGoogle Scholar
  17. Hiz MC, Canher B, Niron H, Turet M (2014) Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions. PLoS ONE 9(3):e92598PubMedCentralCrossRefPubMedGoogle Scholar
  18. Huq SMI, Larher F (1983) Osmoregulation in higher plants: effect of NaCl salinity on non-nodulated Phaseolus aureus L. New Phytol 93:209–216CrossRefGoogle Scholar
  19. Jabborova D, Egamberdieva D, Räsänen L, Liao H (2013) Salt tolerant Pseudomonas strain improved growth, nodulation and nutrient uptake of soybean grown under hydroponic salt stress condition. In: XVII. International Plant Nutrition Colloquium and Boron Satellite Meeting Proceedings Book (2013). Sabanci University, Istanbul, Turkey. 2013ipnc-b-proceedings.html, pp. 260-261
  20. Khan MIR, Khan NA (2013) Salicylic acid and jasmonates: approaches in abiotic stress tolerance. J Plant Biochem Physiology 1:4. doi:10.4172/2329-9029.1000e113 Google Scholar
  21. Kushiev H, Noble AD, Abdullaev I, Toshbekov V (2005) Remediation of abandoned saline soils using Glycyrrhiza glabra: a study for the hungry steppes of Central Asia. Inter J Agric Sustain 3:102–113CrossRefGoogle Scholar
  22. Li L, Sinkko H, Montonen L, Wei G, Lindström K, Räsänen LA (2012) Biogeography of symbiotic and other endophytic bacteria isolated from medicinal Glycyrrhiza species in China. FEMS Microb Ecol 79:46–68. doi:10.1111/j.1574-6941.2011.01198.x CrossRefGoogle Scholar
  23. Li W, Hou J, Wang W, Tang X, Liu C, Xing D (2011) Effect of water deficit on biomass production and accumulation of secondary metabolites in roots of Glycyrrhiza uralensis. Russian J Plant Physiol 58:538–542. doi:10.1134/S1021443711030101 CrossRefGoogle Scholar
  24. Lewis G, Schrire B, Mackinder B, Lock M (2005) Legumes of the world royal botanic gardens. Kew, LondonGoogle Scholar
  25. Mateos PF, Jimenez-Zurdo JI, Chen J, Squartini AS, Haack SK, Martinez-Molina E, Hubbell DH, Dazzo FB (1992) Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 58(6):1816–1822PubMedCentralPubMedGoogle Scholar
  26. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663CrossRefPubMedGoogle Scholar
  27. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1016/j.tplants.2014.02.001 CrossRefPubMedGoogle Scholar
  28. Marui A, Nagafuchi T, Shinogi Y, Yasufuku N, Omine K, Kobayashi T, Shinka T, Tuvshintogtokh I, Mandakh B, Munkhjargal B (2012) Soil physical properties to grow the wild licorice at semi-arid area in Mongolia. J Arid Land Studies 22(1):33–36Google Scholar
  29. Mensah JK, Ihenyen J (2009) Effects of salinity on germination, seedling establishment and yield of three genotypes of mung bean (Vigna mungo L. Hepper) in Edo State, Nigeria. Nigerian Ann Nat Sci 8(2):17–24Google Scholar
  30. Mizutani K, Kuramoto T, Tamura Y, Ohtake N, Doi S, Nakaura M, Tanaka O (1994) Sweetness of glycyrrhetinic acid 3-O-mono-β-D-glucuronide and related glycosides. Biosci Biotechnol Biochem 58:554–555CrossRefPubMedGoogle Scholar
  31. Ondrasek G, Rengel Z, Romic D, Poljak M, Romic M (2009) Accumulation of non/essential elements in radish plants grown in salt-affected and cadmium contaminated environment. Cereal Res Comm 37:9–12Google Scholar
  32. Patil SM, Patil MB, Sapkale GN (2009) Antimicrobial activity of Glycyrrhiza glabra Linn. roots. Int J Chem Sci 7(1):585–591Google Scholar
  33. Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34:737–752. doi:10.1007/s13593-014-0233-6 CrossRefGoogle Scholar
  34. Paungfoo-Lonhienne C, Rentsch D, Robatzek S, Webb RI, Sagulenko E, Näsholm T, Schmidt S, Lonhienne TGA (2010) Turning the table: plants consume microbes as a source of nutrients. PLoS ONE 5(7):e11915. doi:10.1371/journal.pone.0011915 PubMedCentralCrossRefPubMedGoogle Scholar
  35. Penttinen P, Räsänen LA, Lortet G, Lindström K (2013) Stable isotope labelling reveals that NaCl stress decreases the production of Ensifer (Sinorhizobium) arboris lipochitooligosaccharide signaling molecules. FEMS Microbiol Lett 349:117–126. doi:10.1111/1574-6968.12303 CrossRefPubMedGoogle Scholar
  36. Prieto P, Schilirò E, Maldonado-González MM, Valderrama R, Barroso-Albarracín JB, Mercado-Blanco J (2011) Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity. Microb Ecol 62:435–445. doi:10.1007/s00248-011-9827-6 PubMedCentralCrossRefPubMedGoogle Scholar
  37. Prakamhang J, Tittabutr P, Boonkerd N, Teamtisong K, Uchiumi T, Abe M, Teaumroong N (2015) Proposed some interactions at molecular level of PGPR co-inoculated with Bradyrhizobium diazoefficiens USDA110 and B. japonicum THA6 on soybean symbiosis and its potential of field application. Appl Soil Ecol 85:38–49. doi:10.1016/j.apsoil.2014.08.009 CrossRefGoogle Scholar
  38. Rabie GH, Almadini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotech 4(3):210–222Google Scholar
  39. Sánchez AC, Gutiérrez RT, Santana RC, Urrutia AR, Fauvart M, Michiels J, Vanderleyden J (2014) Effects of co-inoculation of native Rhizobium and Pseudomonas strains on growth parameters and yield of two contrasting Phaseolus vulgaris L. genotypes under Cuban soil conditions. Eur J Soil Biol 62:105–112. doi:10.1016/j.ejsobi.2014.03.004 CrossRefGoogle Scholar
  40. Sanchez DH, Lippold F, Redestig H, Hannah MA, Erban A, Krämer U, Kopka J, Udvardi MK (2008) Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant J 53:973–987CrossRefPubMedGoogle Scholar
  41. Shabani L, Ehsanpour AA, Asghari G, Emami J (2009) Glycyrrhizin production by in vitro cultured Glycyrrhiza glabra elicited by methyl jasmonate and salicylic acid. Russian J Plant Physiol 56:621–626CrossRefGoogle Scholar
  42. Simons M, van der Bij AJ, Brand I, de Weger LA, Wijffelman CA, Lugtenberg B (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol Plant-Microbe Inter 9:600–607CrossRefGoogle Scholar
  43. Shanker AK, Venkateswarlu B (2011) Abiotic stress in plants—mechanisms and adaptations. InTech, RijekaCrossRefGoogle Scholar
  44. Schulz V, Hänsel R, Tyler VE (1998) Rational phytotherapy. A physicians’ guide to herbal medicine. Springer, Berlin, pp 160–187CrossRefGoogle Scholar
  45. Sindhu SS, Dadarwal KR (2001) Chitinolytic and cellulolytic Pseudomonas sp. antagonistic to fungal pathogens enhances nodulation by Mesorhizobium sp. cicer in chickpea. Microbiol Res 156:353–358CrossRefPubMedGoogle Scholar
  46. Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, LondonGoogle Scholar
  47. 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 9:49–53CrossRefGoogle Scholar
  48. Soil Science Society of America (2001) Glossary of soil science terms. Soil Science Society of America, MadisonGoogle Scholar
  49. 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. doi:10.1111/j.1365-2389.2006.00771.x CrossRefGoogle Scholar
  50. Van Hoorn JW, Katerji N, Hamdy A, Mastrorilli M (2001) Effect of salinity on yield and nitrogen uptake of four grain legumes and on biological nitrogen contribution from the soil. Agr Water Man 51:87–98. doi:10.1016/S0378-3774(01)00114-7 CrossRefGoogle Scholar
  51. Vincent JM (1970) A manual for the practical study of root nodule bacteria. Blackwell, OxfordGoogle Scholar
  52. Warrence NJ, Bauder JW, Pearson KE (2004) Salinity, sodicity and flooding tolerance of selected plant species of the northern Cheyenne Reservation. Montana State University, MissoulaGoogle Scholar
  53. Wei GH, Yang XY, Zhang ZX, Yang YZ, Lindström K (2008) Strain Mesorhizobium sp. CCNWGX035: a stress-tolerant isolate from Glycyrrhiza glabra displaying a wide host range of nodulation. Pedosphere 18(1):102–112. doi:10.1016/S1002-0160(07)60108-8 CrossRefGoogle Scholar
  54. Xie F, Murray JD, Kim J, Heckmann AB, Edwards A, Oldroyd JED, Downie JA (2012) Legume pectate lyase required for root infection by rhizobia. PNAS 109:633–638PubMedCentralCrossRefPubMedGoogle Scholar
  55. 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 5:792–799Google Scholar
  56. Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Dilfuza Egamberdieva
    • 1
  • Li Li
    • 2
  • Kristina Lindström
    • 3
  • Leena A. Räsänen
    • 3
  1. 1.Institute for Landscape Biogeochemistry, Leibniz Centre for Agricultural Landscape Research (ZALF)MünchebergGermany
  2. 2.Key Laboratory of Biogeography and Bioresource in Arid Land, Chinese Academy of Science, Xinjiang Institute of Ecology and GeographyChinese Academy of SciencesUrumqiPeople’s Republic of China
  3. 3.Department of Food and Environmental SciencesUniversity of HelsinkiHelsinkiFinland

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