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Alleviation of salt stress response in soybean plants with the endophytic bacterial isolate Curtobacterium sp. SAK1

  • Muhammad Aaqil Khan
  • Sajjad Asaf
  • Abdul Latif Khan
  • Ihsan Ullah
  • Sajid Ali
  • Sang-Mo Kang
  • In-Jung LeeEmail author
Original Article
  • 40 Downloads

Abstract

Background

Salinity has been a major abiotic stressor that reduce the productivity. Previous studies reported that endophytic bacteria produce plant stress response hormones, antioxidants, and enzymes such as ACC deaminase. Augmentation of these metabolites and enzymes by endophytes mitigates the stress effects of salinity and improves plant growth and productivity.

Methods

Bacterial endophytes were isolated from Artemisia princeps Pamp, and evaluated for indole-3-acetic acid (IAA), abscisic acid (ABA), siderophore, and 1-aminocyclopropane-1-carboxylate (ACC) deaminase production and the ability to solubilize phosphate in the presence of NaCl (100–400 mM). SAK1 was applied to Glycine max cv. Pungsannamul to investigate salinity stress.

Results

Our results revealed that with an increase in NaCl concentration, the amount of ABA production in SAK1 increased, whereas IAA levels decreased. Bacterial ABA and JA degrade the reactive oxygen species and protect plants against stressors. Gas chromatography-mass spectrometry (GC-MS) analysis detected different gibberellins (GAs) and organic acids in SAK1. Interestingly, SAK1 inoculation significantly increased plant growth attributes under normal and salinity stress conditions, whereas a decrease in endogenous jasmonic acid and ABA content in the plants was recorded under salinity stress. IAA and GAs enhance number of root tips and hence improve nutrients uptake in plants. Polyphenolic oxidase and peroxidase were alleviated by elevated SAK1 in G. max plants under stress. ACC deaminase of SAK1 resulted deamination of ACC, up to 330 nmol α-ketobutyrate mg−1 h−1 which could be a major reason of ethylene reduction promoting plant growth.

Conclusion

SAK1 relieved salinity stress in plants by producing different phytohormones, antioxidants, and ACC deaminase enzyme. SAK1 could be a new addition in batch of plant stress hormone-regulating endophytic bacteria that mitigates the effects of salt stress and promotes plant growth in G. max.

Keywords

Endophytic bacteria ACC deaminase Salt stress Phytohormones Antioxidant 

Notes

Authors’ contributions

MAK, SA, SMK, and SA conducted the experiments. ALK and IU helped in writing of the manuscript. IJL designed, supervised, and financed the research. All authors have read and agreed to its content and also that the manuscript conforms to the journal’s policies.

Funding

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2016R1A6A1A05011910).

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

N/A

Informed consent state

N/A

References

  1. Ahmad M, Zahir ZA, Asghar HN, Asghar M (2011) Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant-growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 57:578–589.  https://doi.org/10.1139/w11-044 CrossRefGoogle Scholar
  2. Ali S, Kim W-C (2018) Plant growth promotion under water: decrease of waterlogging-induced acc and ethylene levels by ACC deaminase-producing bacteria. Front Microbiol 9:1096–1096.  https://doi.org/10.3389/fmicb.2018.01096 CrossRefGoogle Scholar
  3. Ali S, Charles TC, Glick BR (2014) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167.  https://doi.org/10.1016/j.plaphy.2014.04.003 CrossRefGoogle Scholar
  4. Ali S, Khan MA, Kim W-C (2018) Pseudomonas veronii KJ mitigates flood stress-associated damage in Sesamum indicum L. Appl Biol Chem 61:575–585.  https://doi.org/10.1007/s13765-018-0392-2 CrossRefGoogle Scholar
  5. Barnawal D, Bharti N, Tripathi A, Pandey SS, Chanotiya CS, Kalra A (2016) ACC-deaminase-producing endophyte brachybacterium paraconglomeratum strain smr20 ameliorates chlorophytum salinity stress via altering phytohormone generation. J Plant Growth Regul 35:553–564.  https://doi.org/10.1007/s00344-015-9560-3 CrossRefGoogle Scholar
  6. Belimov AA, Dodd IC, Safronova VI, Shaposhnikov AI, Azarova TS, Makarova NM, Davies WJ, Tikhonovich IA (2015) Rhizobacteria that produce auxins and contain 1-amino-cyclopropane-1-carboxylic acid deaminase decrease amino acid concentrations in the rhizosphere and improve growth and yield of well-watered and water-limited potato (Solanum tuberosum). Ann Appl Biol 167:11–25.  https://doi.org/10.1111/aab.12203 CrossRefGoogle Scholar
  7. Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107.  https://doi.org/10.1093/jxb/erp140 CrossRefGoogle Scholar
  8. Bianco C, Defez R (2010) Improvement of phosphate solubilization and Medicago plant yield by an indole-3-acetic acid-overproducing strain of Sinorhizobium meliloti. Appl Environ Microbiol 76:4626–4632.  https://doi.org/10.1128/AEM.02756-09 CrossRefGoogle Scholar
  9. 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.  https://doi.org/10.1016/0003-2697(76)90527-3
  10. Chen J-H, Jiang H-W, Hsieh E-J, Chen H-Y, Chien C-T, Hsieh H-L, Lin T-P (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351.  https://doi.org/10.1104/pp.111.181875 CrossRefGoogle Scholar
  11. Cheng Z, Park E, Glick BR (2007) 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can J Microbiol 53:912–918.  https://doi.org/10.1139/W07-050 CrossRefGoogle Scholar
  12. Cohen AC, Bottini R, Piccoli PN (2008) Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in arabidopsis plants. Plant Growth Regul 54:97–103.  https://doi.org/10.1007/s10725-007-9232-9 CrossRefGoogle Scholar
  13. Csiszár J, Horvath E, Vary Z, Galle A, Bela K, Brunner S, Tari I (2014) Glutathione transferase supergene family in tomato: salt stress-regulated expression of representative genes from distinct GST classes in plants primed with salicylic acid. Plant Physiol Biochem 78:15–26.  https://doi.org/10.1016/j.plaphy.2014.02.010 CrossRefGoogle Scholar
  14. Diaz-Vivancos P, de Simone A, Kiddle G, Foyer CH (2015) Glutathione linking cell proliferation to oxidative stress. Free Radic Biol Med 89:1154–1164.  https://doi.org/10.1016/j.freeradbiomed.2015.09.023 CrossRefGoogle Scholar
  15. Egamberdieva D, Jabborova D, Hashem A (2015) Pseudomonas induces salinity tolerance in cotton (Gossypium hirsutum) and resistance to Fusarium root rot through the modulation of indole-3-acetic acid. Saudi J Biol Sci 22:773–779.  https://doi.org/10.1016/j.sjbs.2015.04.019 CrossRefGoogle Scholar
  16. El-Awady MAM, Hassan MM, Al-Sodany YM (2015) Isolation and characterization of salt tolerant endophytic and rhizospheric plant growth-promoting bacteria (PGPB) associated with the halophyte plant (Sesuvium verrucosum) grown in KSA. Int J Appl Sci Biotechnol 3:9.  https://doi.org/10.3126/ijasbt.v3i3.13440 CrossRefGoogle Scholar
  17. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77.  https://doi.org/10.1016/0003-9861(59)90090-6
  18. Fatma M, Asgher M, Masood A, Khan NA (2014) Excess sulfur supplementation improves photosynthesis and growth in mustard under salt stress through increased production of glutathione. Environ Exp Bot 107:55–63.  https://doi.org/10.1016/j.envexpbot.2014.05.008
  19. Gamalero E, Berta G, Massa N, Glick BR, Lingua G (2010) Interactions between Pseudomonas putida UW4 and Gigaspora rosea BEG9 and their consequences for the growth of cucumber under salt-stress conditions. J Appl Microbiol 108:236–245.  https://doi.org/10.1111/j.1365-2672.2009.04414.x CrossRefGoogle Scholar
  20. Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212.  https://doi.org/10.1016/j.plaphy.2013.05.032 CrossRefGoogle Scholar
  21. Grant CM, MacIver FH, Dawes IW (1997) Glutathione synthetase is dispensable for growth under both normal and oxidative stress conditions in the yeast Saccharomyces cerevisiae due to an accumulation of the dipeptide gamma-glutamylcysteine. Mol Biol Cell 8:1699–1707CrossRefGoogle Scholar
  22. Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240.  https://doi.org/10.1007/s11274-010-0572-7 CrossRefGoogle Scholar
  23. Guan R, Qu Y, Guo Y, Yu L, Liu Y, Jiang J, Chen J, Ren Y, Liu G, Tian L, Jin L, Liu Z, Hong H, Chang R, Gilliham M, Qiu L (2014) Salinity tolerance in soybean is modulated by natural variation in GmSALT3. Plant J 80:937–950.  https://doi.org/10.1111/tpj.12695 CrossRefGoogle Scholar
  24. Gururani MA, Upadhyaya CP, Strasser RJ, Yu JW, Park SW (2013) Evaluation of abiotic stress tolerance in transgenic potato plants with reduced expression of PSII manganese stabilizing protein. Plant Sci 198:7–16.  https://doi.org/10.1016/j.plantsci.2012.09.014 CrossRefGoogle Scholar
  25. Habib SH, Kausar H, Saud HM (2016) Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed Res Int 2016:10.  https://doi.org/10.1155/2016/6284547 CrossRefGoogle Scholar
  26. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499.  https://doi.org/10.1146/annurev.arplant.51.1.463 CrossRefGoogle Scholar
  27. Hyo Shim Han KDL (2005) Physiological responses of soybean—inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions research. J Agric Biol Sci 1:216–221Google Scholar
  28. Irizarry I, White JF (2017) Application of bacteria from non-cultivated plants to promote growth, alter root architecture and alleviate salt stress of cotton. J Appl Microbiol 122(4):1110–1120.  https://doi.org/10.1111/jam.13414
  29. Jaemsaeng R, Jantasuriyarat C, Thamchaipenet A (2018) Molecular interaction of 1-aminocyclopropane-1-carboxylate deaminase (ACCD)-producing endophytic Streptomyces sp. GMKU 336 towards salt-stress resistance of Oryza sativa L. cv. KDML105. Sci Rep 8:1950.  https://doi.org/10.1038/s41598-018-19799-9 CrossRefGoogle Scholar
  30. Jalili F, Khavazi K, Pazira E, Nejati A, Rahmani HA, Sadaghiani HR, Miransari M (2009) Isolation and characterization of ACC deaminase-producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth. J Plant Physiol 166:667–674.  https://doi.org/10.1016/j.jplph.2008.08.004 CrossRefGoogle Scholar
  31. Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30:435–458.  https://doi.org/10.1080/07352689.2011.605739 CrossRefGoogle Scholar
  32. Kang SM, Khan AL, Hamayun M, Shinwari ZKS, Kim YH, Joo GJ, Lee IJ (2012) Acinetobacter calcoaceticus ameliorated plant growth and influenced gibberellins and functional biochemical. Pak J Bot 44:365–372Google Scholar
  33. Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57:315–319CrossRefGoogle Scholar
  34. Katznelson H, Bose B (1959) Metabolic activity and phosphate-dissolving capability of bacterial isolates from wheat roots, rhizosphere, and non-rhizosphere soil. Can J Microbiol 5:79–85CrossRefGoogle Scholar
  35. Khan AL, Hamayun M, Kang S-M, Kim Y-H, Jung H-Y, Lee J-H, and Lee I-J (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiology 12:3.  https://doi.org/10.1186/1471-2180-12-3
  36. Khan AL, Waqas M, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, Jung HY, Lee IJ (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689–695.  https://doi.org/10.1007/s12275-014-4002-7 CrossRefGoogle Scholar
  37. Khan AL, Al-Harrasi A, Al-Rawahi A, Al-Farsi Z, Al-Mamari A, Waqas M, Asaf S, Elyassi A, Mabood F, Shin JH, Lee IJ (2016) Endophytic fungi from frankincense tree improves host growth and produces extracellular enzymes and indole acetic acid. PLoS One 11:e0158207.  https://doi.org/10.1371/journal.pone.0158207 CrossRefGoogle Scholar
  38. Khan MA, Ullah I, Waqas M, Hamayun M, Khan AL, Asaf S, Kang SM, Kim KM, Jan R, Lee IJ (2018) Halo-tolerant rhizospheric Arthrobacter woluwensis AK1 mitigates salt stress and induces physio-hormonal changes and expression of GmST1 and GmLAX3 in soybean. Symbiosis.  https://doi.org/10.1007/s13199-018-0562-3
  39. Kim SY, Lim JH, Park MR, Kim YJ, Park TI, Seo YW, Choi KG, Yun SJ (2005) Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. J Biochem Mol Biol 38:218–224Google Scholar
  40. Kushnir S, Babiychuk E, Kampfenkel K, Belles-Boix E, Van Montagu M, Inze D (1995) Characterization of Arabidopsis thaliana cDNAs that render yeasts tolerant toward the thiol-oxidizing drug diamide. Proc Natl Acad Sci U S A 92:10580–10584CrossRefGoogle Scholar
  41. Li Z, Chang S, Ye S, Chen M, Lin L, Li Y, Li S, An Q (2015) Differentiation of 1-aminocyclopropane-1-carboxylate (ACC) deaminase from its homologs is the key for identifying bacteria containing ACC deaminase. FEMS Microbiol Ecol 91.  https://doi.org/10.1093/femsec/fiv112
  42. Maxton A, Singh P, Masih SA (2018) ACC deaminase-producing bacteria mediated drought and salt tolerance in Capsicum annuum. J Plant Nutr 41:574–583.  https://doi.org/10.1080/01904167.2017.1392574 CrossRefGoogle Scholar
  43. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572.  https://doi.org/10.1016/j.plaphy.2004.05.009 CrossRefGoogle Scholar
  44. McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430–435.  https://doi.org/10.1007/s004250050210 CrossRefGoogle Scholar
  45. Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113.  https://doi.org/10.1093/jxb/erh113 CrossRefGoogle Scholar
  46. Palaniyandi SA, Damodharan K, Yang SH, Suh JW (2014) Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’ tomato plants. J Appl Microbiol 117:766–773.  https://doi.org/10.1111/jam.12563 CrossRefGoogle Scholar
  47. Papiernik SK, Grieve CM, Lesch SM, Yates SR (2005) Effects of salinity, imazethapyr, and chlorimuron application on soybean growth and yield. Commun Soil Sci Plant Anal 36:951–967.  https://doi.org/10.1081/CSS-200050280 CrossRefGoogle Scholar
  48. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801.  https://doi.org/10.1128/aem.68.8.3795-3801.2002 CrossRefGoogle Scholar
  49. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase containing plant growth promoting rhizobacteria. Physiol Plant 118(1):10–15.  https://doi.org/10.1034/j.1399-3054.2003.00086.x
  50. Pimentel D, Berger B, Filiberto D, Newton M, Wolfe B, Karabinakis E, Clark S, Poon E, Abbett E, Nandagopal S (2004) Water resources: agricultural and environmental issues. BioScience 54:909–918. https://doi.org/10.1641/0006-3568(2004)054[0909:WRAAEI]2.0.CO;2Google Scholar
  51. Pitman MG, Lauchli A (2002) Global impact of salinity and agricultural ecosystems. Salinity: environment–plants–molecules. pp 3–20.  https://doi.org/10.1007/0-306-48155-3_1
  52. Qi Q, Rose PA, Abrams GD, Taylor DC, Abrams SR, Cutler AJ (1998) (+)-Abscisic acid metabolism, 3-ketoacyl-coenzyme A synthase gene expression, and very-long-chain monounsaturated fatty acid biosynthesis in Brassica napus embryos. Plant Physiol 117:979–987CrossRefGoogle Scholar
  53. Sambrook JF, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York, p 19–20Google Scholar
  54. Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292.  https://doi.org/10.1111/j.1365-2672.2006.03179.x CrossRefGoogle Scholar
  55. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56CrossRefGoogle Scholar
  56. Sergeeva E, Shah S, Glick BR (2006) Growth of transgenic canola (Brassica napus cv. Westar) expressing a bacterial1-aminocyclopropane-1-carboxylate (ACC) deaminase gene on high concentrations of salt. World J Microbiol Biotechnol 22:277–282.  https://doi.org/10.1007/s11274-005-9032-1 CrossRefGoogle Scholar
  57. Sgroy V, Cassan F, Masciarelli O, Del Papa MF, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotechnol 85:371–381.  https://doi.org/10.1007/s00253-009-2116-3 CrossRefGoogle Scholar
  58. Shaharoona B, Bibi R, Arshad M, Ahmed Z, Zahir Z, Hassan Z-U (2006) 1-Aminocylopropane-1-carboxylate (acc)- deaminase rhizobacteria extenuates acc-induced classical triple response in etiolated pea seedlings. Pak J Bot 38:1491–1499Google Scholar
  59. Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131.  https://doi.org/10.1016/j.sjbs.2014.12.001 CrossRefGoogle Scholar
  60. Sziderics AH, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53:1195–1202.  https://doi.org/10.1139/w07-082 CrossRefGoogle Scholar
  61. Szymanska S, Plociniczak T, Piotrowska-Seget Z, Hrynkiewicz K (2016) Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L. community structure and metabolic potential. Microbiol Res 192:37–51.  https://doi.org/10.1016/j.micres.2016.05.012 CrossRefGoogle Scholar
  62. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefGoogle Scholar
  63. Ullah I, Khan AR, Park G-S, Lim J-H, Waqas M, Lee I-J, Shin J-H (2013) Analysis of phytohormones and phosphate solubilization in Photorhabdus spp. Food Sci Biotechnol 22:25–31.  https://doi.org/10.1007/s10068-013-0044-6 CrossRefGoogle Scholar
  64. Ullah I, Al-Johny BO, Al-Ghamdi KMS, Al-Zahrani HAA, Anwar Y, Firoza A, Al-Kenani N, Almatrya MAA (2019) Endophytic bacteria isolated from Solanum nigrum L., alleviate cadmium (Cd) stress response by their antioxidant potentials, including SOD synthesis by sodA gene. Ecotoxicol Environ Saf 174:197–207.  https://doi.org/10.1016/j.ecoenv.2019.02.074 CrossRefGoogle Scholar
  65. Wang Y, Mopper S, Hasenstein KH (2001) Effects of salinity on endogenous ABA, IAA, JA, and SA in Iris hexagona. J Chem Ecol 27:327–342.  https://doi.org/10.1023/a:1005632506230 CrossRefGoogle Scholar
  66. Yaish MW, Antony I, Glick BR (2015) Isolation and characterization of endophytic plant growth-promoting bacteria from date palm tree (Phoenix dactylifera L.) and their potential role in salinity tolerance. Antonie Van Leeuwenhoek 107:1519–1532.  https://doi.org/10.1007/s10482-015-0445-z CrossRefGoogle Scholar
  67. Yue H, Mo W, Li C, Zheng Y, Li H (2007) The salt stress relief and growth promotion effect of Rs-5 on cotton. Plant Soil 297:139–145.  https://doi.org/10.1007/s11104-007-9327-0 CrossRefGoogle Scholar
  68. Zhang J, Klueva NY, Wang Z, Wu R, Ho T-HD, Nguyen HT (2000) Genetic engineering for abiotic stress resistance in crop plants in vitro cellular & developmental biology. Plant 36:108–114.  https://doi.org/10.1007/s11627-000-0022-6 Google Scholar
  69. Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119.  https://doi.org/10.1016/j.fcr.2005.08.018 CrossRefGoogle Scholar
  70. Zhao S, Zhou N, Zhao ZY, Zhang K, Wu GH, Tian CY (2016) Isolation of endophytic plant growth-promoting bacteria associated with the halophyte Salicornia europaea and evaluation of their promoting activity under salt stress. Curr Microbiol 73:574–581.  https://doi.org/10.1007/s00284-016-1096-7 CrossRefGoogle Scholar

Copyright information

© Università degli studi di Milano 2019

Authors and Affiliations

  • Muhammad Aaqil Khan
    • 1
  • Sajjad Asaf
    • 2
  • Abdul Latif Khan
    • 2
  • Ihsan Ullah
    • 3
  • Sajid Ali
    • 1
  • Sang-Mo Kang
    • 1
  • In-Jung Lee
    • 1
    • 4
    Email author
  1. 1.School of Applied BiosciencesKyungpook National UniversityDaeguRepublic of Korea
  2. 2.Natural and Medical Science Research CenterUniversity of NizwaNizwaOman
  3. 3.Department of Biological Sciences, Faculty of ScienceKing Abdulaziz UniversityJeddahSaudi Arabia
  4. 4.Research Institute for Dok-do and Ulleung-do IslandKyungpook National UniversityDaeguRepublic of Korea

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