Effects of plant growth promoting rhizobacteria on salinity tolerance of ornamental ‎cabbage (Brassica oleraceae L. cv. Kamome)‎

Document Type : Full Paper


1 Associate Professor, Faculty of Agriculture, University of Zanjan, Zanjan, Iran, ‎Postal Code: 45371-38791.‎

2 Ph. D. Student,, Faculty of Agriculture, University of Zanjan, Zanjan, Iran, Postal Code: 45371-‎‎38791.‎

3 M. Sc., Faculty of Agriculture, University of Zanjan, Zanjan, Iran, Postal Code: 45371-38791‎

4 Assistant Professor, Faculty of Agriculture, University of Zanjan, Zanjan, Iran, Postal Code: 45371-38791.‎


In order to study the morphologies and biochemistry of ornamental cabbage under salt stress, a factorial experiment was carried out based on completely randomized design in three replications. The treatments included salinity at three levels (4 and 8 dS.m-1 and control (no salinity) and growth stimulating bacteria at three levels (no inoculation Pseudomonas putida and Bacillus subtilis). Plant growth characteristics, including plant height, number of leaves, fresh and dry weight of leaves, fresh and dry weight of plant and root, showed a significant decrease compared to the control treatment with increasing salinity stress, and inoculation with growth-promoting bacteria, especially Pseudomonas putida, improved these attributes. Antioxidant activity and total phenol increased with increasing salinity, so that the highest amount of phenol and antioxidant was observed at treatment 8 dS/m (1.08 mg/g FW and 62.52 μmol/g FW, respectively). On the other hand, the use of Bacillus bacteria could increase the amount of total phenol and antioxidants in contrast with salinity (1.08 mg/g FW and 62.78 μmol/g FW). The amount of proline in leaves also had an increasing trend at different levels of salinity stress, and its highest level was observed at the highest level of salinity stress and the application of Bacillus subtilis bacteria. The interaction between bacteria and salinity stress reduced the accumulation of sodium element and increased the amount of potassium element. The results of this experiment showed that growth-promoting bacteria, especially Pseudomonas putida bacteria, reduce the damage caused by salt stress in ornamental cabbage plants.


  1. Abeer, H., Abdallah, E.F., Alqarawi, A.A., Al-Huqail, A.A., Alshalawi, S.R.M., Wirth, S. & Dilfuza, E. (2015). Impact of plant growth promoting Bacillus subtilis on growth and physiological parameters of Bassia indica (Indian Bassia) grown under salt stress. Pakistan Journal of Botany, 47(5), 1735-1741. ‏
  2. Ahmad, P., Abdel Lateef, A.A., Hashem, A., Abd-Allah, E.F., Gucel, S. & Tran, L.S. P. (2016). Nitric oxide mitigates salt stress by regulating levels of osmoles and antioxidant enzymes in chickpea. Frontiers in Plant Science, 7:347-351.
  3. Akladious, S.A. & Mohamed, H.I. (2018). Ameliorative effects of calcium nitrate and humic acid on the growth, yield component and biochemical attribute of pepper (Capsicum annuum) plants grown under salt stress. Scientia Horticulturae, 236, 244-250.
  4. Alqarawi, A.A., Abd Allah, E.F. & Hashem, A. (2014). Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. Journal of Plant Interactions, 9(1), 802-810.
  5. Álvarez, S. & Sánchez‐Blanco, M. J. (2014). Long‐term effect of salinity on plant quality, water relations, photosynthetic parameters and ion distribution in Callistemon citrinus. Plant Biology, 16(4), 757-764. ‏
  6. Arnon, D.I. 1949. Copper enzymes in isolated chloroplasts. Polyphenol oxidases in Beta vulgaris. Plant Physiology, 24: 1-15.
  7. Ashraf, M., & McNeilly, T. (2004). Salinity tolerance in Brassica oilseeds. Critical Reviews in Plant Sciences, 23(2), 157-174. ‏
  8. Azarmi Atajan, F. & Sayyari-Zohan, M. H. (2020). Alleviation of salt stress in lettuce (Lactuca sativa) by plant growth-promoting rhizobacteria. Journal of Horticulture and Postharvest Research, 3, 67-78. ‏
  9. Bargaz, A., Zaman-Allah, M., Farissi, M., Lazali, M., Drevon, J. J., Maougal, R. T. & Georg, C. (2015). Physiological and molecular aspects of tolerance to environmental constraints in grain and forage legumes. International Journal of Molecular Sciences, 16(8), 18976-19008.
  10. Bates, L.S., Waldren, R.P. & Teare, I.D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205-207. ‏
  11. Bedreag, C.F.G., Trifan, A., Bucur, L.A., Arcus, M., Tebrencu, C., Miron, A. & Costache, I.I. (2014). Chemical and antioxidant studies on Crataegus pentagyna leaves and flowers. Romanian Biotechnological Letters, 19(6), 98-59. ‏
  12. Ben Hamed, K.B., Castagna, A., Salem, E., Ranieri, A. & Abdelly, C. (2007). Sea fennel (Crithmum maritimum) under salinity conditions: a comparison of leaf and root antioxidant responses. Plant Growth Regulation, 53(3), 185-194. ‏
  13. Bernstein, N. (2019). Plants and salt: Plant response and adaptations to salinity. In Model Ecosystems in Extreme Environments. (pp. 101-112.) Academic Press.
  14. Chapman, H.D. & Pratt, F.P. (1982). Determination of minerals by titration method. Methods of Analysis for Soils, Plants and Water. Ph.D. Thiesis. Oakland, CA: Agriculture Division, California University.
  15. Chen, Z., Newman, I., Zhou, M., Mendham, N., Zhang, G. & Shabala, S. (2005). Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant, Cell and Environment, 28(10), 1230-1246. ‏
  16. Danish, S.U.B.H.A.N., Zafar-ul-Hye, M.U.H.A.M.M.A.D., Hussain, S., Riaz, M.U.H.A.M.M.A.D. & Qayyum, M.F. (2020). Mitigation of drought stress in maize through inoculation with drought tolerant ACC deaminase containing PGPR under axenic conditions. Pakistan Journal of Botany, 52(1), 49-60. ‏
  17. Dodd, I. C. & Perez-Alfocea, F. (2012). Microbial amelioration of crop salinity stress. Journal Experimental Botany, 63: 3415-3428.
  18. Duraiswamy, H., Nallaiyan, S., Nelson, J., Samy, P. R., Johnson, M. & Varaprasadam, I. (2010). The effect of extracts of Selaginella involvens and Selaginella inaequalifolia leaves on poultry pathogens. Asian Pacific Journal of Tropical Medicine, 3(9), 678-681. ‏
  19. Eckardt, N.A. (2009). A new chlorophyll degradation pathway. The Plant Cell, 21(3),700-701.
  20. Nor Elahi, N., Shafique, M., Imtiaz, M., Farooq, U. & Rashid, M. (2020). Amelioration of Salt Stress in Cicer arietinum by Plant Growth Promoting Rhizobacteria. Sarhad Journal of Agriculture, 36(1), 249-257. ‏
  21. El-Sayed, S.Y. & Hagab, R.H. (2020). Effect of organic acids and plant growth promoting rhizobacteria (PGPR) on biochemical content and productivity of wheat under saline soil conditions. The Middle East Journal, 9(2), 227-242.
  22. Esan, A.M., Olaiya, C.O., Anifowose, L.O., Lana, I.O., Ailenokhuoria, B.V., Fagbami, O. & Adeyemi, H.R.Y. (2020). Effect of plant growth-promoting rhizobacteria and gibberellic acid on salt stress tolerance in tomato genotypes. African Crop Science Journal, 28(3), 341-362. ‏
  23. Forouzi, A., Ghasemnezhad, A. & Nasrabad, R. G. (2020). Phytochemical response of Stevia plant to growth promoting microorganisms under salinity stress. South African Journal of Botany, 134, 109-118. ‏
  24. Ghasemi Ghahsareh, M.& Membini, M. (2015). Evaluation of tolerance of ornamental cabbage of Queen cultivar to trifluralin toxin, 9th Congress of Horticultural Sciences. 27-31 July. Minneapolis, Minnesota USA. 326-332. (In Farsi).
  25. Guinn, E.J., Pegram, L.M., Capp, M.W., Pollock, M.N. & Record, M.T. (2011). Quantifying why urea is a protein denaturant, whereas glycine betaine is a protein stabilizer. Proceedings of the National Academy of Sciences, 108(41), 16932-16937.
  26. Han, H.S. & Lee, K.D. (2005). Plant Growth Promoting Rhizobacteria Effect on Antioxidant Status, Photosynthesis, Mineral Uptake and Growth of Lettuce under Soil Salinity. Research Journal of Agriculture and Biological Sciences, 1(3), 210-215. ‏
  27. Hahm, M.S., Son, J.S., Hwang, Y.J., Kwon, D.K., and Ghim, S.Y. 2017. Alleviation of salt stress in pepper (Capsicum annum) plants by plant growth-promoting rhizobacteria. Journal of Microbiology and Biotechnology, 27(10), 1790-1797.
  28. Hariprasad, P. & Niranjana, S.R. (2009). Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato. Plant and Soil, 316(1-2), 13-24. ‏
  29. Israr, D., Mustafa, G., Khan, K.S., Shahzad, M., Ahmad, N. & Masood, S. )2016(. Interactive effects of phosphorus and Pseudomonas putida on chickpea (Cicer arietinum) growth, nutrient uptake, antioxidant enzymes and organic acids exudation. Plant Physiology and Biochemistry, 108, 304-312. ‏
  30. Kaya, C., Ashraf, M., Sonmez, O., Polat, T. & Tuna, A. L. (2019). The Combined Effects of Nitric Oxide and Thiourea on Plant Growth and Mineral Nutrition of Salt-Stressed Plants of Two Maize Cultivars with Differential Salt Tolerance. ‏Journal of Plant Nutrition, 42 (1), 231-239.
  31. Kibria, M.G., Hossain, M., Murata, Y. & Hoque, M.A. (2017). Antioxidant defense mechanisms of salinity tolerance in rice genotypes. Rice Science, 24(3), 155-162.
  32. Kumar, M., Yadav, V., Tuteja, N. & Johri, A.K. (2009). Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology, 155(3), 780-790
  33. Liu, F., Xing, S., Ma, H., Du, Z. & Ma, B. (2013). Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in platycladus orientalis container seedlings. Applied Microbiology and Biotechnology, 97(20), 9155-9164.
  34. Mahmoud, O. M. B., Hidri, R., Talbi-Zribi, O., Taamalli, W., Abdelly, C. & Djébali, N. (2020). Auxin and proline producing rhizobacteria mitigate salt-induced growth inhibition of barley plants by enhancing water and nutrient status. South African Journal of Botany, 128, 209-217. ‏
  35. Meda, A., Lamien, C. E., Romito, M., Millogo, J. & Nacoulma, O. G. (2005). Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity. Food Chemistry, 91(3), 571-577. ‏
  36. Moncada, A., Vetrano, F. & Miceli, A. (2020). Alleviation of salt stress by plant growth-promoting bacteria in hydroponic leaf lettuce. Agronomy, 10(10), 15-23. ‏
  37. Munns, R. (2002). Comparative physiology of salt and water stress. Plant, Cell & Environment, 25(2), 239-250. ‏
  38. Nadeem, S.M., Zahir, Z.A., Naveed, M., Arshad, M. & Shahzad, S.M. (2006). Variation in growth and ion uptake of maize due to inoculation with plant growth promoting rhizobacteria under salt stress. Soil & Environment, 25(2), 78-84. ‏
  39. Nadeem, S.M., Zahir, Z.A., Naveed, M. & Arshad, M. (2007). Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Canadian Journal of Microbiology, 53(10), 1141-1149.
  40. Nadeem, S.M., Imran, M., Naveed, M., Khan, M.Y., Ahmad, M., Zahir, Z. A., & Crowley, E. (2017). Synergistic use of biochar, compost and plant growth‐promoting rhizobacteria for enhancing cucumber growth under water deficit conditions. Journal of the Science of Food and Agriculture, 97(15), 5139-5145.
  41. Németh, M., Janda, T., Horváth, E., Páldi, E. & Szalai, G. (2002). Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Science, 162(4), 569-574. ‏
  42. Neocleous, D. & Vasilakakis, M. (2007). Effects of NaCl stress on red raspberry (Rubus idaeus ‘Autumn Bliss’). Scientia Horticulturae, 112(3), 282-289. ‏
  43. Niu, S.W., Wang, N., Irfan, M., Xu, J.Y., Zhang, Y.J. & Cai, G.X. (2019). Effect of Fermentation Broth of Endophytic Fungi on Physiological and Biochemical Characteristics of Tomato Seedling Under Calcium Nitrate Stress. Iranian Journal of Science and Technology, Transactions A: Science, 43(4), 1427-1432. ‏
  44. Ozen, T., Demirtas, I. & Aksit, H. (2011). Determination of antioxidant activities of various extracts and essential oil compositions of Thymus praecox subsp. skorpilii var. skorpilii. Food Chemistry, 124(1), 58-64.
  45. Parihar, P., Singh, S., Singh, R., Singh, V.P. & Prasad, S.M. (2015). Effect of salinity stress on plants and its tolerance strategies: a review. Environmental Science and Pollution Research, 22(6), 4056-4075.
  46. Patel, P. J., Trivedi, G. R., Shah, R. K. & Saraf, M. (2018). Selenorhizobacteria: As biofortification tool in sustainable agriculture. Biocatalysis and Agricultural Biotechnology, 14, 198-203.
  47. Radi, A. A., Farghaly, F. A. & Hamada, A. M. (2013). Physiological and biochemical responses of salt-tolerant and salt-sensitive wheat and bean cultivars to salinity. Journal of Biology and Earth Sciences, 3(1), 72-88.
  48. Rostami Kia, Y. Little Tabari, M. Asgharzadeh, A. & Rahmani, A. (2017). The effect of growth-promoting bacteria on vegetative traits and nutrients of hazelnut seedlings (Coryllus avellana) in Ardabil hazelnut nurseries. Iranian Journal of Forest and Poplar Research, 25(1), 116-126. (In Farsi).
  49. Saleem, M., Arshad, M., Hussain, S. & Bhatti, A.S. (2007). Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. Journal of Industrial Microbiology & Biotechnology, 34(10), 635-648. ‏
  50. Salehi, F., Aelaei, M., Mortazavi, S.N., Salami.S.A. & Rezadoost Chahardeh, H. (2022). Study of morphophysiological attributes of two saffron ecotypes treated with Bacillus subtilis under Zanjan climatic conditions. Iranian Journal of Horticultural Science, 53(1), 15-30. (in Farsi).
  51. Seyed Sharifi, R., Moradi, L., Khomari, S. & Salim, f. (2018). The effect of seed inoculation with growth-promoting bacteria on germination components, sodium and potassium content of rye seedlings in soil salinity conditions, Congress for the Development of Regional Scientific Cooperation of Food Industry and Agriculture, 24 August. Mashhad Institute of Food Sciences and Industries, pp. 325-329. (In Farsi).
  52. Sheikhalipour, M., Bolandndnazar, S.A., Sarikhani, M.A., Panahandeh, J. (2019). Effect of application of biofertilizers on yield, quality and antioxidant capacity oftomato fruit. Iranian Journal of Horticultural Science, 50(3), 621-632. (in Farsi).
  53. Taghizadeh, M. & Solgi, M. (2014). Introduction of commercial protocol for in vitro propagation of ornamental cabbage (Brassica oleraceae ). Horticultural Sciences, 45(4), 484-475. (In Farsi).
  54. Tang, X., Mu, X., Shao, H., Wang, H. & Brestic, M. (2015). Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Critical Reviews in Biotechnology, 35(4), 425-437. ‏
  55. Tavallali, V., Rahemi, M., Maftoun, M., Panahi, B., Karimi, S., Ramezanian, A. & Vaezpour, M. (2009). Zinc influence and salt stress on photosynthesis, water relations, and carbonic anhydrase activity in pistachio. Scientia Horticulturae, 123(2), 272-279. ‏
  56. Trabelsi, L., Gargouri, K., Hassena, A. B., Mbadra, C., Ghrab, M., Ncube, B. & Gargouri, R. (2019). Impact of drought and salinity on olive water status and physiological performance in an arid climate. Agricultural Water Management, 213, 749-759.
  57. Tuna, A. L., Kaya, C., Ashraf, M., Altunlu, H., Yokas, I. & Yagmur, B. (2007). The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. Environmental and Experimental Botany, 59(2), 173-178. ‏
  58. Verslues, P. E., Agarwal, M., Katiyar‐Agarwal, S., Zhu, J. & Zhu, J. K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal, 45(4), 523-539.
  59. Weisany, W., Sohrabi, Y., Heidari, G., Siosemardeh, A. & Badakhshan, H. (2014). Effects of zinc application on growth, absorption and distribution of mineral nutrients under salinity stress in soybean (Glycine max). Journal of Plant Nutrition, 37(14), 2255-2269. ‏
  60. Xiang-dong, X., Yan, S., Bo, S., Jian, Z. & Xiao-qin, G. (2010). Effects of exogenous melatonin on active oxygen metabolism of cucumber seedlings under high temperature stress. Yingyong Shengtai Xuebao, 21(5), 125-126. ‏
  61. Xiaohui, F. A. N., Zhang, S., Xiaodan, M. O., Yuncong, L. I., Yuqing, F. U. & Zhiguang, L. I. U. )2017(. Effects of plant growth-promoting rhizobacteria and N source on plant growth and N and P uptake by tomato grown on calcareous soils. Pedosphere, 27(6), 1027-1036.
  62. Yadav, S. P., Bharadwaj, R., Nayak, H., Mahto, R., Singh, R. K. & Prasad, S. K. )2019(. Impact of salt stress on growth, productivity and physicochemical properties of plants A Review. International Journal of Communication Systems, 7(2), 1793-1798.
  63. Zafar-Ul-Hye, M., Mahmood, F., Danish, S., Hussain, S., Gul, M., Yaseen, R., & Shaaban, M. 2020. Evaluating efficacy of plant growth promoting rhizobacteria and potassium fertilizer on spinach growth under salt stress. Pakistan Journal of Botany, 52(4), 1441-1447.