Supplemental potassium mediates antioxidant metabolism, physiological processes, and osmoregulation to confer salt stress tolerance in cabbage (Brassica oleracea L.)

  • Waqas Ahmad
  • Chaudhary Muhammad Ayyub
  • Muhammad Asif ShehzadEmail author
  • Khurram Ziaf
  • Muhammad Ijaz
  • Ahmad Sher
  • Tahira Abbas
  • Jamil Shafi
Research Report


Soil salinity is one of the severe threats of climate change that inflicts heavy losses to vegetable production. Potassium (K) has been considered essential approach against abiotic stresses in food crops, however, understanding of K regulated mechanisms for inducing tolerance to NaCl stress in cabbage (Brassica oleracea L.) plants is, still elusive. Here, we report the supplemental K effects on antioxidant defense system and physiological processes that may influence the cabbage production under saline conditions. Initially, cabbage varieties (‘Stone Head’, ‘Golden Acre’, ‘9j-940’, ‘Beauty Ball’, ‘Green Ball’, ‘Green Rise’, ‘Marco F-1’) were tested under NaCl stress (50, 100, 150, and 200 mM) for their higher growth, vigor index and mineral contents. The identified cabbage var. salt-tolerant, cv. Beauty Ball (BB) and salt-sensitive cv. Green Ball (GB) were further exposed to foliar K (5 and 10 mM solutions of KNO3) under the same NaCl regimes. NaCl stress markedly inhibited photosynthetic efficiency, water status and chlorophyll pigments, thereby, resulted in reduced dry biomass of both varieties. Nevertheless, exogenous K spray at 10 mM caused positive gain in leaf water relations, chlorophyll contents in both cabbage varieties. The ameliorative impacts of K were more pronounced in salt-tolerant cv. BB as compared to salt-sensitive cv. GB in terms of higher accumulation of total soluble proteins, total free amino acids, proline contents, upregulated antioxidant activities and enhanced gas exchange characteristics. Hence, improvement in growth and K+/Na+ ratio of cabbage plants by foliar K application (10 mM) were related to up-regulation of physiological and biochemical mechanisms under saline conditions.


Antioxidants Chlorophyll Cabbage NaCl stress Potassium 



Many thanks to Higher Education Commission, Pakistan for financial support to conduct this research work under HEC-Indigenous Fellowship Program.

Authors’ contribution

WA, CMA and KZ perceived and planned the study. Statistical analysis and manuscript write up was done by MAS. MI and AS provided technical assistance for analytical work, JS accomplished treatments’ application, TA reviewed and finalized the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this paper.


  1. Abbasi GH, Akhtar J, Anwar-ul-Haq M, Ali S, Chen Z, Malik W (2014) Exogenous potassium differentially mitigates salt stress in tolerant and sensitive maize hybrids. Pak J Bot 46:135–146Google Scholar
  2. Abbasi GH, Akhtar J, Ahmad R, Jamil M, Anwar-ul-Haq M, Ali S, Ijaz M (2015) Potassium application mitigates salt stress differentially at different growth stages in tolerant and sensitive maize hybrids. Plant Growth Regul 76:111–125CrossRefGoogle Scholar
  3. Abdul-Baki AA, Anderson JD (1973) Vigor determination of soybean seed by multiple criteria. Crop Sci 13:630–633CrossRefGoogle Scholar
  4. Ali AA, Alqurainy F (2006) Activities of antioxidants in plants under environmental stress. In: Motohashi N (ed) The lutein-prevention and treatment for diseases. Trans World Research Network, Trivandrum, pp 187–256Google Scholar
  5. Arnon DI (1949) Copper enzymes in isolated chloroplast. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15PubMedPubMedCentralCrossRefGoogle Scholar
  6. Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora 199:361–376CrossRefGoogle Scholar
  7. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93PubMedCrossRefGoogle Scholar
  8. Ashraf M, McNeilly T (2004) Salinity tolerance in Brassica oilseeds. Crit Rev Plant Sci 23:157–174CrossRefGoogle Scholar
  9. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Sci 39:205–207Google Scholar
  10. Bednarz CW, Oosterhuis DM, Evans RD (1998) Leaf photosynthesis and carbon isotope discrimination of cotton in response to potassium deficiency. Environ Exp Bot 39:131–139CrossRefGoogle Scholar
  11. Bohra JS, Doerffling K (1993) Potassium nutrition of rice (Oryza sativa L.) varieties under NaCl salinity. Plant Soil 152:299–303CrossRefGoogle Scholar
  12. Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530CrossRefGoogle Scholar
  13. Cao F, Wei YS (2010) Effect of potassium nitrate on proline metabolism in tobacco (Nicotiana tabacum L.) under osmotic. Agric Boreali-Occident Sin 19:144–148 (in Chinese) Google Scholar
  14. Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiol 131:676–683PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chance M, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–817CrossRefGoogle Scholar
  16. Cramer GR, Lauchli A, Epstein E (1988) Kinetics of root elongation of maize in response to short term exposure to NaCl and elevated calcium concentration. J Exp Bot 39:1513–1522CrossRefGoogle Scholar
  17. Cuin TA, Shabala S (2007) Compatible solutes reduce ROS induced potassium efflux in Arabidopsis roots. Plant Cell Environ 30:875–885PubMedCrossRefGoogle Scholar
  18. Curtiss J, Rodriguez-Uribe L, Stewart JM, Zhang J (2011) Identification of differentially expressed genes associated with semigamy in Pima cotton (Gossypium barbadense L.) through comparative microarray analysis. BMC Plant Biol 11:2–9CrossRefGoogle Scholar
  19. da Silva EN, Ribeiro RV, Ferreira-Silva SL, Viégas RA, Silveira JAG (2011) Salt stress induced damages on the photosynthesis of physic nut young plants. Sci Agric 68:62–68CrossRefGoogle Scholar
  20. Egilla JN, Davies FT, Boutton TW (2005) Drought stress influences leaf water content, photosynthesis, and water-use efficiency of Hibiscus rosa-sinensis at three potassium concentrations. Photosynthetica 43:135–140CrossRefGoogle Scholar
  21. El-Bassiouny HMS, Bekheta MA (2005) Effect of salt stress on relative water content, lipid peroxidation, polyamines, amino acids and ethylene of two wheat cultivars. Int J Agric Biol 7:363–368Google Scholar
  22. Evans HJ, Wildes RA (1971) Potassium and its role in enzyme activation. In: Potassium in biochemistry and physiology. Proceedings of the 8th colloquium of the International Potash InstituteGoogle Scholar
  23. Evelin H, Devi TS, Gupta S, Kapoor R (2019) Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci 10:470PubMedPubMedCentralCrossRefGoogle Scholar
  24. Farooq M, Hussain M, Wakeel A, Siddique KHM (2015) Salt stress in maize: effects, resistance mechanisms, and management. A review. Agron Sustain Dev 35:461–481CrossRefGoogle Scholar
  25. Fayez KA, Bazaid SA (2014) Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. J Saudi Soc Agric Sci 13:45–55Google Scholar
  26. Fougere F, Le Rudulier D, Streeter JG (1991) Effect of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids and cytosol of alfalfa (Medicago sativa). Plant Physiol 96:1228–1236PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gao HJ, Yang HY, Bai JP, Liang XY, Lou Y, Zhang JL, Wang D, Zhang JL, Niu SQ, Chen Y (2015) Ultrastructural and physiological responses of potato (Solanum tuberosum) plantlets to gradient saline stress. Front Plant Sci 5:1–14CrossRefGoogle Scholar
  28. Ghosh S, Bagchi S, Majumder AL (2001) Chloroplast fructose-1,6-bisphosphatase from Oryza differs in salt tolerance property from the Porteresia enzyme and is protected by osmolytes. Plant Sci 160:1171–1181PubMedCrossRefPubMedCentralGoogle Scholar
  29. Hamilton PB, Van Slyke DD (1973) Amino acids determination with ninhydrin. J Biol Chem 150:231–233Google Scholar
  30. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefPubMedCentralGoogle Scholar
  31. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments. Plant Signal Behav 7:1456–1466PubMedPubMedCentralCrossRefGoogle Scholar
  32. Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice 5:1–18CrossRefGoogle Scholar
  33. Jabeen N, Ahmad R (2011) Foliar application of potassium nitrate affects the growth and nitrate reductase activity in sunflower and safflower leaves under salinity. Not Bot Hortic Agrobot 39:172–178CrossRefGoogle Scholar
  34. Jbir-Koubaa R, Charfeddine S, Ellouz W, Saidi MN, Drira N, Gargouri-Bouzid R, Nouri-Ellouz O (2014) Investigation of the response to salinity and to oxidative stress of interspecific potato somatic hybrids grown in a greenhouse. Plant Cell Tiss Org Cult 120:933–947CrossRefGoogle Scholar
  35. Jia Y, Yang X, Islam E, Feng Y (2008) Effects of potassium deficiency on chloroplast ultrastructure and chlorophyll fluorescence in inefficient and efficient genotypes of rice. J Plant Nutr 31:2105–2118CrossRefGoogle Scholar
  36. Kaya C, Kirnak H, Higgs H (2001a) Enhancement of growth and normal growth parameters by foliar application of potassium and phosphorus on tomato cultivars grown at high (NaCl) salinity. J Plant Nutr 24:357–367CrossRefGoogle Scholar
  37. Kaya C, Kirnak H, Higgs H (2001b) Effects of supplementary potassium and phosphorus on physiological development and mineral nutrition of cucumber and pepper cultivars grown at high salinity (NaCl). J Plant Nutr 24:1457–1471CrossRefGoogle Scholar
  38. Khaje-Hosseini M, Powell AA, Bingham IJ (2003) The interaction between salinity stress and seed vigour during germination of soyabean seeds. Seed Sci Technol 31:715–725CrossRefGoogle Scholar
  39. Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advances in polyamine research in 2007. J Plant Res 120:345–350PubMedCrossRefPubMedCentralGoogle Scholar
  40. Lavee S, Hoffman M (1971) The effect of potassium ions on peroxidase activity and its isozyme composition as related to apple callus growth in vitro. Bot Gaz 132:232–237CrossRefGoogle Scholar
  41. Lovelock CE, Ball MC (2002) Influence of salinity on photosynthesis of halophytes. In: Läuchli A, Lüttge U (eds) Salinity: environment-plants-molecules. Kluwer, Dordrecht, pp 315–339Google Scholar
  42. Manaa A, Ben Ahmed H, Valot B, Bouchet JP, Aschi-Smiti S, Causse M, Faurobert M (2011) Salt and genotype impact on plant physiology and root proteome variations in tomato. J Exp Bot 62:2797–2813PubMedCrossRefGoogle Scholar
  43. Mandhania S, Madan S, Sawhney V (2006) Antioxidant defense mechanism under salt stress in wheat seedlings. Biol Plant 50:227–231CrossRefGoogle Scholar
  44. Mansour MMF (1998) Protection of plasma membrane of onion epidermal cells by glycinebetaine and proline against NaCl stress. Plant Physiol Biochem 36:767–772CrossRefGoogle Scholar
  45. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, San DiegoGoogle Scholar
  46. Mengel K, Kirkby EA (2001) Principles of plant nutrition, 5th edn. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  47. Mengel K, Kirkby EA (2012) Principles of plant nutrition. Springer, BerlinGoogle Scholar
  48. Misra AN, Sahu SM, Misra M, Singh P, Meera I, Das N, Kar M, Shau P (1997) Sodium chloride induced changes in leaf growth, and pigment and protein contents in two rice cultivars. Biol Plant 39:257–262CrossRefGoogle Scholar
  49. Moghaieb REA, Saneoka H, Fujita K (2004) Effect of salinity on osmotic adjustment, glycinebetaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritime. Plant Sci 166:1345–1349CrossRefGoogle Scholar
  50. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefPubMedCentralGoogle Scholar
  51. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  52. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefPubMedCentralGoogle Scholar
  53. Pitann B, Kranz T, Mühling KH (2009) The apoplastic pH and its significance in adaptation to salinity in corn (Zea mays L.): comparison of fluorescence microscopy and pH-sensitive microelectrodes. Plant Sci 176:497–504PubMedCrossRefPubMedCentralGoogle Scholar
  54. Qu C, Liu C, Gong X, Li C, Hong M, Wang L, Hong F (2012) Impairment of maize seedling photosynthesis caused by a combination of potassium deficiency and salt stress. Environ Exp Bot 75:134–141CrossRefGoogle Scholar
  55. Quintero JM, Fournier JM, Benlloch M (2007) Na+ accumulation in shoot is related to water transport in K+ starved sunflower plants but not in plants with a normal K+ status. J Plant Physiol 164:60–67PubMedCrossRefPubMedCentralGoogle Scholar
  56. Ramoliya P, Pandey A (2002) Effect of increasing salt concentration on emergence, growth and survival of seedlings of Salvadora oleoides (Salvadoraceae). J Arid Environ 51:121–132CrossRefGoogle Scholar
  57. Ranganayakulu GS, Veeranagamallaiah G, Sudhakar C (2013) Effect of salt stress on osmolyte accumulation in two groundnut cultivars (Arachis hypogaea L.) with contrasting salt tolerance. Afr J Plant Sci 7:586–592CrossRefGoogle Scholar
  58. Riazi A, Matruda K, Arslam A (1985) Water stress induce changes in concentration of proline and other solutes in growing regions. J Exp Bot 36:1716–1725CrossRefGoogle Scholar
  59. Ruan J, Wu X, Ye Y, Hardter R (1998) Effect of potassium, magnesium and sulphur applied in diþerent forms of fertilisers on free amino acid content in leaves of tea (Camellia sinensis L.). J Sci Food Agric 76:389–396CrossRefGoogle Scholar
  60. Sacala E (2017) The influence of increasing doses of silicon on maize seedlings grown under salt stress. J Plant Nutr 40:819–827CrossRefGoogle Scholar
  61. Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biol Plant 49:85–91CrossRefGoogle Scholar
  62. Sangakkara U, Frehner M, Nösberger J (2001) Influence of soil moisture and fertilizer potassium on the vegetative growth of mungbean (Vigna radiata L. Wilczek) and cowpea (Vigna unguiculata L. Walp). J Agron Crop Sci 186:73–81CrossRefGoogle Scholar
  63. Shahid MA, Pervez MA, Balal RM, Ahmad R, Ayyub CM, Abbas T, Akhtar N (2011) Salt stress effects on some morphological and physiological characteristics of okra (Abelmoschus esculentus L.). Soil Environ 30:66–73Google Scholar
  64. Shirazi MU, Asif SM, Khanzada B, Khan MA, Ali M, Mumtaz S, Yousufzai MN, Saif MS (2001) Growth and ion accumulation in some wheat genotypes under NaCl stress. Pak J Biol Sci 4:388–391CrossRefGoogle Scholar
  65. Simon-Sarkadi L, Kocsy G, Sebestyén Z (2002) Effect of salt stress on free amino acid and polyamine content in cereals. Acta Biol Szeged 46:73–75Google Scholar
  66. Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Biotechnol 14:407–426CrossRefGoogle Scholar
  67. Sivakumar P, Sharmila P, Pardha Saradhi P (2000) Proline alleviates salt-stress induced enhancement in ribulose-1,5-biphosphate oxygenase activity. Biochem Biophys Res Commun 279:512–515PubMedPubMedCentralCrossRefGoogle Scholar
  68. Smirnoff N (2005) Antioxidants and reactive oxygen species in plants. Blackwell Publishing Book, Oxford, p 2005CrossRefGoogle Scholar
  69. Soleimanzadeh HD, Habibi MR, Ardakani F, Paknejad RF (2010) Effect of potassium levels on antioxidant enzymes and malondialdehyde content under drought stress in sunflower (Helianthus annuus L.). Am J Agric Biol Sci 5:56–61CrossRefGoogle Scholar
  70. Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481–486CrossRefGoogle Scholar
  71. Sümer A, Zörb C, Yan F, Schubert S (2004) Evidence of sodium toxicity for the vegetative growth of maize (Zea mays L.) during the first phase of salt stress. J Appl Bot 78:135–139Google Scholar
  72. Szalai G, Janda T (2009) Effect of salt stress on the salicylic acid synthesis in young maize (Zea mays L.) plants. J Agron Crop Sci 195:165–171CrossRefGoogle Scholar
  73. Wasti S, Manaa A, Mimouni H, Nsairi A, Ibtissem M, Gharbi E, Gautier H, Ahmed HB (2017) Exogenous application of calcium silicate improves salt tolerance in two contrasting tomato (Solanum lycopersicum) cultivars. J Plant Nutr 40:673–684CrossRefGoogle Scholar
  74. Willadino L, Camara T, Boget N, Claparols I, Santos M, Torne JM (1996) Polyamine and free amino acid variations in NaCl-treated embryogenic maize callus from sensitive and resistant cultivars. J Plant Physiol 149:179–185CrossRefGoogle Scholar
  75. Wolf B (1982) A comprehensive system of leaf analysis and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13:1035–1059CrossRefGoogle Scholar
  76. Yang JY, Zheng W, Tian Y et al (2011) Effects of various mixed salt-alkaline stresses on growth, photosynthesis, and photosynthetic pigment concentrations of Medicago ruthenica seedlings. Photosynthetica 49:275–284CrossRefGoogle Scholar
  77. Yang Y, Zheng Q, Liu M, Long X, Liu Z, Shen Q, Guo S (2012) Difference in sodium spatial distribution in the shoot of two canola cultivars under saline stress. Plant Cell Physiol 53:1083–1092PubMedCrossRefGoogle Scholar
  78. Yu Y, Assmann SM (2016) The effect of NaCl on stomatal opening in Arabidopsis wild type and agb1 heterotrimeric G-protein mutant plants. Plant Signal Behav 11:1–3Google Scholar
  79. Zhang J, Kirkham MB (1994) Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791CrossRefGoogle Scholar
  80. Zhao X, Tan HJ, Liu YB, Li XR, Chen GX (2009) Effect of salt stress on growth and osmotic regulation in Thellungiella and Arabidopsis callus. Plant Cell Tiss Organ Cult 98:97–103CrossRefGoogle Scholar
  81. Zhu JK (2001) Plant salt tolerance: regulatory pathway, genetic improvement and model systems. Trends Plant Sci 6:66–71PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Korean Society for Horticultural Science 2019

Authors and Affiliations

  • Waqas Ahmad
    • 1
  • Chaudhary Muhammad Ayyub
    • 2
  • Muhammad Asif Shehzad
    • 3
    Email author
  • Khurram Ziaf
    • 2
  • Muhammad Ijaz
    • 1
  • Ahmad Sher
    • 1
  • Tahira Abbas
    • 1
  • Jamil Shafi
    • 4
  1. 1.College of AgricultureBZU, Bahadur Sub-CampusLayyahPakistan
  2. 2.Institute of Horticultural SciencesUniversity of AgricultureFaisalabadPakistan
  3. 3.Department of AgronomyMNS-University of AgricultureMultanPakistan
  4. 4.Department of Pesticide Science, Plant Protection CollegeShenyang Agricultural UniversityShenyangChina

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