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Acta Physiologiae Plantarum

, Volume 33, Issue 4, pp 1113–1122 | Cite as

Salt-induced modulation in growth, photosynthetic capacity, proline content and ion accumulation in sunflower (Helianthus annuus L.)

  • Muhammad Shahbaz
  • Muhammad AshrafEmail author
  • Nudrat Aisha AkramEmail author
  • Asma Hanif
  • Shumaila Hameed
  • Sundus Joham
  • Rehana Rehman
Original Paper

Abstract

Salt-induced changes in growth, photosynthetic pigments, various gas exchange characteristics, relative membrane permeability (RMP), relative water content (RWC) and ion accumulation were examined in a greenhouse experiment on eight sunflower (Helianthus annuus L.) cultivars. Sunflower cultivars, namely Hysun-33, Hysun-38, M-3260, S-278, Alstar-Rm, Nstt-160, Mehran-II and Brocar were subjected to non-stress (0 mM NaCl) or salt stress (150 mM NaCl) in sand culture. On the basis of percent reduction in shoot biomass, cvs. Hysun-38 and Nstt-160 were found to be salt tolerant, cvs. Hysun-33, M-3260, S-278 and Mehran-II moderately tolerant and Alstar-Rm and Brocar salt sensitive. Salt stress markedly reduced growth, different gas exchange characteristics such as photosynthetic rate (A), water-use efficiency (WUE) calculated as A/E, transpiration rate (E), internal CO2 concentration (C i) and stomatal conductance (g s) in all cultivars. The effect of 150 mM NaCl stress was non-significant on chlorophyll a and b contents, chlorophyll a/b ratio, RWC, RMP and leaf and root Cl, K+ and P contents; however, salt stress markedly enhanced C i /C a ratio, free proline content and leaf and root Na+ concentrations in all sunflower cultivars. Of all cultivars, cv. Hysun-38 was higher in gas exchange characteristics, RWC and proline contents as compared with the other cultivars. Overall, none of the earlier-mentioned physiological attributes except leaf K+/Na+ ratio was found to be effective in discriminating the eight sunflower cultivars as the response of each cultivar to salt stress appraised using various physiological attributes was cultivar-specific.

Keywords

Sunflower Salt stress Photosynthesis Relative membrane permeability Relative water content Inorganic nutrients 

Notes

Acknowledgments

The corresponding author gratefully acknowledges the funding from the Higher Education Commission (HEC) through Grant No. 20-403. The results presented in this paper are a part of MSc studies of Asma Hanif, Shumaila Hameed, Sundus Joham and Rehana Rehman.

References

  1. Abbas W, Ashraf M, Akram NA (2010) Alleviation of salt-induced adverse effects in eggplant (Solanum melongena L.) by glycinebetaine and sugarbeet extracts. Sci Hort 125:188–195CrossRefGoogle Scholar
  2. Akram MS, Ashraf M, Akram NA (2009) Effectiveness of potassium sulfate in mitigating salt-induced adverse effects on different physio biochemical attributes in sunflower (Helianthus annuus L.). Flora 204:471–483Google Scholar
  3. Ali Q, Athar HR, Ashraf M (2008) Modulation of growth, photosynthetic capacity and water relations in salt stressed wheat plants by exogenously applied 24-epibrassinolide. Plant Growth Regul 56:107–116CrossRefGoogle Scholar
  4. Allen SK, Dobrenz AK, Schonhorst MH, Stoner JE (1986) Heritability of NaCl tolerance in germinating alfalfa seeds. Agron J 77:90–96Google Scholar
  5. Alvarez I, Tomaro ML, Benavides MP (2003) Changes in polyamines, proline and ethylene in sunflower calluses treated with NaCl. Plant Cell Tissue Organ Culture 74:51–59CrossRefGoogle Scholar
  6. Arfan M, Athar HR, Ashraf M (2007) Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? J Plant Physiol 164:685–694PubMedCrossRefGoogle Scholar
  7. Arnon DT (1949) Copper enzyme in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15PubMedCrossRefGoogle Scholar
  8. Ashraf M (2002) Salt tolerance of cotton: some new advances. Crit Rev Plant Sci 21:1–30CrossRefGoogle Scholar
  9. Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora 199:361–376Google Scholar
  10. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93PubMedCrossRefGoogle Scholar
  11. Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  12. Ashraf M, Athar HR, Harris PJC, Kwon TR (2008) Some prospective strategies for improving crop salt tolerance. Adv Agron 97:45–110CrossRefGoogle Scholar
  13. Ashraf M, Akram NA, Arteca RN, Foolad MR (2010) The physiological, biochemical and molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance. Crit Rev Plant Sci 29:162–190CrossRefGoogle Scholar
  14. Aslam M, Qureshi RH, Ahmad NA (1993) Rapid screening technique for salt tolerance in rice (Oryza sativa L.). Plant Soil 150:99–107CrossRefGoogle Scholar
  15. Athar H, Ashraf M (2005) Photosynthesis under drought stress. In: Pessarakli M (ed) Photosynthesis. CRC Press, New York, pp 795–810Google Scholar
  16. Athar HR, Khan A, Ashraf M (2009) Inducing salt tolerance in wheat by exogenously applied ascorbic acid through different modes. J Plant Nutr 32(11):1799–1817CrossRefGoogle Scholar
  17. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Sci 39:205–207Google Scholar
  18. Bayuelo-Jiménez JS, Craig R, Lynch JP (2002) Salinity tolerance of Phaseolus species during germination and early seedling growth. Crop Sci 42:1584–1594CrossRefGoogle Scholar
  19. Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stress. Plant Cell 7:1109–1111CrossRefGoogle Scholar
  20. Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single cell measurement of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiol 131:676–683PubMedCrossRefGoogle Scholar
  21. Dash M, Panda SK (2001) Salt stress induced changes in growth and enzyme activities in germinating Phaseolus mungo seeds. Biol Plant 44:587–589CrossRefGoogle Scholar
  22. Davenport RJ, Reid RJ, Smith FA (1997) Sodium–calcium interactions in two wheat species differing in salinity tolerance. Physiol Plant 99:323–327CrossRefGoogle Scholar
  23. Desingh R, Kanagaraj G (2007) Influence of salinity stress on photosynthesis and antioxidative systems in two cotton varieties. Genet Appl Plant Physiol 33:221–234Google Scholar
  24. Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635PubMedCrossRefGoogle Scholar
  25. Dubey RS (2005) Photosynthesis in plants under stress full conditions. In: Pessarakli M (ed) Photosynthesis. CRC Press, New York, pp 717–718Google Scholar
  26. Farooq S, Azam F (2006) The use of cell membrane stability (CMS) technique to screen for salt tolerant wheat varieties. J Plant Physiol 163:629–637PubMedCrossRefGoogle Scholar
  27. Garcia AB, de Almeida Engler J, Iyer S, Gerats T, Van Monatgu M, Caplan AB (1997) Effects of osmoprotectants upon NaCl in rice. Plant Physiol 115:159–169PubMedGoogle Scholar
  28. Ghoulam C, Foursy A, Fares K (2002) Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ Exp Bot 47:39–50CrossRefGoogle Scholar
  29. Golan-Goldhirsh A, Hankamer B, Lips SH (1990) Hydroxyproline and proline content of cell walls of sunflower, peanut and cotton grown under salt stress. Plant Sci 69:27–32CrossRefGoogle Scholar
  30. Greenway H, Munns R (1980) Mechanism of salt tolerance in non-halophytes. Annu Rev Plant Physiol 31:149–190CrossRefGoogle Scholar
  31. Hajibagheri MA, Yeo AR, Flowers TJ, Colins JC (1989) Salinity resistance in Zea mays: fluxes of potassium, sodium and chloride, cytoplasmic concentrations and microsomal membrane lipids. Plant Cell Environ 12:753–757CrossRefGoogle Scholar
  32. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Mol Biol 51:463–499CrossRefGoogle Scholar
  33. Hernandez JA, Olmos E, Corpas FJ, Sevilla F, Del Rio LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105:151–167CrossRefGoogle Scholar
  34. Hui H, Xu X, Li S (2004) Possible mechanism of inhibition on photosynthesis of Lycium barbarum under salt stress. Chin J Ecol 23:5–9Google Scholar
  35. Hurkman WJ (1992) Effect of salt stress on germination expression: a review. Plant Soil 146:145–151CrossRefGoogle Scholar
  36. Jackson ML (1962) Soil chemical analysis. Contable Co Ltd., LondonGoogle Scholar
  37. Jain M, Mathur G, Koul S, Sarin NB (2001) Ameliorative effects of proline on salt stress-induced lipid peroxidation in cell lines of groundnut (Arachis hypogea L). Plant Cell Rep 20:463–468CrossRefGoogle Scholar
  38. Jamil M, Shafiq ur Rehman, Lee KJ, Kim JM, Hyun-Soon K, Rha ES (2007) Salinity reduced growth PSII photochemistry and chlorophyll content in radish. Sci Agric 64(2):111–118Google Scholar
  39. Kaya C, Kirnak H, Higgs D (2001) 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
  40. Khan A, Ahmad MSA, Athar HR, Ashraf M (2006) Interactive effect of foliar applied ascorbic acid and salt stress on wheat (Triticum aestivum L.) at seedling stage. Pak J Bot 39(5):1407–1414Google Scholar
  41. Lawlor DW (2002) Limitation to photosynthesis in water stressed leaves: stomata vs. metabolism and the role of ATP. Ann Bot 89:1–15CrossRefGoogle Scholar
  42. Leidi EO, Saiz JF (1997) Is salinity tolerance related to Na+ accumulation in upland cotton seedlings? Plant Soil 190:67–75CrossRefGoogle Scholar
  43. Maas EV, Nieman RH (1978) Physiology of plant tolerance to salinity. In: Jung GA (ed) Crop tolerance to suboptimal land conditions. Soil Science Society of America, Special Publication, Madison, pp 277–299Google Scholar
  44. Marcelis LFM, Hooijdonk JV (1999) Effect of salinity on growth, water use and nutrient use in radish (Raphanus sativus L.). Plant Soil 215(1):57–64CrossRefGoogle Scholar
  45. Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76CrossRefGoogle Scholar
  46. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  47. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167(3):645–663PubMedCrossRefGoogle Scholar
  48. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  49. Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043PubMedCrossRefGoogle Scholar
  50. Naheed G, Shahbaz M, Latif A, Rha ES (2007) Alleviation of the adverse effects of salt stress on rice (Oryza sativa L.) by phosphorus applied through rooting medium: growth and gas exchange characteristics. Pak J Bot 39(3):729–737Google Scholar
  51. Naheed G, Shahbaz M, Akram NA (2008) Interactive effect of rooting medium application of phosphorus and NaCl on plant biomass and mineral nutrients of rice (Oryza sativa L.). Pak J Bot 40(4):1601–1608Google Scholar
  52. Nawaz K, Ashraf M (2010) Exogenous application of glycinebetaine modulates activities of antioxidants in maize plants subjected to salt stress. J Agron Crop Sci 196(1):28–37CrossRefGoogle Scholar
  53. Nazir N, Ashraf M, Ejaz R (2001) Genomic relationships in oilseed Brassica with respect to salt tolerance-photosynthetic capacity and ion relations. Pak J Bot 33:483–501Google Scholar
  54. Noreen S, Ashraf M (2008) Alleviation of adverse effects of salt stress on sunflower (Helianthus annuus L) by exogenous application of salicylic acid: growth and photosynthesis. Pak J Bot 40(4):1657–1663Google Scholar
  55. Noreen Z, Ashraf M (2009a) Assessment of variation in antioxidative defense system in salt treated pea (Pisum sativum L.) cultivars and its putative use as salinity tolerance markers. J Plant Physiol 166:1764–1774PubMedCrossRefGoogle Scholar
  56. Noreen Z, Ashraf M (2009b) Changes in antioxidant enzymes and some key metabolites in some genetically diverse cultivars of radish (Raphanus sativus L.). Environ Exp Bot 67:395–402CrossRefGoogle Scholar
  57. Noreen Z, Ashraf M, Akram NA (2010) Salt-induced regulation of some key antioxidant enzymes and physio-biochemical phenomena in five diverse cultivars of turnip (Brassica rapa L.). J Agron Crop Sci 196:273–285Google Scholar
  58. Palmgren MG, Sommarine M, Serrano R, Larsson G (1991) Identification of an auto inhibitory domain in the G-terminal region of the plant plasma membrane H+-ATPase. J Biol Chem 266:20470–20475PubMedGoogle Scholar
  59. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: A Review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefGoogle Scholar
  60. Parida AK, Das AB, Das P (2002) NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. J Plant Biol 45:28–36CrossRefGoogle Scholar
  61. Parida AK, Das AB, Mittra B (2004) Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees Struct Funct 18:167–174CrossRefGoogle Scholar
  62. Parveen N, Ashraf M (2010) Role of silicon in mitigating the adverse effects of salt stress on growth and photosynthetic attributes of two maize (Zea mays L.) cultivars grown hydroponically. Pak J Bot 42(3):1675–1684Google Scholar
  63. Ratajczak R (2000) Structure, function and regulation of the plant vacuolar H+-translocating ATPase. Biochim Biophys Acta 1465:17–36PubMedCrossRefGoogle Scholar
  64. Raza SH, Athar HR, Ashraf M (2006) Influence of exogenously applied glycinebetaine on the photosynthetic capacity of two differently adapted wheat cultivars under salt stress. Pak J Bot 38(2):341–351Google Scholar
  65. Raza SH, Athar HR, Ashraf M, Hameed A (2007) Glycinebetaine-induced modulation of antioxidant enzymes activities and ion accumulation in two wheat cultivars differing in salt tolerance. Environ Exp Bot 60:368–376CrossRefGoogle Scholar
  66. Sabir P, Ashraf M, Hussain M, Jamil A (2009) Relationship of photosynthetic pigments and water relations with salt tolerance of proso millet (Panicum miliaceum L.) accessions. Pak J Bot 41(6):2957–2964Google Scholar
  67. Sairam RK, Roa KV, Srivastava GC (2002) Differential response of wheat cultivar genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163:1037–1048CrossRefGoogle Scholar
  68. Santarius KA (1969) The influence of electrolytes on chloroplasts during freezing and drying. Planta 89:23–46CrossRefGoogle Scholar
  69. Santarius KA, Heber U (1970) The kinetics of the inactivation of thylakoid membranes by freezing and high concentrations of electrolytes. Cryobiology 7:71–78PubMedCrossRefGoogle Scholar
  70. Shi K, Huang YY, Xia XJ, Zhang YL, Zhou YH, Yu JQ (2008) Protective role of putrescine against salt stress is partially related to the improvement of water relation and nutritional imbalance in cucumber. J Plant Nutr 31:1820–1831CrossRefGoogle Scholar
  71. Siddiqi EH, Ashraf M, Akram NA (2007) Variation in seed germination and seedling growth in some diverse lines of safflower (Carthamus tinctorius L.) under salt stress. Pak J Bot 39(6):1937–1944Google Scholar
  72. Singla R, Garg N (2005) Influence of salinity on growth and yield attributes in chickpea cultivars. Turk J Agric Forest 29:231–235Google Scholar
  73. Stoeva M, Kaymakanova M (2008) Effect of salt stress on the growth and photosynthesis rate of bean plants (Phaseolus vulgaris L.). J Cent Eur Agric 9:385–392Google Scholar
  74. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–507PubMedCrossRefGoogle Scholar
  75. Tiwari BS, Bose A, Ghosh B (1997) Photosynthesis in rice under salinity stress. Photosynthetica 34:303–306CrossRefGoogle Scholar
  76. Turan MA, Elkarim AHA, Taban A, Taban S (2010) Effect of salt stress on growth and ion distribution and accumulation in shoot and root of maize plant. Afr J Agric Res 5(7):584–588Google Scholar
  77. Ulfat M, Athar HR, Ashraf M, Akram NA, Jamil A (2007) Appraisal of physiological and biochemical selection criteria for evaluation of salt tolerance in canola (Brassica napus L.). Pak J Bot 39:1593–1608Google Scholar
  78. Wenxue W, Bilsborrow PE, Hooley P, Fincham DA, Lombi E, Forster BP (2003) Salinity induced differences in growth, ion distribution and partitioning in barley between the cultivar Maythorpe and its derived mutant Golden Promise. Plant Soil 250:183–191CrossRefGoogle Scholar
  79. Yang G, Rhodes G, Joly RG (1996) Effects of high temperature on membrane stability and chlorophyll fluorescence in glycinebetaine-deficiency and glycinebetaine-containing maize lines. Aust J Plant Physiol 23:437–443CrossRefGoogle Scholar
  80. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCrossRefGoogle Scholar
  81. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445PubMedCrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2010

Authors and Affiliations

  • Muhammad Shahbaz
    • 1
  • Muhammad Ashraf
    • 1
    • 2
    Email author
  • Nudrat Aisha Akram
    • 1
    Email author
  • Asma Hanif
    • 1
  • Shumaila Hameed
    • 1
  • Sundus Joham
    • 1
  • Rehana Rehman
    • 1
  1. 1.Department of BotanyUniversity of AgricultureFaisalabadPakistan
  2. 2.King Saud University RiyadhRiyadhSaudi Arabia

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