Skip to main content

Differential responses to drought stress in leaves and roots of wild jujube, Ziziphus lotus

Abstract

The aim of this study was to investigate the effects of drought stress induced by polyethylene glycol-6000 in wild jujube, Ziziphus lotus. One-month-old, hydroponically grown seedlings were subjected to three treatments, i.e. normal watering (−0.2 MPa), moderate (−1.2 MPa) and severe (−2.1 MPa) drought stress for 14 days under controlled climatic conditions. Plant growth was markedly reduced with increasing osmotic stress. The shoot water potential (Ψw) and leaf relative water content followed similar patterns and significantly decreased with increasing osmolality of solutions. As a consequence of drought, contents in proline and soluble sugars were found to be more elevated in leaves than in roots. The level of lipid peroxidation in terms of malonyldialdehyde contents increased in both leaves and roots of drought-stressed plants. Wild jujube displayed higher activities of antioxidant enzymes in the roots than in the leaves. Catalase and guaiacol peroxidase activities increased significantly in drought-stressed roots, whereas ascorbate peroxidase activity showed a slight decline with no significant changes. These findings suggest that Z. lotus was able to adapt to severe drought stress by accumulation of compatible solutes and by activation of free radical-scavenging enzymes. Overall, defence mechanisms in Z. lotus against oxidative stress are organized differently in plant tissues, with higher solute accumulation in leaves and increased activity of antioxidants in roots, during drought stress.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

DM:

Dry mass

MDA:

Malondialdehyde

FM:

Fresh mass

PEG:

Polyethylene glycol

POD:

Guaiacol peroxidase

RWC:

Relative water content

Ψw :

Water potential

TM:

Turgid mass

References

  1. Aebi H (1984) Catalase: in vitro. In: Colowick SP, Kaplan NO (eds) Methods in Enzymology, Vol 105. Academic Press, New York, pp 121–126

  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  PubMed  Article  Google Scholar 

  3. Arndt SK, Wanek W, Clifford SC, Popp M (2000) Contrasting adaptations to drought stress in field-grown Ziziphus mauritiana and Prunus persica trees: water relations, osmotic adjustment and carbon isotope composition. Aust J Plant Physiol 27:985–996

    Google Scholar 

  4. Arndt SK, Clifford SC, Wanek W, Jones HG, Popp M (2001) Physiological and morphological adaptations of the fruit tree Ziziphus rotundifolia in response to progressive drought stress. Tree Physiol 21:705–715

    CAS  PubMed  Article  Google Scholar 

  5. Arnon DI, Hoagland DR (1940) Crop production in artificial solutions and in soils with special reference to factors affecting yields and absorption of inorganic nutrient. Soil Sci 50:463–484

    CAS  Google Scholar 

  6. Attipali RR, Kolluru VC, Munusamy V (2004) Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  Google Scholar 

  7. Bacelar EA, Santos DL, Moutinho-Pereira JM, Goncalves BC, Ferreira HF, Correia CM (2006) Immediate responses and adaptative strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci 170:596–605

    CAS  Article  Google Scholar 

  8. Bacelar EA, Moutinho – Pereira JM, Goncalves BC, Ferreira HF, Correia CM (2007) Changes in growth, gas exchange, xylem hydraulic properties and water use efficiency of three olive cultivars under contrasting water availability regimes. Environ Exp Bot 60:183–192

    CAS  Article  Google Scholar 

  9. Bates LS, Waldren RP, Teare IK (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–208

    CAS  Article  Google Scholar 

  10. Ben Ahmed Ch, Ben Rouina B, Sensoy S, Boukhris M, Ben Abdallah F (2009) Changes in gas exchange, proline accumulation and antioxidative enzyme activities in three olive cultivars under contrasting water availability regimes. Environ Exp Bot 67:345–352

    CAS  Article  Google Scholar 

  11. Bian S, Jiang Y (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci Hortic 120:264–270

    CAS  Article  Google Scholar 

  12. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress. Ann Bot 91:179–194

    CAS  PubMed  Article  Google Scholar 

  13. Blum A, Munns R, Passioura JB, Turner NC (1996) Genetically engineered plants resistant to soil dry and salt stress: how to interpret osmotic relations? Plant Physiol 110:1050–1053

    Google Scholar 

  14. Bohnert HJ, Jenson RG (1996) Strategies for engineering water stress tolerance in plants. Trends Biotech 14:89–97

    CAS  Article  Google Scholar 

  15. Borgi W, Chouchane N (2009) Anti-spasmodic effects of Zizyphus lotus (L.) Desf. extracts on isolated rat duodenum. J Ethnopharmacol 126:571–573

    PubMed  Article  Google Scholar 

  16. Borgi W, Recio MC, Rios JL, Chouchane N (2008) Anti-inflammatory and analgesic activities of flavonoid and saponin fractions from Zizyphus lotus (L.) Lam. S Afr J Bot 74:320–324

    CAS  Article  Google Scholar 

  17. Boussadia O, Ben Mariem F, Mechri B, Boussetta W, Braham M, Ben El Hadj S (2008) Response to drought of two olive tree cultivars (cv Koroneki and Meski). Sci Hortic 116:388–393

    Article  Google Scholar 

  18. 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

    CAS  PubMed  Article  Google Scholar 

  19. Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775

    Article  Google Scholar 

  20. Choudhary R, Sankhla N, Trivedi S, Joshi S (1996) Photosynthesis, chlorophyll fluorescence, osmoregulatory solutes and enzyme activities in ber (Ziziphus rotundifolia) under moisture stress. Proc Plant Growth Regul Soc Am 23:206–210

    Google Scholar 

  21. Clifford SC, Arndt SK, Corlett JE, Joshi S, Sankhla N, Popp M, Jones HG (1998) The role of solute accumulation, osmotic adjustment and changes in cell wall elasticity in drought tolerance in cell wall elasticity in drought tolerance in Ziziphus mauritiana (Lamk.). J Exp Bot 49:967–977

    CAS  Article  Google Scholar 

  22. DaCosta M, Huang B (2007) Changes in antioxidant enzyme activities and lipid peroxidation for bentgrass species in responses to drought stress. J Am Soc Hortic Sci 132:319–326

    CAS  Google Scholar 

  23. De Smedt S, Cuní Sanchez A, Van den Bilcke N, Simbo D, Potters G, Samson R (2012) Functional responses of baobab (Adansonia digitata L.) seedlings to drought conditions: differences between western and south-eastern Africa. Environ Exp Bot 75:181–187

    Article  Google Scholar 

  24. Dichio B, Romano M, Nuzzo V, Xiloyannis C (2002) Soil water availability and relationship between canopy and roots in young olive trees (cv Coratina). Acta Hortic 586:255–258

    Google Scholar 

  25. Dichio B, Xiloyannis C, Sofo A, Montanaro G (2005) Osmotic regulation in leaves and roots of olives trees during a water deficit and rewatering. Tree Physiol 26:179–185

    Article  Google Scholar 

  26. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    CAS  Article  Google Scholar 

  27. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclamatory stress tolerance and signaling. Plant Physiol 100:241–254

    CAS  Article  Google Scholar 

  28. Gindaba J, Rozanov A, Negash L (2004) Response of seedlings of two Eucalyptus and three deciduous tree species from Ethiopia to severe water stress. For Ecol Manag 201:119–129

    Article  Google Scholar 

  29. Gorai M, Maraghni M, Neffati M (2010) The relationship between phenological traits and water potential patterns of the wild jujube Ziziphus lotus in southern Tunisia. Plant Ecol Divers 3:273–280

    Article  Google Scholar 

  30. Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    CAS  PubMed  Article  Google Scholar 

  31. Guo Z, Huang EM, Lu ES, Yaqing EZ, Zhong EQ (2007) Differential response to paraquat induced oxidative stress in two rice cultivars on antioxidants and chlorophyll a fluorescence. Acta Physiol Plant 29:39–46

    CAS  Article  Google Scholar 

  32. Hassine AB, Lutts S (2010) Differential responses of salt bush Atriplex halimus L. exposed to salinity and water stress in relation to senescing hormones abscisic acid and ethylene. Plant Physiol 167:1448–1456

    Article  Google Scholar 

  33. Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonw Bur Hort Tech Com 22:431–446

  34. Hudges DM, Delong JM, Forney FC, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  Google Scholar 

  35. Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Ann Rev Plant Physiol Plant Mol Biol 47:377–403

    CAS  Article  Google Scholar 

  36. Jacobson L (1951) Maintenance of iron supply in nutrient solutions by a single addition of ferric-potassium-ethylene-diamine-tetracetate. Plant Physiol 26:411–413

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  37. Jones HG (1999) Selection of drought-tolerant fruit trees for summer rainfall regions of Southern Africa and India. European Commission STD-3, Brussels, Belgium, CTA, pp 118–120

  38. Kulkarni M, Schneider B, Raveh E, Tel-Zur N (2010) Leaf anatomical characteristics and physiological responses to short-term drought in Ziziphus mauritiana (Lamk.). Sci Hortic 124:316–322

    CAS  Article  Google Scholar 

  39. Larcher W (2003) Physiological plant ecology. Springer-Verlag, New York

  40. Le Floc’h E (1983) Contribution a une étude ethnobotanique de la flore de la Tunisie. Imprimerie officielle de la Republique Tunisienne, Tunis

    Google Scholar 

  41. Ludlow MM, Muchow RC (1990) A critical evaluation of traits for improving crop yields in water-limited environments. Adv Agron 43:107–153

    Article  Google Scholar 

  42. Maraghni M, Gorai M, Neffati M (2010) Seed germination at different temperatures and water stress levels, and seedling emergence from different depths of Ziziphus lotus. S Afr J Bot 76:453–459

    CAS  Article  Google Scholar 

  43. Maraghni M, Gorai M, Neffati M (2011) The influence of water-deficit stress on growth, water relations and solute accumulation in wild jujube (Ziziphus lotus). J Ornam Hortic Plant 1:63–72

    Google Scholar 

  44. Marnett LJ (1999) Lipid peroxidation—DNA damage by malondialdehyde. Mutat Res 424:83–95

    CAS  PubMed  Article  Google Scholar 

  45. Michel BE, Kaufmann MR (1973) The osmotic potential of polyethylene glycol-6000. Plant Physiol 51:914–916

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  46. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 9:405–410

    Article  Google Scholar 

  47. Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    PubMed  Article  Google Scholar 

  48. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  49. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    CAS  PubMed  Article  Google Scholar 

  50. Pareek OP (2001) Fruits for the Future 2: Ber. International Centre for Underutilised Crops, University of Southampton, Southampton

    Google Scholar 

  51. Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750

    CAS  PubMed  Article  Google Scholar 

  52. Sankhla N (1998) Work done in India. In: Jones HG (ed) Selection of drought tolerant fruit trees for summer rainfall regions of Southern Africa and India. EU-STD, Brussels, Belgium

    Google Scholar 

  53. Schwanz P, Polle A (2001) Differential stress responses of antioxidative system to drought in Quercus robur and Pinus pinaster grown under high CO2 concentrations. J Exp Bot 52:133–143

    CAS  PubMed  Article  Google Scholar 

  54. Serraj R, Sinclair TR (2002) Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ 25:333–341

    PubMed  Article  Google Scholar 

  55. Sofo A, Dichio B, Xiloyannis C, Masia A (2004) Effects of different irradiance levels on some antioxidant enzymes and on malondialdehyde content during rewatering in olive tree. Plant Sci 166:293–302

    CAS  Article  Google Scholar 

  56. Sofo A, Manfreda S, Dichio B, Florentino M, Xiloyannis C (2007) The olive tree: a paradigm for drought tolerance in Mediterranean climates. Hydrol Earth Syst Sci Disc 4:2811–2835

    Article  Google Scholar 

  57. Sundaresan S, Sudhakaran PR (1995) Water stress-induced alterations in the proline metabolism of drought-susceptible and -tolerant cassava (Maniohot esculenta) cultivars. Plant Physiol 94:635–642

    CAS  Article  Google Scholar 

  58. Todaka D, Matsushima H, Morohashi Y (2000) Water stress enhances beta-amylase activity in cucumber cotyledons. Environ Exp Bot 51:739–745

    CAS  Article  Google Scholar 

  59. Turkan I, Bor M, Ozdemir F, Koca H (2005) Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Sci 168:223–231

    Article  Google Scholar 

  60. Yordanov I, Velikova V, Tsonev T (2000) Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 38:171–186

    CAS  Article  Google Scholar 

  61. Zhu JK (2002) Salt and drought stress signal transduction in plants. Plant Biol 53:247–273

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mustapha Gorai.

Additional information

Communicated by G. Bartosz.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Maraghni, M., Gorai, M., Neffati, M. et al. Differential responses to drought stress in leaves and roots of wild jujube, Ziziphus lotus . Acta Physiol Plant 36, 945–953 (2014). https://doi.org/10.1007/s11738-013-1473-9

Download citation

Keywords

  • Ziziphus lotus
  • Drought
  • Growth
  • Water relations
  • Osmotic adjustment
  • Oxidative stress