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Salinity-induced Physiological Modification in the Callus from Halophyte Nitraria tangutorum Bobr.

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Abstract

Little is known about the physiological adaptation mechanisms of the desert halophyte Nitraria tangutorum Bobr. to the environment. In this study, callus from Nitraria tangutorum Bobr. was used to investigate physiological responses to salinity and the regulatory function of nitric oxide (NO) on catalase (CAT) activity. Increased dry weight and soluble proteins were observed in the callus exposed to lower salinity (50 and 100 mM NaCl), whereas 200 mM NaCl led to significant decreases of these two growth parameters, and the levels of proline and soluble carbohydrates also were enhanced under NaCl treatment. In addition, short-term stress from 50 mM NaCl and the application of lower sodium nitroprusside (SNP, a NO donor) concentration resulted in decreased levels of malondialdehyde (MDA). In contrast, higher concentrations of NaCl and SNP induced significant oxidative damage in Nitraria tangutorum Bobr. callus. Analysis based on the fluorescent probe DAF-FM DA revealed that NaCl and SNP treatment led to enhanced levels of NO in the callus cells. Moreover, the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (c-PTIO) reduced endogenous NO concentrations and abolished the enhancement in dry weight and the decrease in MDA level under 50-mM-NaCl treatment. CAT activity increased under salt stress, and the 50-mM-NaCl effect was alleviated by treatment with c-PTIO or the nitric oxide synthase inhibitor Nω-nitro-l-arginine. We suggest that Nitraria tangutorum Bobr. callus exhibited tolerance to lower-salinity stress. We also showed that increased NO generation in response to salinity might be associated with regulation of growth, protection against oxidative damage, and excitation of CAT activity in Nitraria tangutorum Bobr. callus under salt stress.

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References

  • Aebi H (1974) Catalase. In: Bergmeyer HU (ed) In methods of enzymatic analysis. Academic Press, New York, pp 673–677

    Google Scholar 

  • Ahmad MS, Javed F, Javed S, Alvi AK (2009) Relationship between callus growth and mineral nutrients uptake in salt-stressed indica rice callus. J Plant Nutr 32:382–394

    Article  CAS  Google Scholar 

  • Al Hakimi A, Monneveux P, Galiba G (1995) Soluble sugars, proline, and relative water content (RWC) as traits for improving drought tolerance and divergent selection for RCW from T. polonicum into T. durum. J Genet Breed 49:237–244

    CAS  Google Scholar 

  • Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 172:876–887

    Article  CAS  Google Scholar 

  • Asada K (1992) Ascorbic peroxidase—a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241

    Article  CAS  Google Scholar 

  • Balibrea ME, Dell’Amico J, Bolarin MC, Perez-Alfocea F (2000) Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Plant Physiol 110:503–511

    Article  CAS  Google Scholar 

  • Bates CJ, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221

    Article  CAS  PubMed  Google Scholar 

  • Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650

    Article  CAS  PubMed  Google Scholar 

  • Bor M, Özdemir F, Türkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Sci 164:77–84

    Article  CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  CAS  PubMed  Google Scholar 

  • Chowdhury JB, Jain S, Jain RK (1993) Biotechnological approaches for developing salt-tolerant crops. J Plant Biochem Biotechnol 2:1–7

    Google Scholar 

  • Çiğdem SE, Işıl İ, Gül CÖ, Meral Ü, Semahat Y (2008) The effects of nitric oxide on some early germination parameters and mitotic activity in lentil (Lens Culunaris Medik.). J Appl Biol Sci 2:1–7

    Google Scholar 

  • Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13:1380–1384

    Article  CAS  PubMed  Google Scholar 

  • De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, di Toppi LS, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228

    Article  PubMed  Google Scholar 

  • Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223

    Article  CAS  Google Scholar 

  • Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212

    Article  CAS  PubMed  Google Scholar 

  • Dracup M (1991) Increasing salt tolerance of plants through cell culture requires greater understanding of tolerance mechanisms. Austr J Plant Physiol 18:1–15

    Article  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 38:350–356

    Article  Google Scholar 

  • Dubovskaya LV, Kolesneva EV, Knyazev DM, Volotovskii ID (2007) Protective role of nitric oxide during hydrogen peroxide-induced oxidative stress in tobacco plants. Russ J Plant Physiol 54:755–762

    Article  CAS  Google Scholar 

  • El-baky A, Hanaa H, Hussein MM, Mohamed AA (2003) Influence of salinity on lipid peroxidation, antioxidant enzymes and electrophoretic patterns of protein and isoenzymes in leaves of some onion cultivars. Asian J Plant Sci 2:633–638

    Article  Google Scholar 

  • Golan-Goldhirsh A, Barazanil O, Nepovim A, Soudek P, Smrcek S, Dufkova L, Krenkova S, Yrjala K, Schröder P, Vanek T (2004) Plant response to heavy metals and organic pollutants in cell culture and at whole plant level. J Soils Sediments 4:133–140

    Article  CAS  Google Scholar 

  • Gueta-Dahan Y, Yaniv Z, Zilinskas BA, Ben-Hayyim G (1997) Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in citrus. Planta 203:460–469

    Article  CAS  PubMed  Google Scholar 

  • Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17:3436–3450

    Article  CAS  PubMed  Google Scholar 

  • Guo YQ, Tian ZY, Yan DL, Zhang J, Qin P (2009) Effects of nitric oxide on salt stress tolerance in Kosteletzkya virginica. Life Sci J 6:67–75

    CAS  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  • Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487

    Article  CAS  Google Scholar 

  • Koca H, Özdemir F, Türkan I (2007) The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60:344–351

    Article  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lehnera C, Kerschbauma HH, Lütz-Meindl U (2009) Nitric oxide suppresses growth and development in the unicellular green alga Micrasterias denticulate. J Plant Physiol 166:117–127

    Article  Google Scholar 

  • Li Y (2008) Kinetics of the antioxidant response to salinity in the halophyte Limonium bicolor. Plant Soil Environ 54:493–497

    CAS  Google Scholar 

  • Liu YG, Wu RR, Wan Q, Xie GQ, Bi YR (2007) Glucose-6-phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in Red Kidney bean roots. Plant Cell Physiol 48:511–522

    Article  CAS  PubMed  Google Scholar 

  • Maggio A, Reddy MP, Joly RJ (2000) Leaf gas exchange and solute accumulation in the halophyte Salvadora persica grown at moderate salinity. Environ Exp Bot 44:31–38

    Article  CAS  PubMed  Google Scholar 

  • Megdiche W, Amor NDA, Hessini K, Ksouri R, Zuily-Fodil Y, Abdelly C (2007) Salt tolerance of the annual halophyte Cakile maritima as affected by the provenance and the developmental stage. Acta Physiol Plant 29:375–384

    Article  CAS  Google Scholar 

  • Miller AJ, Smith SJ (2008) Change in cytosolic nitrate status as a signal regulating nitrate processing. Ann Bot 101:485–489

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99:1161–1173

    Article  CAS  PubMed  Google Scholar 

  • Munns R, James RJ, Lauchli A (2005) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 46:921–927

    Google Scholar 

  • Muscolo A, Sidari M, Rosaria PM (2003) Tolerance of kikuyu grass to long term salt stress is associated with induction of antioxidant defences. Plant Growth Regul 41:57–62

    Article  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1247

    Article  CAS  PubMed  Google Scholar 

  • Pandey R, Ganapathy PS (1985) The proline enigma: NaCl-tolerant and NaCl-sensitive callus lines of Cicer arietinum. Plant Sci 40:13–17

    Article  CAS  Google Scholar 

  • Pang CH, Zhang SJ, Gong ZZ, Wang BS (2008) NaCl treatment markedly enhances H2O2-scavenging system in leaves of halophyte Suaeda salas. Physiol Plant 125:490–499

    Google Scholar 

  • Radyukina NL, Kartashov AV, Ivanov YV, Shevyakova NI, Kuznetsov VV (2007) Functioning of defense system in halophytes and glycophytes under progressing salinity. Russ J Plant Physiol 54:806–815

    Article  CAS  Google Scholar 

  • Rosa M, Hilal M, González JA, Prado FE (2009) Low-temperature effect on enzyme activities involved in sucrose–starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa (Chenopodium quinoa Willd.) seedlings. Plant Physiol Biochem 47:300–307

    Article  CAS  PubMed  Google Scholar 

  • Sekmen AH, Turkan I, Takio S (2007) Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiol Plant 131:399–411

    Article  CAS  PubMed  Google Scholar 

  • Shalata A, Tal M (1998) The effects of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol Plant 104:169–174

    Article  CAS  Google Scholar 

  • Slama I, Ghnaya T, Messedi D, Hessini K, Labidi N, Savoure A, Abdelly C (2007) Effect of sodium chloride on the response of the halophyte species Sesuvium portulacastrum grown in mannitol-induced water stress. J Plant Res 120:291–299

    Article  CAS  PubMed  Google Scholar 

  • Stewart GR, Lee IA (1974) The role of proline accumulation in halophytes. Planta 120:279–289

    Article  CAS  Google Scholar 

  • Suriyan C, Chalermpol K (2009) Proline accumulation, photosynthetic abilities and growth characters of sugarcane (Saccharum officinarum L.) plantlets in response to iso-osmotic salt and water-deficit stress. Agric Sci China 8:51–58

    Google Scholar 

  • Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009a) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804

    Article  CAS  PubMed  Google Scholar 

  • Tanou G, Molassiotis A, Diamantidis G (2009b) Hydrogen peroxide- and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. J Plant Physiol 166:1904–1913

    Article  CAS  PubMed  Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923

    Article  CAS  PubMed  Google Scholar 

  • Wang SH, Yang ZM, Yang H, Lu B, Li SQ, Lu YP (2004) Copper-induced stress and antioxidative responses in roots of Brassica juncea L. Bot Bull Acad Sin 45:203–212

    CAS  Google Scholar 

  • Widholm JM (1988) In vitro selection with plant cell and tissue cultures. Iowa State J Res 62:587–595

    Google Scholar 

  • Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208

    Article  CAS  PubMed  Google Scholar 

  • Yang SM, Furukawa I (2006) Anatomical adaptations of three species of Chinese xerophytes (Zygophyllaceae). J Forestry Res 17:247–251

    Article  Google Scholar 

  • Yildiz M (2007) Two-dimensional electrophoretic analysis of soluble leaf proteins of a salt-sensitive (Triticum aestivum) and a salt-tolerant (T. durum) cultivar in response to NaCl stress. J Integr Plant Biol 49:975–981

    Article  CAS  Google Scholar 

  • Zhang F, Wang YP, Yang YL, He WL, Wang D, Liu JQ (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30:775–785

    Article  PubMed  Google Scholar 

  • Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857

    Article  CAS  PubMed  Google Scholar 

  • Zhou Q (2001) The measurement of malondialdehyde in plants. In: Zhou Q (ed) In methods in plant physiology. Agricultural Press, Beijing, pp 173–174

    Google Scholar 

  • Zhou BY, Guo ZF, Xing JP, Huang BR (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (No. 30960064), and the National Science Foundation for Distinguished Young Scholars of China (Grant No. 30625008).

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Authors and Affiliations

  1. School of Life Science, Northwest Normal University, 730070, Lanzhou, Gansu, People’s Republic of China

    Yingli Yang, Xueling Wei, Ruxia Shi & Qing Fan

  2. State Key Laboratory of Arid Agroecology, School of Life Science, Lanzhou University, 730000, Lanzhou, People’s Republic of China

    Lizhe An

  3. Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences, 730000, Lanzhou, People’s Republic of China

    Yingli Yang & Lizhe An

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  1. Yingli Yang
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  2. Xueling Wei
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Correspondence to Yingli Yang.

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Yang, Y., Wei, X., Shi, R. et al. Salinity-induced Physiological Modification in the Callus from Halophyte Nitraria tangutorum Bobr.. J Plant Growth Regul 29, 465–476 (2010). https://doi.org/10.1007/s00344-010-9158-8

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