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Effect of NaCl-induced changes in growth, photosynthetic characteristics, water status and enzymatic antioxidant system of Calligonum caput-medusae seedlings

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Photosynthetica

Abstract

Calligonum caput-medusae is known to grow well when irrigated with water containing NaCl. The aim of this study was to investigate ecophysiological responses of C. caput-medusae to different NaCl concentrations. In our study, we examined the effect of 0, 50, 100, 200, and 400 mM NaCl. Our results demonstrated that maximum seedling growth occurred at 50 mM NaCl. Photosynthetic parameters, such as the photosynthetic pigment content and gas exchange parameters, correlated with growth response. High salinity (≥ 100 mM NaCl) resulted in a significant reduction of the plant growth. Similarly, marked declines in the pigment content, maximal efficiency of PSII photochemistry, net photosynthetic rate, transpiration rate, and stomatal conductance were also detected. However, intercellular CO2 concentration showed a biphasic response, decreasing with water containing less than 200 mM NaCl and increasing with NaCl concentration up to 400 mM. Water-use efficiency and intrinsic water-use efficiency exhibited the opposite response. The reduction of photosynthesis at the high NaCl concentration could be caused by nonstomatal factors. High salinity led also to a decrease in the relative water content and water potential. Correspondingly, an accumulation of soluble sugars and proline was also observed. Na+ and Cl− concentrations increased in all tissues and K+ concentrations were maintained high during exposure to NaCl compared with the control. High salinity caused oxidative stress, which was evidenced by high malondialdehyde and hydrogen peroxide contents. In order to cope with oxidative stress, the activity of antioxidative enzymes increased to maximum after 50 mM NaCl treatment. The data reported in this study indicate that C. caput-medusae can be utilized in mild salinity-prone environments.

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Abbreviations

APX:

ascorbate peroxidase

CAT:

catalase

Car:

carotenoids

Chl:

chlorophyll

C i :

intercellular CO2 concentration

DM:

dry mass

E :

transpiration rate

FM:

fresh mass

Fv/Fm :

maximal quantum yield of PSII photochemistry

g s :

stomatal conductance

MDA:

malondialdehyde

P N :

net photosynthetic rate

POD:

guaiacol peroxidase

ROS:

reactive oxygen species

RWC:

relative water content

SOD:

superoxide dismutase

WUE:

water-use efficiency

WUEi :

intrinsic water-use efficiency

ψw :

water potential

References

  • Aebi H.: Catalase in vitro. - Method. Enzymol. 105: 121–126, 1984.

    Article  CAS  Google Scholar 

  • Agrawal R., Gupta S., Gupta N.K. et al.: Effect of sodium chloride on gas exchange, antioxidative defense mechanism and ion accumulation in different cultivars of Indian jujube (Ziziphus mauritinana L.). - Photosynthetica 51: 95–101, 2013.

    Article  CAS  Google Scholar 

  • Amor N.B., Hamed K.B., Debez A. et al: Physiological and antioxidant responses of the perennial halophyte Crithmum maritimum to salinity.–Plant Sci. 168: 889–899, 2005.

    Article  Google Scholar 

  • Arndt S.K., Arampatsis C., Foetzki A. et al.: Contrasting patterns of leaf solute accumulation and salt adaptation in four phreatophytic desert plants in a hyperarid desert with saline ground water. C J. Arid Environ. 59: 259–270, 2004.

    Article  Google Scholar 

  • Ashraf M., Harris P.J.C.: Potential biochemical indicators of salinity tolerance in plants. - Plant Sci. 166: 3–16, 2004.

    Article  CAS  Google Scholar 

  • Baker N.R.: A possible role for photosystem IIin environmental perturbations of photosynthesis. - Plant Physiol. 81: 563–570, 1991.

    Article  CAS  Google Scholar 

  • Bates L.S., Waldren R.P., Teare I.D.: Rapid determination of free proline for water stress studies. - Plant Soil 39: 205–207, 1973.

    Article  CAS  Google Scholar 

  • Beauchamp C., Fridovich I.: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. - Anal. Biochem. 44: 276–287, 1971.

    Article  CAS  PubMed  Google Scholar 

  • Blokhina O., Virolainen E., Fagerstedt K.V.: Antioxidants, oxidative damage and oxygen deprivation stress: a review. - Ann. Bot.-London 91: 179–194, 2003.

    Article  CAS  Google Scholar 

  • Bradford M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248–254, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Castelli S.L., Grunberg K., Muñoz N. et al.: Oxidative damage and antioxidant defenses as potential indicators of salt-tolerant Cenchrus ciliaris L. genotypes. - Flora 205: 622–626, 2010.

    Article  Google Scholar 

  • Chance B., Maehly A.C.: Assay of catalases and peroxidases. - In: Colowick S.P., Kaplan N.O. (ed.): Methods in Enzymology. Pp. 764–775. Academic Press, New York 1955.

    Google Scholar 

  • Chaves M.M., Flexas J., Pinheiro C.: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. - Ann. Bot.-London 103: 551–560, 2009.

    Article  CAS  Google Scholar 

  • Dan T.V., KrishnaRaj S., Saxena P.K.: Metal tolerance of scented geranium (Pelargonium sp. ¡®Frensham¡¯): effects of cadmium and nickel on chlorophyll fluorescence kinetics. - Int. J. Phytoremediat. 2: 91–104, 2000.

    Article  CAS  Google Scholar 

  • Dubey R.S.: Photosynthesis in plants under stress full conditions. - In: Pessarakli M. (ed.): Photosynthesis. Pp. 717–718. CRC Press, New York 2005.

    Google Scholar 

  • Dubey R.S.: Photosynthesis in plants under stressful conditions. - In: Pessarakli M. (ed.): Handbook of Photosynthesis. Pp. 859–975. Marcel Dekker, New York 1997.

    Google Scholar 

  • Feng Z.T., Deng Y.Q., Fan H. et al.: Effects of NaCl stress on the growth and photosynthetic characteristics of Ulmus pumila L. seedlings in sand culture. - Photosynthetica 52: 313–320, 2014.

    Article  CAS  Google Scholar 

  • Gimeno V., Syvertsen J.P., Simón I. et al.: Physiological and morphological responses to flooding with fresh or saline water in Jatropha curcas. - Environ. Exp. Bot. 78: 47–55, 2012.

    Article  CAS  Google Scholar 

  • Gorai M., Neffati M.: Osmotic adjustment, water relation and growth attributes of the xero-halophyte Reaumuria vermiculata L. (Tamaricaceae) in response to salt stress. - Acta Physiol. Plant. 33: 1425–1433, 2011.

    Article  CAS  Google Scholar 

  • Gorham J., Wyn Jones R.G., McDonell E.: Some mechanisms of salt tolerance in crop plants. - Plant Soil 89: 15–40, 1985.

    Article  CAS  Google Scholar 

  • Grant J.J., Loake G.J.: Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. - Plant Physiol. 124: 21–30, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guzmán-Murillo M.A., Ascencio F., Larrinaga-Mayoral J.A.: Germination and ROS detoxification in bell pepper (Capsicum annuum L.) under NaCl stress and treatment with microalgae extracts. - Protoplasma 250: 33–42, 2013.

    Article  PubMed  Google Scholar 

  • Han W., Xu X.W., Li L. et al.: Chlorophyll a fluorescence responses of Haloxylon ammodendron seedlings subjected to progressive saline stress in the Tarim desert highway ecological shelterbelt. - Photosynthetica 48: 635–640, 2010.

    Article  CAS  Google Scholar 

  • Hare P.D., Cress A., Van Staden J.: Dissecting the roles of osmolyte accumulation during stress. - Plant Cell Environ. 21: 535–553, 1998.

    Article  CAS  Google Scholar 

  • Hassine A.B., Lutts S.: Differential responses of saltbush Atriplex halimus L. exposed to salinity and water stress in relation to senescing hormones abscisic acid and ethylene. - C J. Plant Physiol. 167: 1448–1456, 2010.

    Article  Google Scholar 

  • Havaux M., Niyogi K.K.: The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. - C P. Natl. Acad. Sci. USA 96: 8762–8767, 1999.

    Article  CAS  Google Scholar 

  • Hernández J.A., Almansa M.S.: Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. - Physiol. Plantarum 115: 251–257, 2002.

    Article  Google Scholar 

  • Hichem H., Ei Naceur A., Mounir D.: Effects of salt stress on photosynthesis, PSII photochemistry and thermal energy dissipation in leaves of two corn (Zea mays L.) varieties. - Photosynthetica 47: 517–526, 2009.

    Article  CAS  Google Scholar 

  • Hong Z., Lakkineni K., Zhang Z. et al.: Removal of feedback inhibition of ¦¤(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. - Plant Physiol. 122: 1129–1136, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang C.J., Wei G., Jie Y.C. et al.:. Effects of concentrations of sodium chloride on photosynthesis, antioxidative enzymes, growth and fiber yield of hybrid ramie. - Plant Physiol. Bioch. 76: 86–93, 2014.

    Article  CAS  Google Scholar 

  • Hussin S., Geissler N., Koyro H.-W.: Effect of NaCl salinity on Atriplex nummularia (L.) with special emphasis on carbon and nitrogen metabolism. - Acta Physiol. Plant. 35: 1025–1038, 2013.

    Article  CAS  Google Scholar 

  • Jia L.N., Wu B., Ding G.D. et al.: Community characters and trapping capability of three common species of psammophyte in Yanchi county, Ningxia. - C J. Northeast Forest. Univ. 37: 56–63, 2009. [In Chinese]

    Google Scholar 

  • Kosugi H., Kikugawa K.: Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. - Lipids 20: 915–920, 1985.

    Article  CAS  Google Scholar 

  • Koyro H.-W., Hussain T., Huchzermeyer B. et al.: Photosynthetic and growth responses of a perennial halophytic grass Panicum turgidum to increasing NaCl concentrations. - Environ. Exp. Bot. 91: 22–29, 2013.

    Article  CAS  Google Scholar 

  • Kramer P.J.: Water Relations of Plants. Pp. 215–234. Academic Press, San Diego 1983.

    Book  Google Scholar 

  • Li C.J., Lei J.Q., Zhao Y. et al.: Effect of saline water irrigation on soil development and plant growth in the Taklimakan Desert Highway shelterbelt. - Soil Till. Res. 146: 99–107, 2015.

    Article  Google Scholar 

  • Lichtenthaler H.K.: Chlorophylls and carotenoids-pigments of photosynthetic biomembranes. - In: Colowick S.P., Kaplan N.O. (ed.): Methods in Enzymology. Pp. 350–382. Academic Press, San Diego 1987.

    Google Scholar 

  • Lokhande V.H., Mulye K., Patkar R. et al.: Biochemical and physiological adaptations for halophyte Sesuvium portulacastrum (L.) L., (Aizoaceae) to salinity. - Arch. Agr. Soil Sci. 59: 1373–1391, 2013.

    Article  CAS  Google Scholar 

  • Lu Y., Li X.R., He M.Z. et al.: Seedling growth and antioxidative enzymes activities in leaves under metal stress differ between two desert plants: a perennial (Peganum harmala) and an annual (Halogeton glomeratus) grass. - Acta Physiol. Plant. 32: 583–590, 2010.

    Article  CAS  Google Scholar 

  • Mišić D., Šiler B., Živković J.N. et al.: Contribution of inorganic cations and organic compounds to osmotic adjustment in root cultures of two Centaurium species differing in tolerance to salt stress. - Plant Cell Tiss. Org. 108: 389–400, 2012.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Munns R.: Tester M.: Mechanisms of salinity tolerance. - Annu. Rev. Plant Biol. 59: 651–681, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Munns R.: Comparative physiology of salt and water stress. - Plant Cell Environ. 25: 239–250, 2002.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Palma F., Lluch C., Iribarne C. et al.: Combined effect of salicylic acid and salinity on some antioxidant activities, oxidative stress and metabolite accumulation in Phaseolus vulgaris. - Plant Growth Regul. 58: 307–316, 2009.

    Article  CAS  Google Scholar 

  • Parida A.K., Jha B.: Inductive responses of some organic metabolites for osmotic homeostasis in peanut (Arachis hypogaea L.) seedlings during salt stress. - Acta Physiol. Plant. 35: 2821–2832, 2013.

    Article  CAS  Google Scholar 

  • Prasad K.V.S.K., Pardha Saradhi P.: Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts. - Plant Sci. 166: 1197–1212, 2004.

    Article  CAS  Google Scholar 

  • Sai Kachout S., Ben Mansoura A., Jaffel Hamza K. et al.: Leafwater relations and ion concentrations of halophyte Atriplex hortensis in response to salinity and water stress. - Acta Physiol. Plant. 33: 335–342, 2011.

    Article  Google Scholar 

  • Sánchez F.J., de Andrés E.F., Tenorio J.L. et al.: Growth of epicotyls, turgor maintenance and osmotic adjustment in pea plants (Pisum sativum L.) subjected to water stress. - Field Crop Res. 86: 81–90, 2004.

    Article  Google Scholar 

  • Sekmen A.H., Turkan I., Tanyolac Z.O. et al.: Different antioxidant defense responses to salt stress during germination and vegetative stages of endemic halophyte Gypsophila oblanceolata Bark. - Environ. Exp. Bot. 77: 63–76, 2012.

    Article  CAS  Google Scholar 

  • Sergiev I., Alexieva V., Karanov E.: Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. - C CRAcad. Bulg. Sci. 51: 121–124, 1997.

    Google Scholar 

  • Sergio L., De Paola A., Cantore V. et al.: Effect of salt stress on growth parameters, enzymatic antioxidant system, and lipid peroxidation in wild chicory (Cichorium intybus L.). - Acta Physiol. Plant. 34: 2349–2358, 2012.

    Article  CAS  Google Scholar 

  • Serrano R., Rodriguez-Navarro A.: Ion homeostasis during salt stress in plants. - Curr. Opin. Cell Biol. 13: 399–404, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Sharma V., Ramawat K.G.: Salt stress enhanced antioxidant response in callus of three halophytes (Salsola baryosma, Trianthema triquetra, Zygophyllum simplex) of Thar Desert. - Biologia 69: 178–185, 2014.

    CAS  Google Scholar 

  • Sibole J.V., Cabot C., Poschenrieder C. et al.: Efficient leaf ion partitioning, an overriding condition for abscisic acidcontrolled stomatal and leaf growth responses to NaCl salinization in two legumes. - C J. Exp. Bot. 54: 2111–2119, 2003.

    Article  CAS  Google Scholar 

  • Smart R.E., Bingham G.E.: Rapid estimation of relative water content. - Plant Physiol. 53: 258–260, 1974.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J.K., Li T., Xia J.B. et al.: Influence of salt stress on ecophysiological parameters of Periploca sepium Bunge. - Plant Soil Environ. 57: 139–144, 2011.

    CAS  Google Scholar 

  • Thomas F.M., Foetzki A., Arndt S.K. et al.: Water use by perennial plants in the transition zone between river oasis and desert in NWChina. - Basic Appl. Eco. 7: 253–267, 2006.

    Article  Google Scholar 

  • Wang H., Jia G.: Satellite-based monitoring of decadal soil salinization and climate effects in a semi-arid region of China. - Adv. Atmos. Sci. 29: 1089–1099, 2012.

    Article  CAS  Google Scholar 

  • Yan H., Hu X.T., Li F.S.: Leaf photosynthesis, chlorophyll fluorescence, ion content and free amino acids in Caragana korshinskii Kom exposed to NaCl stress. - Acta Physiol. Plant. 34: 2285–2295, 2012.

    Article  CAS  Google Scholar 

  • Yang J.S.: Development and prospect of the research on saltaffected soils in China. - Acta Pedol. Sin. 45: 837–845, 2008. [In Chinese]

    Google Scholar 

  • Yildiztugay E., Ozfidan-Konakci C., Kucukoduk M.: Sphaerophysa kotschyana, an endemic species from Central Anatolia: antioxidant system reponses under salt stress. - C J. Plant Res. 126: 729–742, 2013.

    Article  CAS  Google Scholar 

  • Yildiztugay E., Sekmen A. H., Turkan I. et al.: Elucidation of physiological and biochemical mechanisms of an endemic halophyte Centaurea tuzgoluensis under salt stress. - Plant Physiol. Bioch. 49: 816–824, 2011.

    Article  CAS  Google Scholar 

  • Zhu C.G., Chen Y.N., Li W.H. et al.: Effect of herbivory on the growth and photosynthesis of replanted Calligonum caputmedusae saplings in an infertile arid desert. - Plant Ecol. 215: 155–167, 2014.

    Article  Google Scholar 

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Authors and Affiliations

  1. State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, 830011, Urumqi, China

    Y. Lu, J.-Q. Lei, F.-J. Zeng, B. Zhang, G.-J. Liu, B. Liu & X.-Y. Li

  2. Cele National Station of Observation and Research for Desert-Grassland Ecosystems, 848300, Cele, China

    Y. Lu, J.-Q. Lei, F.-J. Zeng, B. Zhang, G.-J. Liu, B. Liu & X.-Y. Li

  3. Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, 830011, Urumqi, China

    Y. Lu, J.-Q. Lei, F.-J. Zeng, B. Zhang, G.-J. Liu, B. Liu & X.-Y. Li

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  1. Y. Lu
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  2. J.-Q. Lei
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  3. F.-J. Zeng
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  4. B. Zhang
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  5. G.-J. Liu
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  6. B. Liu
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  7. X.-Y. Li
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Correspondence to F.-J. Zeng.

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Acknowledgements

This work was sponsored by the Chinese National Natural Scientific Foundation (41301103) and Science and Technology Service Network Initiative (KFJ-SW-STS-176).

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Lu, Y., Lei, JQ., Zeng, FJ. et al. Effect of NaCl-induced changes in growth, photosynthetic characteristics, water status and enzymatic antioxidant system of Calligonum caput-medusae seedlings. Photosynthetica 55, 96–106 (2017). https://doi.org/10.1007/s11099-016-0234-6

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