Abstract
The effects of salinity (0–400 mM NaCl, marked S0, S100, S200, and S400) on growth, photosynthesis, photosystem 2 (PS2) efficiency, ion relations, and pigment contents were studied in two seashore Cakile maritima ecotypes (Tabarka and Jerba, respectively, sampled from humid and arid bioclimatic areas). Growth of Jerba plants was improved at S100 as compared to S0. Tabarka growth was inhibited by salinity at all NaCl concentrations. Leaf sodium and chloride concentrations increased with medium salinity and were higher in Jerba than in Tabarka plants. Chlorophyll content, net photosynthetic rate, stomatal conductance (g s), and intracellular CO2 concentration were stimulated at moderate salinity (S100) in Jerba plants and inhibited at higher salt concentrations in both ecotypes: g s was the most reduced parameter. The maximum quantum efficiency of PS2 (Fv/Fm), quantum yield, linear electron transport rate, and efficiency of excitation energy capture by open PS2 reaction centres showed no significant changes with increasing salt concentration in Jerba plant and were decreased in Tabarka subjected to S400. However, the efficiency of dissipation of excess photon energy in the PS2 antenna was maintained in Jerba and was increased in Tabarka plants challenged with S400. Hence the relative salt tolerance of Jerba was associated with a better ability to use Na+ and Cl− for osmotic adjustment, the absence of pigment degradation, and the concomitant PS2 protection from photodamage.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
References
Abdelly, C., Lachâal, M., Grignon, C., Soltani, A., Hajji, M.: Association épisodique d’halophytes strictes et de glycophytes dans un écosystème hydromorphe salé en zone semisalé.-Agronomie 15: 557–568, 1995.
Adams, W.W., III, Volk, M., Hoehn, A., Demmig-Adams, B.: Leaf orientation and the response of xanthophyll cycle to incident light.-Oecologia 90: 404–410, 1992.
Ahmad, S., Wahid, A., Rasul, E., Wahid, A.: Comparative morphological and physiological responses of green gram genotypes to salinity applied at different growth stages.-Bot. Bull. Acad. sin. 46: 135–142, 2005.
Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris L.-Plant Physiol. 24: 1–15, 1949.
Aro, E.-M., McCaffery, S., Anderson, J.M.: Recovery from photoinhibition in peas (Pisum sativum L.) acclimated to varying growth irradiances. Role of D1 protein turnover.-Plant Physiol. 104: 1033–1041, 1994.
Baker, N.R., Rosenqvist, E.: Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities.-J. exp. Bot. 55: 1607–1621, 2004.
Bañuls, J., Primomilo, E.: Effects of chloride and sodium on gas exchange parameters and water relations of Citrus plants.-Physiol. Plant. 86: 115–123, 1992.
Belkhodja, R., Morales, F., Abadía, A., Gómez-Aparisi, J., Abadía, J.: Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.).-Plant Physiol. 104: 667–673, 1994.
Ben Amor, N., Jiménez, A., Megdiche, W., Lundqvist, M., Sevilla, F., Abdelly, C.: Response of antioxidant systems to NaCl stress in the halophyte Cakile maritima.-Physiol. Plant. 126: 446–457, 2006.
Bilger, W., Björkman, O.: Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in Hedera canariensis.-Photosynth. Res. 25: 173–185, 1990.
Bilger, W., Schreiber, U., Lange, O.L.: Chlorophyll fluorescence as an indicator of heat induced limitation of photosynthesis in Arbutus unedo L.-In: Tenhunen, J.D., Catarino, F.M., Lange, O.L., Oechel, W.C. (ed.): Plant Response to Stress. Pp. 391–399. Springer-Verlag, Berlin-Heidelberg-New York-London-Paris-Tokyo 1987.
Björkman, O., Demmig-Adams, B.: Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants.-In: Schulze, E.D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 17–47. Springer-Verlag, Berlin 1994.
Broetto, F., Duarte, H.M., Lüttge, Q.: Responses of chlorophyll fluorescence parameters of the facultative halophyte and C3-CAM intermediate species Mesembryanthemum crystallinum to salinity and high irradiance stress.-J. Plant Physiol. 164: 904–912, 2007.
Clark, H., Newton, P.C.D., Barker, D.J.: Physiological and morphological responses to elevated CO2 and a soil moisture deficit of temperate pasture species growing in an established plant community.-J. exp. Bot. 50: 233–242, 1999.
Davy, A.J., Scott, R., Cordazzo, C.V.: Biological flora of the British Isles: Cakile maritima Scop.-J. Ecol. 94: 695–711, 2006.
de Mattos, E.A., Herzog, B., Lüttge, U.: Chlorophyll fluorescence during CAM-phases in Clusia minor L. under drought stress.-J. exp. Bot. 50: 253–261, 1999.
de Pascale, S., Maggio, A., Fogliano, V., Ambrosino, P., Ritieni, A.: Irrigation with saline water improves carotenoids content and antioxidant activity of tomato.-J. hort. Sci. Biotech. 76: 447–453, 2001.
De Vos, C.H.R., Schat, H., Vooijs, R., Ernst, W.H.O.: Copper-induced damage to the permeability barrier in roots of Silene cucubalus.-J. Plant Physiol. 135: 164–169, 1989.
Debez, A., Saadaoui, D., Ramani, B., Ouerghi, Z., Koyro, H.-W., Huchzermeyer, B., Abdelly, C.: Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity.-Environ. exp. Bot. 57: 285–295, 2006.
Delfine, S., Alvino, A., Zacchini, M., Loreto, F.: Consequences of salt stress on conductance to CO2 diffusion, Rubisco characteristics and anatomy of spinach leaves.-Aust. J. Plant Physiol. 25: 395–402, 1998.
Demmig-Adams, B., Adams, W.W., III: Photoprotection and other responses of plants to high light stress.-Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 599–626, 1992.
Demmig-Adams, B., Adams, W.W., III: The role of xanthophyll cycle carotenoids in the protection of photosynthesis.-Trends Plant Sci. 1: 21–26, 1996.
Demmig-Adams, B., Adams, W.W., Barker, D.H., Logan, B.A., Bowling, D.R., Verhoeven, A.S.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation.-Physiol. Plant. 98: 253–264, 1996.
Dubey, R.S.: Protein synthesis by plants under stressful conditions.-In: Pessarakli, M. (ed.): Handbook of Plant and Crop Stress. Pp. 277–299. Marcel Dekker, New York 1994.
Everard, J.D., Gucci, R., Kahn, S.C., Flore, J.A., Loescher, W.H.: Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity.-Plant Physiol. 106: 281–292, 1994.
Flexas, J., Bota, J., Escalona, J.M., Sampol, B., Medrano, H.: Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations.-Funct. Plant Biol. 29: 461–471, 2002.
Foyer, C.H., Lelandais, M., Kunert, K.J.: Photooxidative stress in plants.-Physiol. Plant. 92: 696–717, 1994.
Gebauer, J., El-Siddig, K., Salih, A.A., Ebert, G.: Tamarindus indica L. seedlings are moderately salt tolerant when exposed to NaCl-induced salinity.-Sci. Horticult. 103: 1–8, 2004.
Genty, B., Briantais, J.-M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.-Biochim. biophys. Acta 990: 87–92, 1989.
Ghars, M.A., Debez, A., Smaoui, A., Zarrouk, M., Grignon, C., Abdelly, C.: Variability of fruit and seed-oil characteristics in Tunisian accessions of the halophyte Cakile maritima (Brassicaceae).-In: Khan, M.A., Weber, D.L. (ed.): Ecophysiology of High Salinity Tolerant Plants. Pp. 55–67. Springer, Berlin 2006.
Gilmore, A.M.: Mechanistic aspects of xanthophyll cycle-dependant photoprotection in higher plant chloroplast and leaves.-Physiol. Plant. 99: 197–209, 1997.
Haupt-Herting, S., Fock, H.P.: Exchange of oxygen and its role in energy dissipation during drought stress in tomato plants.-Physiol. Plant. 110: 489–495, 2000.
Havaux, M.: Carotenoids as membrane stabilizers in chloroplasts.-Trends Plant Sci. 3: 147–151, 1998.
Hewitt, E.J.: Sand and Water Culture Methods Used in the Study of Plant Nutrition.-Commonwealth Bureau of Horticulture tech. Rep. 22: 431–446, 1966.
Hocking, P.J.: Salt and mineral nutrient levels in fruits of two strand species, Cakile maritima and Arctotheca populifolia, with special reference to the effect of salt on the germination of Cakile.-Ann. Bot. 50: 335–343, 1982.
Hunt, R.: Basic Growth Analysis. Plant Growth Analysis for Beginners.-Unwin Hyman, London 1990.
Jagtap, V., Bhargava, S., Streb, P., Feierabend, J.: Comparative effect of water, heat and light stresses on photosynthetic reactions in Sorghum bicolor (L.) Moench.-J. exp. Bot. 49: 1715–1721, 1998.
Jaleel, C.A., Gopi, R., Manivannan, P., Panneerselvam, R.: Antioxidative potentials as a protective mechanism in Catharanthus roseus (L.) G. Don. plants under salinity stress.-Turk. J. Bot. 31: 245–251, 2007a.
Jaleel, C.A., Gopi, R., Sankar, B., Manivannan, P., Kishorekumar, A., Sridharan, R., Panneerselvam, R.: Alterations in germination, seedling vigour, lipid peroxidation and proline metabolism in Catharanthus roseus seedlings under salt stress.-S. afr. J. Bot. 73: 190–195, 2007b.
Jaleel, C.A., Manivannan, P., Lakshmanan, G.M.A., Sridharan, R., Panneerselvam, R.: NaCl as a physiological modulator of proline metabolism and antioxidant potential in Phyllanthus amarus.-Compt. rend. Biol. 330: 806–813, 2007c.
Kanhaiya, L.: Biochemical studies on relation to adaptability of sugarcane cultivars under saline soil.-Bharatia Suggestion 22: 23–26, 1996.
Keiller, D.R., Slocombe, S.P., Cockburn, W.: Analysis of chlorophyll a fluorescence in C3 and CAM forms of Mesembryanthemum crystallinum.-J. exp. Bot. 45: 325–334, 1994.
Koyro, H.-W.: Study of potential cash crop halophytes in a quick check system task.-Veget. Sci. 38: 5–17, 2003.
Koyro, H.-W.: Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.).-Environ. exp. Bot. 56: 136–146, 2006.
Krall, J.P., Edwards, G.E.: Relationship between photosystem II activity and CO2 fixation in leaves.-Physiol. Plant. 86: 180–187, 1992.
Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: The basics.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313–349, 1991.
Lakshmi, A., Ramanjulu, S., Veeranjaneyulu, K., Sudhakar, C.: Effect of NaCl on photosynthesis parameters in two cultivars of mulberry.-Photosynthetica 32: 285–289, 1996.
Lee, G., Carrow, R.N., Duncan, R.R.: Salinity tolerance of selected seashore paspalums and bermudagrasses: root and verdure responses and criteria.-Hort. Sci. 39: 1143–1147, 2004.
Leegood, R.C., Edwards, G.E.: Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors.-In: Baker, N.R. (ed.): Photosynthesis and the Environment. Pp. 191–221. Kluwer Academic Publ., Dordrecht-Boston-London 1996.
Lu, C., Jiang, G., Wang, B., Kuang, T.: Photosystem 2 photochemistry and photosynthetic pigment composition in salt-adapted halophyte Artemisia anethifolia grown under outdoor conditions.-J. Plant Physiol. 160: 403–408, 2003.
Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence — a practical guide.-J. exp. Bot. 51: 659–668, 2000.
Megdiche, W., Ben Amor, N., Debez, A., Hessini, K., Ksouri, R., Zuily-Fodil, Y., Abdelly, C.: Salt tolerance of the annual halophyte Cakile maritima as affected by the ecotype and the developmental stage.-Acta Physiol. Plant. 29: 375–384, 2007.
Misra, A.J., Sahu, S.M., Misra, M., Singh, P., Meera, I., Das, N., Kar, M., Shau, P.: Sodium chloride induced changes in leaf growth, and pigment and protein contents in two rice cultivars.-Biol. Plant. 39: 257–262, 1997.
Misra, A.N., Srivastava, A., Strasser, R.J.: Utilization of fast chlorophyll a fluorescence technique in assessing the salt/ion sensitivity of mung bean and Brassica seedlings.-J. Plant Physiol. 158: 1173–1181, 2001.
Munns, R.: Comparative physiology of salt and water stress.-Plant Cell Environ. 25: 239–250, 2002.
Noctor, G., Gomez, L., Vanacker, H., Foyer, C.H.: Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling.-J. exp. Bot. 53: 1283–1304, 2002.
Owens, S.: Salt of the earth.-EMBO Rep. 2: 877–879, 2001.
Parida, A.K., Das, A.B.: Salt tolerance and salinity effects on plants: a review.-Ecotoxicol. environ. Safety 60: 324–349, 2005.
Qiu, N., Lu, Q., Lu, C.: Photosynthesis, photosystem II efficiency and the xanthophyll cycle in the salt-adapted halophyte Atriplex centralasiatica.-New Phytol. 159: 479–486, 2003.
Ranjbarfordoei, A., Samson, R., Lemeur, R., Van Damme, P.: Effects of osmotic drought stress induced by a combination of NaCl and polyethylene glycol on leaf water status, photosynthetic gas exchange, and water use efficiency of Pistacia khinjuk and P. mutica.-Photosynthetica 40: 165–169, 2002.
Ranjbarfordoei, A., Samson, R., Van Damme, P.: Chlorophyll fluorescence performance of sweet almond [Prunus dulcis (Miller) D. Webb] in response to salinity stress induced by NaCl.-Photosynthetica 44: 513–522, 2006.
Roháček, K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships.-Photosynthetica 40: 13–29, 2002.
Rouhi, V., Samson, R., Lemeur, R., Van Damme, P.: Photosynthetic gas exchange characteristics in three different almond species during drought stress and subsequent recovery.-Environ. exp. Bot. 52: 117–129, 2007.
Schönfeld, M.A., Johnson, R.C., Carver, B.F., Mornhinweg, D.W.: Water relations in winter wheat as drought resistance indicator.-Crop Sci. 28: 526–531, 1988.
Schreiber, U., Bilger, W., Neubauer, C.: Chlorophyll fluorescence as a non-invasive indicator for rapid assessment of in vivo photosynthesis.-In: Schulze, E.-D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 49–70. Springer-Verlag, Berlin-Heidelberg-New York 1995.
Schreiber, U., Schliwa, U., Bilger, W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.-Photosynth. Res. 10: 51–62, 1986.
Singh, A.K., Dubey, R.S.: Changes in chlorophyll a and b contents and activities of photosystems 1 and 2 in rice seedlings induced by NaCl.-Photosynthetica 31: 489–499, 1995.
Sixto, H., Aranda, I., Grau, J.M.: Assessment of salt tolerance in Populus alba clones using chlorophyll fluorescence.-Photosynthetica 44: 169–173, 2006.
Slama, I., Ghnaya, T., Savoure, A., Abdelly, C.: Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum.-Compt. Rend. Biol. in press, 2008.
Torrecillas, A., León, A., Del Amor, F., Mártinez-Monpeán, M.C.: [Rapid determination of chlorophyll in leaf discs of lemon tree.]-Fruits 39: 617–622, 1984.
Van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology.-Photosynth. Res. 25: 147–150, 1990.
Wahid, A., Hameed, M., Rasul, E.: Salt-induced injury symptoms, changes in nutrient and pigment composition, and yield characteristics of mungbean.-Integr. J. agr. Biol. 6: 1143–1152, 2004.
Wang, Y., Meng, Y.-L., Ishikawa, H., Hibino, T., Tanaka, Y., Nii, N., Takabe, T.: Photosynthetic adaptation to salt stress in three-color leaves of a C4 plant Amaranthus tricolor.-Plant Cell Physiol. 40: 668–674, 1999.
Yamane, Y., Shikanai, T., Kashino, Y., Koike, H., Satoh, K.: Reduction of QA in the dark: Another cause of fluorescence Fo increases by high temperatures in higher plants.-Photosynth. Res. 63: 23–34, 2000.
Zhao, G.Q., Ma, B.L., Ren, C.Z.: Growth, gas exchange, chlorophyll fluorescence, and ion content of naked oat in response to salinity.-Crop Sci. 47: 123–131, 2007.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Megdiche, W., Hessini, K., Gharbi, F. et al. Photosynthesis and photosystem 2 efficiency of two salt-adapted halophytic seashore Cakile maritima ecotypes. Photosynthetica 46, 410–419 (2008). https://doi.org/10.1007/s11099-008-0073-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-008-0073-1