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Photosynthesis and photosystem 2 efficiency of two salt-adapted halophytic seashore Cakile maritima ecotypes

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Photosynthetica

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.

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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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris L.-Plant Physiol. 24: 1–15, 1949.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Davy, A.J., Scott, R., Cordazzo, C.V.: Biological flora of the British Isles: Cakile maritima Scop.-J. Ecol. 94: 695–711, 2006.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Foyer, C.H., Lelandais, M., Kunert, K.J.: Photooxidative stress in plants.-Physiol. Plant. 92: 696–717, 1994.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Gilmore, A.M.: Mechanistic aspects of xanthophyll cycle-dependant photoprotection in higher plant chloroplast and leaves.-Physiol. Plant. 99: 197–209, 1997.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Havaux, M.: Carotenoids as membrane stabilizers in chloroplasts.-Trends Plant Sci. 3: 147–151, 1998.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Hunt, R.: Basic Growth Analysis. Plant Growth Analysis for Beginners.-Unwin Hyman, London 1990.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kanhaiya, L.: Biochemical studies on relation to adaptability of sugarcane cultivars under saline soil.-Bharatia Suggestion 22: 23–26, 1996.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Koyro, H.-W.: Study of potential cash crop halophytes in a quick check system task.-Veget. Sci. 38: 5–17, 2003.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Krall, J.P., Edwards, G.E.: Relationship between photosystem II activity and CO2 fixation in leaves.-Physiol. Plant. 86: 180–187, 1992.

    Article  CAS  Google Scholar 

  • Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: The basics.-Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313–349, 1991.

    Article  CAS  Google Scholar 

  • Lakshmi, A., Ramanjulu, S., Veeranjaneyulu, K., Sudhakar, C.: Effect of NaCl on photosynthesis parameters in two cultivars of mulberry.-Photosynthetica 32: 285–289, 1996.

    CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence — a practical guide.-J. exp. Bot. 51: 659–668, 2000.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Owens, S.: Salt of the earth.-EMBO Rep. 2: 877–879, 2001.

    PubMed  CAS  Google Scholar 

  • Parida, A.K., Das, A.B.: Salt tolerance and salinity effects on plants: a review.-Ecotoxicol. environ. Safety 60: 324–349, 2005.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Roháček, K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships.-Photosynthetica 40: 13–29, 2002.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Sixto, H., Aranda, I., Grau, J.M.: Assessment of salt tolerance in Populus alba clones using chlorophyll fluorescence.-Photosynthetica 44: 169–173, 2006.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology.-Photosynth. Res. 25: 147–150, 1990.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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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

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