Photosynthetica 2003, 41(2):191 | DOI: 10.1023/B:PHOT.0000011951.37231.69

Effects of NaCl Stress on the Structure, Pigment Complex Composition, and Photosynthetic Activity of Mangrove Bruguiera parviflora Chloroplasts

A.K. Parida1, A.B. Das1,2, B. Mittra3
1 National Institute for Plant Biodiversity Conservation and Research, Nayapalli, Bhubaneswar, Orissa, India
2 Regional Plant Resource Centre, Nayapalli, Bhubaneswar, Orissa, India
3 Centre for Environmental Management of Degraded Ecosystems, School of Environmental Studies, North Campus, University of Delhi, Delhi-, India

Exposure of two-month-old seedlings of Bruguiera parviflora to NaCl stress (0 to 400 mM) for 45 d under hydroponic culture caused notable disorganisation of the thylakoid structure of chloroplasts in NaCl-treated leaves as revealed from transmission electron microscopy. The absorption spectra of treated and control thylakoid samples were similar having a red peak at 680 nm and Soret peaks at 439 and 471 nm in the blue region of the spectrum. The spectra of treated samples differed from control samples by gradual decrease in absorbance of 100, 200, and 400 mM NaCl treated samples at 471 and 439 nm, which could be due to scattering of radiation in these samples. Thus, absorption characteristics of thylakoid membranes indicated no major alterations in the structural integrity of the photosynthetic membranes during salt stress in B. parviflora. Analysis of pigment protein complexes of thylakoids on non-denaturing gel showed that CP1 complex consisting of photosystem (PS) 1 reaction centre decreased marginally by 19% and the CP47 constituting the core antenna of PS2 declined significantly by 30% in 400 mM NaCl treated samples in respect to control. This decrease in structural core antenna might cause inefficient photon harvesting capacity. However, CP43 content did not alter. An increase in CP2/CP1 ratio from 3.2 in control to 4.0 in 400 mM NaCl treated samples indicated significant structural changes in the thylakoids of salt treated plants. Haem staining of thylakoids revealed significant losses in cytochrome (Cyt)f and Cyt b 6 contents by NaCl stress. However, Cyt b 559 content remained nearly constant in both control and NaCl treated samples. SDS-PAGE of thylakoid proteins showed that the intensity of many of Coomassie stained polypeptide bands ranging from 15-22 and 28-66 kDa regions decreased significantly in NaCl treated samples as compared to control. Electron transport activity of thylakoids, measured in terms of DCPIP photoreduction, was 22% lower in 400 mM NaCl treated plants than in the control ones. Hence, NaCl induces oxidative stress in chloroplasts causing structural alterations in thylakoids. These structural alterations might be responsible for declined efficiency of photosystems and reduced electron transport activity.

Additional key words: electron transport; hydroponic plants; light-harvesting complexes; pigment-protein complexes; photosystems; polypeptides; salt stress; thylakoids

Published: June 1, 2003  Show citation

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Parida, A.K., Das, A.B., & Mittra, B. (2003). Effects of NaCl Stress on the Structure, Pigment Complex Composition, and Photosynthetic Activity of Mangrove Bruguiera parviflora Chloroplasts. Photosynthetica, 41(2), 191. doi: 10.1023/B:PHOT.0000011951.37231.69
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    References

    1. Adams, P., Thomas, J.C., Vernon, D.M., Bohnert, H.J., Jensen, R.G.: Distinct cellular and organismic responses to salt stress. - Plant Cell Physiol. 33: 1215-1223, 1992.
    2. Allakhverdiev, S.I., Sakamoto, A., Nishiyama, Y., Inaba, M., Murata, N.: Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. - Plant Physiol. 123: 1047-1056, 2000a. Go to original source...
    3. Allakhverdiev, S.I., Sakamoto, A., Nishiyama, Y., Murata, N.: Inactivation of photosystems I and II in response to osmotic stress in Synechococcus: contribution of water channels. - Plant Physiol. 122: 1201-1208, 2000b. Go to original source...
    4. Allen, J.F., Holmes, N.G.: Electron transport and redox titrations. - In: Hipkins, M.F., Baker, N.R. (ed.): Photosynthesis - Energy Transduction - a Practical Approach. Pp. 103-141. IRL Press, Oxford 1986.
    5. Bansal, K.C., Sabat, S.C., Abrol, Y.P.: Thylakoid Hill activity in relation to ploidy in wheat. - Photosynthetica 25: 307-311, 1991.
    6. Bruns, S., Hecht-Buchholz, C.: Light and electron microscope studies on the leaves of several potato cultivars after application of salt at various developmental stages. - Potato Res. 33: 33-41, 1990. Go to original source...
    7. Burguess, J.: An Introduction to Plant Cell Development. 1st Ed. - Pp. 42-47. Cambridge University Press, Cambridge 1985.
    8. Das, P., Basak, U.C., Das, A.B.: Restoration of mangrove vegetation in mahanadi delta of Orissa, India. - Mangroves Saltmarshes 1: 155-161, 1997. Go to original source...
    9. De la Torre, W.R. Burkey, K.O.: Acclimation of barley to change in light intensity: photosynthetic electron transport activity and components. - Photosynth. Res. 24: 127-136, 1990. Go to original source...
    10. Delepelaire, P, Chua, N.-H.: Lithium dodecyl sulfate/polyacrylamide gel electrophoresis of thylakoid membranes at 4 ºC: Characterizations of two additional chlorophyll a-protein complexes. - Proc. nat. Acad. Sci. USA 76: 111-115, 1979. Go to original source...
    11. Delphine, 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. Go to original source...
    12. Flowers, T.J., Troke, P.F., Yeo, A.R.: The mechanism of salt tolerance in halophytes. - Annu. Rev. Plant Physiol. 28: 89-121, 1977. Go to original source...
    13. Green, B.R.: The chlorophyll-protein complexes of higher plant photosynthetic membranes, or Just what green band is that? - Photosynth. Res. 15: 3-32, 1988. Go to original source...
    14. Harding, S.A., Guikema, J.A., Paulsen, G.M.: Photosynthetic decline from high temperature stress during maturation of wheat. I. Interaction with senescence processes. - Plant Physiol. 92: 648-653, 1990. Go to original source...
    15. Hasegawa, P.M., Bressan, R.A., Zhu, J.-K., Bohnert, H.J.: Plant cellular and molecular responses to high salinity. - Annu. Rev. Plant Physiol. Plant mol. Biol. 51: 463-499, 2000. Go to original source...
    16. Hernández, J.A., Olmos, E., Corpas, F.J., Sevilla, F., del Rio, L.A.: Salt-induced oxidative stress in chloroplasts of pea plants. - Plant Sci. 105: 151-167, 1995. Go to original source...
    17. Hoagland, D.R., Arnon, D.I.: Crop production in artificial solutions and in soil with special reference to factors influencing yield and absorption of inorganic nutrients. - Soil Sci. 50: 463-471, 1940.
    18. Holloway, P.J., Maclean, D.J., Scott, K.J.: Rate-limiting steps of electron transport in chloroplasts during ontogeny and senescence of barley. - Plant Physiol. 72: 795-801, 1983. Go to original source...
    19. Høyer-Hensen, G.: Identification of haem proteins in thylakoid polypeptide patterns of barley. - Carlsberg Res. Commun. 45: 167-176, 1980. Go to original source...
    20. Kao, W.-Y, Tsai, H.-C.: The photosynthesis and chlorophyll a fluorescence in seedlings of Kandelia candel (L.) Druce grown under different nitrogen and NaCl controls. - Photosynthetica 37: 405-412, 1999. Go to original source...
    21. Khavari-Nejad, R.A., Mostofi, Y.: Effects of NaCl on photosynthetic pigments, saccharides, and chloroplast ultrastructure in leaves of tomato cultivars. - Photosynthetica 35: 151-154, 1998. Go to original source...
    22. Kuwabara, T., Murata, N.: Inactivation of photosynthetic oxygen evolution and concomitant release of three polypeptides in the photosystem II particles of spinach chloroplasts. - Plant Cell Physiol. 23: 533-539, 1982. Go to original source...
    23. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. - Nature 227: 680-685, 1970. Go to original source...
    24. Leong, A.L., Anderson, J.M.: Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. I. Study on the distribution of chlorophyll-protein complexes. - Photosynth. Res. 5: 105-109, 1984. Go to original source...
    25. Lichtenthaler, H.K.: Chlorophylls and carotenoids - pigments of photosynthetic biomembranes. - In: Colowick, S.P., Kaplan, N.O. (ed.): Methods in Enzymology. Vol. 148. Pp. 350-382. Academic Press, San Diego - New York - Berkeley - Boston - London - Sydney - Tokyo - Toronto 1987. Go to original source...
    26. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J.: Protein measurement with the Folin phenol reagent. - J. biol. Chem. 193: 265-275, 1951. Go to original source...
    27. Mallery, C.H., Teas, H.J.: The mineral ion relations of mangroves. I. Root cell compartments in a salt excluder and a salt excreter species at low salinities. - Plant Cell Physiol. 25: 1123-1131, 1984.
    28. Mitsuya, S., Takeoka, Y., Miyake, H.: Effects of sodium chloride on foliar ultrastructure of sweet potato (Ipomoea batatas Lam.) plantlets grown under light and dark conditions in vitro. - J. Plant Physiol. 157: 661-667, 2000. Go to original source...
    29. Miyao, M., Murata, N.: Calcium ions can be substituted for the 24-kDa polypeptide in photosynthetic oxygen evolution. - FEBS Lett. 168: 118-120, 1984. Go to original source...
    30. Muranaka, S., Shimizu, K., Kato, M.: A salt-tolerant cultivar of wheat maintains photosynthetic activity by suppressing sodium uptake. - Photosynthetica 40: 509-515, 2002. Go to original source...
    31. Murata, N., Mohanty, P.S., Hayashi, H., Papageorgiou, G.: Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. - FEBS Lett. 296: 187-189, 1992. Go to original source...
    32. Nakatani, H.Y., Barber, J.: An improved method for isolating chloroplasts retaining their outer membranes. - Biochim. biophys. Acta 461: 510-512, 1977. Go to original source...
    33. Nazarenko, L.V., Serebryakova, V.N.: [Ultrastructural changes in Euglena cells of different nutritional types under the influence of salinity.] - Fiziol. Rast. 37: 142-146, 1990. [In Russ.]
    34. Öquist, G., Samuelsson, G., Bishop, N.I.: On the role of β-carotene in the reaction center chlorophyll a antennae of photosystem I. - Physiol. Plant. 50: 63-70, 1980. Go to original source...
    35. Parida, A.K., Das, A.B., Das, P.: NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. - J. Plant Biol. 45: 28-36, 2002. Go to original source...
    36. Prasad, S.M., Singh, J.B, Rai, L.C., Kumar, H.D.: Metal-induced inhibition of photosynthetic electron transport chain of the cyanobacterium Nostoc muscorum. - FEMS Microbiol. Lett. 82: 95-100, 1991. Go to original source...
    37. Robinson, S.P.: Transport of glycerate across the envelope membrane of isolated spinach chloroplasts. - Plant Physiol. 70: 1032-1038, 1982. Go to original source...
    38. Scholander, P.F.: How mangroves desalinate seawater. - Physiol. Plant. 21: 251-261, 1968. Go to original source...
    39. Staehelin, L.A., Van der Staay, G.W.M.: Structure, composition, functional organization and dynamic properties of thylakoid membranes. - In: Ort, D.R., Yocum, C.F. (ed.): Oxygenic Photosynthesis. The Light Reactions. Pp. 11-30. Kluwer Academic Publishers, Dordrecht - Boston - London 1996. Go to original source...
    40. Takemura, T., Hanagata, N., Sugihara, K., Baba, S., Karube, I., Dubinsky, Z.: Physiological and biochemical responses to salt stress in the mangrove, Bruguiera gymnorrhiza. - Aquat. Bot. 68: 15-28, 2000. Go to original source...
    41. Tiwari, B.S., Bose, A., Ghosh, B.: Photosynthesis in rice under a salt stress. - Photosynthetica 34: 303-306, 1997. Go to original source...
    42. Tomlinson, P.B.: The Botany of Mangroves. - Cambridge University Press, Cambridge 1986.
    43. Tripathy, B.C., Bhatia, B., Mohanty, P.: Inactivation of chloroplast photosynthetic electron-transport activity by Ni2+. - Biochim. biophys. Acta 638: 217-224, 1981. Go to original source...
    44. Tripathy, B.C., Mohanty, P.: Zinc-inhibited electron transport of photosynthesis in isolated barley chloroplasts. - Plant Physiol. 66: 1174-1180, 1980. Go to original source...
    45. Valcke, R., van Poucke, M.: The effect of water stress on greening of primary barley (Hordeum vulgare L. cv. Menuet) leaves. - In: Marcelle, R., Clijsters, H., van Poucke, M. (ed.): Effects of Stress on Photosynthesis. Pp. 141-150. Martinus Nijhoff/Dr W. Junk Publ., The Hague - Boston - London 1983. Go to original source...
    46. Vani, B.: Studies on High Temperature Induced Alterations in Photochemical Activities in Oryza sativa. - Ph.D. Thesis. Jamia Millia Islamia, New Delhi 1998.
    47. Vani, B., Pardha Saradhi, P., Mohanty, P.: Characterization of high temperature induced stress impairments in thylakoids of rice seedlings. - Indian J. exp. Biol. 38: 220-229, 2001.
    48. Werner, A., Stelzer, R,: Physiological responses of the mangrove Rhizophora mangle grown in the absence and presence of NaCl. - Plant Cell Environ. 13: 243-255, 1990. Go to original source...
    49. Wignarajah, K., Baker, N.R.: Salt induced responses of chloroplast activities in species of differing salt tolerance. Photosynthetic electron transport in Aster tripolium and Pisum sativum. - Physiol. Plant. 51: 387-393, 1981. Go to original source...

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