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Involvement of betacyanin in chilling-induced photoinhibition in leaves of Suaeda salsa

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Photosynthetica

Abstract

Seeds of Suaeda salsa were cultured in dark for 3 d and betacyanin accumulation in seedlings was promoted significantly. Then the seedlings with accumulated betacyanin (C+B) were transferred to 14/10 h light/dark and used for chilling treatment 15 d later. Photosystem 2 (PS2) photochemistry, D1 protein content, and xanthophyll cycle during the chilling-induced photoinhibition (exposed to 5 °C at a moderate photon flux density of 500 µmol m−2 s−1 for 3 h) and the subsequent restoration were compared between the C+B seedlings and the control (C) ones. The maximal efficiency of PS2 photochemistry (Fv/Fm), the efficiency of excitation energy capture by open PS2 centres (Fv′/Fm′), and the yield of PS2 electron transport (ΦPS2) of the C+B and C leaves both decreased during photoinhibition. However, smaller decreases in Fv/Fm, Fv′/Fm′, and ΦPS2 were observed in the C+B leaves than in C ones. At the same time, the deepoxidation state of xanthophyll cycle, indicated by (A+Z)/(V+A+Z) ratio, increased rapidly but the D1 protein content decreased considerably during the photoinhibition. The increase in rate of (A+Z)/(V+A+Z) was higher but the D1 protein turnover was slower in C+B than C leaves. After photoinhibition treatment, the plants were transferred to a dim irradiation (10 µmol m−2 s−1) at 25 °C for restoration. During restoration, the chlorophyll (Chl) fluorescence parameters, D1 protein content, and xanthophyll cycle components relaxed gradually, but the rate and level of restoration in the C+B leaves was greater than those in the C leaves. The addition of betacyanins to the thylakoid solution in vitro resulted in similar changes of Fv/Fm, D1 protein content, and (A+Z)/(V+A+Z) ratio during the chilling process. Therefore, betacyanin accumulation in S. salsa seedlings may result in higher resistance to photoinhibition, larger slowing down of D1 protein turnover, and enhancement of non-radiative energy dissipation associated with xanthophyll cycle, as well as in greater restoration after photoinhibition than in the control when subjected to chilling at moderate irradiance.

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References

  • Aro, E.-M., Hundal, T., Carlberg, I., Andersson, B.: In vitro studies on light-induced inhibition of Photosystem II and D1-protein degradation at low temperatures.-Biochim. biophys. Acta 1019: 269–275, 1990.

    Article  CAS  Google Scholar 

  • Aro, E.-M., McCaffery, S., Anderson, J.M.: Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances.-Plant Physiol. 103: 835–843, 1993.

    PubMed  CAS  Google Scholar 

  • Aro, E.-M., Virgin, I., Andersson, B.: Photoinhibition of Photosystem II. Inactivation, protein damage and turnover.-Biochim. biophys. Acta 1143: 113–134, 1993.

    Article  PubMed  CAS  Google Scholar 

  • Barbato, R., Friso, G., Giardi, M.T., Rigoni, F., Giacometti, G.M.: Breakdown of the photosystem II reaction center D1 protein under photoinhibitory conditions: identification and localization of the C-terminal degradation products.-Biochemistry 30: 10220–10226, 1991.

    Article  PubMed  CAS  Google Scholar 

  • Barber, J.: Molecular basis of the vulnerability of photosystem II to damage by light.-Aust. J. Plant Physiol. 22: 201–208, 1994.

    Article  Google Scholar 

  • Butera, D., Tesoriere, L., Di Gaudio, F., Bongiorno, A., Allegra, M., Pintaudi, A.M., Kohen, R., Livrea, M.A.: Antioxidant activities of sicilian prickly pear (Opuntia ficus indica) fruit extracts and reducing properties of its betalains: betanin and indicaxanthin.-J. agr. Food Chem. 50: 6895–6901, 2002.

    Article  CAS  Google Scholar 

  • Cai, Y., Sun, M., Corke, H.: Antioxidant activity of betalains from plants of the Amaranthaceae.-J. agr. Food Chem. 51: 2288–2294, 2003.

    Article  CAS  Google Scholar 

  • Clement, J.S., Mabry, T.J.: Pigment evolution in the Caryophyllales: a systematic overview.-Bot. Acta 109: 360–367, 1996.

    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 

  • Dörnenburg, H., Knorr, D.: Generation of colors and flavours in plant cell and tissue cultures.-Crit. Rev. Plant Sci. 15: 141–168, 1996.

    Google Scholar 

  • Foyer, C.H.: Oxygen metabolism and electron transport in photosynthesis.-In: Scandalios, J.G. (ed.): Oxidative Stress and the Molecular Biology of Antioxidant Defenses. Pp. 587–621. Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1997.

    Google Scholar 

  • Genty, B., Briantais, J.-M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of Chl fluorescence.-Biochim. biophys. Acta 990: 87–92, 1989.

    CAS  Google Scholar 

  • Harbinson, J., Genty, B., Baker, N.R.: Relationship between the quantum efficiencies of photosystems I and II in pea leaves.-Plant Physiol. 90: 1029–1034, 1989.

    PubMed  CAS  Google Scholar 

  • Haussühl, K., Andersson, B., Adamska, I.: A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II.-EMBO J. 20: 713–722, 2001.

    Article  PubMed  Google Scholar 

  • Hideg, É., Spetea, C., Vass, I.: Singlet oxygen and free radical production during acceptor-and donor-side-induced photoinhibition. Studies with spin trapping EPR spectroscopy.-Biochim. biophys. Acta 1186: 143–152, 1994.

    Article  CAS  Google Scholar 

  • Huner, N.P.A., Öquist, G., Hurry, V.M., Krol, M., Falk, S., Griffith, M.: Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants.-Photosynth. Res. 37: 19–39, 1993.

    Article  CAS  Google Scholar 

  • Ibdah, M., Krins, A., Seidlitz, H.K., Heller, W., Strack, D., Vogt, T.: Spectral dependence of flavonol and betacyanin accumulation in Mesembryanthemum crystallinum under enhanced ultraviolet radiation.-Plant Cell Environ. 25: 1145–1154, 2002.

    Article  CAS  Google Scholar 

  • Jennings, R.C., Garlaschi, F.M., Gerola, P.D., Etzion-Katz, R., Forti, G.: Proton-induced grana formation in chloroplasts. Distribution of Chl-protein complexes and photosystem II photochemistry.-Biochim. biophys. Acta 638: 100–107, 1981.

    Article  CAS  Google Scholar 

  • Ji, B.H., Jiao, D.M.: Photoinhibition and photooxidation in leaves of indica and japonica rice (Oryza sativa L.) under different temperatures and light intensities.-Acta bot. sin. 43: 714–720, 2001.

    CAS  Google Scholar 

  • Kraay, G.W., Zapata, M., Veldhuis, M.J.W.: Separation of chlorophylls c 1, c 2, and c 3 of marine phytoplankton by reversedphase-C18-high-performance liquid chromatography.-J. Phycol. 28: 708–712, 1992.

    Article  CAS  Google Scholar 

  • Kramer, H., Mathis, P.: Quantum yield and rate of formation of the carotenoid triplet state in photosynthetic structures.-Biochim. biophys. Acta 593: 319–329, 1980.

    Article  PubMed  CAS  Google Scholar 

  • Leitsch, J., Schnettger, B., Critchley, C., Krause, G.H.: Two mechanisms of recovery from photoinhibition in vivo: Reactivation of photosystem II related and unrelated to D1-protein turnover.-Planta 194: 15–21, 1994.

    Article  CAS  Google Scholar 

  • Lindahl, M., Spetea, C., Hundal, T., Oppenheim, A.B., Adam, Z., Andersson, B.: The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein.-Plant Cell 12: 419–431, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Mackinney, G.: Absorption of light by chlorophyll solutions.-J. biol. Chem. 140: 315–322, 1941.

    CAS  Google Scholar 

  • Macpherson, A.N., Telfer, A., Barber, J., Truscott, T.G.: Direct detection of singlet oxygen from isolated Photosystem II reaction centres.-Biochim. biophys. Acta 1143: 301–309, 1993.

    Article  CAS  Google Scholar 

  • Okuda, T., Matsuda, Y., Yamanaka, A., Sagisaka, S.: Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment.-Plant Physiol. 97: 1265–1267, 1991.

    Article  PubMed  CAS  Google Scholar 

  • Osmond, C.B.: What is photoinhibition? Some insights from comparisons of shade and sun plants.-In: Baker, N.R., Bowyer, J.R. (ed.): Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. Pp. 1–24. BIOS Scientific Publ., Oxford 1994.

    Google Scholar 

  • Park, Y.I., Chow, W.S., Anderson, J.M.: Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure.-Planta 196: 401–411, 1995.

    Article  CAS  Google Scholar 

  • Pedreňo, M.A., Escribano, J.: Correlation between antiradical activity and stability of betanine from Beta vulgaris L roots under different pH, temperature and light conditions.-J. Sci. Food Agr. 81: 627–631, 2001.

    Article  Google Scholar 

  • Prášil, O., Adir, N., Ohad, I.: Dynamics of photosystem II: Mechanism of photoinhibition and recovery processes.-In: Barber, J. (ed.): The Photosystems: Structure, Function and Molecular Biology. Pp. 295–348. Elsevier, Amsterdam 1992.

    Google Scholar 

  • Russell, A.W., Critchley, C., Robinson, S.A., Franklin, L.A., Seaton, G.G.R., Chow, W.S., Anderson, J.M., Osmond, C.B.: Photosystem II regulation and dynamics of the chloroplast D1 protein in Arabidopsis leaves during photosynthesis and photoinhibition.-Plant Physiol. 107: 943–952, 1995.

    PubMed  CAS  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 

  • Sepúlveda-Jiménez, G., Rueda-Benitez, P., Porta, H., Rocha-Sosa, M.: Betacyanin synthesis in red beet (Beta vulgaris) leaves induced by wounding and bacterial infiltration is preceded by an oxidative burst.-Physiol. mol. Plant Pathol. 64: 125–133, 2004.

    Article  CAS  Google Scholar 

  • Sepúlveda-Jiménez, G., Rueda-Benitez, P., Porta, H., Rocha-Sosa, M.: A red beet (Beta vulgaris) UDP-glucosyltransferase gene induced by wounding, bacterial infiltration and oxidative stress.-J. exp. Bot. 56: 605–611, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Shipton, C.A., Barber, J.: Characterization of photoinduced breakdown of the D1-polypeptide in isolated reaction centres of photosystem II.-Biochim. biophys. Acta 1099: 85–90, 1992.

    Article  PubMed  CAS  Google Scholar 

  • Sonoike, K.: The different roles of chilling temperatures in the photoinhibition of photosystem I and photosystem II.-J. Photochem. Photobiol. B 48: 136–141, 1999.

    Article  CAS  Google Scholar 

  • Stafford, H.A.: Anthocyanins and betalains: evolution of the mutually exclusive pathways.-Plant Sci. 101: 91–98, 1994.

    Article  CAS  Google Scholar 

  • Steglich, W., Strack, D.: Betalains.-In: Brossi, A. (ed.): The Alkaloids, Chemistry and Pharmacology. Pp. 1–62. Academic Press, London 1990.

    Google Scholar 

  • Stingtzing, F.C., Carle, R.: Functional properties of betacyanins and betalains in plants, food, and in human nutrition.-Trends Food Sci. Technol. 15: 19–38, 2004.

    Article  CAS  Google Scholar 

  • Thiele, A., Schirwitz, K., Winter, K., Krause, G.H.: Increased xanthophyll cycle activity and reduced D1 protein inactivation related to photoinhibition in two plant systems acclimated to excess light.-Plant Sci. 115: 237–250, 1996.

    Article  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 

  • Vass, I., Styring, S., Hundal, T., Koivuniemi, A., Aro, E.M., Andersson, B.: Reversible and irreversible intermediates during photoinhibition of photosystem II: Stable reduced QA species promote chlorophyll triplet formation.-Proc. nat. Acad. Sci. USA 89: 1408–1412, 1992.

    Article  PubMed  CAS  Google Scholar 

  • Virgin, I., Styring, S., Andersson, B.: Photosystem II disorganization and manganese release after photoinhibition of isolated spinach thylakoid membranes.-FEBS Lett. 233: 408–412, 1988.

    Article  CAS  Google Scholar 

  • Vogt, T., Ibdah, M., Schmidt, J., Wray, V., Nimtz, M., Strack, D.: Light induced betacyanin and flavonols accumulation in bladder cells of Mesembryanthemum crystallinum.-Phytochemistry 52: 583–592, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Wang, C.Q., Chen, M., Wang, B.S.: Betacyanin accumulation in the leaves of C3 halophyte Suaeda salsa L. is induced by watering roots with H2O2.-Plant Sci. 172: 1–7, 2007.

    Article  CAS  Google Scholar 

  • Wang, C.Q., Liu, T.: Cryptochrome 2 is involved in betacyanin decomposition induced by blue light in Suaeda salsa.-Funct. Plant Biol. 33: 697–702, 2006.

    Article  CAS  Google Scholar 

  • Wang, C.Q., Zhao, J.Q., Chen, M., Wang, B.S.: Identification of betacyanin and effects of environmental factors on its accumulation in halophyte Suaeda salsa.-J. Plant Physiol. mol. Biol. 31: 195–201, 2006.

    Google Scholar 

  • Wise, R.R.: Chilling-enhanced photooxidation: the production, action and study of reactive oxygen species produced during chilling in the light.-Photosynth. Res. 45: 79–97, 1995.

    Article  CAS  Google Scholar 

  • Zhao, K.F.: The Halophytes in China.-Science Press of China, Beijing 1998.

    Google Scholar 

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  1. College of Life Science, Shandong University of Technology, Zibo City, Shandong, 255049, China

    C.-Q. Wang & T. Liu

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  1. C.-Q. Wang
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Wang, CQ., Liu, T. Involvement of betacyanin in chilling-induced photoinhibition in leaves of Suaeda salsa . Photosynthetica 45, 182–188 (2007). https://doi.org/10.1007/s11099-007-0030-4

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