Photosynthetica, 2010 (vol. 48), issue 3

Photosynthetica 2010, 48(3):457-468 | DOI: 10.1007/s11099-010-0060-1

Influence of low temperatures on photosystem II photochemistry and expression of the NADPH:protochlorophyllide oxidoreductase in the alpine, subnival perennial, Chorispora bungeana

Y. H. Li1, Z. L. Sun1, X. L. Xu1, M. Jin1, Y. J. Liu1, H. Zhang1, L. Z. An1,*
1 Key Laboratory of Arid and Pasture Agroecology of Ministry of Education, School of Life Sciences, Lanzhou University, Lanzhou, Gansu, P.R. China

Low temperature significantly influences chloroplast development and chlorophyll (Chl) biosynthesis, so effect of coldness on Chl content and Chl fluorescence characteristics was investigated in C. bungeana (Chorispora bungeana Fisch. & C.A. Mey). The levels of transcript and protein of an enzymatic step during Chl biosynthesis in response to chilling (4°C) and freezing (-4°C) were also examined in this work. Significant reduction in total Chl content was observed, but the reduction was much less at 4°C than that at -4°C. Moreover, the maximal quantum efficiency of photosystem II (PSII) photochemistry, indicated by Fv/Fm, decreased in the first 12 h, but then started to increase and reached higher levels than the control at 24 h and 48 h at 4°C, but decreased continuously at -4°C. Whereas quantum yield of PSII (ΦPSII) showed no significant difference between the chilling-stressed and the control seedlings, at -4°C, ΦPSII was markedly reduced with the prolonged treatment. In general, there were no significant responses of photochemical quenching (qP) and non-photochemical quenching (NPQ) to cold treatment. Meanwhile, the full-length cDNA of NADPH:protochlorophyllide oxidoreductase (POR, EC 1.3.1.33) was isolated and termed CbPORB (GenBank Accession No. FJ390503). Its transcript and protein content only slightly declined at 4°C, but dramatically reduced at -4°C with the time. These results strongly suggest that CbPORB possesses certain resistant characteristics and is a major player in Chl biosynthesis process involved in plant growth and development of C. bungeana under cold environmental conditions.

Keywords: chlorophyll biosynthesis; chlorophyll fluorescence; Chorispora bungeana; low temperature; NADPH: protochlorophyllide oxidoreductase

Received: January 31, 2010; Accepted: May 28, 2010; Published: September 1, 2010Show citation

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Li, Y.H., Sun, Z.L., Xu, X.L., Jin, M., Liu, Y.J., Zhang, H., & An, L.Z. (2010). Influence of low temperatures on photosystem II photochemistry and expression of the NADPH:protochlorophyllide oxidoreductase in the alpine, subnival perennial, Chorispora bungeana. Photosynthetica, 48(3), 457-468. doi: 10.1007/s11099-010-0060-1.
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    References

    1. An, L.Z., Liu, Y.H., Feng, G.N., Feng, H.Y., Chen, T., Cheng, G.D.: Studies on ecological properties of altifrigetic subnival vegetation at the source area of Urumqi river. - Acta Bot. Boreal-Occident. Sin. 20: 98-105, 2000.
    2. Apel, K., Santel, H.J., Redlinger, T.E., Falk, H.: The protochlorophyllide holochrome of barley (Hordeum vulgare L.). Isolation and characterization of the NADPH: protochlorophyllide oxidoreductase. - Eur. J. Biochem. 111: 251-258, 1980. Go to original source...
    3. Armstrong, G.A.: Greening in the dark: light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms. - J. Photochem. Photobiol. B Biol. 43: 87-100, 1998. Go to original source...
    4. Armstrong, G.A., Runge, S., Frick, G., Sperling, U., Apel, K.: Identification of NADPH:protochlorophyllide oxidoreductase A and oxidoreductase B. A branched pathway for light dependent chlorophyll biosynthesis in Arabidopsis thaliana. - Plant Physiol. 108: 1505-1517, 1995. Go to original source...
    5. Arnon, D.I.: Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949. Go to original source...
    6. Artus, N.N., Uemura, M., Steponkus, P.L., Gilmour, S.J., Lin, C.T., Thomashow, M.F.: Constitutive expression of the coldregulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. - Proc. Natl. Acad. Sci. USA 93: 13404-13409, 1996. Go to original source...
    7. Asada, K.: Radical production and scavenging in the chloroplasts. - In: Baker, N.R. (ed.): Photosynthesis and the Environment. Pp. 123-150. Kluwer Academic Publ., Dordrecht - Boston - London 1996. Go to original source...
    8. Ayitu, R., Tan, D.Y., Li, Z.J., Yao, F.: [The relationship between the structures of vegetative organs in Chorispora bungeana and its environment.] - J. Xinjiang Agr. Univ. 21:273-277, 1998. [In Chin.]
    9. Bannai, H., Tamada, Y., Maruyama, O., Nakai, K., Miyano, S.: Extensive feature detection of N-terminal protein sorting signals. - Bioinformatics 18: 298-305, 2002. Go to original source...
    10. 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. Go to original source...
    11. Chang, J.F., Fu, X.Y., An, L.Z., Xu, S.J., Wang, J.H., Zhang, M.X., Feng, H.Y., Chen, T.: Properties of cellular ubiquinone and stress-resistance in suspension-cultured cells of Chorispora bungeana during early chilling. - Environ. Exp. Bot. 57: 116-122, 2006. Go to original source...
    12. DeRidder, B.P., Crafts-Brandner, S.J.: Chilling stress response of postemergent cotton seedlings. - Physiol. Plant. 134: 430-439, 2008. Go to original source...
    13. Dutta, S., Mohanty, S., Tripathy, B.C.: Role of temperature stress on chloroplast biogenesis and protein import in pea. - Plant Physiol. 150: 1050-1061, 2009. Go to original source...
    14. Forreiter, C., van Cleve, B., Schmidt, A., Apel, K.: Evidence for a general light-dependent negative control of NADPH-protochlorophyllide oxidoreductase in angiosperms. - Planta 183: 126-132, 1991. Go to original source...
    15. Frick, G., Su, Q., Apel, K., Armstrong, G.A.: An Arabidopsis porB porC double mutant lacking light-dependent NADPH: protochlorophyllide oxidoreductases B and C is highly chlorophyll-deficient and developmentally arrested. - Plant J. 35: 141-153, 2003. Go to original source...
    16. Fu, X.Y., Chang, J.F., An, L.Z., Zhang, M.X., Xu, S.J., Chen, T., Liu, Y.H., Xin, H., Wang, J.H.: Association of the cold-hardness of Chorispora bungeana with the distribution and accumulation of calcium in the cells and tissues. - Environ. Exp. Bot. 55: 282-293, 2006. Go to original source...
    17. Fujita, Y., Takagi, H., Hase, T.: Cloning of the gene encoding a protochlorophyllide reductase: the physiological significance of the co-existence of light-dependent and -independent protochlorophyllide reduction systems in the cyanobacterium Plectonema boryanum. - Plant Cell Physiol. 39: 177-185, 1998. Go to original source...
    18. Gajewska, E., Skłodowska, M., Słaba, M., Mazur, J.: Effect of nickel on antioxidative enzyme activities, proline and chlorophyll contents in wheat shoots. - Biol. Plant. 50: 653-659, 2006. Go to original source...
    19. Genty, B., Briantais, J.M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electrontransport and quenching of chlorophyll fluorescence. - Biochim. Biophys. Acta 990: 87-92, 1989. Go to original source...
    20. Griffiths, W.T.: Reconstitution of chlorophyllide formation by isolated etioplast membranes. - Biochem. J. 174: 681-692, 1978. Go to original source...
    21. Häuser, I., Dehesh, K., Apel, K.: The proteolytic degradation in vitro of the NADPH-protochlorophyllide oxidoreductase of barley (Hordeum vulgate L.). - Arch. Biochem. Biophys. 228:557-586, 1984. Go to original source...
    22. Hodgins, R., van Huystee, R.B.: Porphyrin metabolism in chill stressed maize (Zea mays L.). - J. Plant Physiol. 125: 325-336, 1986a. Go to original source...
    23. Holtorf, H., Reinbothe, S., Reinbothe, C., Bereza, B., Apel, K.: Two routes of chlorophyllide synthesis that are differentially regulated by light in barley (Hordeum vulgare L.). - Proc. Natl. Acad. Sci. USA 92: 3254-3258, 1995. Go to original source...
    24. Hormaetxe, K., Becerril, J.M., Hernández, A., Esteban, R., García-Plazaola, J.I.: Plasticity of photoprotective mechanisms of Buxus sempervirens L. leaves in response to extreme temperatures. - Plant Biol. 9: 59-68, 2007. Go to original source...
    25. Horton, P., Ruban, A.V.: Regulation of photosystem II. - Photosynth. Res. 34: 375-385, 1992. Go to original source...
    26. Ikeuchi, M., Murakami, S.: Behavior of the 36,000-dalton protein in the internal membranes of squash etioplasts during greening. - Plant Cell Physiol. 23: 575-583, 1982.
    27. Joyard, J., Block, M., Pineau, B., Albrieux, C., Douce, R.: Envelope membranes from mature spinach chloroplasts contain a NADPH:protochlorophyllide reductase on the cytosolic side of the outer membrane. - J. Biol. Chem. 265: 21820-21827, 1990.
    28. Krause, G.H.: Photoinhibition induced by low temperatures. - In: Baker, N.R., Bowyer, J.R. (ed.): Photoinhibition of Photosynthesis from Molecular Mechanisms to the Field. - Pp. 331-348. BIOS Scientific Publ., Oxford 1994.
    29. Kuroda, H., Masuda, T., Ohta, H., Shioi, Y., Takamiya, K.: Effects of light, developmental age and phytohormones on the expression of the gene encoding NADPH-protochlorophyllide oxidoreductase in Cucumis sativus. - Plant Physiol. Biochem. 34: 17-22, 1996.
    30. Kuroda, H., Masuda, T., Fusada, N., Ohta, H., Takamiya, K.: Expression of NADPH-protochlorophyllide oxidoreductase gene in fully green leaves of cucumber. - Plant Cell Physiol. 41: 226-229, 2000. Go to original source...
    31. Kuroda, H., Masuda, T., Fusada, N., Ohta, H., Takamiya, K.: Cytokinin-induced transcriptional activation of NADPH-protochlorophyllide oxidoreductase gene in cucumber. - J. Plant Res. 114: 1-7, 2001. Go to original source...
    32. Masuda, T., Fusada, N., Shiraishi, T., Kuroda, H., Awai, K., Shimada, H., Ohta, H., Takamiya, K.: Identification of two differentially regulated isoforms of protochlorophyllide oxidoreductase (POR) from tobacco revealed a wide variety of lightand development-dependent regulations of POR gene expression among angiosperms. - Photosynth. Res. 74: 165-172, 2002. Go to original source...
    33. Masuda, T., Fusada, N., Oosawa, N., Takamatsu, K., Yamamoto, Y.Y., Ohto, M., Nakamura, K., Goto, K., Shibata, D., Shirano, Y., Hayashi, H., Kato, T., Tabata, S., Shimada, H., Ohta, H., Takamiya, K.: Functional analysis of isoforms of NADPH:protochlorophyllide oxidoreductase (POR), PORB and PORC, in Arabidopsis thaliana. - Plant Cell Physiol. 44:963-974, 2003. Go to original source...
    34. Masuda, T., Takamiya, K.I.: Novel insights into the enzymology, regulation and physiological functions of light-dependent protochlorophyllide oxidoreductase in angiosperms. - Photosynth. Res. 81: 1-29, 2004. Go to original source...
    35. Maxwell, K., Johnson, G.N.: Chorophyll fluorescence - a practical guide. - J. Exp. Bot. 51: 659-668, 2000. Go to original source...
    36. Mohanty, S., Grimm, B., Tripathy, B.C.: Light and dark modulation of chlorophyll biosynthetic genes in response to temperature. - Planta 224: 692-699, 2006. Go to original source...
    37. Müller, P., Li, X.P., Niyogi, K.K.: Non-photochemical quenching. A response to excess light energy. - Plant Physiol. 125: 1558-1566, 2001. Go to original source...
    38. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures. - Physiol. Plant. 15: 473-497, 1962. Go to original source...
    39. Oosawa, N., Masuda, T., Awai, K., Fusada, N., Shimada, H., Ohta, H., Takamiya, K.: Identification and light-induced expression of a novel gene of NADPH-protochchlorophyllide oxidoreductase isoform in Arabidopsis thaliana. - FEBS Lett. 474: 133-136, 2000. Go to original source...
    40. Pattanayak, G.K., Tripathy, B.C.: Catalytic function of a novel protein protochlorophyllide oxidoreductase C of Arabidopsis thaliana. - Biochem. Biophys. Res. Commun. 291: 921-924, 2002. Go to original source...
    41. Pineau, B., Gerard-Hirne, C., Douce, R., Joyard, J.: Identification of the main species of tetrapyrrolic pigments in envelope membranes from spinach chloroplasts. - Plant Physiol. 102: 821-828, 1993. Go to original source...
    42. Redondo-Gómez, S., Wharmby, C., Castillo, J.M., Mateos-Naranjo, E., Luque, C.J., de Cires, A., Luque, T., Davy, A.J., Figueroa, M.E.: Growth and photosynthetic responses to salinity in an extreme halophyte, Sarcocornia fruticosa. - Physiol. Plant. 128: 116-124, 2006. Go to original source...
    43. Redondo-Gómez, S., Mateos-Naranjo, E., Figueroa, M.E., Davy, A.J.: Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. - Plant Biol. 12: 79-87, 2010. Go to original source...
    44. Reinbothe, S., Reinbothe, C., Holtorf, H., Apel, K.: Two NADPH:protochlorophyllide oxidoreductases in barley: evidence for the selective disappearance of PORA during the light-induced greening of etiolated seedlings. - Plant Cell 7: 1933-1940, 1995.
    45. Schreiber, U., Schliwa, W., Bilger, U.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorimeter. - Photosynth. Res. 10: 51-62, 1986. Go to original source...
    46. Seyedi, M., Selstam, E., Timko, M.P., Sundqvist, C.: The cytokinin 2-isopentenyladenine causes partial reversion to skotomorphogenesis and induces formation of prolamellar bodies and protochlorophyllide 657 in the lip1 mutant of pea. - Physiol. Plant. 112: 161-272, 2001a. Go to original source...
    47. Sonoike, K.: Photoinhibition of photosystem I: Its physiological significance in the chilling sensitivity of plants. - Plant Cell Physiol. 37: 239-247, 1996. Go to original source...
    48. Strasser, R.J., Butler, W.L.: Fluorescence emission spectra of photosystem I, photosystem II and the light-harvesting chlorophyll a/b complex of higher plants. - Biochim. Biophys. Acta 17: 307-313, 1977. Go to original source...
    49. Su, Q., Frick, G., Armstrong, G., Apel, K.: POR C of Arabidopsis thaliana: a third light- and NADPH-dependent protochlorophyllide oxidoreductase that is differentially regulated by light. - Plant Mol. Biol. 47: 805-813, 2001. Go to original source...
    50. Teakle, G.R., Griffiths, W.T.: Cloning, characterization and import studies on protochlorophyllide reductase from wheat (Triticum aestivum). - Biochem. J. 296: 225-230, 1993. Go to original source...
    51. Tewari, A.K., Tripathy, B.C.: Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. - Plant Physiol. 117: 851-858, 1998. Go to original source...
    52. Tewari, A.K., Tripathy, B.C.: Acclimation of chlorophyll biosynthetic reactions to temperature stress in cucumber (Cucumis sativus L.). - Planta 208: 431-437, 1999. Go to original source...
    53. Van Hasselt, P.R., Strikwerda, J.T.: Pigment degradation in discs of the thermophilic Cucumis sativus as affected by light, temperature, sugar application and inhibitors. - Physiol. Plant. 37: 253-257, 1976. Go to original source...
    54. Werner, C., Correia, O., Beyschlag, W.: Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem. - Funct. Plant Biol. 29: 991-1011, 2002. Go to original source...
    55. Yang, M.T., Chen, S.L., Lin, C.Y., Chen, Y.M.: Chilling stress suppresses chloroplast development and nuclear gene expression in leaves of mung bean seedlings. - Planta 221: 374-385, 2005. Go to original source...
    56. Zhang, T.G., Liu, Y.B., Xue, L.G., Xu, S.J., Chen, T., Yang, T.W., Zhang, L.J., An, L.Z.: Molecular cloning and characterization of a novel MAP kinase gene in Chorispora bungeana. - Plant Physiol. Biochem. 44: 78-84, 2006. Go to original source...

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