Abstract
To elucidate the mechanism of irradiance-dependent adjustments in the chlorophyll antenna size of photosynthesis, we addressed the regulation of expression of genes encoding a variety of chlorophyll biosynthesis enzymes and that of the Lhcb genes in the model organism Dunaliella salina. Among the chlorophyll biosynthesis enzymes tested, only the chlorophyll a oxygenase (CAO) gene responded to changes in the level of irradiance with substantial mRNA level and kinetics of change that were similar to those of the Lhcb genes. Evidence is presented for the operation of a cytosolic signal transduction pathway for the rapid (order of minutes) regulation of both CAO and Lhcb gene expression by irradiance. Inhibitor studies and transient activation of Ca2+-dependent kinase suggested phopholipase-C activation to Ca2+ release, and activation of a specific Ca2+/CaM-dependent protein kinase in this cytosolic signal transduction pathway. The redox state of the plastoquinone pool also serves to regulate CAO and Lhcb gene expression on a slower time scale (hours) and probably serves as a plastidic-origin signal that acts coordinately with the cytosolic signal transduction pathway. It is proposed that irradiance-dependent adjustments in the chlorophyll antenna size occur by coordinate regulation of CAO and Lhcb gene expression via two distinct signal transduction pathways in photosynthetic organisms.
Similar content being viewed by others
References
Allen, J.F., Alexciev, K. and Håkansson, G. 1995. Photosynthesis. Regulation by redox signaling. Curr. Biol. 5: 869–872.
Anderson, K.M. 1986. Photoregulation of the composition, function and structure of thylakoid membranes. Annu. Rev. Plant. Physiol. 37: 93–136.
Arnon, D. 1949. Cooper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol. 24: 1–15.
Beale, S.I. 1999. Enzymes of chlorophyll biosynthesis. Photosynth. Res. 60: 43–73.
Björkman, O., Boadman, N.K., Anderson, J.M., Thorne, S.W., Goodchild, D.J. and Phliotis, N.A. 1972. Effect of light intensity during growth of Atriplex patula on the capacity of photosynthetic reactions, chloroplast components and structure. Carnegie Inst. Wash. Yearb. 71: 115–135.
Bowler, C, Neuhause, G., Yamagata, H. and Chua, N.-H. 1994. Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77: 73–81.
Bradford, M.M. 1976. A rapid and sensitive method of the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.
Bush, D.S. 1995. Calcium regulation in plant cells and its role in signaling. Annu. Rev. Plant Physiol. PlantMol. Biol. 46: 95–122.
Dohlman, H.G., Thorner, J., Caron, M.G. and Lefkowitz, R.J. 1991. Model systems for the study of seven-tranmembrane-segment receptors. Annu. Rev. Biochem. 60: 653–688.
Durnford, D.G. and Falkowski, P.G. 1997. Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth. Res. 53: 229–241.
Einspahr, K.J., Peeler, T.C. and Thompson, Jr., G.A. 1989. Phosphatidylinositol 4,5-bisphosphate phospholipase C and phosphomonoesterase in Dunaliella salina membranes. Plant Physiol. 90: 1115–1120.
Escoubas J.M., Lomas, M., LaRoche, J. and Falkowski, P.G. 1995. Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl. Acad. Sci. USA 92: 10237–10241.
Goueli, B.S., Hsiao, K., Tereba, A. and Goueli, S.A. 1995. A novel and simple method to assay the activity of individual protein kinases in a crude tissue extract. Anal. Biochem. 225: 10–17.
Grimm, B., Smith, A.J., Kannangara, C.G. and Smith, M. 1991. Gabaculine-resistant glutamate 1-semialdehyde aminotransferase of Synechococcus. Deletion of a tripeptide close to the NH2 terminus and internal amino acid substitution. J. Biol. Chem. 266: 12495–12501.
Hansen, M., Boitano, S., Dirksen, E.R. and Sanderson, M.J. 1995. A role for phospholipase C activity but not ryanodine receptors in the initiation and propagation of intercellular calcium waves. J. Cell Sci. 108: 2583–2590.
Harrison, M.A. and Melis, A. 1992. Organization and stability of polypeptides associated with the chlorophyll a-b light-harvesting complex of photosystem-II. Plant Cell Physiol. 33: 627–637.
Higo, K., Ugawa, Y., Iwamoto, M. and Korenaga, T. 1999. Plant cisacting regulatory DNA elements (PLACE) database. Nucl. Acids Res. 27: 297–300.
Huner, N.P.A., Oquist, G. and Sarhan, F. 1998. Energy balance and acclimation to light and cold. Trends Plant Sci. 3: 224–230.
Im, C.-S. and Beale, S.I. 2000. Identification of possible signal transduction components mediating light induction of the Gsa gene for an early chlorophyll biosynthetic step in Chlamydomonas reinhardtii. Planta 210: 999–1005.
Im, C.-S., Matters, G.L. and Beale, S.I. 1996. Calcium and calmodulin are involved in blue light induction of the gsa gene for an early chlorophyll biosynthetic step in Chalmydomonas. Plant Cell 8: 2245–2253.
Johanningmeier, U. 1988. Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. Eur. J. Biochem. 177: 417–424.
Johanningmeier, U. and Howell, S.H. 1984. Regulation of lightharvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii. J. Biol. Chem. 259: 13541–13549.
Keller, L.R., Schloss, J.A., Siflow, C.D. and Rosenbaum, J.L. 1984. Transcription of β-and β-tubulin genes in vitro in isolated Chlamydomonas reinhardtii nuclei. J. Cell Biol. 98: 1138–1143.
Kropat, J., Oster, U., Rüdiger, W. and Beck, C.F. 1997. Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc. Natl. Acad. Sci. USA 94: 14168–14172.
Kropat, J., Oster, U., Rüdiger, W. and Beck, C.F. 2000. Chloroplast signaling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J. 24: 523–531.
Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.
Lam, E., Benedyk, M. and Chua, N.-H. 1989. Characterization of phytochrome-regulated gene expression in a photoautotrophic cell suspension: possible role for calmodulin. Mol. Cell Biol. 9: 4819–4823.
LaRoche, J., Mortain-Bertrand, A. and Falkowski, P.G. 1991. Light intensity-induced changes in cab mRNA and light harvesting complex II apoprotein levels in the unicellular chlorophyte Dunaliella tertiolecta. Plant Physiol. 97: 147–153.
Larsson, U.K., Anderson, J.M. and Andersson, B. 1987. Variations in the relative content of the peripheral and inner light-harvesting chlorophyll a/b-protein complex (LHC-II) subpopulations during thylakoid light adaptation and development. Biochim. Biophys. Acta 894: 69–75.
Leong, T.A. and Anderson, J.M. 1984. Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. I. Study on the distribution of chlorophyll-protein complexes. Photosynth. Res. 5: 105–115.
Lu, Y.-T., Hidaka, H. and Feldman, L.J. 1996. Characterization of a calcium/calmodulin-dependent protein kinase homolog from maize roots showing light-regulated gravitropism. Planta 199: 18–24.
Ma, H. 1994. GTP-binding protein in plants: new members of an old family. Plant Mol. Biol. 26: 1611–1636.
Masuda, T., Polle, J.E.W. and Melis, A. 2002. Biosynthesis and distribution of Chl among the photosystems during recovery of the green alga Dunaliella salina from irradiance stress. Plant Physiol. 128: 603–614.
Matters, G.L. and Beale, S.I. 1994. Structure and light-regulated expression of the gsa gene encoding the chlorophyll biosynthetic enzyme, glutamate 1-semialdehyde aminotransferase in Chlamydomonas reinhardtii. Plant Mol. Biol. 24: 617–629.
Melis, A. 1991. Dynamics of photosynthetic membrane composition and function. Biochim. Biophys. Acta 1058: 87–106.
Melis, A. 1996. Excitation energy transfer: Functional and dynamic aspects of Lhc (cab) proteins. In: D.R. Ort and C.F. Yocum (Eds.) Oxygenic Photosynthesis: The Light Reactions, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 523–538.
Melis, A. 1998. Photostasis in plants: mechanisms and regulation. In: T.P. Williams and A. Thistle (Eds.) Photostasis and Related Phenomena, Plenum, New York, pp. 207–221.
Melis, A., Spangfort, M. and Andersson, B. 1987. Light-absorption and electron transport balance between photosystem-II and photosystem-I in spinach chloroplasts. Photochem. Photobiol. 45: 129–136.
Melis, A., Murakami, A., Nemson, J.A., Aizawa, K., Ohki, K. and Fujita, Y. 1996. Chromatic regulation in Chlamydomonas reinhardtii alters photosystem stoichiometry and improves the quantum efficiency of photosynthesis. Photosynth. Res. 47: 253–265.
Munnik, T., Irvine, R.F. and Musgrave, A. 1998. Phospholipid signaling in plants. Biochim. Biophys. Acta 1389: 222–272.
Nakayama, M., Masuda, T., Bando, T., Yamagata, H., Ohta, H. and Takamiya, K. 1998. Cloning and expression of the soybean chlH gene encoding a subunit of Mg-chelatase and localization of the Mg2+ concentration-dependent ChlH protein within chloroplast. Plant Cell Physiol. 39: 275–284.
Neidhardt, J., Benemann, J.R., Zhang, L. and Melis, A. 1998. Photosystem II repair and chloroplast recovery from irradiance stress: relationship between chronic photoinhibition, lightharvesting chlorophyll antenna size and photosynthetic productivity in Dunaliella salina (green algae). Photosynth Res. 56: 175–184.
Neuhaus, G., Bowler, C., Kern, R. and Chua, N.-H. 1993. Calcium/calmodulin-dependent and-independent phytochrome signal transduction pathways. Cell 73: 937–952.
Nishigaki, A., Ohshima, S. and Nakayama, K. 2000. Characterization of three forms of light-harvesting chlorophyll a/bprotein complexes of photosystem II isolated from the green alga Dunaliella salina. Plant Cell Physiol. 41: 591–599.
Okamoto, H., Matui, M. and Deng, X.W. 2001. Overexpression of the heterotrimeric G-protein β-subunit enhances phytochromemediated inhibition by hypocotyl elongation in Arabidopsis. Plant Cell 13: 1639–1651.
Peter, G.F. and Thornber, J.P. 1991. Biochemical composition and organization of higher plant photosystem-II light-harvesting pigment-proteins. J. Biol. Chem. 266: 16745–16754.
Pick, U., Karni, L. and Avron, M. 1986. Determination of ion content and ion fluxes in the halotolerant alga Dunaliella salina. Plant Physiol. 81: 92–96.
Pingret, J.-L., Journet, E.-P. and Barker, D.G. 1998. Rhizobium Nod factor signaling: evidence for a G-protein-mediated transduction mechanism. Plant Cell 10: 659–671.
Pinontoan, R., Yuasa, T., Anderca, M.I., Matsuoka, T., Uozumi, N., Mori, H. and Muto, S. 2000. Cloning of a cDNA encoding a 66-kDa Ca2+-dependent protein kinase (CDPK) from Dunaliella tertiolecta (Chlorophyta). J. Phycol. 36: 545–552.
Plakidou-Dymock, S., Dymock, D. and Hooley, R. 1998. A higher plant seven-transmembrane receptor that influences sensitivity to cytokinins. Curr. Biol. 8: 315–324.
Starr, R.C. 1978. The culture collection of algae at the University of Texas at Austin. J. Phycol. 14: 47–100.
Smith, B.M., Morrissey, P.J., Guenther, J.E., Nemson, J.A., Harrison, M.A., Allen, J.F. and Melis, A. 1990. Response of the photosynthetic apparatus in Dunaliella salina (green algae) to irradiance stress. Plant Physiol. 93: 1433–1440.
Sukenik, A., Wyman, K.D., Bennett, J. and Falkowski, P.G. 1987. A novel mechanism for regulating the excitation of photosystem II in a green alga. Nature 327: 704–707.
Tanaka, A., Ito, H., Tanaka, R., Tanaka, N.K., Yoshida, K. and Okada, K. 1998. Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc. Natl. Acad. Sci. USA 95: 12719–12723.
Tanaka, A. and Melis, A. 1997. Irradiance-dependent changes in the size and composition of the chlorophyll a-b light-harvesting complex in the green alga Dunaliella salina. Plant Cell Physiol. 38: 17–24.
Tanaka, R., Koshino, Y., Sawa, S., Ishiguro, S., Okada, K. and Tanaka, A. 2001. Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thaliana. Plant J. 26: 365–373.
Thornber, J.P. 1979. Chlorophyll-proteins: light-harvesting and reaction center components of plants. Annu. Rev. Plant. Physiol. 26: 127–158.
Thompson, A.K., Mostafapour, S.P., Denlinger, L.C., Bleasdale, J.E. and Fisher, S.K. 1991. The aminosteroid U-73122 inhibits muscarinic receptor sequestration and phosphoinositide hydrolysis in SK-N-SH neuroblastoma cells. A role for Gp in receptor compartmentation. J. Biol. Chem. 266: 23856–23862.
Vandonselaar, M., Hickie, R.A., Quail, J.W. and Delbaere, L.T. 1994. Trifluoroperazine-induced conformational change in Ca2+-calmodulin. Nature Struct. Biol. 1: 795–801.
Webb, M.R. and Melis, A. 1995. Chloroplast response in Dunaliella salina to irradiance stress: effect on thylakoid membrane protein assembly and function. Plant Physiol. 107: 885–893.
Willows, R. and Beale, S.I. 1998. Heterologous expression of the Rhodobacter capsulatus BchI, -D, and -H genes that encode magnesium chelatase subunits and characterization of the reconstituted enzyme. J. Biol. Chem. 273: 34206–34213.
Yuasa, T., Takahashi, K. and Muto, S. 1995. Purification and characterization of a Ca2+-dependent protein kinase from the halotolerant green alga Dunaliella tertiolecta. Plant Cell Physiol. 36: 699–708.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Masuda, T., Tanaka, A. & Melis, A. Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression. Plant Mol Biol 51, 757–771 (2003). https://doi.org/10.1023/A:1022545118212
Issue Date:
DOI: https://doi.org/10.1023/A:1022545118212