Subscribe to RSS
DOI: 10.1055/s-2004-817893
Georg Thieme Verlag Stuttgart KG · New York
Hg2+ Reacts with Different Components of the NADPH : Protochlorophyllide Oxidoreductase Macrodomains
Publication History
Publication Date:
14 May 2004 (online)
Abstract
The molecular background of Hg2+-induced inhibition of protochlorophyllide (Pchlide) photoreduction was investigated in homogenates of dark-grown wheat leaves. Our earlier work showed that 15 min incubation with 10-2 M Hg2+ completely inhibits the activity of NADPH : Pchlide oxidoreductase ([Lenti et al., 2002]). Detailed analysis of spectra recorded at 10 K indicated the appearance of emission bands at 638 and 650 nm, which are characteristic for NADP+-Pchlide complexes. Fluorescence emission spectra recorded with different excitation wavelengths, fluorescence lifetime measurements and the analysis of acetone extractions revealed that Hg2+ can also react directly with Pchlide, resulting in protopheophorbide formation. At 10-3 M Hg2+, the phototransformation was complete but the blue shift of the chlorophyllide emission band speeded up remarkably. This indicates oxidation of the NADPH molecules that have a structural role in keeping together the etioplast inner membrane components. We suggest a complex model for the Hg2+ effect: depending on concentration it can react with any components of the NADPH : Pchlide oxidoreductase macrodomains.
Key words
Mercury - Hg2+ - protochlorophyllide - NADPH - protopheophorbide - Shibata shift - activity loss
References
- 1 Aronsson H., Sundqvist C., Timko M. P., Dahlin C.. The importance of the C-terminal region and Cys residues for the membrane association of the NADPH:protochlorophyllide oxidoreductase in pea. FEBS Lett.. (2001); 502 11-15
- 2 Aylward G. H., Findlay T. J. V.. S. I. Chemical Data. Sydney; John Wiley and Sons (1974)
- 3 Barlton D., Smith A. M.. Mercury binding to human haemoglobin. Experientia. (1973); 29 1178-1179
- 4 Böddi B.. Spectral, biochemical and structural changes connected to protochlorophyllide photoreduction in chlorophyll biosynthesis. Human Envir. Sci.. (1994); 3 39-55
- 5 Böddi B., Franck F.. Room temperature fluorescence spectra of protochlorophyllide and chlorophyllide forms in etiolated bean leaves. J. Photochem. Photobiol.. (1997); 41 73-82
- 6 Böddi B., Lindsten A., Ryberg M., Sundqvist C.. On the aggregational states of protochlorophyllide and its protein complexes in wheat etioplasts. Physiol. Plant.. (1989); 76 135-143
- 7 Böddi B., Oravecz A. R., Lehoczki E.. Effect of cadmium on organization and photoreduction of protochlorophyllide in dark-grown leaves and etioplast inner membrane preparations of wheat. Photosynthetica. (1995); 31 411-420
- 8 Böddi B., Popovic R., Franck F.. Early reactions of light-induced protochlorophyllide and chlorophyllide transformations analyzed in vivo at room temperature with a diode array spectrofluorometer. J. Photochem. Photobiol. B: Biol.. (2003); 69 31-39
- 9 Böddi B., Ryberg M., Sundqvist C.. The formation of a short-wavelength chlorophyllide form at partial phototransformation of protochlorophyllide in etioplast inner membranes. Photochem. Photobiol.. (1991); 53 667-673
- 10 Böddi B., Ryberg M., Sundqvist C.. Identification of four universal protochlorophyllide forms in dark-grown leaves by analyses of the 77 K fluorescence emission spectra. J. Photochem. Photobiol. B: Biol.. (1992); 12 389-401
- 11 Böddi B., Ryberg M., Sundqvist C.. Analysis of the 77 K fluorescence excitation spectra of isolated etioplast inner membranes. J. Photochem. Photobiol. B: Biol.. (1993); 21 125-133
- 12 Boening D. W.. Ecological effects, transport, and fate of mercury: a general review. Chemosphere. (2000); 40 1335-1351
- 13 Cho U. H., Park J. O.. Mercury-induced oxidative stress in tomato seedlings. Plant Sci.. (2000); 156 1-9
- 14 Clijsters H., van Asche F.. Inhibition of photosynthesis by heavy metals. Photosynth. Res.. (1985); 7 31-40
- 15 Dahlin C., Aronsson H., Wilks H. M., Lebedev N., Sundqvist C., Timko M. P.. The role of protein surface charge in catalytic activity and chloroplast membrane association of the pea NADPH-protochlorophyllide oxidoreductase as revealed by alanine scanning mutagenesis. Plant. Mol. Biol.. (1999); 39 309-323
- 16 De Filippis L. F.. The effect of heavy metals on the absorption spectra of Chlorella cells and chlorophyll solutions. Z. Pflanzenphysiol.. (1979); 93 129-137
- 17 De Filippis L. F., Pallaghy C. K.. The effect of sub-lethal concentrations of mercury and zinc on Chlorella. II. Photosynthesis and pigment composition. Z. Pflanzenphysiol.. (1976); 78 314-322
- 18 De Filippis L. F., Hampp R., Ziegler H.. The effects of sublethal concentrations of zinc, cadmium and mercury on Euglena. Growth and pigments. Z. Pflanzenphysiol.. (1981 a); 101 37-47
- 19 De Filippis L. F., Hampp R., Ziegler H.. The effects of sublethal concentrations of zinc, cadmium and mercury on Euglena. II. Respiration, photosynthesis and photochemical activities. Arch. Microbiol.. (1981 b); 128 407-411
- 20 El Hamouri B., Sironval C.. NADP+/NADPH control of the protochlorophyllide-, chlorophyllide-proteins in cucumber etioplasts. Photochem. Photobiophys.. (1980); 1 219-223
- 21 Eullaffroy P., Salvetat R., Franck F., Popovic R.. Temperature dependence of chlorophyll(ide) spectral shifts and photoactive protochlorophyllide regeneration after flash in etiolated barley leaves. Photochem. Photobiol.. (1995); 62 751-756
- 22 Foster T. J.. Plasmid determined resistance to antimicrobial drugs and toxic metal ions in bacteria. Microbiol. Rev.. (1983); 47 361-409
- 23 Franck F., Bereza B., Böddi B.. Protochlorophyllide-NADP+ and protochlorophyllide-NADPH complexes and their regeneration after flash illumination in leaves and etioplast membranes of dark-grown wheat. Photosynth. Res.. (1999); 59 53-61
- 24 Funahashi S., Inada Y., Inamo M.. Dynamic study of metal-ion incorporation into porphyrins based on the dynamic characterization of metal ions and sitting-atop complex formation. Anal. Sci.. (2001); 17 917-927
-
25 Goedheer J. C..
Visible absorption and fluorescence of chlorophyll and its aggregates in solution. Vernon, L. P. and Seely, G. R., eds. The Chlorophylls. New York, Boston; Academic Press (1966): 147-184 - 26 Gratton E., Limkeman M.. A continuously variable frequency cross-correlation phase fluorometer with picosecond resolution. Biophys. J.. (1983); 44 315-324
- 27 Griffiths W. T.. Reconstitution of chlorophyll formation by isolated etiplast membranes. Biochem. J.. (1978); 174 681-692
-
28 Griffiths W. T..
Protochlorophyllide photoreduction. Scheer H., ed. Chlorophylls. Boca Raton, Florida; CRC Press Inc. (1991): 433-450 - 29 Heyes D. J., Martin G. E. M., Reid R. J., Hunter C. N., Wilks H. M.. NADPH: protochlorophyllide oxidoreductase from Synechocystis: overexpression, purification and preliminary characterisation. FEBS Lett.. (2000); 483 47-51
- 30 Hu Q., Yang G., Yin J., Yao Y.. Determination of trace lead, cadmium and mercury by on-line column enrichment followed by RP-HPLC as metal-tetra-(4-bromophenyl)-porphyrin chelates. Talanta. (2002); 57 751-756
- 31 Kis-Petik K., Böddi B., Kaposi A. D., Fidy J.. Protochlorophyllide forms and energy transfer in dark-grown wheat leaves. Studies by conventional and laser excited fluorescence spectroscopy between 10 K-100 K. Photosynth. Res.. (1999); 60 87-98
- 32 Klein S., Schiff J. A.. The correlated appearance of prolamellar bodies, protochlorophyll(ide) species, and the Shibata shift during development of bean etioplasts in the dark. Plant. Physiol.. (1972); 49 619-626
- 33 Küpper H., Küpper F., Spiller M.. Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. J. Exp. Bot.. (1996); 47 259-266
- 34 Küpper H., Küpper F., Spiller M.. In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth. Res.. (1998); 58 123-133
- 35 Küpper H., Šetlik I., Spiller M., Küpper F. C., Prášil O.. Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J. Phycol.. (2002); 38 429-441
- 36 Lakowicz J. R., Lacko G., Cherek H., Gratton E., Limkeman M.. Analysis of fluorescence decay kinetics from variable-frequency phase shift and modulation data. Biophys. J.. (1984); 46 463-477
- 37 Lau S., Sarkar B.. Inorganic mercury(II)-binding component in normal human blood serum. J. Toxicol. Environ. Health. (1979); 5 907-916
- 38 Lebedev N., Timko M. P.. Protochlorophyllide photoreduction. Photosynth. Res.. (1998); 58 5-23
- 39 Lenti K., Fodor F., Böddi B.. Mercury inhibits the activity of the NADPH:protochlorophyllide oxidoreductase (POR). Photosynthetica. (2002); 40 145-151
- 40 Magnaval R., Batti R., Thiessard J.. Methylmercury effect on rat liver mitochondrial deshydrogenases. Experimentia. (1975); 31 406-407
-
41 Myśliwa-Kurdziel B., Strzałka K..
Influence of metals on biosynthesis of photosynthetic pigments. Prasad, M. N. V. and Strzałka, K., eds. Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Dordrecht, Boston, London; Kluwer Academic Publishers (2002): 201-227 - 42 Myśliwa-Kurdziel B., Franck F., Strzałka K.. Analysis of fluorescence lifetime of protochlorophyllide and chlorophyllide in isolated etioplast membranes measured from multifrequency cross-correlation phase fluorometry. Photochem. Photobiol.. (1999); 70 616-623
- 43 Ogawa M., Tsutsui Y., Konishi M.. Effects of illumination on absorption peak shifts in spectra of intact etiolated cotyledons of Pharbitis nil. II. Effects of leaf age on protochlorophyllide regeneration and the Shibata shift. Plant Cell Physiol.. (1978); 19 127-132
- 44 Oosawa N., Masuda T., Awai K., Fusada N., Shimada H., Ohto H., Takamiya K.. Identification and light-induced expression of a novel gene of NADPH:protochlorophyllide oxidoreductase isoform in Arabidopsis thaliana. . FEBS Lett.. (2000); 474 113-136
- 45 Ouazzani-Chahdi M. A., Schoefs B., Franck F.. Isolation and characterisation of photoactive complexes of NADPH:protochlorophyllide oxidoreductase from wheat. Planta. (1998); 206 673-680
- 46 Patra M., Sharma A.. Mercury toxicity in plants. Bot. Rev.. (2000); 66 379-422
- 47 Pearson R. G.. Hard and soft acids and bases. J. Am. Chem. Soc.. (1963); 85 3533-3539
-
48 Romanowska E..
Gas exchange functions in metal stressed plants. Prasad, M. N. V. and Strzałka, K., eds. Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Dordrecht, Boston, London; Kluwer Academic Publishers (2002): 257-285 - 49 Ryberg M., Dehesh K.. Localization of NADPH:protochlorophyllide oxidoreductase in dark-grown wheat (Triticum aestivum) by immuno-electron microscopy before and after transformation of the prolamellar bodies. Physiol. Plant.. (1986); 66 616-624
- 50 Ryberg M., Sundqvist C.. Spectral forms of protochlorophyllide in prolamellar bodies and prothylakoids fractionated from wheat etioplasts. Physiol. Plant.. (1982); 56 133-138
- 51 Ryberg M., Sundqvist C.. The regular ultrastructure of isolated prolamellar bodies depends on the presence of membrane-bound NADPH-protochlorophyllide oxidoreductase. Physiol. Plant.. (1988); 73 218-226
- 52 Savitzky A., Golay M. J. E.. Smoothing and differentiation of data by simplified least square procedures. Anal. Chem.. (1964); 36 1627
- 53 Schlegel H., Douglas L., Hüttermann A.. Whole plant aspects of heavy metal induced changes in CO2 uptake and water relations of spruce (Picea abies) seedlings. Physiol. Plant.. (1987); 69 265-270
- 54 Shibata K.. Spectroscopic studies on chlorophyll formation in intact leaves. J. Biochem.. (1957); 44 147-173
- 55 Smeller L.. How precise are the positions of computer-determined peaks?. Appl. Spectrosc.. (1998); 52 1623-1626
- 56 Sperling U., Franck F., van Cleve B., Frick G., Apel K., Armstrong G. A.. Etioplast differentation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-P655 to the cop1 photomorphogenic mutant. Plant Cell. (1998); 10 283-296
- 57 Sundberg J., Ersson B., Lönnerdal B., Oskarsson A.. Protein binding of mercury in milk and plasma from mice and man - a comparison between methylmercury and inorganic mercury. Toxicology. (1999); 137 169-184
- 58 Suszcyńsky E. M., Shann J. R.. Phytotoxicity and accumulation of mercury in tobacco subjected to different exposure routes. Environ. Toxicol. Chem.. (1995); 14 61-67
- 59 Tabata M.. Kinetic evidence for short-lived intermediates in metalloporphyrin formation. J. Mol. Liquids. (1995); 65 - 66 221-228
- 60 Teakle G. R., Griffiths W. T.. Cloning, characterization and import studies on protochlorophyllide reductase from wheat (Triticum aestivum). . Biochem. J.. (1993); 296 225-230
- 61 Vallee B. L., Ulmer D. D.. Biochemical effects of mercury, cadmium and lead. Ann. Rev. Biochem.. (1972); 41 91-128
- 62 Van Bochove A. C., Griffiths W. T., Van Grondelle R.. The primary reaction in the photoreduction of protochlorophyllide monitored by nanosecond fluorescence measurements. Photochem. Photobiol.. (1984); 39 101-106
- 63 Wiktorsson B., Engdahl S., Zhong L. B., Böddi B., Ryberg M., Sundqvist C.. The effect of cross-linking of the subunits of NADPH:protochlorophyllide oxidoreductase on the aggregational state of protochlorophyllide. Photosynthetica. (1993); 29 205-218
- 64 Wiktorsson B. M., Ryberg M., Gough S., Sundqvist C.. Isoelectric focusing of pigment-protein complexes solubilized from non-irradiated and irradiated prolamellar bodies. Physiol. Plant.. (1992); 85 659-669
- 65 Zalups R. K., Barfuss D. W.. Nephrotoxicity of inorganic mercury co-administered with L-cysteine. Toxicology. (1996); 109 15-29
B. Böddi
Department of Plant Anatomy
Eötvös University
Pázmány P. sétány 1/C
Budapest H-1117
Hungary
Email: bbfotos@ludens.elte.hu
Guest Editor: F. Loreto