Abstract
The effects of high concentrations of Hg2+ (10-2 M and 10-3 M) were investigated on the ultrastructure and on the light-induced transformation of isolated prolamellar bodies (PLBs) of dark-grown wheat leaves. Our earlier work on wheat leaf homogenates ([Solymosi et al. [2004]], Plant Biology 6, 358 - 368) showed that, depending on the concentration, Hg2+ reacts with protochlorophyllide, NADPH and the NADPH : protochlorophyllide oxidoreductase (POR, EC 1.3.1.33) enzyme and induces disaggregation of the macrodomain structure of this latter. Spectroscopic analyses confirmed that 15 min incubation with 10-2 M Hg2+ at 4 °C completely inhibited the activity of POR also in isolated PLBs. Ultrastructural investigations revealed the loosening of the PLB structure in the Hg2+-treated sample, i.e., intensive vesicle formation on the surface of the PLB membranes. The hexagonal geometry of the inner lattice was not disturbed, however, the unit cell size significantly increased. The disruption of the PLB membranes upon irradiation was studied after 40 min incubation with 10-3 M Hg2+ at 4 °C and a subsequent irradiation for 40 min at 20 °C. Equimolar concentrations (10-3 M) of NADPH and Hg2+ were added to the samples 10 min prior or after the addition of Hg2+. Our results suggest that Hg2+ accelerates the disruption of the PLB membranes and that NADPH can only partially prevent this process. These membrane transformations were similar to those observed in the initial steps of the Shibata shift of control samples.
Key words
Hg2+
- prolamellar body - protochlorophyllide - chlorophyllide - Shibata shift
References
-
1
Böddi B., Lindsten A., Ryberg M., Sundqvist C..
On the aggregational states of protochlorophyllide and its protein complexes in wheat etioplasts.
Physiologia Plantarum.
(1989);
76
135-143
-
2
Böddi B., Lindsten A., Ryberg M., Sundqvist C..
Phototransformation of aggregated forms of protochlorophyllide in isolated etioplast inner membranes.
Photochemistry and Photobiology.
(1990);
52
83-87
-
3
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
-
4
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.
Journal of Photochemistry and Photobiology, B: Biology.
(1992);
12
389-401
-
5
Boening D. W..
Ecological effects, transport, and fate of mercury: a general review.
Chemosphere.
(2000);
40
1335-1351
-
6
Butler W. L., Briggs W. R..
The relation between structure and pigments during the first stages of proplastid greening.
Biochimica et Biophysica Acta.
(1966);
112
45-53
-
7
Cho U. H., Park J. O..
Mercury-induced oxidative stress in tomato seedlings.
Plant Science.
(2000);
156
1-9
-
8
Domanskii V. P., Rüdiger W..
On the nature of the two pathways in chlorophyll formation from protochlorophyllide.
Photosynthesis Research.
(2001);
68
131-139
-
9
Domanskii V. P., Rassadina V., Gus-Mayer S., Wanner G., Schoch S., Rüdiger W..
Characterization of two phases of chlorophyll formation during greening of etiolated barley leaves.
Planta.
(2003);
216
475-483
-
10
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.
Photochemistry and Photobiology.
(1995);
62
751-756
-
11
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.
Photosynthesis Research.
(1999);
59
53-61
-
12
Franck F., Inoue Y..
Light driven reversible transformation of chlorophyllide P696, 682 into chlorophyllide P688, 678 in illuminated etiolated bean leaves.
Photobiochemistry and Photobiophysics.
(1984);
8
85-96
-
13
Franck F., Mathis P..
A short-lived intermediate in the photoenzymatic reduction of protochlorophyll(ide) into chlorophyll(ide) at a physiological temperature.
Photochemistry and Photobiology.
(1980);
32
799-803
-
14 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
-
15
Gunning B. E. S..
The greening process in plastids. 1. The structure of the prolamellar body.
Protoplasma.
(1965);
60
111-130
-
16
Gunning B. E. S..
Membrane geometry of “open” prolamellar bodies.
Protoplasma.
(2001);
215
4-15
-
17
Henningsen K. W..
Macromolecular physiology of plastids VI. Changes in membrane structure associated with shifts in the absorption maxima of the chlorophyllous pigments.
Journal of Cell Science.
(1970);
7
587-621
-
18
Henningsen K. W., Boynton J. E..
Macromolecular physiology of plastids. VII. The effect of brief illumination on plastids of dark-grown barley leaves.
Journal of Cell Science.
(1969);
5
757-793
-
19
Henningsen K. W., Kahn A., Houssier C..
Circular dichroism of protochlorophyllide and chlorophyllide holochrome subunit.
FEBS Letters.
(1973);
37
103-108
-
20
Kahn A., Boardman N. K., Thorne S. W..
Energy transfer between protochlorophyllide molecules: evidence for multiple chromophores in the photoactive protochlorophyllide-protein complex in vivo and in vitro.
.
Journal of Molecular Biology.
(1970);
48
85-101
-
21
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.
Photosynthesis Research.
(1999);
60
87-98
-
22
Klockare B., Virgin H. I..
Chlorophyll(ide) forms after partial phototransformation of protochlorophyll(ide) in etiolated wheat leaves.
Physiologia Plantarum.
(1983);
57
28-34
-
23
Le Lay P., Böddi B., Kovacevic D., Juneau P., Dewez D., Popovic R..
Spectroscopic analysis of desiccation-induced alterations of the chlorophyllide transformation pathway in etiolated barley leaves.
Plant Physiology.
(2001);
127
202-211
-
24
Lenti K., Fodor F., Böddi B..
Mercury inhibits the activity of the NADPH : protochlorophyllide oxidoreductase (POR).
Photosynthetica.
(2002);
40
145-151
-
25
Lindsten A., Wiktorsson B., Ryberg M., Sundqvist C..
Chlorophyll synthetase activity is relocated from transforming prolamellar bodies to developing thylakoids during irradiation of dark-grown wheat.
Physiologia Plantarum.
(1993);
88
29-36
-
26
Masuda T., Takamiya K..
Novel insights into the enzymology, regulation and physiological functions of light-dependent protochlorophyllide oxidoreductase in angiosperms.
Photosynthesis Research.
(2004);
81
1-29
-
27
Murakami S., Yamada N., Nagano M., Osumi M..
Three dimensional structure of the prolamellar body in squash etioplasts.
Protoplasma.
(1985);
128
147-156
-
28
Myśliwa-Kurdziel B., Franck F., Ouazzani-Chahdi M. A., Strzałka K..
Changes in endothermic transitions associated with light-induced chlorophyllide formation, as investigated by differential scanning calorimetry.
Physiologia Plantarum.
(1999);
107
230-239
-
29 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
-
30
Myśliwa-Kurdziel B., Strzałka K..
Influence of Cd(II), Cr(VI) and Fe(III) on early steps of deetiolation process in wheat: fluorescence spectral changes of protochlorophyllide and newly formed chlorophyllide.
Agriculture, Ecosystems and Environment.
(2005);
106
199-207
-
31
Nyitrai P., Bóka K., Gáspár L., Sárvári É., Lenti K., Keresztes Á..
Characterization of the stimulating effect of low-dose stressors in maize and bean seedlings.
Journal of Plant Physiology.
(2003);
160
1175-1183
-
32
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
-
33
Pandey N., Sharma C. P..
Effect of heavy metals Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage.
Plant Science.
(2002);
163
753-758
-
34
Patra M., Sharma A..
Mercury toxicity in plants.
Botanical Review.
(2000);
66
379-422
-
35
Poirier I., Bertrand M..
Photosynthetic organisms and excess of metals.
Photosynthetica.
(2005);
43
345-353
-
36
Prasad D. D. K., Prasad A. R. K..
Effect of lead and mercury on chlorophyll synthesis in mung bean seedlings.
Phytochemistry.
(1987 a);
26
881-883
-
37
Prasad D. D. K., Prasad A. R. K..
Altered delta-aminolevulinic acid metabolism by lead and mercury in germinating seedlings of bajra (Pennisetum typhoideum).
Journal of Plant Physiology.
(1987 b);
127
241-249
-
38
Rassadina V., Domanskii V., Averina N. G., Schoch S., Rüdiger W..
Correlation between chlorophyllide esterification, Shibata shift and regeneration of protochlorophyllide650 in flash-irradiated etiolated barley leaves.
Physiologia Plantarum.
(2004);
121
556-567
-
39
Rüdiger W..
Chlorophyll metabolism: from outer space down to the molecular level.
Phytochemistry.
(1997);
46
1151-1167
-
40
Rüdiger W., Benz J., Guthoff C..
Detection and partial characterization of activity of chlorophyll synthetase in etioplast membranes.
European Journal of Biochemistry.
(1980);
190
193-200
-
41
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.
Physiologia Plantarum.
(1986);
66
616-624
-
42
Ryberg M., Sundqvist C..
Characterization of prolamellar bodies and prothylakoids fractionated from wheat etioplasts.
Physiologia Plantarum.
(1982 a);
56
125-132
-
43
Ryberg M., Sundqvist C..
Spectral forms of protochlorophyllide in prolamellar bodies and prothylakoids fractionated from wheat etioplasts.
Physiologia Plantarum.
(1982 b);
56
133-138
-
44
Ryberg M., Sundqvist C..
The regular ultrastructure of isolated prolamellar bodies depends on the presence of membrane-bound NADPH-protochlorophyllide oxidoreductase.
Physiologia Plantarum.
(1988);
73
218-226
-
45
Schlegel H., Godbold D. L., Huttermann A..
Whole plant aspects of heavy metal induced changes in CO2 uptake and water relations of spruce (Picea abies) seedlings.
Physiologia Plantarum.
(1987);
69
265-270
-
46
Schoefs B., Bertrand M., Franck F..
Spectroscopic properties of protochlorophyllide analyzed in situ in the course of etiolation and in illuminated leaves.
Photochemistry and Photobiology.
(2000);
72
85-93
-
47
Schoefs B..
The protochlorophyllide-chlorophyllide cycle.
Photosynthesis Research.
(2001);
70
257-271
-
48
Schoefs B..
Protochlorophyllide reduction - what is new in 2005?.
Photosynthetica.
(2005);
43
329-343
-
49
Schoefs B., Franck F..
Photoreduction of protochlorophyllide to chlorophyllide in 2-d-old dark-grown bean (Phaseolus vulgaris cv. Commodore) leaves. Comparison with 10-d-old dark-grown (etiolated) leaves.
Journal of Experimental Botany.
(1993);
44
1053-1057
-
50
Selstam E., Schelin J., Brain T., Williams W. P..
The effects of low pH on the properties of protochlorophyllide oxidoreductase and the organization of prolamellar bodies of maize (Zea mays).
European Journal of Biochemistry.
(2002);
269
2336-2346
-
51
Shibata K..
Spectroscopic studies on chlorophyll formation in intact leaves.
Journal of Biochemistry.
(1957);
44
147-173
-
52
Smeller L., Solymosi K., Fidy J., Böddi B..
Activation parameters of the blue shift (Shibata shift) subsequent to protochlorophyllide phototransformation.
Biochimica Biophysica Acta.
(2003);
1651
130-138
-
53
Solymosi K., Lenti K., Myśliwa-Kurdziel B., Fidy J., Strzałka K., Böddi B..
Hg2+ reacts with different components of the NADPH : protochlorophyllide oxidoreductase macrodomains.
Plant Biology.
(2004);
6
358-368
-
54
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-F655 to the cop1 photomorphogenic mutant.
Plant Cell.
(1998);
10
283-296
-
55
Stobart A. K., Griffiths W. T., Ameen-Bukhari I., Sherwood R. P..
The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley.
Physiologia Plantarum.
(1985);
63
293-298
-
56
Sundqvist C., Dahlin C..
With chlorophyll pigments from prolamellar bodies to light-harvesting complexes.
Physiologia Plantarum.
(1997);
100
748-759
-
57
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
-
58
Wiktorsson B., Ryberg M., Gough S., Sundqvist C..
Isoelectric focusing of pigment-protein complexes solubilized from non-irradiated and irradiated prolamellar bodies.
Physiologia Plantarum.
(1992);
85
659-669
-
59
Williams W. P., Selstam E., Brain T..
X‐ray diffraction studies of the structural organisation of prolamellar bodies isolated from Zea mays.
.
FEBS Letters.
(1998);
422
252-254
-
60
Willows R. D..
Biosynthesis of chlorophylls from protoporphyrin IX.
Natural Product Reports.
(2003);
20
327-341
B. Böddi
Department of Plant Anatomy
Eötvös University
Pázmány P. sétány 1/C
Budapest, 1117
Hungary
Email: bbfotos@ludens.elte.hu
Editor: R. C. Leegood