Abstract
The effect of high light on spatial distribution of chlorophyll (Chl) fluorescence parameters over a lichen thallus (Umbilicaria antarctica) was investigated by imaging of Chl fluorescence parameters before and after exposure to high light (1500 µmol m-2 s-1 , 30 min at 5 °C). False colour images of FV /FM and ΦII distribution, taken over thallus with 0.1 mm2 resolution, showed that maximum FV /FM and ΦII values were located close to the thallus centre. Minimum values were typical for thallus margins. After exposure to high light, a differential response of FV /FM and ΦII was found. The marginal thallus part exhibited a loss of photosynthetic activity, manifested as a lack of Chl fluorescence signal, and close-to-centre parts showed a different extent of FV /FM and ΦII decrease. Subsequent recovery in the dark led to a gradual return of FV /FM and ΦII to their initial values. Fast (30 min) and slow (1 - 22 h) phase of recovery were distinguished, suggesting a sufficient capacity of photoprotective mechanisms in U. antarctica to cope with low-temperature photoinhibition. Glutathione and xanthophyll cycle pigments were analyzed by HPLC. High light led to an increase in oxidized glutathione (GSSG), and a conversion of violaxanthin to zeaxanthin, expressed as their de-epoxidation state (DEPS). The responses of GSSG and DEPS were reversible during subsequent recovery in the dark. GSSG and DEPS were highly correlated to non-photochemical quenching (NPQ), indicating involvement of these antioxidants in the resistance of U. antarctica to high-light stress. Heterogeneity of Chl fluorescence parameters over the thallus and differential response to high light are discussed in relation to thallus anatomy and intrathalline distribution of the symbiotic alga Trebouxia sp.
Key words
Antioxidants - lichen - low temperature - oxidative stress - photoinhibition - photosynthesis
References
1 Ahmadjian V.. The Lichen Symbiosis. New York, Chechester, Brisbane, Toronto, Singapore; John Wiley & Sons (1993): 250
2
Arora A., Sairam R. K., Srivastava G. C..
Oxidative stress and antioxidative system in plants.
Current Science,.
(2002);
10
1227-1238
3
Ascaso C., Valladares F..
Comparative stereological study of the photobiont of Lasallia hispanica (Frey) Sancho and Crespo and Umbilicaria spodochroa var. Carpetana prov.
Symbiosis.
(1991);
11
147-162
4
Barták M., Hájek J., Gloser J..
Heterogeneity of chlorophyll fluorescence over thalli of several foliose macrolichens exposed to adverse environmental factors: Interspecific differences as related to thallus hydration and high irradiance.
Photosynthetica.
(2000);
38
531-537
5
Barták M., Vráblíková H., Hájek J..
Sensitivity of photosystem 2 of Antarctic lichens to high irradiance stress: A fluorometric study of fruticose (Usnea antarctica) and foliose (Umbilicaria decussata) species.
Photosynthetica.
(2003);
41
497-504
6
Bilger W., Rimke S., Schreiber U..
Inhibition of energy-transfer to photosystem-II in lichens by dehydration - different properties of reversibility with green and blue-green phycobionts.
J. Plant Physiol..
(1989);
134
261-268
7
Büdel B., Lange O. L..
The role of cortical and epinecral layers in the lichen genus Peltula.
.
Cryptogamic Botany.
(1994);
4
262-269
8
Burritt D. J., Mackenzie S..
Antioxidant metabolism during acclimation of Begonia × erythrophylla to high light levels.
Annals of Botany.
(2003);
91
783-794
9
Calatayud A., Deltoro V. I., Barreno E., del Valle-Tascon S..
Changes in in vivo chlorophyll fluorescence quenching in lichen thalli as a function of water content and suggestion of zeaxanthin-associated photoprotection.
Physiologia Plantarum.
(1997);
101
93-102
10
Demmig-Adams B., Adams III. W. W., Czygan F. C., Schreiber U., Lange O. L..
Differences in the capacity for radiationless energy dissipation in the photochemical apparatus of green and blue-green algal lichens associated with differences in carotenoid composition.
Planta.
(1990 a);
180
582-589
11
Demmig-Adams B., Adams III. W. W., Green T. G. A., Czygan F. C., Lange O. L..
Differences in the susceptibility to light stress in two lichens forming a phycosymbiodeme, one partner possessing and one lacking the xanthophyll cycle.
Oecologia.
(1990 b);
84
451-456
12
Friedl T..
New aspects of the reproduction by autospores in the lichen alga Trebouxia (Microthamniales, Chlorophyta).
Arch. Protistenkd..
(1993);
143
153-161
13
Gauslaa Y., Solhaug K. A..
Differences in the susceptibility to light stress between epiphytic lichens of ancient and young boreal forest stand.
Functional Ecology.
(1996);
10
344-354
14
Gauslaa Y., Solhaug K. A..
High-light-intensity damage to the foliose lichen Lobaria pulmonaria within a natural forest: The applicability of chlorophyll fluorescence methods.
Lichenologist.
(2000);
32
271-289
15
Hestmark G..
Growth from the centre in an umbilicate lichen.
Lichenologist.
(1997);
29
379-383
16
Hestmark G., Schroeter B., Kappen L..
Intrathalline and size-dependent patterns of activity in Lasallia pustulata and their possible consequences for competitive interactions.
Functional Ecology.
(1997);
11
318-322
17
Hill D..
Lichens and co-ordination of symbionts.
Microbiology Today.
(2001);
28
124-127
18
Hurry V. M., Gardeström P., Öquist G..
Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability.
Planta.
(1993);
190
484-490
19
Jensen M., Siebke K..
Fluorescence imaging of lichens in the macro scale.
Symbiosis.
(1997);
23
183-196
20
Kappen L., Schroeter B., Green T. G. A., Seppelt R. D..
Chlorophyll a fluorescence and CO2 exchange of Umbilicaria aprina under extreme light stress in the cold.
Oecologia.
(1998);
113
325-331
21
Kennedy A. D..
Antarctic terrestrial ecosystem response to global environmental change.
Ann. Rev. Ecol. Syst..
(1995);
26
683-704
22
Kong F. X., Hu W., Chao S. Y., Sang W. L., Wang L. S..
Physiological responses of the lichen Xanthoparmelia mexicana to oxidative stress of SO2 .
Environmental and Experimental Botany.
(1999);
42
201-209
23 Kranner I.. Determination of glutathione, glutathione disulphide and two related enzymes, glutathione reductase and glucose-6-phosphate deydrogenase, in fungal and plant cells. Varma, A., ed. Mycorrhiza Manual. Berlin; Springer Verlag (1998): 227-241
24
Kranner I..
Glutathione status correlates with different degrees of desiccation tolerance in three lichens.
New Phytologist.
(2002);
154
451-460
25
Kranner I., Grill D..
Determination of glutathione and glutathione disulphide in lichens: A comparison of frequently used methods.
Phytochemical Analysis.
(1996);
7
24-28
26
Leipner J., Oxborough K., Baker N. R..
Primary sites of ozone-induced perturbations of photosynthesis in leaves: identification and characterization in Phaseolus vulgaris using high resolution chlorophyll fluorescence imaging.
J. Exp. Bot..
(2001);
52
1689-1696
27 Lewis Smith R. I.. Signy Island as a paradigm of biological and environmental change in Antarctic terrestrial ecosystems. Kerry, K. R. and Hempel, G., eds. Antarctic Ecosystems - Ecological Change and Conservation. Heidelberg; Springer Verlag (1990): 30-48
28
Maguas C., Valladares F., Brugnoli E..
Effects of thallus size on morphology and physiology of foliose lichens: New findings with a new approach.
Symbiosis.
(1997);
23
149-164
29
Malmezat T., Breuille D., Capitan P., Mirand P. P., Obled C..
Glutathione turnover is increased during the acute phase of sepsis in rats.
Journal of Nutrition.
(2000);
130
1239-1246
30
Manrique E., Balagauer L., Barnes J., Davidson A. W..
Photoinhibition studies in lichens using chlorophyll fluorescence analysis.
Bryologist.
(1993);
96
443-449
31
Meyer S., Saccardy-Adji K., Rizza C., Genty B..
Inhibition of photosynthesis by Colletotrichum lindemuthianum in bean leaves determined by chlorophyll fluorescence imaging.
Plant, Cell and Environment.
(2001);
24
947-956
32
Noctor G., Arisi A.-C. M., Jouanin L., Valadier M.-H., Roux Y., Foyer C. H..
Light-dependent modulation of foliar glutathione synthesis and associated amino acid metabolism in poplar overexpressing γ-glutamylcysteine synthetase.
Planta.
(1997);
202
357-369
33
Noctor G., Arisi A.-C. M., Jouanin L., Kunert K. J., Rennenberg H., Foyer C. H..
Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants.
Journal of Experimental Botany.
(1998);
49
623-647
34
Öquist G., Huner N. P. A..
Cold hardening-induced resistance to photoinhibition of photosynthesis in winter rye is dependent upon an increased capacity for photosynthesis.
Planta.
(1993);
189
150-156
35
Pappas P. V..
The use of chrome alum-gelatin (subbing) solution as a general adhesive for paraffine sections.
Stain. Technol..
(1971);
46
121-124
36 Pfeifhofer H. W., Willfurth R., Zorn M., Kranner I.. Analysis of chlorophylls, carotenoids, and tocopherols in lichens. Kranner, I., Beckett, R. P., and Varma, A. K., eds. Protocols in Lichenology. Berlin; Springer Verlag (2002): 363-378
37
Rohácek K., Barták M..
Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications.
Photosynthetica.
(1999);
37
339-363
38
Sancho L. G., Kappen L..
Photosynthesis and water relations and the role of anatomy in Umbilicariaceae (Lichenes) from central Spain.
Oecologia.
(1989);
81
473-480
39
Sancho L. G., Schroeter B., Valladares F..
Umbilicaria kappeni (Umbilicariaceae) a new lichen species from Antarctica with multiple mechanisms for the simultaneous dispersal of both symbionts.
Nova Hedwigia.
(1998);
67
279-288
40
Sancho L. G., Schulz F., Schroeter B., Kappen L..
Bryophyte and lichen flora of South Bay (Livingston Island: South Shetland Islands, Antarctica).
Nova Hedwigia.
(1999);
68
301-337
41
Schofield S. C., Campbell D. A., Funk Ch., MacKenzie T. D. B..
Changes in macromolecular allocation in nondividing algal symbionts allow for photosynthetic acclimation in the lichen Lobaria pulmonaria.
.
New Phytologist.
(2003);
159
709-718
42
Schroeter B., Green T. G. A., Seppelt R. D., Kappen L..
Monitoring photosynthetic activity of crustose lichens using a PAM-2000 fluorescence system.
Oecologia.
(1992);
92
457-462
43
Schupp R., Rennenberg H..
Light-dependent changes in the glutathione content of Norway spruce (Picea abies [L.] Karst.).
Ann. Sci. For..
(1989);
46
837-841
44
Silberstein L., Siegel B. Z., Siegel S. M., Mukhtar A., Galun M..
Comparative studies of Xanthotia parietina, a pollution-resistant lichen, and Ramalina duriaei, a sensitive species. II. Evaluation of possible pollution protection mechanism.
Lichenologist.
(1996);
28
355-365
45
Stark P..
Climatic warming in the Central Antarctic Peninsula area.
Weather.
(1994);
49
215-220
46
Streb P., Aubert S., Gout E., Bligny R..
Cold- and light-induced changes of metabolite and antioxidant levels in two high mountain plant species Soldanella alpina and Ranunculus glacialis and a lowland species Pisum sativum.
.
Physiologia Plantarum.
(2003);
118
96-104
47
van Kooten O., Snell J. F. H..
The use of chlorophyll fluorescence nomenclature in plant stress physiology.
Photosynthesis Research.
(1990);
25
147-150
48
Valladares F..
Texture and hygroscopic features of the upper surface of the thallus in the lichen family Umbilicariaceae.
Annals of Botany.
(1994);
73
493-500
49
Valladares F., Ascaso C., Sancho L. G..
Intrathalline variability of some structural and physical parameters in the lichen genus Lasallia.
Canadian Journal of Botany.
(1994);
72
415-428
50
Valladares F., Sanches-Hoyos A., Manrique E..
Diurnal changes in photosynthetic efficiency and carotenoid composition of the lichen Anaptychia ciliaris : effect of hydration and light intensity.
Bryologist.
(1995);
98
375-382
51
Valladares F., Sancho L. G., Ascaso C..
Functional analysis of the intrathalline and intracellular chlorophyll concentrations in the lichen family Umbilicariaceae.
Annals of Botany,.
(1996);
78
471-477
52
Valladares F., Sancho L. G., Chico J. M., Manrique E..
Differences in the photosynthetic utilization of high irradiance by co-occuring lichen and vascular plants in the maritime Antarctica.
Bol. R. Soc. Esp. Hist. Nat. (Sec. Biol.).
(1997);
93
119-125
53
Vanacker H., Carver T. L. V., Foyer C. H..
Early H2 O2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction.
Plant Physiology.
(2000);
123
1289-1300
M. Barták
Masaryk University Faculty of Science Department of Plant Physiology and Anatomy
Kotlárská 2
61137 Brno
Czech Republic
eMail: mbartak@sci.muni.cz
Guest Editor: F. Loreto