Abstract
Under high light intensity, low temperatures as well as heavy metals induce photoinhibition of PSII and oxidative stress in leaves. Since cold acclimation of leaves ameliorates their capacity of antioxidative defence, cross tolerance between cold-induced and heavy metal-induced photoinhibition was investigated in pea leaves grown at either 22 °C or 6 °C. The experimental conditions were chosen to induce a uniform level of short-term photoinhibition at low temperature or in the presence of CuSO4 or CdCl2 in leaves grown at 22 °C. Under all conditions photoinhibition of PSII was lower in cold-acclimated (6°C-grown) than in non-acclimated (22°C-grown) pea leaves. In darkness PSII was not affected by all treatments. Other parameters like catalase activity, chlorophyll content and metabolite contents were most sensitive to CuSO4, but less affected by CdCl2 and low temperature treatments. Strong oxidation of ascorbate and concomitant loss of catalase activity showed the enhanced oxidative stress in CuSO4-treated leaves. Generally, all measured parameters were less affected in cold-acclimated leaves than in non-acclimated leaves under all experimental conditions. Cold-acclimated pea leaves contained higher levels of ascorbate and particularly of glutathione and a higher capacity to keep the primary electron acceptor of PSII more oxidised. Incubation with heavy metals caused a nearly complete loss of reduced glutathione. It is suggested that reduced glutathione served as a source for phytochelatin synthesis. The extraordinarily high glutathione content in cold-acclimated pea leaves might therefore increase their ability to chelate heavy metals and thus to protect leaves from heavy-metal induced damage.
Key words: Antioxidative protection, glutathione, metabolites, photooxidative stress tolerance
Full Text
The Full Text of this article is available as a PDF (503.9 KB).
References
- Adams W.W., III, Demmig-Adams B., Rosenstiel T.N., Brightwell A.K., Ebbert V. Photosynthesis and photoprotection in overwintering plants. Plant Biol. 2002;4:535–654. doi: 10.1055/s-2002-35434. [DOI] [Google Scholar]
- Arisi A.-C., Mocquot B., Lagriffoul A., Mench M., Foyer C.H., Jouanin L. Response to cadmium in leaves of transformed poplars overexpressing γ-glutamylcysteine synthetase. Physiol. Plant. 2000;109:143–149. doi: 10.1034/j.1399-3054.2000.100206.x. [DOI] [Google Scholar]
- Aro E.M., Virgin I., Andersson B. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta. 1993;1143:113–134. doi: 10.1016/0005-2728(93)90134-2. [DOI] [PubMed] [Google Scholar]
- Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. An. Rev. Plant Physiol. Plant Mol. Biol. 1999;50:601–639. doi: 10.1146/annurev.arplant.50.1.601. [DOI] [PubMed] [Google Scholar]
- Baryla A., Carrier P., Franck F., Coulomb C., Sahut C., Havaux M. Leaf clorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta. 2001;212:696–709. doi: 10.1007/s004250000439. [DOI] [PubMed] [Google Scholar]
- Chugh L.K., Sawhney S.K. Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium. Plant Physiol. Biochem. 1999;37:297–303. doi: 10.1016/S0981-9428(99)80028-X. [DOI] [Google Scholar]
- Cobbett C., Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. An. Rev. Plant Biol. 2002;53:159–182. doi: 10.1146/annurev.arplant.53.100301.135154. [DOI] [PubMed] [Google Scholar]
- Dietz K.J., Baier M., Krämer U. Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Prasad M.N.V., Hagemeyer J., editors. Heavy Metal Stress in Plants: form molecules to ecosystems. Berlin Heidelberg: Springer Verlag; 1999. pp. 73–97. [Google Scholar]
- Feierabend J., Schaan C., Hertwig B. Photoinactivation of catalase occurs under both high-and low-temperature stress conditions and accompanies photoinhibition of PSII. Plant Physiol. 1992;100:1554–1561. doi: 10.1104/pp.100.3.1554. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Foyer C.H. Oxygen metabolism and electron transport in photosynthesis. In: Scandalios J.G., editor. Oxidative Stress and the Molecular Biology of Antioxidant Defences. Monographs: Cold Spring Harbor Laboratory Press; 1997. pp. 587–621. [Google Scholar]
- Huner N.P.A., Öquist G., Hurry V.M., Krol M., Falk S., Griffith M. Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth. Res. 1993;37:19–39. doi: 10.1007/BF02185436. [DOI] [PubMed] [Google Scholar]
- Huner N.P.A., Öquist G., Sarhan F. Energy balance and acclimation to light and cold. Trends Plant Sci. 1998;3:224–230. doi: 10.1016/S1360-1385(98)01248-5. [DOI] [Google Scholar]
- Kocsy G., Galiba G., Brunold C. Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol. Plant. 2001;113:158–164. doi: 10.1034/j.1399-3054.2001.1130202.x. [DOI] [PubMed] [Google Scholar]
- Mishra S., Srivastava S., Tripathi R.D., Govindarajan R., Kuriakose S.V., Prasad M.N.V. Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol. and Biochem. 2006;44:25–37. doi: 10.1016/j.plaphy.2006.01.007. [DOI] [PubMed] [Google Scholar]
- Ort D.R., Baker N.R. A photoprotective role of O2 as an alternative electron sink in photosynthesis? Curr. Opin. Plant Biol. 2002;5:193–198. doi: 10.1016/S1369-5266(02)00259-5. [DOI] [PubMed] [Google Scholar]
- Pätsikkä E., Aro E.-M., Tyystjärvi E. Mechanism of copper-enhanced photoinhibition in thylakoid membranes. Physiol. Plant. 2001;113:142–150. doi: 10.1034/j.1399-3054.2001.1130119.x. [DOI] [Google Scholar]
- Polle, A. (1997) Defense against photooxidative damage in plants. In: Oxidative Stress and the Molecular Biology of Antioxidant Defences (ed. J.G. Scandalios) Cold Spring Harbor Laboratory Press, Monographs 34, pp. 623–666
- Prasad M.N.V. Metollothioneins and metal binding complexes in plants. In: Prasad M.N.V., Hagemeyer J., editors. Heavy Metal Stress in Plants: form molecules to ecosystems. Berlin Heidelberg: Springer Verlag; 1999. pp. 51–72. [Google Scholar]
- Prasad M.N.V., Strzalka K. Impact of heavy metals on photosynthesis. In: Prasad M.N.V., Hagemeyer J., editors. Heavy Metal Stress in Plants: form molecules to ecosystems. Berlin Heidelberg: Springer Verlag; 1999. pp. 117–138. [Google Scholar]
- Rauser W.E. Phytochelatins. An. Rev. Biochem. 1990;59:61–86. doi: 10.1146/annurev.bi.59.070190.000425. [DOI] [PubMed] [Google Scholar]
- Scheibe R. Malate valves to balance cellular energy supply. Physiol. Plant. 2004;120:21–26. doi: 10.1111/j.0031-9317.2004.0222.x. [DOI] [PubMed] [Google Scholar]
- Sarry J.-E., Kuhn L., Ducruix C., Lafaye A., Junot C., Hugouvieux V., Jourdain A., Bastien O., Fievet J.B., Vailhen D., Amekraz B., Moulin C., Ezan E., Garin J., Bourguignon J. The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics. 2006;6:2180–2198. doi: 10.1002/pmic.200500543. [DOI] [PubMed] [Google Scholar]
- Schöner S., Krause G.H. Protective systems against active oxygen species in spinach: response to cold acclimation in excess light. Planta. 1990;180:383–389. doi: 10.1007/BF01160394. [DOI] [PubMed] [Google Scholar]
- Schützendübel A., Polle A. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 2002;53:1351–1365. doi: 10.1093/jexbot/53.372.1351. [DOI] [PubMed] [Google Scholar]
- Streb P., Aubert S., Gout E., Bligny R. Reversibility of cold-and light-stress tolerance and accompanying changes of metabolite and antioxidant levels in the two high mountain plant species Soldanella alpina and Ranunculus glacialis. J. Exp. Bot. 2003;54:405–418. doi: 10.1093/jxb/54.381.405. [DOI] [PubMed] [Google Scholar]
- Streb P., Feierabend J. Significance of antioxidants and electron sinks for the cold-hardening-induced resistance of winter rye leaves to photo-oxidative stress. Plant Cell Environ. 1999;22:1225–1237. doi: 10.1046/j.1365-3040.1999.00482.x. [DOI] [Google Scholar]
- Streb P., Josse E.-M., Gallouët E., Baptist F., Kuntz M., Cornic G. Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant Cell Environ. 2005;28:1123–1135. doi: 10.1111/j.1365-3040.2005.01350.x. [DOI] [Google Scholar]
- Streb P., Michael-Knauf A., Feierabend J. Preferential photoinactivation of catalase and photoinhibition of photosystem II are common early symptoms under various osmotic and chemical stress conditions. Physiol. Plant. 1993;88:590–598. doi: 10.1111/j.1399-3054.1993.tb01376.x. [DOI] [PubMed] [Google Scholar]
- Streb P., Shang W., Feierabend J. Resistance of cold-hardened winter rye leaves (Secale cereale L.) to photo-oxidative stress. Plant Cell Environ. 1999;22:1211–1223. doi: 10.1046/j.1365-3040.1999.00483.x. [DOI] [Google Scholar]
- Streb P., Shang W., Feierabend J., Bligny R. Divergent strategies of photoprotection in high-mountain plants. Planta. 1998;207:313–324. doi: 10.1007/s004250050488. [DOI] [Google Scholar]
- Tewari R.K., Kumar P., Sharma P.N. Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants. Planta. 2006;223:1145–1153. doi: 10.1007/s00425-005-0160-5. [DOI] [PubMed] [Google Scholar]
- Wise R.R. Chilling-enhanced photooxidation: The production, action and study of reactive oxygen species produced during chilling in the light. Photosynth. Res. 1995;45:79–97. doi: 10.1007/BF00032579. [DOI] [PubMed] [Google Scholar]
- Yruela I., Alfonso M., Baron M., Picorel R. Copper effect on the protein composition of photosystem II. Physiol. Plan. 2000;110:551–557. doi: 10.1111/j.1399-3054.2000.1100419.x. [DOI] [Google Scholar]
- Zhu Y.L., Pilon-Smits E.A.H., Jouanin L., Terry N. Overexpression of glutathione synthetase in indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 1999;119:73–79. doi: 10.1104/pp.119.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu Y.L., Pilon-Smits E.A.H., Tarun A.S., Weber S.U., Jouanin L., Terry N. Cadmium tolerance and accumulation in indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol. 1999;121:1169–1177. doi: 10.1104/pp.121.4.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]