Abstract
Light-intensity and redox-state induced thylakoid proteins phosphorylation involved in structural changes and in regulation of protein turnover. The presence of heavy metal ions triggers a wide range of cellular responses including changes in plant growth and photosynthesis. Plants have evolved a number of mechanisms to protect photosynthetic apparatus. We have characterized the effect of lead on PSII protein phosphorylation in pea (Pisum sativum L.) plants grown in low light conditions. Pb ions affected only slightly photochemical efficiency of PSII and had no effect on organization of thylakoid complexes. Lead activated strongly phosphorylation of PSII core D1 protein and dephosphorylation of this protein did not proceed in far red light. D1 protein was also not degraded in this conditions. However, phosphorylation of LHCII proteins was not affected by lead. These results indicate that Pb2+ stimulate the phosphorylation of PSII core proteins and by disturbing the disassembly of supercomplexes play a role in PSII repair mechanism. LHCII phosphorylation could control the distribution of energy between the photosystems in low light conditions. This demonstrates that plants may respond to heavy metals by induction different pathways responsible for protein protection under stress conditions.
Similar content being viewed by others
References
Allen JF (2003) Botany. State transitions-a question of balance. Science 299:1530–1532
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Aro EM, Rokka A, Vener AV (2004) Determination of phosphoproteins in higher plant thylakoids. In: Carpentier R (ed) Photosynthesis research protocols, methods in molecular biology. Humana Press, USA, pp 271–285
Artetxe U, García-Plazaola JI, Hernández A, Becerril JM (2002) Low light grown duckweed plants are more protected against the toxicity induced by Zn and Cd. Plant Physiol Biochem 40:859–863
Baena-Gonzalez E, Barbato R, Aro EM (1999) Role of phosphorylation in the repair cycle and oligomeric structure of photosystem II. Planta 208:196–204
Bennett J (1991) Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42:281–311
Bergantino E, Sandona D, Cugini D, Bassi R (1998) The photosystem II subunit CP29 can be phosphorylated in both C3 and C4 plants as suggested by sequence analysis. Plant Mol Biol 36:11–22
Bertrand M, Poirier I (2005) Photosynthetic organism and excess of metals. Photosynthetica 43:345–353
Chen LB, Jia HY, Tian Q, Du L, Gao Y, Miao X, Liu Y (2012) Protecting effect of phosphorylation on oxidative damage of D1 protein by down- regulating the production of superoxide anion in photosystem II membranes under high light. Photosynth Res 112:141–148
Cuypers A, Vangronsveld J, Clijsters H (1999) The chemical behaviour of heavy metals plays a prominent role in the induction of oxidative stress. Free Rad Res 31:39–43
Dannehl H, Herbik A, Godde D (1995) Stress induced degradation of the photosynthetic apparatus is accompanied by changes in thylakoid protein-turnover and phosphorylation. Physiol Plant 93:179–186
Eick MJ, Peak JD, Brady PV, Pesek JD (1999) Kinetics of lead adsorption/desorption on goethite: residence time effect. Soil Sci 164:28–39
Elich TD, Edelman M, Mattoo AK (1993) Dephosphorylation of photosystem II core proteins is light-regulated in vivo. EMBO J 12:4857–4862
Fagioni M, D’Amici GM, Timperio AM, Zolla L (2009) Proteomic analysis of multiprotein complexes in the thylakoid membrane upon cadmium treatment. J Proteome Res 8:310–326
Franco E, Alessandrelli S, Masojidek J, Margonelli A, Giardi MT (1999) Modulation of D1 protein turnover under cadmium and heat stresses monitored by (35S) methionine incorporation. Plant Sci 144:53–61
Geiken B, Masojidek J, Rizutto M, Pompili ML, Giardi MT (1998) Incorporation of [S-35] methionine in higher plants reveals that stimulation of the D1 reaction centre II protein turnover accompanies tolerance to heavy metal stress. Plant Cell Environ 21:1265–1273
Giardi MT, Rigoni F, Barbato R (1992) Photosystem II core phosphorylation heterogenity, differential herbicide binding and regulation of electron transfer in photosystem II preparations from spinach. Plant Physiol 100:1948–1954
Hattab S, Dridi B, Chouba L, Kheder MB, Bousetta H (2009) Photosynthesis and growth responses of pea Pisum sativum L. under heavy metals stress. J Environ Sci 21:1552–1556
Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147:806–816
Janik E, Szczepaniuk J, Maksymiec W (2013) Organization and functionality of chlorophyll-protein complexes in thylakoid membranes isolated from Pb-treated Secale cereale. J Photoch Photobio B 125:98–104
Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress. Activation of distinct mitogen- activated protein kinase pathways by copper and cadmium. Plant Physiol 136:3276–3283
Kruse O, Zheleva D, Barber J (1997) Stabilization of photosystem II dimmers by phosphorylation: implication for the regulation of the turnover of the D1 protein. FEBS Lett 408:276–280
Kügler M, Jänsch L, Kruft V, Schmitz UK, Braun H (1997) Analysis of the chloroplast protein complexes by blue-native polyacrylamide gel electrophoresis (BN-PAGE). Photosynth Res 53:35–44
Laemlli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Liu D, Li T, Jin X, Yang X, Islam E, Mahmood Q (2008) Lead induced changes in the growth and antioxidant metabolism of the lead accumulating and non-accumulating ecotypes of Sedum alfredii. J Integr Plant Biol 50:129–140
Mizoguchi T, Irie K, Shinozaki K (1997) Environmental stress response in plants: the role of mitogen- activited protein kinase. Trends Biotechnol 15:15–19
Murata N (1969) Control of excitation transfer in photosynthesis. II. Magnesium ion- dependent distribution of excitation energy between two pigment systems in spinach chloroplasts. Biochim Biophys Acta 189:171–181
Parys E, Romanowska E, Siedlecka M, Poskuta JW (1998) The effect of lead on photosynthesis and respiration in detached leaves and in mesophyll protoplasts of Pisum sativum. Acta Physiol Plant 20:313–322
Parys E, Wasilewska W, Siedlecka M, Zienkiewicz M, Drożak A, Romanowska E (2014) Metabolic Responses to Lead of Metallicolous and Nonmetallicolous Populations of Armeria maritima. Arch Environ Contam Toxicol. doi:10.1007/s00244-014-0057-z
Pesaresi P, Pribil M, Wunder T, Leister D (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of STN7, STN8 and TAP38. Biochim Biophys Acta 1807:887–896
Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. In: Whitacre DM (ed) Reviews of Environmental Contamination and Toxicology. Springer, Berlin, pp 113–136
Pribil M, Pesaresi P, Hertle A, Barbato R, Leister D (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol 8:e1000288
Qufei L, Fashui H (2009) Effects of Pb2+ on the structure and function of photosystem II of Spirodela polyrrhiza. Biol Trace Elem Res 129:251–260
Rintamäki E, Salo R, Kuivuniemi A, Aro EM (1996) Protein phosphorylation and magnesium status regulate the degradation of the D1 reaction center protein of photosystem II. Plant Sci 115:175–182
Rintamäki E, Martinsuo P, Pursiheimo S, Aro EM (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97:11644–11649
Romanowska E (2002) Gas exchange functions in heavy metal stressed plants. In: Prasad MNV (ed) Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Kluwer, London, pp 257–285
Romanowska E, Albertsson PA (1994) Isolation and characterization of the cytochrome b/f complex from whole thylakoids, grana and stroma lamellae vesicles from spinach chloroplasts. Plant Cell Physiol 35:557–568
Romanowska E, Igamberdiev A, Parys E, Gardeström P (2002) Stimulation of respiration by Pb2+ ions in detached leaves and mitochondria of C3 and C4 plants. Physiol Plantarum 116:148–154
Romanowska E, Wróblewska B, Drozak A, Zienkiewicz M, Siedlecka M (2008) Effect of Pb ions on superoxide dismutase and catalase activities in leaves of pea plants grown in high and low irradiance. Biol Plantarum 52:80–86
Romanowska E, Wasilewska W, Fristedt R, Vener AV, Zienkiewicz M (2012) Phosphorylation of PSII proteins in maize thylakoids in the presence of Pb ions. J Plant Physiol 169:345–352
Samol I, Shapiguzov A, Ingelsson B, Fucile G, Crevecoeur M, Vener AV, Rochaix JD, Goldschmidt-Clermonta M (2012) Identification of a photosystem II phosphatase involved in light acclimation in Arabidopsis. Plant Cell 24:2596–2609
Schägger H (2001) Blue-native gels to isolate protein complexes from mitochondria. Method Cell Biol 65:231–244
Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci USA 107:4782–4787
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52
Silverstein T, Cheng L, Allen JF (1993) Chloroplast thylakoid protein phosphatase reactions are redox- independent and kinetically heterogeneous. FEBS Lett 334:101–105
Tikkanen M, Nurmi M, Kangasjärvi S, Aro EM (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim Biophys Acta 1777:1432–1437
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci 76:4350–4354
Varkonyi Z, Nagy G, Lambrev P, Kiss AZ, Szekély N, Rosta L, Garab G (2009) Effect of phosphorylation on the thermal and light stability of the thylakoid membranes. Photosynth Res 99:161–171
Vener AV (2007) Environmentally modulated phosphorylation and dynamics of proteins in photosynthetic membranes. Biochim Biophys Acta 1767:449–457
Yang DH, Webster J, Adam Z, Lindahl M, Andersson B (1998) Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities. Plant Physiol 118:827–834
Yeh PY, Chuang SE, Yeh KH, Song YC, Chang LL, Cheng AL (2004) Phosphorylation of p53 on Thr55 by ERK2 is necessary for doxorubicin-induced p53 activation and cell death. Oncogene 23:3580–3588
Zhang S, Weng J, Pan J, Tu T, Yao S, Xu C (2003) Study on the photo- generation of superoxide radicals in photosystem II with EPR spin trapping techniques. Photosynth Res 75:41–48
Acknowledgments
These studies were founded by the grant NN 303 811740 from the Ministry of Science and High Education of Poland and by State Committee for Scientific Research, through Faculty of Biology, Warsaw University intramural grant, BW 501/86-100047. We are grateful to Dr Tomasz Krupnik for the English correction of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wioleta, W., Anna, D., Ilona, B. et al. Lead induced changes in phosphorylation of PSII proteins in low light grown pea plants. Biometals 28, 151–162 (2015). https://doi.org/10.1007/s10534-014-9811-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-014-9811-y