Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Effect of protein modification by malondialdehyde on the interaction between the oxygen-evolving complex 33 kDa protein and photosystem II core proteins

  • 410 Accesses

  • 30 Citations

Abstract

Previously we observed that the oxygen-evolving complex 33 kDa protein (OEC33) which stabilizes the Mn cluster in photosystem II (PSII), was modified with malondialdehyde (MDA), an end-product of peroxidized polyunsaturated fatty acids, and the modification increased in heat-stressed plants (Yamauchi et al. 2008). In this study, we examined whether the modification of OEC33 with MDA affects its binding to the PSII complex and causes inactivation of the oxygen-evolving complex. Purified OEC33 and PSII membranes that had been removed of extrinsic proteins of the oxygen-evolving complex (PSII∆OEE) of spinach (Spinacia oleracea) were separately treated with MDA. The binding was diminished when both OEC33 and PSII∆OEE were modified, but when only OEC33 or PSII∆OEE was treated, the binding was not impaired. In the experiment using thylakoid membranes, release of OEC33 from PSII and corresponding loss of oxygen-evolving activity were observed when thylakoid membranes were treated with MDA at 40°C but not at 25°C. In spinach leaves treated at 40°C under light, maximal efficiency of PSII photochemistry (F v/F m ratio of chlorophyll fluorescence) and oxygen-evolving activity decreased. Simultaneously, MDA contents in heat-stressed leaves increased, and OEC33 and PSII core proteins including 47 and 43 kDa chlorophyll-binding proteins were modified with MDA. In contrast, these changes were to a lesser extent at 40°C in the dark. These results suggest that MDA modification of PSII proteins causes release of OEC33 from PSII and it is promoted in heat and oxidative conditions.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Abbreviations

BCIP:

Bromo-chloro-indolyl phosphate

CP:

Chlorophyll-binding protein

Fv/Fm:

Maximal efficiency of PSII photochemistry

MDA:

Malondialdehyde

NBT:

Nitroblue tetrazolium

OEC:

Oxygen-evolving complex

OEC33:

Oxygen-evolving complex 33 kDa protein

PSII:

Photosystem II

PSII∆OEE:

PSII containing no extrinsic proteins

PUFA:

Polyunsaturated fatty acid

ROS:

Reactive oxygen species

TBA:

Thiobarbituric acid

References

  1. Alfonso M, Yruela I, Almárcegui S, Torrado E, Pérez MA, Picorel R (2001) Unusual tolerance to high temperature in a new herbicide-resistant D1 mutant from Glycine max (L.) Merr. cell cultures deficient in fatty acid desaturation. Planta 212:573–582

  2. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

  3. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

  4. Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen’s and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

  5. Barber J, Morris E, Büchel C (2000) Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47. Biochim Biophys Acta 1459:239–247

  6. Berg EW, Herrera NM, Modenbach CL (1983) Sublimation of bis(1,3-propanedial) chelates of palladium(II) and chromium(III). Inorg Chem 22:1991–1993

  7. Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543

  8. Davey MW, Stals E, Panis B, Keulemans J, Swennen RL (2005) High-throughput determination of malondialdehyde in plant tissues. Anal Biochem 347:201–207

  9. Debus RJ (2001) Amino acid residues that modulate the properties of tyrosine Yz and the manganese cluster in the water oxidizing complex of photosystem II. Biochim Biophys Acta 1503:164–186

  10. Eckardt N, Portis AR Jr (1997) Heat denaturation profiles of ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase and the inability of Rubisco activase to restore activity of heat-denatured Rubisco. Plant Physiol 113:243–248

  11. Enami I, Kitamura M, Tomo T, Isokawa Y, Ohta H, Katoh S (1994) Is the primary case of thermal inactivation of oxygen evolution in spinach PS II membranes release of the extrinsic 33 kDa protein or of Mn? Biochim Biophys Acta 1186:52–58

  12. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11:81–128

  13. Ettinger W, Theg SM (1991) Physiologically active chloroplasts containing pools of unassembled extrinsic proteins of the photosynthetic oxygen-evolving enzyme complex in the thylakoid lumen. J Cell Biol 115:321–328

  14. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

  15. Ghanotakis DF, Yocum CF (1990) Photosystem II and the oxygen-evolving complex. Annu Rev Plant Physiol Plant Mol Biol 41:255–276

  16. Gleiter HM, Haag E, Shen JRS, Eaton-Rye JJ, Inoue Y, Vermaas WFJ (1994) Functional characterization of mutant strains of the cyanobacterium Synechocystis PCC 6803 lacking short domains within the large, lumen-exposed loop of the chlorophyll protein CP47 in photosystem II. Biochemistry 33:12063–12071

  17. Gleiter HM, Haag E, Shen JR, Eaton-Rye JJ, Seeliger AG, Inoue Y, Vermaas WFJ, Renger G (1995) Involvement of the CP47 protein in stabilization and photoactivation of a functional water-oxidizing complex in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 34:6847–6856

  18. Haag E, Eaton-Rye JJ, Renger G, Vermaas WFJ (1993) Functionally important domains of the large hydrophilic loop of CP47 as probed by oligonucleotide-directed mutagenesis in Synechocystis sp. PCC 6803. Biochemistry 32:4444–4454

  19. Hankamer B, Morris EP, Barber J (1999) Revealing the structure of the oxygen-evolving core dimer of photosystem II by cryoelectron crystallography. Nat Struct Biol 6:560–564

  20. Hashimoto A, Yamamoto Y, Theg SM (1996) Unassembled subunits of the photosynthetic oxygen-evolving complex present in the thylakoid lumen are long-lived and assembly-competent. FEBS Lett 391:29–34

  21. Hayashi H, Fujimura Y, Mohanty PS, Murata N (1993) The role of CP 47 in the evolution of oxygen and the binding of the extrinsic 33-kDa protein to the core complex of photosystem II as determined by limited proteolysis. Photosynth Res 36:35–42

  22. Heldt HW, Werden K, Milovancev M, Geller G (1973) Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim Biophys Acta 314:224–241

  23. Ichihashi K, Osawa T, Toyokuni S, Uchida K (2001) Endogenous formation of protein adducts with carcinogenic aldehydes. J Biol Chem 276:23903–23913

  24. Ishii T, Ito S, Kumazawa S, Sakurai T, Yamaguchi S, Mori T, Nakayama T, Uchida K (2008) Site-specific modification of positively-charged surfaces on human serum albumin by malondialdehyde. Biochem Biophys Res Commun 371:28–32

  25. Johansson E, Olsson O, Nyström T (2004) Progression and specificity of protein oxidation in the life cycle of Arabidopsis thaliana. J Biol Chem 279:22204–22208

  26. Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

  27. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346

  28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

  29. Lydakis-Simantiris N, Hutchison RS, Betts SD, Barry BA, Yocum CF (1999) Manganese stabilizing protein of photosystem II is a thermostable, natively unfolded polypeptide. Biochemistry 38:404–414

  30. Mano J, Miyatake F, Hiraoka E, Tamoi M (2009) Evaluation of the toxicity of stress-related aldehydes to photosynthesis in chloroplasts. Planta 230:639–648

  31. Marnett LJ, Tuttle MA (1980) Comparison of the mutagenicities of malondialdehyde and the side products formed during its chemical synthesis. Cancer Res 40:276–282

  32. Mishra RK, Singhal GS (1992) Function of photosynthetic apparatus of intact wheat leaves under high light and heat stress and its relationship with peroxidation of thylakoid lipids. Plant Physiol 98:1–6

  33. Miura T, Shen JR, Takahashi S, Kamo M, Nakamura E, Ohta H, Kamei A, Inoue Y, Domae N, Takio K, Nakazato K, Inoue Y, Enami I (1997) Identification of domains on the extrinsic 33-kDa protein possibly involved in electrostatic interaction with photosystem II complex by means of chemical modification. J Biol Chem 272:3788–3798

  34. Miyao M, Murata N (1989) The mode of binding of three extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in the photosystem II complex of spinach. Biochim Biophys Acta 977:315–321

  35. Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287:476–479

  36. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

  37. Nield J, Barber J (2006) Refinement of the structural model for the photosystem II supercomplex of higher plants. Biochim Biophys Acta 1757:353–361

  38. Pospíšil P, Šnyrychová I, Nauš J (2007) Dark production of reactive oxygen species in photosystem II membrane particles at elevated temperature: EPR spin-trapping study. Biochim Biophys Acta 1767:854–859

  39. Quiles MJ (2006) Stimulation of chlororespiration by heat and high light intensity in oat plants. Plant Cell Environ 29:1463–1470

  40. Sakurai I, Shen JR, Leng J, Ohashi S, Kobayashi M, Wada H (2006) Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. J Biochem 140:201–209

  41. Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ 28:269–277

  42. Shutova T, Nikitina J, Deikus G, Andersson B, Klimov V, Samuelsson G (2005) Structural dynamics of the manganese-stabilizing proteins-Effect of pH, calcium, and manganese. Biochemistry 44:15182–15192

  43. Tang Y, Chen M, Xu Y, Kuang T (2007) Changes in thermostability of photosystem II and leaf lipid composition of rice mutant with deficiency of light-harvesting chlorophyll a/b protein complexes. J Integr Plant Biol 49:515–522

  44. Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228

  45. Uchida K (2000) Role of reactive aldehyde in cardiovascular diseases. Free Radic Biol Med 28:1685–1696

  46. Weber H, Chételat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J 37:877–888

  47. Yamada S, Kumazawa S, Ishii T, Nakayama T, Itakura K, Shibata N, Kobayashi M, Sakai K, Osawa T, Uchida K (2001) Immunochemical detection of a lipofuscin-like fluorophore derived from malondialdehyde and lysine. J Lipid Res 42:1187–1196

  48. Yamane Y, Kashino Y, Koike H, Satoh K (1998) Effects of high temperatures on the photosynthetic systems in spinach: oxygen-evolving activities, fluorescence characteristics and the denaturation process. Photosynth Res 57:51–59

  49. Yamashita A, Nijo N, Pospíšil P, Morita N, Takenaka D, Aminaka R, Yamamoto Y, Yamamoto Y (2008) Quality control of photosystem II: reactive oxygen species are responsible for the damage to photosystem II under moderate heat stress. J Biol Chem 283:28380–28391

  50. Yamauchi Y, Furutera A, Seki K, Toyoda Y, Tanaka K, Sugimoto Y (2008) Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol Biochem 46:786–793

  51. Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Liang Z, Lu C (2007) Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225:719–733

Download references

Acknowledgments

We acknowledge Dr. Jun’ichi Mano of Yamaguchi University and Dr. Yukihiro Kimura of Kobe University for helpful discussions and kindly reading the manuscript. We thank Dr. Chikahiro Miyake of Kobe University for instructing oxygen evolution analysis. This research was supported by Grants-in-Aid for Exploratory Research (Grant 21658112) to Y.Y. from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

Author information

Correspondence to Yasuo Yamauchi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPT 370 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Yamauchi, Y., Sugimoto, Y. Effect of protein modification by malondialdehyde on the interaction between the oxygen-evolving complex 33 kDa protein and photosystem II core proteins. Planta 231, 1077–1088 (2010). https://doi.org/10.1007/s00425-010-1112-2

Download citation

Keywords

  • Heat stress
  • Lipid peroxidation
  • Malondialdehyde
  • Oxygen-evolving complex
  • Photosystem II
  • 33 kDa protein