AtCYP38 ensures early biogenesis, correct assembly and sustenance of photosystem II

Plant Journal

Volumn 55, Issue 4, 2008, Pages 639-651

  Sirpiö, Sari ^a   Khrouchtchova, Anastassia ^b   Allahverdiyeva, Yagut ^a   Hansson, Maria ^c   Fristedt, Rikard ^c   Vener, Alexander V ^c   Scheller, Henrik Vibe ^b   Jensen, Poul Erik ^b   Haldrup, Anna ^b   Aro, Eva Mari ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LINKÖPING UNIVERSITY   (Sweden)

Author keywords

D1 protein; Immunophilin; Phosphatase; Photosystem II biogenesis; Photosystem II repair; Thylakoid lumen

Indexed keywords

ARABIDOPSIS PROTEIN; CYCLOPHILIN; CYCLOPHILIN 38, ARABIDOPSIS; METHIONINE;

ARABIDOPSIS; ARTICLE; BIOGENESIS; DARKNESS; GENETIC VARIABILITY; GENETICS; KINETICS; LIGHT; METABOLISM; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY; PLANT LEAF; THYLAKOID;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOGENESIS; CYCLOPHILINS; DARKNESS; GENETIC VARIATION; KINETICS; LIGHT; METHIONINE; PHENOTYPE; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT LEAVES; THYLAKOIDS;

EID: 49249096670     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03532.x     Document Type: Article

References (43)

1. Allahverdiyeva, Y., Deak, Z., Szilard, A., Diner, B.A., Nixon, P.J. Vass, I. (2004) The function of D1-H332 in photosystem II electron transport studied by thermoluminescence and chlorophyll fluorescence in site-directed mutants of Synechocystis 6803. Eur. J. Biochem. 271, 3523 3532.
2. Allahverdiyeva, Y., Mamedov, F., Maenpaa, P., Vass, I. Aro, E.M. (2005) Modulation of photosynthetic electron transport in the absence of terminal electron acceptors: characterization of the rbcL deletion mutant of tobacco. Biochim. Biophys. Acta, 1709 (1 69 83.
3. Allahverdiyeva, Y., Mamedov, F., Suorsa, M., Styring, S., Vass, I. Aro, E.M. (2007) Insights into the function of PsbR protein in Arabidopsis thaliana. Biochim. Biophys. Acta, 1767, 677 685.
4. Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653 657.
5. Anderson, L.B., Maderia, M., Ouellette, A.J., Putnam-Evans, C., Higgins, L., Krick, T., MacCoss, M.J., Lim, H., Yates, J.R. 3rd. Barry, B.A. (2002) Posttranslational modifications in the CP43 subunit of photosystem II. Proc. Natl Acad. Sci. USA, 99 (23 14676 14681.
6. Aro, E.M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., Battchikova, N. Rintamaki, E. (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56, 347 356.
7. Baena-Gonzalez, E., Rolland, F., Thevelein, J.M. Sheen, J. (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature, 448 (7156 938 942.
8. Bechtold, U., Murphy, D.J. Mullineaux, P.M. (2004) Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell, 16 (4 908 919.
9. Blomqvist, L.A., Ryberg, M. Sundqvist, C. (2006) Proteomic analysis of the etioplast inner membranes of wheat (Triticum aestivum) by two-dimensional electrophoresis and mass spectrometry. Physiol. Plant. 128, 368 381.
10. Burnap, R.L. (2004) D1 protein processing and mn cluster assembly in light of the emerging photosystem II structure. Phys. Chem. Chem. Phys., 6 (20 4803 4809.
11. Chu, H.A., Nguyen, A.P. Debus, R.J. (1995) Amino acid residues that influence the binding of manganese or calcium to photosystem II. 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry, 34, 5839 5858.
12. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
13. Cser, K., Diner, B.A., Nixon, P.J. Vass, I. (2005) The role of D1-Ala344 in charge stabilization and recombination in photosystem II. Photochem. Photobiol. Sci. 4, 1049 1054.
14. Fu, A., He, Z., Cho, H.S., Lima, A., Buchanan, B.B. Luan, S. (2007) A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 104, 15947 15952.
15. Fulgosi, H., Vener, A.V., Altschmied, L., Herrmann, R.G. Andersson, B. (1998) A novel multi-functional chloroplast protein: identification of a 40 kDa immunophilin-like protein located in the thylakoid lumen. EMBO J. 17, 1577 1587.
16. Göthel, S.F. Marahiel, M.A. (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell. Mol. Life Sci. 55, 423 436.
17. Kanervo, E., Singh, M., Suorsa, M., Paakkarinen, V., Aro, E., Battchikova, N. Aro, E.M. (2008) Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisum sativum). Plant Cell Physiol. 49, 396 410.
18. Kieselbach, T. Schröder, W.P. (2003) The proteome of the chloroplast lumen of higher plants. Photosynth. Res. 78, 249 264.
19. Kjær, B. Scheller, H.V. (1996) An isolated reaction center complex from the green sulfur bacterium Chlorobium vibrioforme can photoreduce ferredoxin at high rates. Photosynth. Res. 47, 33 39.
20. Koivuniemi, A., Aro, E.M. Andersson, B. (1995) Degradation of the D1- and D2-proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry, 34 (49 16022 16029.
21. Laemmli, U.K. (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature, 227, 680 685.
22. Lintala, M., Allahverdiyeva, Y., Kidron, H., Piippo, M., Battchikova, N., Suorsa, M., Rintamaki, E., Salminen, T.A., Aro, E.M. Mulo, P. (2007) Structural and functional characterization of ferredoxin-NADP+-oxidoreductase using knock-out mutants of Arabidopsis. Plant J. 49 (6 1041 1052.
23. Naver, H., Haldrup, A. Scheller, H.V. (1999) Cosuppression of photosystem I subunit PSI-H in Arabidopsis thaliana. Efficient electron transfer and stability of photosystem I is dependent upon the PSI-H subunit. J. Biol. Chem. 274, 10784 10789.
24. Nelson, N. Ben-Shem, A. (2004) The complex architecture of oxygenic photosynthesis. Nat. Rev. Mol. Cell Biol. 5, 971 982.
25. Nour-Eldin, H.H., Hansen, B.G., Nørholm, M.H., Jensen, J.K. Halkier, B.A. (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res. 34, e122.
26. Ohnishi, N., Allakhverdiev, S.I., Takahashi, S., Higashi, S., Watanabe, M., Nishiyama, Y. Murata, N. (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry, 44 (23 8494 8499.
27. Peltier, J.B., Emanuelsson, O., Kalume, D.E. et al. (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell, 14, 211 236.
28. Piippo, M., Allahverdiyeva, Y., Paakkarinen, V., Suoranta, U.M., Battchikova, N. Aro, E.M. (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol. Genomics, 25, 142 152.
29. Porra, R.J., Thompson, W.A. Kriedemann, P.E. (1989) Determination of accurate extinction coefficients and simultaneous-equations for assaying chlorophyll-a and chlorophyll-b extracted with 4 different solvents - verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochim. Biophys. Acta, 975, 384 394.
30. Reinhold, T., Alawady, A., Grimm, B. et al. (2007) Limitation of nocturnal import of ATP into Arabidopsis chloroplasts leads to photooxidative damage. Plant J. 50, 293 304.
31. Ren, D., Yang, H. Zhang, S. (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J. Biol. Chem. 277, 559 565.
32. Rintamäki, E., Kettunen, R. Aro, E.M. (1996) Differential D1 dephosphorylation in functional and photodamaged photosystem II centers - dephosphorylation is a prerequisite for degradation of damaged D1. J. Biol. Chem. 271, 14870 14875.
33. Rintamäki, E., Martinsuo, P., Pursiheimo, S. Aro, E.M. (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc. Natl Acad. Sci. USA, 97 (21 11644 11649.
34. Rokka, A., Aro, E.M., Herrmann, R.G., Andersson, B. Vener, A.V. (2000) Dephosphorylation of photosystem II reaction center proteins in plant photosynthetic membranes as an immediate response to abrupt elevation of temperature. Plant Physiol. 123, 1525 1536.
35. Romano, P., Gray, J., Horton, P. Luan, S. (2005) Plant immunophilins: functional versatility beyond protein maturation. New Phytol. 166, 753 769.
36. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K. Weisshaar, B. (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 53, 247 259.
37. Sirpiö, S., Allahverdiyeva, Y., Suorsa, M., Paakkarinen, V., Vainonen, J., Battchikova, N. Aro, E.M. (2007) TLP18.3, a novel thylakoid lumen protein regulating photosytem II repair cycle. Biochem. J. 406, 415 425.
38. Vass, I., Kirilovsky, D. Etienne, A.L. (1999) UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry, 38, 12786 12794.
39. Vass, I., Turcsanyi, E., Touloupakis, E., Ghanotakis, D. Petrouleas, V. (2002) The mechanism of UV-A radiation-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Biochemistry, 41, 10200 10208.
40. Vener, A.V., van Kan, P.J., Rich, P.R., Ohad, I.I. Andersson, B. (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc. Natl Acad. Sci. USA, 94, 1585 1590.
41. Vener, A.V., Rokka, A., Fulgosi, H., Andersson, B. Herrmann, R.G. (1999) A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts. Biochemistry, 38, 14955 14965.
42. Zambryski, P., Joos, H., Genetello, C., Leemans, J., Vanmontagu, M. Schell, J. (1983) Ti-plasmid vector for the introduction of DNA into plant-cells without alteration of their normal regeneration capacity. EMBO J. 2, 2143 2150.
43. Zhang, L.X., Paakkarinen, V., van Wijk, K.J. Aro, E.M. (1999) Co-translational assembly of the D1 protein into photosystem II. J. Biol. Chem. 274, 16062 16067.