Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen-evolving complex show altered PSII super-complex organization and short-term adaptive mechanisms

Plant Journal

Volumn 75, Issue 4, 2013, Pages 671-684

  Allahverdiyeva, Yagut ^a   Suorsa, Marjaana ^a   Rossi, Fabio ^b   Pavesi, Andrea ^b   Kater, Martin M ^b   Antonacci, Alessia ^c   Tadini, Luca ^d   Pribil, Mathias ^d   Schneider, Anja ^d   Wanner, Gerhard ^d   Leister, Dario ^d,e,f   Aro, Eva Mari ^a   Barbato, Roberto ^c   Pesaresi, Paolo ^b  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF TRENTO   (Italy)

^f RESEARCH AND INNOVATION CENTRE   (Italy)

Author keywords

Arabidopsis thaliana; NPQ; oxygen evolving complex; photosynthesis; protein complex; state transitions

Indexed keywords

ARABIDOPSIS THALIANA; NPQ; OXYGEN-EVOLVING COMPLEXES; PROTEIN COMPLEXES; STATE TRANSITIONS;

OXYGEN; PHOTOSYNTHESIS; PROTEINS; TRANSCRIPTION;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

ARABIDOPSIS PROTEIN; OXYGEN; PROTEIN COMPLEX; PSBQ PROTEIN, ARABIDOPSIS; PSBR PROTEIN, ARABIDOPSIS;

ADAPTATION; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; BIOMASS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NPQ; OXYGEN-EVOLVING COMPLEX; PHENOTYPE; PHOSPHORYLATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; STATE TRANSITIONS; THYLAKOID; TRANSGENIC PLANT;

ARABIDOPSIS THALIANA; NPQ; OXYGEN-EVOLVING COMPLEX; PHOTOSYNTHESIS; PROTEIN COMPLEX; STATE TRANSITIONS;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOMASS; OXYGEN; PHENOTYPE; PHOSPHORYLATION; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS, GENETICALLY MODIFIED; THYLAKOIDS;

EID: 84882451794     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12230     Document Type: Article

References (65)

1. Allahverdiyeva, Y., Mamedov, F., Suorsa, M., Styring, S., Vass, I., and, Aro, E.M., (2007) Insights into the function of PsbR protein in Arabidopsis thaliana. Biochim. Biophys. Acta, 1767, 677-685.
2. Allahverdiyeva, Y., Mamedov, F., Holmstrom, M., Nurmi, M., Lundin, B., Styring, S., Spetea, C., and, Aro, E.M., (2009) Comparison of the electron transport properties of the psbo1 and psbo2 mutants of Arabidopsis thaliana. Biochim. Biophys. Acta, 1787, 1230-1237.
3. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
4. Aseeva, E., Ossenbuhl, F., Sippel, C., et al. (2007) Vipp 1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol. Biochem. 45, 119-128.
5. Blum, H., Beier, H., and, Gross, H.J., (1987) Improved silver staining of plant-proteins, RNA and DNA in polyacrylamide gels. Electrophoresis, 8, 93-99.
6. Bonardi, V., Pesaresi, P., Becker, T., Schleiff, E., Wagner, R., Pfannschmidt, T., Jahns, P., and, Leister, D., (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature, 437, 1179-1182.
7. Bricker, T.M., and, Frankel, L.K., (2011) Auxiliary functions of the PsbO, PsbP and PsbQ proteins of higher plant photosystem II: a critical analysis. J. Photochem. Photobiol., B, 104, 165-178.
8. Bricker, T.M., Odom, W.R., and, Queirolo, C.B., (1988) Close association of the 33-kDa extrinsic protein with the apoprotein of Cpa1 in photosystem II. FEBS Lett. 231, 111-117.
9. Bricker, T.M., Roose, J.L., Fagerlund, R.D., Frankel, L.K., and, Eaton-Rye, J.J., (2012) The extrinsic proteins of photosystem II. Biochim. Biophys. Acta, 1817, 121-142.
10. Caffarri, S., Kouril, R., Kereiche, S., Boekema, E.J., and, Croce, R., (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J. 28, 3052-3063.
11. Calderone, V., Trabucco, M., Vujicic, A., Battistutta, R., Giacometti, G.M., Andreucci, F., Barbato, R., and, Zanotti, G., (2003) Crystal structure of the PsbQ protein of photosystem II from higher plants. EMBO Rep. 4, 900-905.
12. Chow, W.S., Hope, A.B., and, Anderson, J.M., (1989) Oxygen per flash from leaf-disks quantifies photosystem II. Biochim. Biophys. Acta, 973, 105-108.
13. DalCorso, G., Pesaresi, P., Masiero, S., Aseeva, E., Schunemann, D., Finazzi, G., Joliot, P., Barbato, R., and, Leister, D., (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell, 132, 273-285.
14. Dietzel, L., Brautigam, K., Steiner, S., Schuffler, K., Lepetit, B., Grimm, B., Schottler, M.A., and, Pfannschmidt, T., (2011) Photosystem II supercomplex remodeling serves as an entry mechanism for state transitions in Arabidopsis. Plant Cell, 23, 2964-2977.
15. Enami, I., Miyaoka, T., Mochizuki, Y., Shen, J.R., Satoh, K., and, Katoh, S., (1989) Nearest neighbor relationships among constituent proteins of oxygen-evolving photosystem II membranes-binding and function of the extrinsic 33 kDa protein. Biochim. Biophys. Acta, 973, 35-40.
16. Genty, B., Briantais, J.M., and, Baker, N.R., (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta, 990, 87-92.
17. Goulas, E., Schubert, M., Kieselbach, T., Kleczkowski, L.A., Gardestrom, P., Schroder, W., and, Hurry, V., (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J. 47, 720-734.
18. Granlund, I., Hall, M., Kieselbach, T., and, Schroder, W.P., (2009) Light induced changes in protein expression and uniform regulation of transcription in the thylakoid lumen of Arabidopsis thaliana. PLoS ONE, 4, e5649.
19. Grasses, T., Pesaresi, P., Schiavon, F., Varotto, C., Salamini, F., Jahns, P., and, Leister, D., (2002) The role of delta pH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage in Arabidopsis thaliana. Plant Physiol. Biochem. 40, 41-49.
20. Ido, K., Ifuku, K., Yamamoto, Y., Ishihara, S., Murakami, A., Takabe, K., Miyake, C., and, Sato, F., (2009) Knockdown of the PsbP protein does not prevent assembly of the dimeric PSII core complex but impairs accumulation of photosystem II supercomplexes in tobacco. Biochim. Biophys. Acta, 1787, 873-881.
21. Ifuku, K., Nakatsu, T., Kato, H., and, Sato, F., (2004) Crystal structure of the PsbP protein of photosystem II from Nicotiana tabacum. EMBO Rep. 5, 362-367.
22. Ifuku, K., Nakatsu, T., Shimamoto, R., Yamamoto, Y., Ishihara, S., Kato, H., and, Sato, F., (2005a) Structure and function of the PsbP protein of photosystem II from higher plants. Photosynth. Res. 84, 251-255.
23. Ifuku, K., Yamamoto, Y., Ono, T.A., Ishihara, S., and, Sato, F., (2005b) PsbP protein, but not PsbQ protein, is essential for the regulation and stabilization of photosystem II in higher plants. Plant Physiol. 139, 1175-1184.
24. Ifuku, K., Ishihara, S., Shimamoto, R., Ido, K., and, Sato, F., (2008) Structure, function, and evolution of the PsbP protein family in higher plants. Photosynth. Res. 98, 427-437.
25. Ifuku, K., Endo, T., Shikanai, T., and, Aro, E.M., (2011a) Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant Cell Physiol. 52, 1560-1568.
26. Ifuku, K., Ido, K., and, Sato, F., (2011b) Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex. J. Photochem. Photobiol. B, 104, 158-164.
27. Ihnatowicz, A., Pesaresi, P., Varotto, C., Richly, E., Schneider, A., Jahns, P., Salamini, F., and, Leister, D., (2004) Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. Plant J. 37, 839-852.
28. Jarvi, S., Suorsa, M., Paakkarinen, V., and, Aro, E.M., (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem. J. 439, 207-214.
29. Kakiuchi, S., Uno, C., Ido, K., Nishimura, T., Noguchi, T., Ifuku, K., and, Sato, F., (2012) The PsbQ protein stabilizes the functional binding of the PsbP protein to photosystem II in higher plants. Biochim. Biophys. Acta, 1817, 1346-1351.
30. Kavelaki, K., and, Ghanotakis, D.F., (1991) Effect of the manganese complex on the binding of the extrinsic proteins (17-kDa, 23-kDa and 33-kDa) of photosystem II. Photosynth. Res. 29, 149-155.
31. 6f complex in Arabidopsis. Plant Cell, 13, 2539-2551.
32. Li, X.P., Bjorkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S., and, Niyogi, K.K., (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature, 403, 391-395.
33. Liu, H., Frankel, L.K., and, Bricker, T.M., (2009) Characterization and complementation of a psbR mutant in Arabidopsis thaliana. Arch. Biochem. Biophys. 489, 34-40.
34. Lunde, C., Jensen, P.E., Haldrup, A., Knoetzel, J., and, Scheller, H.V., (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature, 408, 613-615.
35. Lundin, B., Nurmi, M., Rojas-Stuetz, M., Aro, E.M., Adamska, I., and, Spetea, C., (2008) Towards understanding the functional difference between the two PsbO isoforms in Arabidopsis thaliana-insights from phenotypic analyses of psbo knockout mutants. Photosynth. Res. 98, 405-414.
36. Martinez-Garcia, J.F., Monte, E., and, Quail, P.H., (1999) A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. Plant J. 20, 251-257.
37. Mayfield, S.P., Bennoun, P., and, Rochaix, J.D., (1987) Expression of the nuclear encoded OEE1 protein is required for oxygen evolution and stability of photosystem II particles in Chlamydomonas reinhardtii. EMBO J. 6, 313-318.
38. Miyao, M., and, 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.
39. Murakami, R., Ifuku, K., Takabayashi, A., Shikanai, T., Endo, T., and, Sato, F., (2002) Characterization of an Arabidopsis thaliana mutant with impaired PsbO, one of two genes encoding extrinsic 33-kDa proteins in photosystem II. FEBS Lett. 523, 138-142.
40. Murakami, R., Ifuku, K., Takabayashi, A., Shikanai, T., Endo, T., and, Sato, F., (2005) Functional dissection of two Arabidopsis PsbO proteins: PsbO1 and PsbO2. FEBS J. 272, 2165-2175.
41. Pagliano, C., La Rocca, N., Andreucci, F., Deak, Z., Vass, I., Rascio, N., and, Barbato, R., (2009) The extreme halophyte Salicornia veneta is depleted of the extrinsic PsbQ and PsbP proteins of the oxygen-evolving complex without loss of functional activity. Ann. Bot. 103, 505-515.
42. Pesaresi, P., Hertle, A., Pribil, M., et al. (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell, 21, 2402-2423.
43. Pribil, M., Pesaresi, P., Hertle, A., Barbato, R., and, Leister, D., (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol. 8, e1000288.
44. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K., and, 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.
45. Schagger, H., and, von Jagow, G., (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379.
46. Seidler, A., Rutherford, A.W., and, Michel, H., (1996) On the role of the N-terminus of the extrinsic 33 kDa protein of photosystem II. Plant Mol. Biol. 31, 183-188.
47. Sessions, A., Burke, E., Presting, G., et al. (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell, 14, 2985-2994.
48. Sirpiö, S., Allahverdiyeva, Y., Holmström, M., Khrouchtchova, A., Haldrup, A., Battchikova, N., and, Aro, E.M., (2009) Novel nuclear-encoded subunits of the chloroplast NAD(P)H dehydrogenase complex. J. Biol. Chem. 284, 905-912.
49. Stockhaus, J., Hofer, M., Renger, G., Westhoff, P., Wydrzynski, T., and, Willmitzer, L., (1990) Antisense RNA efficiently inhibits formation of the 10 kDa polypeptide of photosystem II in transgenic potato plants: analysis of the role of the 10 kDa protein. EMBO J. 9, 3013-3021.
50. Sundaresan, V., Springer, P., Volpe, T., Haward, S., Jones, J.D., Dean, C., Ma, H., and, Martienssen, R., (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9, 1797-1810.
51. Suorsa, M., Sirpio, S., Allahverdiyeva, Y., Paakkarinen, V., Mamedov, F., Styring, S., and, Aro, E.M., (2006) PsbR, a missing link in the assembly of the oxygen-evolving complex of plant photosystem II. J. Biol. Chem. 281, 145-150.
52. Takabayashi, A., Ishikawa, N., Obayashi, T., Ishida, S., Obokata, J., Endo, T., and, Sato, F., (2009) Three novel subunits of Arabidopsis chloroplastic NAD(P)H dehydrogenase identified by bioinformatic and reverse genetic approaches. Plant J. 57, 207-219.
53. Thornton, L.E., Ohkawa, H., Roose, J.L., Kashino, Y., Keren, N., and, Pakrasi, H.B., (2004) Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803. Plant Cell, 16, 2164-2175.
54. Tikkanen, M., Piippo, M., Suorsa, M., Sirpio, S., Mulo, P., Vainonen, J., Vener, A.V., Allahverdiyeva, Y., and, Aro, E.M., (2006) State transitions revisited-a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol. Biol. 62, 779-793.
55. Trotta, A., Redondo-Gomez, S., Pagliano, C., Clemente, M.E., Rascio, N., Rocca, N.L., Antonacci, A., Andreucci, F., and, Barbato, R., (2012) Chloroplast ultrastructure and thylakoid polypeptide composition are affected by different salt concentrations in the halophytic plant Arthrocnemum macrostachyum. J. Plant Physiol. 169, 111-116.
56. Umena, Y., Kawakami, K., Shen, J.R., and, Kamiya, N., (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature, 473, 55-60.
57. Vainonen, J.P., Sakuragi, Y., Stael, S., et al. (2008) Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. FEBS J. 275, 1767-1777.
58. Vass, I., Kirilovsky, D., and, 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.
59. Vergnolle, C., Vaultier, M.N., Taconnat, L., Renou, J.P., Kader, J.C., Zachowski, A., and, Ruelland, E., (2005) The cold-induced early activation of phospholipase C and D pathways determines the response of two distinct clusters of genes in Arabidopsis cell suspensions. Plant Physiol. 139, 1217-1233.
60. Verwoerd, T.C., Dekker, B.M., and, Hoekema, A., (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17, 2362.
61. Yi, X., McChargue, M., Laborde, S., Frankel, L.K., and, Bricker, T.M., (2005) The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J. Biol. Chem. 280, 16170-16174.
62. Yi, X., Hargett, S.R., Frankel, L.K., and, Bricker, T.M., (2006) The PsbQ protein is required in Arabidopsis for photosystem II assembly/stability and photoautotrophy under low light conditions. J. Biol. Chem. 281, 26260-26267.
63. Yi, X., Hargett, S.R., Liu, H., Frankel, L.K., and, Bricker, T.M., (2007) The PsbP protein is required for photosystem II complex assembly/stability and photoautotrophy in Arabidopsis thaliana. J. Biol. Chem. 282, 24833-24841.
64. Yi, X., Hargett, S.R., Frankel, L.K., and, Bricker, T.M., (2008) The effects of simultaneous RNAi suppression of PsbO and PsbP protein expression in photosystem II of Arabidopsis. Photosynth. Res. 98, 439-448.
65. Yi, X., Hargett, S.R., Frankel, L.K., and, Bricker, T.M., (2009) The PsbP protein, but not the PsbQ protein, is required for normal thylakoid architecture in Arabidopsis thaliana. FEBS Lett. 583, 2142-2147.