Skip to main content
SpringerLink
Log in

State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

An Erratum to this article was published on 06 October 2006

Abstract

The mobile part of the light-harvesting chlorophyll (chl) a/b protein complex (LHCII), composed of the Lhcb1 and Lhcb2 proteins, is the basic unit of chloroplast state transitions—the short term tuning system in balancing the excitation energy between Photosystem (PS) II and PSI. State transitions are catalysed by the thylakoid associated STN7 kinase, and we show here that besides the phosphorylation of the Lhcb1 and Lhcb2 proteins, also the phosphorylation of Lhcb4.2 (CP29) is under the control of the STN7 kinase. Upon growth of Arabidopsis WT and stn7 mutant plants under low and moderate light conditions, the WT plants favoured state 2 whereas stn7 was locked in state 1. The lack of the STN7 kinase and state transitions in stn7 also modified the thylakoid protein contents upon long-term low light acclimation resulting, for example, in low Lhcb1 and in elevated Lhca1 and Lhca2 protein amounts as compared to WT. Adjustments of thylakoid protein contents probably occurred at post-transcriptional level since the DNA microarray experiments from each growth condition did not reveal any significant differences between stn7 and WT transcriptomes. The resulting high Lhcb2/Lhcb1 ratio in stn7 upon growth at low light was accompanied by lower capacity for NPQ than in WT. On the contrary, higher amounts of PsbS in stn7 under moderate and high light growth conditions resulted in higher NPQ compared to WT and consequently also in a protection of PSII against photoinhibition. STN7 kinase and the state transitions are suggested to have a physiological significance for dynamic acclimation to low but fluctuating growth light conditions. They are shown to function as a buffering system upon short high light illumination peaks by shifting the thylakoids from state 2 to state 1 and thereby down regulating the induction of stress-responsive genes, a likely result from transient over-reduction of PSI acceptors.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

chl:

chlorophyll

F v/F m :

photochemical efficiency of PSII

HSP:

heat shock protein

LHCII:

light harvesting chlorophyll a/b protein complex

NPQ:

non-photochemical energy quenching

PSI:

photosystem I

PSII:

photosystem II

References

  • Allahverdiyeva Y, Mamedov F, Maenpää 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 1709:69–83

    Article  PubMed  CAS  Google Scholar 

  • Allen JF, Bennett J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291:25–29

    Article  CAS  Google Scholar 

  • Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326

    Article  PubMed  CAS  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol Plant Mol Biol 37:93–136

    Article  CAS  Google Scholar 

  • Anderson JM, Chow WS, Park Y-I (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139

    Article  CAS  Google Scholar 

  • Anderson JM, Osmond CB (1987) Sun-shade responses: compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB, Arnzen CJ (eds), Photoinhibition. Elsevier, Amsterdam, pp 1–38

    Google Scholar 

  • Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P, Jansson S (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness. Plant J 35:350–361

    Article  PubMed  CAS  Google Scholar 

  • Aro E-M, McCaffery S, Anderson JM (1993) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 103:835–843

    PubMed  CAS  Google Scholar 

  • Aro E-M, Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Signal 1:55–67

    Article  CAS  Google Scholar 

  • Aro E-M, Rokka A, Vener AV (2004) Determination of phosphoproteins in higher plant thylakoids. Methods Mol Biol 274:271–285

    PubMed  CAS  Google Scholar 

  • Bailey S, Horton P, Walters RG (2004) Acclimation of Arabidopsis thaliana to the light environment: the relationship between photosynthetic function and chloroplast composition. Planta 218:793–802

    Article  PubMed  CAS  Google Scholar 

  • Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801

    Article  PubMed  CAS  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    Article  PubMed  CAS  Google Scholar 

  • Bennett J (1977) Phosphorylation of chloroplast membrane polypeptides. Nature 269:344–346

    Article  CAS  Google Scholar 

  • Bennett J, Steinback KE, Arntzen CJ (1980) Chloroplast phosphoproteins: Regulation of excitation energy transfer by phosphorylation of thylakoid membrane polypeptides. Proc Natl Acad Sci USA 77:5253–5257

    Article  PubMed  CAS  Google Scholar 

  • Bergantino E, Dainese P, Cerovic Z, Sechi S, Bassi R (1995) A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress. J Biol Chem 270:8474–8481

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, van Breemen JF, van Roon H, Dekker JP (2000) Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301:1123–1133

    Article  PubMed  CAS  Google Scholar 

  • Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182

    Article  PubMed  CAS  Google Scholar 

  • Caffarri S, Croce R, Cattivelli L, Bassi R (2004) A look within LHCII: differential analysis of the Lhcb1–3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43:9467–9476

    Article  PubMed  CAS  Google Scholar 

  • Chow WS, Anderson JM (1987) Photosynthetic responses of Pisum sativum to an increase in irradiance during growth. II. Thylakoid membrane components. Aust J Plant Physiol 14:9–19

    Article  CAS  Google Scholar 

  • Dall ’Osto L, Caffarri S, Bassi R (2005) A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17:1217–1232

    Article  CAS  Google Scholar 

  • Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B (2003) Linking the xanthophyll cycle with thermal energy dissipation. Photosynth Res 76:73–80

    Article  PubMed  CAS  Google Scholar 

  • Depege N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    Article  PubMed  CAS  Google Scholar 

  • Desikan R, Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172

    Article  PubMed  CAS  Google Scholar 

  • Endo T, Shikanai T, Takabayashi A, Asada K, Sato F (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett 457:5–8

    Article  PubMed  CAS  Google Scholar 

  • Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, Shabanovitz J, Hunt DF, White FM (2002) Phosphoproteome analysis and its application to Saccharomyces cerevisiae. Nat Biotech 20:301–305

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  PubMed  CAS  Google Scholar 

  • Ganeteg U, Kulheim C, Andersson J, Jansson S (2004) Is each light-harvesting complex protein important for plant fitness? Plant Physiol 134:502–509

    Article  PubMed  CAS  Google Scholar 

  • Hansson M, Vener AV (2003) Identification of three previously unknown in vivo Protein phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Mol Cell Proteomics 2:550–559

    PubMed  CAS  Google Scholar 

  • Horton P, Black MT (1981) Light-dependent quenching of chlorophyll fluorescence in pea chloroplast induced by adenosine 5′-triphosphate. Biochim Biophys Acta 635:53–62

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  PubMed  CAS  Google Scholar 

  • Hou CX, Rintamaki E, Aro E-M (2003) Ascorbate-mediated LHCII protein phosphorylation-LHCII kinase regulation in light and in darkness. Biochemistry 42:5828–5836

    Article  PubMed  CAS  Google Scholar 

  • Jansson S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184:1–19

    Article  PubMed  CAS  Google Scholar 

  • Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240

    Article  PubMed  Google Scholar 

  • Kanervo E, Suorsa M, Aro E-M (2005) Functional flexibility and acclimation of the thylakoid membrane. Photochem Photobiol Sci 4:1072–1080

    Article  PubMed  CAS  Google Scholar 

  • Kargul J, Turkina MV, Nield J, Benson S, Vener AV, Barber J (2005) Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J 272:4797–4806

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Yamamoto YY, Seki M, Sakurai T, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K, Matsui M (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem Photobiol 77:226–233

    Article  PubMed  CAS  Google Scholar 

  • Kruse O (2001) Light-induced short-term adaptation mechanisms under redox control in the PS II-LHCII supercomplex: LHC II state transitions and PS II repair cycle. Naturwissenschaften 88:284–292

    Article  PubMed  CAS  Google Scholar 

  • Kulheim C, Agren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    Article  PubMed  CAS  Google Scholar 

  • Lunde C, Jensen PE, Rosgaard L, Haldrup A, Gilpin MJ, Scheller HV (2003) Plants impaired in state transitions can to a large degree compensate for their defect. Plant Cell Physiol 44:44–54

    Article  PubMed  CAS  Google Scholar 

  • Mussgnug JH, Wobbe L, Elles I, Claus C, Hamilton M, Fink A, Kahmann U, Kapazoglou A, Mullineaux CW, Hippler M, Nickelsen J, Nixon PJ, Kruse O (2005) NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell 17:3409–3421

    Article  PubMed  CAS  Google Scholar 

  • Mäenpää P, Andersson B (1989) Photosystem II heterogeneity and long-term acclimation of light-harvesting. Z Naturforsch 44C:403–406

    Google Scholar 

  • Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis?. J Exp Bot 56:375–382

    Article  PubMed  CAS  Google Scholar 

  • Oswald O, Martin T, Dominy PJ, Graham IA (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98:2047–2052

    Article  PubMed  CAS  Google Scholar 

  • 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 13:142–152

    Google Scholar 

  • Pursiheimo S, Martinsuo P, Rintamaki E, Aro E-M (2003) Photosystem II protein phosphorylation follows four distinctly different regulatory patterns induced by environmental cues. Plant Cell Environ 26:1995–2003

    Article  CAS  Google Scholar 

  • Rintamaki 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 97:11644–11649

    Article  PubMed  CAS  Google Scholar 

  • Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130:1109–1120

    Article  PubMed  CAS  Google Scholar 

  • Scheller HV, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221:5–8

    Article  PubMed  CAS  Google Scholar 

  • Schulenberg B, Aggeler R, Beechem JM, Capaldi RA, Patton WF (2003) Analysis of steady-state protein phosphorylation in mitochondria using a novel fluorescent phosphosensor dye. J Biol Chem 278:27251–27255

    Article  PubMed  CAS  Google Scholar 

  • Suorsa M, Regel RE, Paakkarinen V, Battchikova N, Herrmann RG, Aro E-M (2004) Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. Eur J Biochem 271:96–107

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S, Seki M, Ishida J, Satou M, Sakurai T, Narusaka M, Kamiya A, Nakajima M, Enju A, Akiyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Mol Biol 56:29–55

    Article  PubMed  CAS  Google Scholar 

  • Vainonen JP, Hansson M, Vener AV (2005) STN8 protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins. J Biol Chem 280:33679–33686

    Article  PubMed  CAS  Google Scholar 

  • Vener AV, Harms A, Sussman MR, Vierstra RD (2001) Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J Biol Chem 276:6959–6966

    Article  PubMed  CAS  Google Scholar 

  • Vener AV, van Kan PJ, Rich PR, Ohad 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

    Article  PubMed  CAS  Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447

    Article  PubMed  CAS  Google Scholar 

  • Zelisko A, Garcia-Lorenzo M, Jackowski G, Jansson S, Funk C (2005) AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc Natl Acad Sci USA 102:13699–13704

    Article  PubMed  CAS  Google Scholar 

  • Yakushevska AE, Jensen PE, Keegstra W, van Roon H, Scheller HV, Boekema EJ, Dekker JP (2001) Supermolecular organization of photosystem II and its associated light-harvesting antenna in Arabidopsis thaliana. Eur J Biochem 268:6020–6028

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We wish to thank Dr. Natalia Battchikova and Virpi Paakkarinen for technical help and Dr. Saijaliisa Kangasjärvi for critical reading of the manuscript. Drs Roberto Barbato, Toril Hundal, Stefan Jansson, Peter Nixon and Francis-André Wollman are acknowledged for antibodies. We are grateful to the Center of Biotechnology (CBT) for sequencing the cDNA clones and to the proteomics unit in CBT for advice in mass spectrometry. This study was supported by the Academy of Finland and The Finnish Ministry of Agriculture and Forestry (The NKJ project).

Author information

Authors and Affiliations

  1. Plant Physiology and Molecular Biology, Department of Biology, University of Turku, FIN-20014, Turku, Finland

    Tikkanen Mikko, Piippo Mirva, Suorsa Marjaana, Sirpiö Sari, Mulo Paula, Vainonen Julia, Allahverdiyeva Yagut & Aro Eva-Mari

  2. Division of Cell Biology, Linkoping University, SE-581 85, Linkoping, Sweden

    Vener Alexander V

Authors
  1. Tikkanen Mikko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Piippo Mirva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suorsa Marjaana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sirpiö Sari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mulo Paula
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vainonen Julia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vener Alexander V
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Allahverdiyeva Yagut
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Aro Eva-Mari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aro Eva-Mari.

Additional information

M. Tikkanen and M. Piippo contributed equally to this work.

An erratum to this article can be found at http://dx.doi.org/10.1007/s11103-006-9088-9

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mikko, T., Mirva, P., Marjaana, S. et al. State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis . Plant Mol Biol 62, 779–793 (2006). https://doi.org/10.1007/s11103-006-9044-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-006-9044-8

Keywords

Search

Navigation