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Essential role of the PSI–LHCII supercomplex in photosystem acclimation to light and/or heat conditions by state transitions

Photosynthesis Research volume 131, pages 41–50 (2017)Cite this article

Abstract

Light and temperature affect state transitions through changes in the plastoquinone (PQ) redox state in photosynthetic organisms. We demonstrated that light and/or heat treatment induced preferential photosystem (PS) I excitation by binding light-harvesting complex II (LHCII) proteins. The photosystem of wheat was in state 1 after dark overnight treatment, wherein PQ was oxidized and most of LHCII was not bound to PSI. At the onset of the light treatment [25 °C in the light (100 µmol photons m−2 s−1)], two major LHCIIs, Lhcb1 and Lhcb2 were phosphorylated, and the PSI–LHCII supercomplex formed within 5 min, which coincided with an increase in the PQ oxidation rate. Heat treatment at 40 °C of light-adapted wheat led to further LHCII protein phosphorylation of, resultant cyclic electron flow promotion, which was accompanied by ultrafast excitation of PSI and structural changes of thylakoid membranes, thereby protecting PSII from heat damage. These results suggest that LHCIIs are required for the functionality of wheat plant PSI, as it keeps PQ oxidized by regulating photochemical electron flow, thereby helping acclimation to environmental changes.

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Abbreviations

α-DM:

n-dodecyl-α-d-maltoside

AL:

Actinic light

BL:

Blue light

BN-PAGE:

Blue native-polyacrylamide gel electrophoresis

CEF:

Cyclic electron flow

ETR:

Photosynthetic electron transport rate

FR:

Far-red light

LEF:

Linear electron flow

LHCII:

Light-harvesting complex II

NPQ:

Nonphotochemical quenching

φII:

Photosystem II quantum efficiency

PQ:

Plastoquinone

PS:

Photosystem

STN:

Ser–Thr kinase

TEM:

Transmission electron microscopy

TRFS:

Time-resolved fluorescence spectra

References

  • Akimoto S, Yokono M, Yokono E, Aikawa S, Kondo A (2014) Short-term light adaptation of a cyanobacterium, Synechocystis sp. PCC 6803, probed by time-resolved fluorescence spectroscopy. Plant Physiol Biochem 81:149–154

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Chuartzman SG, Nevo R, Shimoni E, Charuvi D, Kiss V, Ohad I, Brumfeld V, Reich Z (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20:1029–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clausen Casper H, Brooks Matthew D, Li TD, Grob P, Kemalyan G, Nogales E, Niyogi KK, Fletcher Daniel A (2014) Dynamic mechanical responses of Arabidopsis thylakoid membranes during PSII-specific illumination. Biophys J 106:1864–1870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ducruet JM, Peeva V, Havaux M (2007) Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants. Photosynth Res 93:159–171

    Article  CAS  PubMed  Google Scholar 

  • Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix JD, Zito F, Forti G (2002) Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep 3:280–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fristedt R, Willig A, Granath P, Crevecoeur M, Rochaix JD, Vener AV (2009) Phosphorylation of photosystem II controls functional macroscopic folding of photosynthetic membranes in Arabidopsis. Plant Cell 21:3950–3964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galka P, Santabarbara S, Khuong TT, Degand H, Morsomme P, Jennings RC, Boekema EJ, Caffarri S (2012) Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24:2963–2978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gounaris K, Brain ARR, Quinn PJ, Williams WP (1984) Structural reorganization of chloroplast thylakoid membranes in response to heat stress. Biochim Biophys Acta 766:198–208

    Article  CAS  Google Scholar 

  • Havaux M, Greppin H, Strasser R (1991) Functioning of photosystems I and II in pea leaves exposed to heat stress in the presence or absence of light. Planta 186:88–98

    Article  CAS  PubMed  Google Scholar 

  • Järvi S, Suorsa M, Paakkarinen V, Aro EM (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem J 439:207–214

    Article  PubMed  Google Scholar 

  • Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteom 5:749–757

    Article  CAS  Google Scholar 

  • Kouřil R, Zygadlo A, Arteni AA, de Wit CD, Dekker JP, Jensen PE, Scheller HV, Boekema EJ (2005) Structural characterization of a complex of photosystem i and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44:10935–10940

    Article  PubMed  Google Scholar 

  • Leoni C, Pietrzykowska M, Kiss AZ, Suorsa M, Ceci LR, Aro EM, Jansson S (2013) Very rapid phosphorylation kinetics suggest a unique role for Lhcb2 during state transitions in Arabidopsis. Plant J 76:236–246

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marutani Y, Yamauchi Y, Kimura Y, Mizutani M, Sugimoto Y (2012) Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes. Planta 236:753–761

    Article  CAS  PubMed  Google Scholar 

  • Marutani Y, Yamauchi Y, Miyoshi A, Inoue K, Ikeda K, Mizutani M, Sugimoto Y (2014) Regulation of photochemical energy transfer accompanied by structural changes in thylakoid membranes of heat-stressed wheat. Int J Mol Sci 15:23042–23058

    Article  PubMed  PubMed Central  Google Scholar 

  • Minagawa J (2011) State transitions – the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta 1807:897–905

    Article  CAS  PubMed  Google Scholar 

  • Pålsson LO, Tjus SE, Andersson B, Gillbro T (1995) Energy transfer in photosystem I. Time resolved fluorescence of the native photosystem I complex and its core complex. Chem Phys 194:291–302

    Article  Google Scholar 

  • Peng L, Shimizu H, Shikanai T (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J Biol Chem 283:34873–34879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider A, Pfannschmidt T, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–2423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pietrzykowska M, Suorsa M, Semchonok DA, Tikkanen M, Boekema EJ, Aro E-M, Jansson S (2014) The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in Arabidopsis. Plant Cell 26:3646–3660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52:712–722

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Wientjes E, van Amerongen H, Croce R (2013) LHCII is an antenna of both photosystems after long-term acclimation. Biochim Biophys Acta 1827:420–426

    Article  CAS  PubMed  Google Scholar 

  • Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 16:3623–3630

    Article  Google Scholar 

  • Yamane Y, Shikanai T, Kashino Y, Koike H, Satoh K (2000) Reduction of QA in the dark: another cause of fluorescence Fo increases by high temperatures in higher plants. Photosynth Res 63:23–34

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Scheller HV (2004) Light-harvesting complex II binds to several small subunits of photosystem I. J Biol Chem 279:3180–3187

    Article  CAS  PubMed  Google Scholar 

  • Zhang R, Sharkey T (2009) Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth Res 100:29–43

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Grant-in-Aids for Scientific Research (Y. Y., 23580456) from the Ministry of Education, Culture, Sports, Science and Technology, Japan, and JSPS Research Fellowship for Young Scientists (Y. M., 251843).

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Author notes

  1. Yoko Marutani

    Present address: Technology Innovation Center, Sumika Chemical Analysis Service, Ltd., 3-1-135, Kasugade-naka, Konohana-ku, Osaka, 554-0022, Japan

Authors and Affiliations

  1. Graduate School of Agricultural Science, Kobe University, Nada-ku, Kobe, 657-8501, Japan

    Yoko Marutani, Yasuo Yamauchi, Mari Higashiyama, Kanako Inoue, Ken-ichi Ikeda, Masaharu Mizutani & Yukihiro Sugimoto

  2. Faculty of Agriculture, Kobe University, Nada-ku, Kobe, 657-8501, Japan

    Akihito Miyoshi

  3. Molecular Photoscience Research Center, Kobe University, Nada-ku, Kobe, 657-8501, Japan

    Seiji Akimoto

  4. Research Center for Ultra-High Voltage Electron Microscopy, Osaka University, Ibaraki, Osaka, 567-0047, Japan

    Kanako Inoue

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  1. Yoko Marutani
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Correspondence to Yasuo Yamauchi.

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Marutani, Y., Yamauchi, Y., Higashiyama, M. et al. Essential role of the PSI–LHCII supercomplex in photosystem acclimation to light and/or heat conditions by state transitions. Photosynth Res 131, 41–50 (2017). https://doi.org/10.1007/s11120-016-0295-1

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Keywords

  • Heat stress
  • Photosynthetic electron flow
  • Photosystem
  • Protein phosphorylation
  • State transition
  • Thylakoid membrane
  • Wheat