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The absence of chlorophyll b affects lateral mobility of photosynthetic complexes and lipids in grana membranes of Arabidopsis and barley chlorina mutants

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Abstract

The lateral mobility of integral components of thylakoid membranes, such as plastoquinone, xanthophylls, and pigment–protein complexes, is critical for the maintenance of efficient light harvesting, high rates of linear electron transport, and successful repair of damaged photosystem II (PSII). The packaging of the photosynthetic pigment–protein complexes in the membrane depends on their size and stereometric parameters which in turn depend on the composition of the complexes. Chlorophyll b (Chlb) is an important regulator of antenna size and composition. In this study, the lateral mobility (the mobile fraction size) of pigment–protein complexes and lipids in grana membranes was analyzed in chlorina mutants of Arabidopsis and barley lacking Chlb. In the Arabidopsis ch1-3 mutant, diffusion of membrane lipids decreased as compared to wild-type plants, but the diffusion of photosynthetic complexes was not affected. In the barley chlorina f2 3613 mutant, the diffusion of pigment–protein complexes significantly decreased, while the diffusion of lipids increased, as compared to wild-type plants. We propose that the size of the mobile fractions of pigment–protein complexes in grana membranes in vivo is higher than reported previously. The data are discussed in the context of the protein composition of antennae, characteristics of the plastoquinone pool, and production of reactive oxygen species in leaves of chlorina mutants.

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Abbreviations

Chl:

Chlorophyll

Cyt b6/f:

Cytochrome b6/f

FRAP:

Fluorescence recovery after photobleaching

LHC:

Light-harvesting complex

PC:

Plastocyanin

PPFR:

Photosynthetic photon flux rate

PQ:

Plastoquinone

PSI:

Photosystem I

PSII:

Photosystem II

Q A, Q A :

Primary, secondary PSII acceptor

RC:

Reaction center

ROS:

Reactive oxygen species

TEM:

Transmission electron microscopy

VDE:

Violaxanthinde-epoxidase

WT:

Wild type; the genotype with normal chlorophyll synthesis

References

  • Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657:23–32

    Article  CAS  PubMed  Google Scholar 

  • Apel P (1967) Photosynthesemessungen an Chlorophyllmutanten von Gerste (Lichtkurven, "light-Atmung", Starklichtemfindlichkeit). Stud Biophys 5:105–110

    Google Scholar 

  • Arnon D (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassi R, Hinz U, Barbato R (1985) The role of the light harvesting complex and photosystem II in thylakoid stacking in the chlorina-f2 barley mutant. Carlsberg Res Commun 50:347–367

    Article  CAS  Google Scholar 

  • Blackwell MF, Gibas C, Gygax S, Roman D, Wagner B (1994) The plastoquinone diffusion coefficient in chloroplasts and its mechanistic implications. Biochim Biophys Acta 1183:533–543

    Article  CAS  Google Scholar 

  • Borisova-Mubarakshina MM, Ivanov BN, Vetoshkina DV, Lubimov VY, Fedorchuk TP, Naydov IA, Kozuleva MA, Rudenko NN, Dall’Osto La, Cazzaniga S, Bassi R (2015) Long-term acclimatory response to excess excitation energy: evidence for a role of hydrogen peroxide in the regulation of photosystem II antenna size. J Exp Bot 66:7151–7164

    Article  CAS  PubMed  Google Scholar 

  • Bossmann BL, Knoetzel J, Jansson S (1997) Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins. Photosynth Res 52:127–136

    Article  CAS  Google Scholar 

  • Bossmann BL, Grimme H, Knoetzel J (1999) Protease-stable integration of Lhcb1 into thylakoid membranes is dependent on chlorophyll b in allelic chlorina-f2 mutants of barley (Hordeum vulgare L). Planta 207:551–558

    Article  CAS  Google Scholar 

  • Brestic M, Zivcak M (2013) PSII Fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In: Rout GR, Das AB (eds) Molecular stress physiology of plants. Springer, Dordrecht, pp 87–131

    Chapter  Google Scholar 

  • de Bianchi S, Dall’Osto L, Tognon G, Morosinotto T, Bassi R (2008) Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell 20:1012–1028

    Article  PubMed  PubMed Central  Google Scholar 

  • de Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall’Osto L (2011) Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. Plant Cell 23:2659–2679

    Article  PubMed  PubMed Central  Google Scholar 

  • Dmitrieva VA, Ivanova AN, Tyutereva EV, Evkaikina AI, Klimova EA, Voitsekhovskaja OV (2017) Chlorophyllide-a-Oxygenase (CAO) deficiency affects the levels of singlet oxygen and formation of plasmodesmata in leaves and shoot apical meristems of barley. Plant Signal Behav. doi:10.1080/15592324.2017.1300732

    PubMed  Google Scholar 

  • Dulin D, Le Gall A, Perronet K, Soler N, Fourmy D, Yoshizawa S, Bouyer P, Westbrook N (2010) Reduced photobleaching of BODIPY-FL. Phys Proc 3:1563–1567

    Article  CAS  Google Scholar 

  • Espineda CE, Alicia SL, Domenica D, Brusslan JA (1999) The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b. Proc Natl Acad Sci USA 96:10507–10511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goral TK, Johnson MP, Brain APR, Kirchhoff H, Ruban AV, Mullineaux CW (2010) Visualizing the mobility and distribution of chlorophyll proteins in higher plant thylakoid membranes: effects of photoinhibition and protein phosphorylation. Plant J 62:948–959

    CAS  PubMed  Google Scholar 

  • Goral TK, Johnson MP, Duffy CDP, Brain APR, Ruban AV, Mullineaux CW (2012) Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. Plant J 69:289–301

    Article  CAS  PubMed  Google Scholar 

  • Haferkamp S, Haase W, Pascal AA, van Amerongen H, Kirchhoff H (2010) Efficient light harvesting by photosystem II requires an optimized protein packing density in grana thylakoids. J Biol Chem 108:17020–17028

    Article  Google Scholar 

  • Härtel H, Lokstein H, Grimm B, Rank B (1996) Kinetic studies on the xanthophyll cycle in barley leaves (Influence of antenna size and relations to nonphotochemical chlorophyll fluorescence quenching). Plant Physiol 110:471–482

    Article  PubMed  PubMed Central  Google Scholar 

  • Havaux M, Dall’osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Highkin HR, Frenkel AW (1962) Studies of growth and metabolism of a barley mutant lacking chlorophyll b. Plant Physiol 37:814-820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanov AG, Allakhverdiev SI, Huner NP, Murata N (2012) Genetic decrease in fatty acid unsaturation of phosphatidylglycerol increased photoinhibition of photosystem I at low temperature in tobacco leaves. Biochim Biophys Acta 1817:1374–1379

    Article  CAS  PubMed  Google Scholar 

  • Ivanov BN, Borisova-Mubarakshina MM, Kozuleva MA (2017) Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signaling by hydrogen peroxide. Funct Plant Biology. doi:10.1071/FP16322

  • Johnson M, Goral TK, Duffy CDP, Brain APR, Mullineaux CW, Ruban AV (2011) Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23:1468–1479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson M, Vasilev C, Olsen JD, Hunter CN (2014) Nanodomains of cytochrome b6f and photosystem II complexes in spinach grana thylakoid membranes. Plant Cell 26:3051–3061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dabrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli D, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serodio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khorobrykh SA, Ivanov BN (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids. Photosynth Res 71:209–219

    Article  CAS  PubMed  Google Scholar 

  • Kim EH, Li XP, Razeghifard R, Anderson JM, Niyogi KK, Pogson BJ, Chow WS (2009) The multiple roles of light-harvesting chlorophyll a/b-protein complexes define structure and optimize function of Arabidopsis chloroplasts: a study using two chlorophyll b-less mutants. Biochim Biophys Acta 1787:973–984

    Article  CAS  PubMed  Google Scholar 

  • Kirchhoff H (2013) Architectural switches in plant thylakoid membranes. Photosynth Res 116:481–487

    Article  CAS  PubMed  Google Scholar 

  • Kirchhoff H (2014) Diffusion of molecules and macromolecules in thylakoid membranes. Biochim Biophys Acta 1837:495–502

    Article  CAS  PubMed  Google Scholar 

  • Kirchhoff H, Horstmann S, Weis E (2000) Control of the photosynthetic electron transport by PQ diffusion microdomains in thylakoids of higher plants. Biochim Biophys Acta 1459:148–168

    Article  CAS  PubMed  Google Scholar 

  • Kirchhoff H, Mukherjeei U, Galla H-J (2002) Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemisrty 41:4872–4882

    Article  CAS  Google Scholar 

  • Kirchhoff H, Haferkamp S, Allen JF, Epstein DBA, Mullineaux CW (2008) Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiol 146:1571–1578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kouril R, Wientjes E, Bultema JB, Croce R, Boekema EJ (2013) High-light vs low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochym Biophys Acta 1827:411-419

    CAS  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Kreslavski V, Carpentier R, Klimov V, Murata N, Allakhverdiev S (2007) Molecular mechanisms of stress resistance of the photosynthetic apparatus. Biochem (Mosc) Suppl Ser A 1:185–205

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kunugi M, Satoh S, Ihara K, Shibata K, Yamagishi Y, Kogame K, Obokata J, Takabayashi A, Tanaka A (2016) Evolution of green plants accompanied changes in light-harvesting systems. Plant Cell Physiol 57:1231–1243

    Article  CAS  PubMed  Google Scholar 

  • Lavergne J, Bouchaud J-P, Joliot P (1992) Plastoquinone compartmentation in chloroplasts. II theoretical aspects. Biochim Biophys Acta 1101:13–22

    Article  CAS  Google Scholar 

  • Leverenz JW, Öquist G, Winglse G (1992) Photosynthesis and photoinhibition in leaves of chlorophyll b-less barley in relation to absorbed light. Physiol Plant 85:495–502

    Article  CAS  Google Scholar 

  • Lin Z-F, Lin G-Z, Peng C-L (2009) Enhancement of susceptivity to photoinhibition and photooxidation in rice chlorophyll b-less mutants. Photosynthetica 47:46–54

    Article  CAS  Google Scholar 

  • Los DA, Mironov KS, Allakhverdiev SI (2013) Regulatory role of membrane fluidity in gene expression and physiological functions. Photosynth Res 116:489–509

    Article  CAS  PubMed  Google Scholar 

  • Miller KR, Miller GJ, McIntyre KR (1976) The light-harvesting chlorophyll-protein complex of photosystem II Its location in the photosynthetic membrane. J Cell Biol 71:624–638

    Article  CAS  PubMed  Google Scholar 

  • Morosinotto T, Bassi R, Frigerio S, Finazzi G, Morris E, Barber J (2006) Biochemical and structural analyses of a higher plant photosystem II supercomplex of a photosystem I-less mutant of barley consequences of a chronic over-reduction of the plastoquinone pool. FEBS J 273:4616–4630

    Article  CAS  PubMed  Google Scholar 

  • Mueller AH, Dockter C, Gough SP, Lundqvist U, von Wettstein D, Hansson M (2012) Characterization of mutations in barley fch2 encoding chlorophyllide a oxygenase. Plant Cell Physiol 53:1232–1246

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84:1–7

    Article  CAS  PubMed  Google Scholar 

  • Ramel F, Ksas B, Akkari E, Mialoundama AS, Monnet F, Krieger-Liszkay A et al (2013) Light-induced acclimation of the arabidopsis chlorina1 mutant to singlet oxygen. Plant Cell 25:1445–1462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reits EA, Neefjes JJ (2001) From fixed to FRAP: measuring protein mobility and activity in living cells. Nat Cell Biol 3(6):E145–E147

    Article  CAS  PubMed  Google Scholar 

  • Sagromsky H (1974) Zur physiologischen Bedeutung von Chlorophyll b. Biochem Physiol Pflanzen 166:95-104

    Article  CAS  Google Scholar 

  • Schmitt FJ, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim Biophys Acta 1837:835–848

    Article  CAS  PubMed  Google Scholar 

  • Semenova GA (1995) Particle regularity on thylakoid fracture faces is influenced by storage-conditions. Can J Bot 73:1676–1682. doi:10.1139/b95-181

    Article  Google Scholar 

  • Simpson DJ (1978) Freeze-fracture studies on barley plastid membranes II Wild-type chloroplasts. Carlsberg Res Commun 43:365–389

    Article  Google Scholar 

  • Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M, Kühlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24:919–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor & Francis, London

    Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2004) Analysis of the chlorophyll a fluorescence transient, advances in photosynthesis and respiration. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Kluwer Academic, Dordrecht

    Google Scholar 

  • Takabayashi A, Kurihara K, Kuwano M, Kasahara Y, Tanaka R, Tanaka A (2011) The oligomeric states of the photosystems and the light-harvesting complexes in the Chl b-less mutant. Plant Cell Physiol 52:2103–2114

    Article  CAS  PubMed  Google Scholar 

  • Tanaka R, Tanaka A (2011) Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochim Biophys Acta 1807:968–976

    CAS  Google Scholar 

  • Tietz S, Puthiyaveetil S, Enlow HM, Yarbrough R, Wood M, Semchonok DA et al (2015) Functional implications of photosystem II crystal formation in photosynthetic membranes. J Biol Chem 290:14091–14106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tremmel I, Kirchhoff H, Weis E, Farquhar CD (2003) Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochym Biophys Acta 1607:97–109

    CAS  Google Scholar 

  • Tyutereva EV, Voitsekhovskaja OV (2011) Responses of chlorophyll b-less chlorina 3613 barley mutant to a prolonged decrease in illuminance: 1. Dynamics of chlorophyll content, growth, and productivity. Russ J Plant Physiol 58:1–8

    Article  CAS  Google Scholar 

  • Voitsekhovskaja OV, Tyutereva EV (2015) Chlorophyll b in angiosperms: functions in photosynthesis, signaling and ontogenetic regulation. J Plant Physiol 189:51–64

    Article  CAS  PubMed  Google Scholar 

  • Whitehouse DG, Moore AL (1993) Isolation and purification of functionally intact chloroplasts from leaf tissue and leaf tissue protoplasts. In: Graham JM, Higgins JA (eds) Methods in molecular biology, vol. 19: biomembrane protocols: I. Isolation and analysis. Humana Press, Totowa, pp 123–151

    Google Scholar 

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Acknowledgements

This paper is dedicated to the memory of Prof. em. Dr. Ulrich Heber (1930–2016). We thank Dr. Tomas Morosinotto (University of Padova, Italy) for kindly sharing with us the protocol of grana isolation. We are grateful to Ms Valeria A. Dmitrieva for help with some experiments and to Dr. Boris N. Ivanov for sharing unpublished results. This study was supported by the Russian Science Foundation (project #14-16-00120 to OVV). The Core Facilities Center “Cell and Molecular Technologies in Plant Science” at the Komarov Botanical Institute RAS (Saint-Petersburg, Russia) and the Research Resource Centre for Molecular and Cell Technologies of Saint-Petersburg State University are gratefully acknowledged for technical support.

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  1. Laboratory of Plant Ecological Physiology, Komarov Botanical Institute, Russian Academy of Sciences, ul. Professora Popova 2, 197376, Saint-Petersburg, Russia

    Elena V. Tyutereva, Anastasiia I. Evkaikina & Olga V. Voitsekhovskaja

  2. Laboratory of Plant Anatomy and Morphology, Komarov Botanical Institute, Russian Academy of Sciences, ul. Professora Popova 2, 197376, Saint-Petersburg, Russia

    Alexandra N. Ivanova

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  1. Elena V. Tyutereva
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  2. Anastasiia I. Evkaikina
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  4. Olga V. Voitsekhovskaja
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Correspondence to Olga V. Voitsekhovskaja.

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Tyutereva, E.V., Evkaikina, A.I., Ivanova, A.N. et al. The absence of chlorophyll b affects lateral mobility of photosynthetic complexes and lipids in grana membranes of Arabidopsis and barley chlorina mutants. Photosynth Res 133, 357–370 (2017). https://doi.org/10.1007/s11120-017-0376-9

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