Skip to main content
SpringerLink
Log in

Presence of ‘PSI free’ LHCI and monomeric LHCII and subsequent effects on fluorescence characteristics in lincomycin treated maize

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The cause of the strong non-photochemical fluorescence quenching was examined in maize (Zea mays L.) plants that were treated with lincomycin during the 72 h period of greening. They were deficient in core complexes but seemed to contain the full complement of antennae. The following results were obtained: (1) High F o could not be attributed to the dark reduction of Q A but to the presence of a high amount of not properly organized antenna complexes due to the inhibited synthesis of reaction centres. (2) On illumination fluorescence intensity dropped considerably below F o within 20 s, and reached a steady state still below F o . (3) Slowly relaxing part of non-photochemical quenching was significantly higher than in control plants. (4) De-epoxidation state was constant, and corresponded to the maximal value of the control. (5) Free Lhca1/4 dimers could be detected in all submembrane fractions, including the grana, obtained by digitonin fractionation. (6) Increase in the 679 and 700 nm fluorescence emissions could be attributed to the monomerisation of part of LHCII and to the presence of free Lhca2 or LHCII aggregates, respectively. (7) LHCII or PSII+LHCII and Lhca1/4 interaction may contribute to the increase of long-wavelength fluorescence in the granal fraction. We assume that the elevated fluorescence quenching of monomeric LHCII as well as the interaction between LHCII or PSII+LHCII and Lhca1/4 can be considered as an explanation for the extensive non-photochemical fluorescence quenching in lincomycin treated plants. The permanent presence of zeaxanthin may have contributed to the fast formation of quenching.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

CA:

Connecting antenna

CC:

Core complex

CP:

Chlorophyll protein

DEPS:

De-epoxidation state

LHC:

Light harvesting complex

NPQ:

Non-photochemical quenching calculated by the Stern-Volmer equation

PAGE:

Polyacrylamide gel electrophoresis

PPFD:

Photosynthetic photon flux density

PS:

Photosystem

qE, qI and qT :

Chlorophyll fluorescence quenching related to membrane energisation, photoinhibition and state transition, respectively

qN and qP:

Non-photochemical and photochemical quenching coefficient, respectively

VAZ:

Violaxanthin (V), antheraxanthin (A), zeaxanthin (Z)

References

  • Abadía J, Abadía A (1993) Iron and plant pigments. In: Barton LL, Hemming BC (eds) Iron chelation in plants and soil microorganisms. Academic, San Diego, pp 327–344

    Google Scholar 

  • Albertsson P-Å (1995) The structure and function of the chloroplast photosynthetic membrane—a model for the domain organization. Photosynth Res 46:141–149

    Article  CAS  Google Scholar 

  • Aliev JA, Suleimanov SY, Guseinova IM, Ismailov MA, Asadov AA (1993) Effect of specific translation inhibitors on polypeptide composition and spectral characteristics of wheat thylakoid membranes. Photosynthetica 29:361–367

    CAS  Google Scholar 

  • Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P, Jansson S (2003) Absense 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 

  • Bachmann KM, Ebbert V, Adams WW III, Verhoeven AS, Logan BA, Demmig-Adams B (2004) Effects of lincomycin on PSII efficiency, non-photochemical quenching, D1 protein and xanthophyll cycle during photoinhibition and recovery. Funct Plant Biol 31:803–813

    Article  CAS  Google Scholar 

  • Belkhodja R, Morales F, Quílez R, López-Millán A-F, Abadía A, Abadía J (1998) Iron deficiency causes changes in chlorophyll fluorescence due to the reduction in the dark of the Photosystem II acceptor side. Photosynth Res 56:265–276

    Article  CAS  Google Scholar 

  • Boardman NK (1971) Subchloroplast fragments: digitonin method. In: San Pietro A (ed) Methods in enzymology, photosynthesis, part A, vol XXIII. Academic, New York, pp 268–276

    Chapter  Google Scholar 

  • Bossmann B, 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 

  • Buschmann C (1995) Variation of the quenching of chlorophyll fluorescence under different intensities of actinic light in wildtype plants of tobacco and in an aurea mutant deficient of light-harvesting-complex. J Plant Biol 145:245–252

    CAS  Google Scholar 

  • Caffarri S, Frigerio S, Olivieri E, Righetti PG, Bassi R (2005) Differential accumulation of Lhcb gene products in thylakoid membranes of Zea mays plants grown under contrasting light and temperature conditions. Proteomics 5:758–768

    Article  PubMed  CAS  Google Scholar 

  • Campbell JM, Reusser F, Caskey CT (1979) Specificity of lincomycin action on peptidyl transferase activity. Biochem Biophys Res Commun 90:1032–1038

    Article  PubMed  CAS  Google Scholar 

  • Croce R, Morosinotto T, Ihalainen JA, Chojnicka A, Breton J, Dekker JP, van Grondelle R, Bassi R (2004) Origin of the 701-nm fluorescence emission of the Lhca2 subunit of higher plant Photosystem I. J Biol Chem 279:48543–48549

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • de las Rivas J, Abadía A, Abadía J (1989) A new reversed phase HPLC method resolving all major higher plant photosynthetic pigments. Plant Physiol 91:190–192

    PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26

    Article  Google Scholar 

  • Desquilbet TE, Duval J-C, Robert B, Houmard J, Thomas JC (2003) In the unicellular red alga Rhodella violacea iron deficiency induces an accumulation of uncoupled LHC. Plant Cell Physiol 44:1141–1151

    Article  PubMed  CAS  Google Scholar 

  • Doan J-M, Schoefs B, Ruban AV, Etienne A-L (2003) Changes in the LHCI aggregation state during iron repletion in the unicellular red alga Rhodella violacea. FEBS Lett 533:59–62

    Article  PubMed  CAS  Google Scholar 

  • Duysen M, Huckle L, Mogen K, Freeman T (1987) Chloramphenicol effects on chlorophyll degradation and photosystem I assembly in the chlorina CD3 wheat mutant. Photosynth Res 14:159–169

    Article  CAS  Google Scholar 

  • Ellis RJ (1975) Inhibition of chloroplast protein synthesis by lincomycin and 2-(4-methyl-2,6-dinitroanilino)-n-methylpropionamide. Phytochemistry 17:89–93

    Article  Google Scholar 

  • Fernandez-Muñoz R, Monro RE, Torres-Pinedo R, Vazquez D (1971) Substrate- and antibiotic-binding sites at the peptidyl-transferase centre of Escherichia coli ribosomes. Eur J Biochem 23:185–193

    Article  PubMed  Google Scholar 

  • Fodor F, Cseh E, Varga A, Zárai Gy (1998) Lead uptake, distribution, and remobilization in cucumber. J Plant Nutr 21:1363–1373

    CAS  Google Scholar 

  • Garab Gy, Cseh Z, Kovács L, Rajagopal S, Várkonyi Zs, Wentworth M, Mustárdy L, Dér A, Ruban AV, Papp E, Holzenburg A, Horton P (2002) Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants:thermo-optic mechanism. Biochemistry 41:15121–15129

    Article  PubMed  CAS  Google Scholar 

  • Green BR, Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47:685–714

    Article  PubMed  CAS  Google Scholar 

  • Hiller RG, Pilger TBG, Genge S (1977) Effect of lincomycin on the chlorophyll protein complex I content and photosystem I activity of greening leaves. Biochim Biophys Acta 460:431–444

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Rees G, Pascal AA, Noctor G, Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett 292:1–4

    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 

  • Jansson S, Stefánsson H, Nyström U, Gustafsson P, Albertsson P-Å (1997) Antenna protein composition of PS I and PS II in thylakoid sub-domains. Biochim Biophys Acta 1320:297–309

    Article  CAS  Google Scholar 

  • Josten JJ, Allen PM (1964) The mode of action of lincomycin. Biochem Biophys Res Commun 14:241–244

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Björkman 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 

  • Melkozernov AN (2001) Excitation energy transfer in photosystem I from oxygenic organisms. Photosynth Res 70:129–153

    Article  PubMed  CAS  Google Scholar 

  • Morales F, Abadía A, Abadía J (1991) Chlorophyll fluorescence and photon yield of oxygen evolution in iron-deficient sugar beet (Beta vulgaris L.) leaves. Plant Physiol 94:607–613

    Article  Google Scholar 

  • Morosinotto T, Castelletti S, Breton J, Bassi R, Croce R (2002) Mutation analysis of Lhca1 antenna complex. J Biol Chem 277:36253–36261

    Article  PubMed  CAS  Google Scholar 

  • Morosinotto T, Caffarri S, Dall’Osto L, Bassi R (2003) Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiol Plant 119:347–354

    Article  CAS  Google Scholar 

  • Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21:6709–6720

    Article  PubMed  CAS  Google Scholar 

  • Mulo P, Pursiheimo S, Hou C-X, Tyystjärvi T, Aro E-M (2003) Multiple effects of antibiotics on chloroplast and nuclear gene expression. Funct Plant Biol 30:1097–1103

    Article  CAS  Google Scholar 

  • Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460

    Article  PubMed  CAS  Google Scholar 

  • Okada K, Satoh K, Katoh S (1991) Chloramphenicol is an inhibitor of photosynthesis. FEBS Lett 295:155–158

    Article  PubMed  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Rochaix J-D (1992) Post-transcriptional steps in the expression of chloroplasts genes. Annu Rev Cell Biol 8:1–28

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Horton P (1992) Mechanism of ΔpH-dependent dissipation of absorbed excitation energy by photosynthetic membranes I. Spectroscopic analysis of isolated light-harvesting complexes. Biochim Biophys Acta 1102:30–38

    Article  CAS  Google Scholar 

  • Ruban AV, Lee PJ, Wentworth M, Young AJ, Horton P (1999) Determination of the stoichiometry and strength of binding of xanthophylls to the photosystem II light harvesting complexes. J Biol Chem 274:10458–10465

    Article  PubMed  CAS  Google Scholar 

  • Sárvári É, Halász G, Nyitrai P, Láng F (1976) Effect of lincocin treatment on the greening process in bean (Phaseolus vulgaris L.) leaves. Physiol Plant 36:187–192

    Article  Google Scholar 

  • Sárvári É, Halász G, Török Sz, Láng F (1978) Light-induced fluorescence decay during the greening of normal and lincomycin-treated maize leaves. Planta 141:135–139

    Article  Google Scholar 

  • Sárvári É, Nyitrai P (1994) Separation of chlorophyll-protein complexes by Deriphat polyacrylamide gradient gel electrophoresis. Electrophoresis 15:1067–1071

    Article  Google Scholar 

  • Sárvári É, Nyitrai P, Gyüre K (1984) Chlorophyll-protein derivative of the peripheral light-harvesting antenna of photosystem I. Photobiochem Photobiophys 8:229–237

    Google Scholar 

  • Sárvári É, Szigeti Z, Nyitrai P (1996) Lincomycin induced changes in the organization and fluorescence properties of developing maize thylakoids. Plant Physiol Biochem (special issue), p 109

  • Scheller HV, Jensen PE, Haldrup A, Lunde C, Knoetzel J (2001) Role of subunits in eukaryotic photosystem I. Biochim Biophys Acta 1507:41–60

    Article  PubMed  CAS  Google Scholar 

  • Tyystjärvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Nat Acad Sci USA 93:2213–2218

    Article  PubMed  Google Scholar 

  • Vijayan P, Browse J (2002) Photoinhibition in mutants of Arabidopsis deficient in thylakoid unsaturation. Plant Physiol 129:876–885

    Article  PubMed  CAS  Google Scholar 

  • Wentworth M, Ruban AV, Horton P (2004) The functional significance of the monomeric and trimeric states of the photosystem II light harvesting complexes. Biochemistry 43:501–509

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Goodman HM, Jansson S (1997) Antisense inhibition of the photosystem I antenna protein Lhca4 in Arabidopsis thaliana. Plant Physiol 115:1525–1531

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Scheller HV (1999) Light-harvesting complex II binds to several small subunits of photosystem I. J Biol Chem 279:3180–3187

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to M. Barón and B. Böddi for valuable discussions. The authors thank the skilful assistance of Zsuzsanna Ostorics. This work was financially supported by the OTKA (T 043646) grant.

Author information

Authors and Affiliations

  1. Department of Plant Physiology and Molecular Plant Biology, Eötvös Loránd University, Pázmány Péter sétány 1/c, 1117, Budapest, Hungary

    László Gáspár, Éva Sárvári & Zoltán Szigeti

  2. Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas, Apdo. 202, E-50080, Zaragoza, Spain

    Fermín Morales

Authors
  1. László Gáspár
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Éva Sárvári
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fermín Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zoltán Szigeti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to László Gáspár.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gáspár, L., Sárvári, É., Morales, F. et al. Presence of ‘PSI free’ LHCI and monomeric LHCII and subsequent effects on fluorescence characteristics in lincomycin treated maize. Planta 223, 1047–1057 (2006). https://doi.org/10.1007/s00425-005-0149-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0149-0

Keywords

Search

Navigation