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Inhibition of photosynthetic oxygen evolution and electron transfer from the quinone acceptor QA − to QB by iron deficiency

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Abstract

The effect of iron deficiency on photosynthetic electron transport in Photosystem II (PS II) was studied in leaves and thylakoid membranes of lettuce (Lactuca sativa, Romaine variety) plants. PS II electron transport was characterized by oxygen evolution and chlorophyll fluorescence parameters. Iron deficiency in the culture medium was shown to affect water oxidation and the advancement of the S-states. A decrease of maximal quantum yield of PS II and an increase of fluorescence intensity at step J and I of OJIP kinetics were also observed. Thermoluminescence measurements revealed that charge recombination between the quinone acceptor of PS II, QB, and the S2 state of the Mn-cluster was strongly perturbed. Also the dark decay of Chl fluorescence after a single turnover white flash was greatly retarded indicating a slower rate of QA − reoxidation.

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Abbreviations

Chl:

Chlorophyll

DCBQ:

2,6-Dichlorobenzoquinone

DCIP:

2,6-Dichlorophenolindophenol

DCMU:

3-(3′,4′-Dichlorophenyl)-1,1-dimethylurea

DBMIB:

2,5-Dibromo-3-methyl-6-isopropyl-p-benzoquinone

FI:

Chlorophyll fluorescence induction

F 0 :

Basal level of chlorophyll fluorescence

F m :

Maximal level of chlorophyll fluorescence

F v :

Variable chlorophyll fluorescence

OEC:

Oxygen evolving complex

P680:

Primary electron donor of photosystem II

Pheo:

Pheophytin

PS:

Photosystem

PQ:

Plastoquinone

QA and QB :

Primary and secondary quinone acceptors of photosystem II

RC:

Reaction center

LHC:

Light-harvesting complex

TL:

Thermoluminescence

T m :

Temperature maximum of thermoluminescence emission

References

  • Andaluz S, Millan AF, De las Rivas J, Aro EM, Abadía J, Abadía A (2006) Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynth Res 89:141–155. doi:10.1007/s11120-006-9092-6

    Article  PubMed  CAS  Google Scholar 

  • Andrizhiyevskaya EG, Schwabe TM, Germano M, D’Haene S, Kruip J, Grondelle RV, Dekker JP (2002) Spectroscopic properties of PSI–IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942. Biochim Biophys Acta 1556:265–272. doi:10.1016/S0005-2728(02)00371-7

    Article  PubMed  CAS  Google Scholar 

  • Barthélemy X, Popovic R, Franck F (1997) Studies on the O-J-I-P transient of chlorophyll fluorescence in relation to photosystem II assembly and heterogeneity in plastids of greening barley. J Photochem Photobiol B Biol 39:213–218. doi:10.1016/S1011-1344(97)00012-2

    Article  Google Scholar 

  • Beauchemin R, Gautier A, Harnois J, Boisvert S, Govindachary S, Carpentier R (2007) Spermine and spermidine inhibition of photosystem II: disassembly of the oxygen evolving complex and consequent perturbation in electron donation from TyrZ to P680+ and the quinone acceptors QA − to QB. Biochim Biophys Acta 1767:905–912. doi:10.1016/j.bbabio.2007.04.001

    Article  PubMed  CAS  Google Scholar 

  • Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll–protein complex induced by iron deficiency in cyanobacteria. Nature 412:745–748. doi:10.1038/35089104

    Article  PubMed  CAS  Google Scholar 

  • Boisvert S, Joly D, Carpentier R (2006) Quantitative analysis of the experimental O-J-I-P chlorophyll fluorescence induction kinetics apparent activation energy and origin of each kinetic step. FEBS J 273:4770–4777. doi:10.1111/j.1742-4658.2006.05475.x

    Article  PubMed  CAS  Google Scholar 

  • Boucher N, Harnois J, Carpentier R (1990) Heat-stress stimulation of electron flow in a photosystem I submembrane fraction. Biochem Cell Biol 68:999–1004

    Article  PubMed  CAS  Google Scholar 

  • Briat JF, Vert G (2004) Acquisition et gestion du fer par les plantes. Cah Agric 13:183–201

    Google Scholar 

  • Ducruet JM (2003) Chlorophyll thermoluminescence of leaf discs: simple instruments and progress in signal interpretation open the way to new ecophysiological indicators. J Exp Bot 54:2419–2430. doi:10.1093/jxb/erg268

    Article  PubMed  CAS  Google Scholar 

  • Ferreira F, Straus NA (1994) Iron deprivation in cyanobacteria. J Appl Phycol 6:199–210

    Article  CAS  Google Scholar 

  • Gauthier A, Govindachary S, Harnois J, Carpentier R (2006) Interaction of N,N,N′,N′-tetramethyl-p-phenylenediamine with photosystem II as revealed by thermoluminescence: reduction of the higher oxidation states of the Mn cluster and displacement of plastoquinone from the QB niche. Biochim Biophys Acta 1757:1547–1556. doi:10.1016/j.bbabio.2006.09.005

    Article  PubMed  CAS  Google Scholar 

  • Guikema JA (1985) Fluorescence induction characteristics of Anacystis nidulans during recovery from iron deficiency. J Plant Nutr 8:891–908. doi:10.1080/01904168509363393

    Article  CAS  Google Scholar 

  • Guikema JA, Sherman LA (1983) Organization and function of chlorophyll in membranes of cyanobacteria during iron starvation. Plant Physiol 73:250–256. doi:10.1104/pp.73.2.250

    Article  PubMed  CAS  Google Scholar 

  • Homann PH (1999) Reliability of photosystem II thermoluminescence measurements after sample freezing: few artefacts with photosystem II membranes but gross distortions with certain leaves. Photosynth Res 62:219–229. doi:10.1023/A:1006372411264

    Article  CAS  Google Scholar 

  • Joly D, Bigras C, Harnois J, Govindachary S, Carpentier R (2005) Kinetic analyses of the OJIP chlorophyll fluorescence rise in thylakoid membranes. Photosynth Res 84:107–112. doi:10.1007/s11120-004-7763-8

    Article  PubMed  CAS  Google Scholar 

  • Krüger GHJ, Tsimilli-Michael M, Strasser RJ (1997) Light stress provokes plastic and elastic modifications in structure and function of Photosystem II in camellia leaves. Physiol Plant 101:265–277

    Article  Google Scholar 

  • Larbi A, Abadía A, Abadía J, Morales F (2006) Down co-regulation of light absorption, photochemistry, and carboxylation in Fe-deficient plants growing in different environments. Photosynth Res 89:113–126. doi:10.1007/s11120-006-9089-1

    Article  PubMed  CAS  Google Scholar 

  • Lax JEM, Arteni AA, Boekema EJ, Pistorius EK, Michel KP, Rögner M (2007) Structural response of Photosystem 2 to iron deficiency: characterization of a new Photosystem 2-IdiA complex from the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1767:528–534. doi:10.1016/j.bbabio.2007.01.003

    Article  PubMed  CAS  Google Scholar 

  • Lazár D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30. doi:10.1071/FP05095

    Article  Google Scholar 

  • Mamedov F, Stefanson H, Albersson PÅ, Styring S (2000) Photosystem II in different parts of the thylakoid membrane: a functional comparison between different domains. Biochemistry 39:10478–10486. doi:10.1021/bi992877K

    Article  PubMed  CAS  Google Scholar 

  • Mamedov F, Rintamäki E, Aro EM, Andersson B, Styring S (2002) Influence of protein phosphorylation on the electron-transport properties of Photosystem II. Photosynth Res 74:61–72

    Article  PubMed  CAS  Google Scholar 

  • Marschner H, Rômheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274. doi:10.1007/BF00008069

    Article  CAS  Google Scholar 

  • Messinger J, Seaton G, Wydrzynski T, Wacker U, Renger G (1997) S-3 state of the water oxidase in photosystem II. Biochemistry 36:6862–6873. doi:10.1021/bi962653r

    Article  PubMed  CAS  Google Scholar 

  • Michel KP, Pistorius EK (2004) Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: the function of IdiA and IsiA. Physiol Plant 120:36–50

    Article  PubMed  CAS  Google Scholar 

  • Michel KP, Thole HH, Pistorius EK (1996) IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942, is required for growth under iron and manganese limitations. Microbiology 142:2635–2645. doi:10.1099/00221287-142-9-2635

    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 97:886–893. doi:10.1104/pp.97.3.886

    Article  PubMed  CAS  Google Scholar 

  • Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodelling of the photosynthetic apparatus. EMBO J 21:6709–6720. doi:10.1093/emboj/cdf666

    Article  PubMed  CAS  Google Scholar 

  • Pakrasi HB, Goldenberg A, Sherman LA (1985a) Membrane development in the cyanobacterium, Anacystis nidulans, during recovery from iron starvation. Plant Physiol 79:290–295. doi:10.1104/pp79.1.290

    Article  PubMed  CAS  Google Scholar 

  • Pakrasi HB, Reitham HC, Sherman LA (1985b) Organization of pigment proteins in the photosystem II complex of the cyanobacterium Anacystis nidulans R2. Proc Natl Acad Sci USA 82:6903–6907

    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. doi:10.1016/S0005-2728(89)80347-0

    Article  CAS  Google Scholar 

  • Pushnik JC, Miller M (1982) The effect of iron and light treatments on chloroplast composition and ultrastructure in iron-deficient barley leaves. J Plant Nutr 5:311–322. doi:10.1080/01904168209362960

    Article  CAS  Google Scholar 

  • Putrenko II, Vasil’ev S, Bruce D (1999) Modulation of flash-induced photosystem II fluorescence by events occurring at the water oxidizing complex. Biochemistry 38:10632–10641

    Article  PubMed  CAS  Google Scholar 

  • Riethman HC, Sherman LA (1988) Purification and characterization of an iron stress-induced chlorophyll-protein from cyanobacterium Anacystic nidulans R2. Biochim Biophys Acta 935:141–151. doi:10.1016/0005-2728(88)90211-3

    Article  PubMed  CAS  Google Scholar 

  • Samson G, Prasil O, Yaakoubd B (1999) Photochemical and thermal phases of chlorophyll a fluorescence. Photosynthetica 37:163–182. doi:10.1023/A:1007095619317

    Article  CAS  Google Scholar 

  • Sandmann G (1985) Consequences of iron deficiency on photosynthetic and respiratory electron transport in blue-green algae. Photosynth Res 6:261–271. doi:10.1007/BF00049282

    Article  CAS  Google Scholar 

  • Sane PV (2004) Thermoluminescence: a technique for probing photosystem II. In: Carpentier R (ed) Photosynthesis research protocols. Humana Press, Totowa, pp 229–248

    Chapter  Google Scholar 

  • Spiller S, Terry N (1980) Limiting factors in photosynthesis. II. Iron stress diminishes photochemical capacity by reducing the number of photosynthetic units. Plant Physiol 65:121–125. doi:10.1104/pp.65.1.121

    Article  PubMed  CAS  Google Scholar 

  • Strasser RJ, Govindjee NR (1992) On the O-J-I-P fluorescence transient in leaves and D1 mutants of Chlamydomonas reinhardtii. In: Murata N (ed) Research in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 29–32

    Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee NR (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:1–8. doi:10.1016/j.pbi.2006.03.011

    Article  Google Scholar 

  • Terry N, Abadia J (1986) Function of iron in chloroplasts. J Plant Nutr 9:609–646. doi:10.1080/01904168609363470

    Article  CAS  Google Scholar 

  • Timperio AM, D’Amici GM, Barta C, Loreto F, Zolla L (2007) Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. J Exp Bot 58:3695–3710. doi:10.1093/jxb/erm219

    Article  PubMed  CAS  Google Scholar 

  • Wydrzynski TJ (1982) Oxygen evolution in photosynthesis. In: Govindjee NR (ed) Photosynthesis: energy conversion by plants and bacteria. Academic Press, New York, pp 469–506

    Google Scholar 

  • Zeinalov Y (2002) An equipment for investigations of photosynthetic oxygen production reactions. Bulg J Plant Physiol 28:57–67

    Google Scholar 

  • Zhu XG, Govindjee NR, Bakereric D, Ort DR, Stephen PL (2005) Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with photosystem II. Planta 223:114–133. doi:10.1007/s00425-005-0064-4

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

This study was supported by Natural Sciences and Engineering Research Council of Canada (NSERC).

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Authors and Affiliations

  1. Groupe de Recherche en Biologie Végétale (GRBV), Université du Québec à Trois-Rivièrs, Trois-Rivières, QC, G9A 5H7, Canada

    Najoua Msilini, Maha Zaghdoudi, Sridharan Govindachary & Robert Carpentier

  2. Unité de Physiologie et de Biochimie de la Tolérance au Sel chez les Plantes, Faculté des Sciences de Tunis, Campus Universitaire, 1060, Tunis, Tunisia

    Najoua Msilini, Maha Zaghdoudi, Mokhtar Lachaâl & Zeineb Ouerghi

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  1. Najoua Msilini
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  2. Maha Zaghdoudi
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  3. Sridharan Govindachary
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  4. Mokhtar Lachaâl
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  5. Zeineb Ouerghi
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  6. Robert Carpentier
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Correspondence to Robert Carpentier.

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Msilini, N., Zaghdoudi, M., Govindachary, S. et al. Inhibition of photosynthetic oxygen evolution and electron transfer from the quinone acceptor QA − to QB by iron deficiency. Photosynth Res 107, 247–256 (2011). https://doi.org/10.1007/s11120-011-9628-2

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