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Inhibition of CO2 fixation by iodoacetamide stimulates cyclic electron flow and non-photochemical quenching upon far-red illumination

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Abstract

The Benson–Calvin cycle enzymes are activated in vivo when disulfide bonds are opened by reduction via the ferredoxin-thioredoxin system in chloroplasts. Iodoacetamide reacts irreversibly with free –SH groups of cysteine residues and inhibits the enzymes responsible for CO2 fixation. Here, we investigate the effect of iodoacetamide on electron transport, when infiltrated into spinach leaves. Using fluorescence and absorption spectroscopy, we show that (i) iodoacetamide very efficiently blocks linear electron flow upon illumination of both photosystems (decrease in the photochemical yield of photosystem II) and (ii) iodoacetamide favors cyclic electron flow upon light excitation specific to PSI. These effects account for an NPQ formation even faster in iodoacetamide under far-red illumination than in the control under saturating light. Such an increase in NPQ is dependent upon the proton gradient across the thylakoid membrane (uncoupled by nigericin addition) and PGR5 (absent in Arabidopsis pgr5 mutant). Iodoacetamide very tightly insulates the electron current at the level of the thylakoid membrane from any electron leaks toward carbon metabolism, therefore, providing choice conditions for the study of cyclic electron flow around PSI.

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References

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098(3):275–335

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8(1):15–19

    Article  PubMed  CAS  Google Scholar 

  • Alric J (2010) Cyclic electron flow around photosystem I in unicellular green algae. Photosynth Res 106(1–2):47–56

    Article  PubMed  CAS  Google Scholar 

  • Alric J, Lavergne J et al (2010) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions. Biochim Biophys Acta 1797(1):44–51

    Article  PubMed  CAS  Google Scholar 

  • Arnon DI, Chain RK (1975) Regulation of ferredoxin-catalyzed photosynthetic phosphorylations. Proc Natl Acad Sci USA 72(12):4961–4965

    Article  PubMed  CAS  Google Scholar 

  • Arnon DI, Allen MB et al (1954) Photosynthesis by isolated chloroplasts. Nature 174(4426):394–396

    Article  PubMed  CAS  Google Scholar 

  • Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochimica et Biophysica Acta (BBA)—Bioenergetics 1318(3):322–373

    Article  CAS  Google Scholar 

  • Breyton C, Nandha B et al (2006) Redox modulation of cyclic electron flow around photosystem I in C3 plants. Biochemistry 45(45):13465–13475

    Article  PubMed  CAS  Google Scholar 

  • Clark RD, Hawkesford MJ et al (1984) Association of ferredoxin-NADP + oxidoreductase with the chloroplast cytochrome b-f complex. FEBS Lett 174(1):137–142

    Article  CAS  Google Scholar 

  • Dal Bosco C, Lezhneva L et al (2004) Inactivation of the chloroplast ATP synthase gamma subunit results in high non-photochemical fluorescence quenching and altered nuclear gene expression in Arabidopsis thaliana. J Biol Chem 279(2):1060–1069

    Article  PubMed  CAS  Google Scholar 

  • Ferri G, Iadarola P et al (1981) Chloroplast glyceraldehyde-3-phosphate dehydrogenase (NADP +). Reactivity of essential cysteine residues in holo- and apoenzyme. Biochim Biophys Acta 660(2):325–332

    Article  PubMed  CAS  Google Scholar 

  • Finazzi G, Rappaport F (1998) In vivo characterization of the electrochemical proton gradient generated in darkness in green algae and its kinetic effects on cytochrome b6f turnover. Biochemistry 37(28):9999–10005

    Article  PubMed  CAS  Google Scholar 

  • Gilmore AM, Björkman O (1995) Temperature-sensitive coupling and uncoupling of ATPase-mediated, nonradiative energy dissipation: similarities between chloroplasts and leaves. Planta 197(4):646–654

    Article  CAS  Google Scholar 

  • Hald S, Nandha B et al (2008) Feedback regulation of photosynthetic electron transport by NADP(H) redox poise. Biochim Biophys Acta 1777(5):433–440

    Article  PubMed  CAS  Google Scholar 

  • Harbinson J, Foyer CH (1991) Relationships between the efficiencies of photosystems I and II and stromal redox state in CO2-free air. Plant Physiol 97(1):41–49

    Article  PubMed  CAS  Google Scholar 

  • Harbinson J, Woodward FI (1987) The use of light-induced absorbance changes at 820 nm to monitor the oxidation state of P-700 in leaves. Plant Cell Environ 10(2):131–140

    CAS  Google Scholar 

  • Heber U (1969) Conformational changes of chloroplasts induced by illumination of leaves in vivo. Biochimica et Biophysica Acta (BBA) —Bioenergetics 180(2):302–319

    Article  CAS  Google Scholar 

  • Horton P, Ruban AV et al (1996) Regulation of Light Harvesting in Green Plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  PubMed  CAS  Google Scholar 

  • Hosler JP, Yocum CF (1987) Regulation of Cyclic Photophosphorylation during Ferredoxin-Mediated Electron Transport : effect of DCMU and the NADPH/NADP Ratio. Plant Physiol 83(4):965–969

    Article  PubMed  CAS  Google Scholar 

  • Iwai M, Takizawa K et al (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464(7292):1210–1213

    Article  PubMed  CAS  Google Scholar 

  • Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108(32):13317–13322

    Article  PubMed  CAS  Google Scholar 

  • Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99(15):10209–10214

    Article  PubMed  CAS  Google Scholar 

  • Joliot P, Joliot A (2008) Quantification of the electrochemical proton gradient and activation of ATP synthase in leaves. Biochim Biophys Acta 1777(7–8):676–683

    PubMed  CAS  Google Scholar 

  • Joliot P, Beal D et al (2004) Cyclic electron flow under saturating excitation of dark-adapted Arabidopsis leaves. Biochim Biophys Acta 1656(2–3):166–176

    PubMed  CAS  Google Scholar 

  • Junge W, Rumberg B et al (1970) The necessity of an electric potential difference and its use for photophosphorylation in short flash groups. Eur J Biochem 14(3):575–581

    Article  PubMed  CAS  Google Scholar 

  • Kohn HI (1935) Inhibition of photosynthesis in chlorella pyrenoidosa by the iodo-acetyl radical. J Gen Physiol 19(1):23–34

    Article  PubMed  CAS  Google Scholar 

  • Kok B, Joliot P et al (1969) Electron transfer between the photoacts. In: Metzner H (ed) Progress in photosynthesis research, vol 2., pp 1042–1056

    Google Scholar 

  • Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155(1):70–78

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Gilmore AM et al (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279(22):22866–22874

    Article  PubMed  CAS  Google Scholar 

  • Munekage Y, Hojo M et al (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110(3):361–371

    Article  PubMed  CAS  Google Scholar 

  • Ott T, Clarke J et al (1999) Regulation of the photosynthetic electron transport chain. Planta 209(2):250–258

    Article  PubMed  CAS  Google Scholar 

  • Radmer RJ, Kok B (1976) Photoreduction of O(2) Primes and Replaces CO(2) Assimilation. Plant Physiol 58(3):336–340

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Pascal AA et al (2002) Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting. J Biol Chem 277(10):7785–7789

    Article  PubMed  CAS  Google Scholar 

  • Rutherford AW, Osyczka A et al (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O(2). FEBS Lett 586(5):603–616

    Article  PubMed  CAS  Google Scholar 

  • Sazanov LA, Burrows P et al (1996) Detection and characterization of a complex I-like NADH-specific dehydrogenase from pea thylakoids. Biochem Soc Trans 24(3):739–743

    PubMed  CAS  Google Scholar 

  • Seelert H, Poetsch A et al (2000) Structural biology. Proton-powered turbine of a plant motor. Nature 405(6785):418–419

    Article  PubMed  CAS  Google Scholar 

  • Siefermann D, Yamamoto HY (1975) Properties of NADPH and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts: a transmembrane model for the violaxanthin cycle. Arch Biochem Biophys 171(1):70–77

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Whitelegge JP et al (2001) Ferredoxin:NADP+ oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. J Biol Chem 276(41):38159–38165

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are indebted to Fabrice Rappaport for a critical reading of the manuscript.

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Correspondence to Pierre Joliot.

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Joliot, P., Alric, J. Inhibition of CO2 fixation by iodoacetamide stimulates cyclic electron flow and non-photochemical quenching upon far-red illumination. Photosynth Res 115, 55–63 (2013). https://doi.org/10.1007/s11120-013-9826-1

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