Interplay between non-photochemical plastoquinone reduction and re-oxidation in pre-illuminated Chlamydomonas reinhardtii: a chlorophyll fluorescence study
Interplay between non-photochemical plastoquinone reduction and re-oxidation in pre-illuminated Chlamydomonas reinhardtii- a chlorophyll fluorescence study.pdf
[en] In photosynthetic eukaryotes, the redox state of the plastoquinone (PQ) pool is an important sensor for mechanisms that regulate the photosynthetic electron transport. In higher plants, a multimeric nicotinamide adenine dinucleotide (phosphate) (NAD(P))H dehydroge- nase (NDH) complex and a plastid terminal oxidase (PTOX) are involved in PQ redox homeostasis in the dark. We recently demonstrated that in the microalgae Chla- mydomonas reinhardtii, which lacks the multimeric NDH complex of higher plants, non-photochemical PQ reduction is mediated by a monomeric type-II NDH (Nda2). In this study, we further explore the nature and the importance of non-photochemical PQ reduction and oxidation in relation to redox homeostasis in this alga by recording the ‘dark’ chlorophyll fluorescence transients of pre-illuminated algal samples. From the observation that this fluorescence tran- sient is modified by addition of propyl gallate, a known inhibitor of PTOX, and in a Nda2-deficient strain we conclude that it reflects post-illumination changes in the redox state of PQ resulting from simultaneous PTOX and Nda2 activity. We show that the post-illumination fluo- rescence transient can be used to monitor changes in the relative rates of the non-photochemical PQ reduction and reoxidation in response to different physiological situa- tions. We study this fluorescence transient in algae acclimated to high light and in a mutant deficient in mitochondrial respiration. Some of our observations indi- cate that the chlororespiratory pathway participates in redox homeostasis in C. reinhardtii.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Houyoux, Pierre-Alain
Ghysels, Bart ; Université de Liège - ULiège > Labo de Bioénergétique
Lecler, Renaud ; Université de Liège - ULiège > Labo de Bioénergétique
Franck, Fabrice ; Université de Liège - ULiège > Labo de Bioénergétique
Language :
English
Title :
Interplay between non-photochemical plastoquinone reduction and re-oxidation in pre-illuminated Chlamydomonas reinhardtii: a chlorophyll fluorescence study
Aluru MR, Stessman DJ, Spalding MH, Rodermel SR (2007) Alterations in photosynthesis in Arabidopsis lacking IMMU-TANS, a chloroplast terminal oxidase. Photosynth Res 91:11-23 (Pubitemid 46466314)
Anderson B, Anderson JM (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta 593:427-440
Asada K, Heber U, Schreiber U (1992) Pool size of electrons that can be donated to P700+, as determined in intact leaves: donation to P700+ from stromal components via the intersystem chain. Plant Cell Physiol 33:927-932
Atteia A, van Lis R, van Hellemond JJ, Tielens AG, Martin W, Henze K (2004) Identification of prokaryotic homologues indicates an endosymbiotic origin for the alternative oxidases of mitochondria (AOX) and chloroplasts (PTOX). Gene 330:143-148 (Pubitemid 38490427)
Badger MR, von Caemmerrer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Phil Trans R Soc Lond B 355:1433-1446
Baurain D, Dinant M, Coosemans N, Matagne RF (2003) Regulation of the alternative oxidase Aoxl gene in Chlamydomonas reinhardtii. Role of nitrogen source on the expression of a reporter gene under the control of the Aox1 promoter. Plant Physiol 131:1418-1430 (Pubitemid 36400372)
Bennoun P (1982) Evidence for a chlororespiratory chain in the chloroplast. Proc Natl Acad Sci USA 79:4352-4356
Bennoun P (1994) Chlororespiration revisited: mitochondrial-plastid interactions in Chlamydomonas. Biochim Biophys Acta 1186:59-66 (Pubitemid 24213674)
Bennoun P (1998) Chlororespiration, sixteen years later. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht
Bukhov N, Carpentier R (2004) Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynth Res 82:17-33 (Pubitemid 39217830)
Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analyses of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868-876 (Pubitemid 28077641)
Cardol P, Gloire G, Havaux M, Remacle C, Matagne RF, Franck F (2003) Photosynthesis and state transition in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. Plant Physiol 133:2010-2020 (Pubitemid 38047327)
Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G, Kuntz M (1999) Mutations in the Arabidopsis gene immutans cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57-68
Cournac L, Guedeney G, Joët T, Rumeau D, Latouche G, Cerovic Z, Redding K, Horvath EM, Medgyesy P, Peltier G (1998) Nonphotochemical reduction of intersystem electron carriers in chloroplasts of higher plants and algae. In: Garab G (ed) Photosynthesis: mechanism and effects. Kluwer Academic Publishers, Dordrecht, pp 1877-1882
Cournac L, Josse EV, Joët T, Rumeau D, Redding K, Kuntz M, Peltier G (2000a) Flexibility in photosynthetic electron transport: a newly identified chloroplast oxidase involved in chlororespiration. Phil Trans R Soc Lond B 355:1447-1454
Cournac L, Redding K, Ravenel J, Rumeau D, Josse EM, Kuntz M, Peltier G (2000b) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem 275:17256-17262 (Pubitemid 30430757)
Cournac L, Latouche G, Cerovic Z, Redding K, Ravenel J, Peltier G (2002) In vivo interactions between photosynthesis, mitorespiration, and chlororespiration in Chlamydomonas reinhardtii. Plant Physiol 129:1921-1928 (Pubitemid 34923257)
Finazzi G, Forti G (2004) Metabolic flexibility of the green alga Chlamydomonas reinhardtii as revealed by the link between state transitions and cyclic electron flow. Photosynth Res 82:327-338 (Pubitemid 40032965)
Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transition, cyclic and linear transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117-129 (Pubitemid 29507551)
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 J 31:280-285 (Pubitemid 34269523)
Finazzi G, Johnson GN, Dall'Osto L, Zito F, Bonente G, Bassi R, Wollman FA (2006) Nonphotochemical quenching of chlorophyll fluorescence in Chlamydomonas reinhardtii. Biochemistry 7:1790-1798
Forti G, Furia A, Bombelli P, Finazzi G (2003) In vivo changes of the oxidation-reduction state of NADP and of the ATP/ADP cellular ratio linked to the photosynthetic activity in Chlamydomonas reinhardtii. Plant Physiol 132:1464-1474 (Pubitemid 36872895)
Franck F, Houyoux PA (2008) The Mehler reaction in Chlamydomonas reinhardtii: efficiency during photosynthetic induction and steady-state photosynthesis in wild-type and in a mitochondrial mutant shifted to energy distribution state 2. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the Sun. Proceedings of the 14th international Congress on photosynthesis. Springer, Heidelberg
Gorman DS, Levine RP (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 54:1665-1669
Groom QJ, Kramer DM, Crofts AR, Ort DR (1993) The nonphotochemical reduction of plastoquinone in leaves. Photosynth Res 36:205-215
Guedeney G, Corneille S, Cuine S, Peltier G (1996) Evidence for an association of ndh B, ndh J gene products and ferredoxin-NADP-reductase as components of a chloroplastic NAD (P) H dehydrogenase complex. FEBS Lett 378:277-280 (Pubitemid 26023466)
Harris HE (1989) The Chlamydomonas sourcebook. Academic Press, San Diego
Heber U, Walker DA (1992) Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiol 100:1621-1626
Jans F, Mignolet E, Houyoux P-A, Cardol P, Cuiné S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type-II NAD (P) H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci USA 105:20546-20551
Joët T, Cournac L, Horvath EM, Megdyesy P, Peltier G (2001) Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADPH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol 125:1919-1929 (Pubitemid 32375774)
Joët T, Genty B, Josse EM, Kuntz M, Cournac L, Peltier G (2002) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J Biol Chem 277:31623-31630 (Pubitemid 34968965)
Johnson GN (2005) Cyclic electron transport in C3 plants: fact or artefact? J Exp Bot 56:407-416 (Pubitemid 40263288)
Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99:10209-10214 (Pubitemid 34831197)
Josse E, Alcaraz J, Laboure A, Kuntz M (2003) In vitro characterization of a plastid terminal oxidase (PTOX). Eur J Biochem 270:3787-3794 (Pubitemid 37123250)
Kofer W, Koop HU, Wanner G, Steinmuller K (1998) Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD (P) H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation. Mol Gen Genet 258:166-173
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350-382
Matagne RF, Remacle C (2002) The genetics and molecular biology of mitochondria in Chlamydomonas. Recent Res Dev Plant Biol 2:15-32
Mathy G, Cardol P, Dinant M, Blomme A, Guérin S, Cloes M, Ghysels B, De Pauw E, Leprince P, Remacle C, Sluse-Goffart C, Franck F, Matagne RF, Sluse FE (2010) Proteomic and functional characterization of a Chlamydomonas reinhardtii mutant lacking the mitochondrial alternative oxidase 1. J Proteome Res 9:2825-2838
Matsumura H, Miyashi S (1983) Cycling assay for nicotinamide adenine dinucleotides. Methods Enzymol 69:465-470
Moseley JL, Chang CW, Grossman AR (2006) Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot Cell 5:26-44 (Pubitemid 43113449)
Mus F, Cournac L, Cardettini V, Caruana A, Peltier G (2005) Inhibitor studies on non-photochemical plastoquinone reduction and H2 photoproduction in Chlamydomonas reinhardtii. Biochim Biophys Acta 1078:322-332 (Pubitemid 40943596)
Niyogi KK, Bjorkman O, Grossman AR (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9:1369-1380 (Pubitemid 28174115)
Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518-521
Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523-550 (Pubitemid 36257506)
Peltier G, Ravenel J, Vermeglio A (1987) Inhibition of a respiratory activity by short saturating flashes in Chlamydomonas: evidence for a chlororespiration. Biochim Biophys Acta 893:83-90
Ravenel J, Peltier G, Havaux M (1994) The cyclic electron pathways around photosystem-I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta 193:251-259 (Pubitemid 2053682)
Rebeille F, Gans P (1988) Interaction between chloroplasts and mitochondria in microalgae. Plant Physiol 88:973-975
Remacle C, Baurain D, Cardol P, Matagne RF (2001) Mutants of Chlamydomonas reinhardtii deficient in mitochondrial complex I: characterization of two mutations affecting the nd1 coding sequence. Genetics 158:1051-1060 (Pubitemid 32667091)
Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L, Geisler M, Stewart G, Krol M, Hurru V, Rodermel SR, Maxwell DP, Hüner N P A (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol 142:574-585 (Pubitemid 44583128)
Sazanov LA, Burrows PA, Nixon PJ (1998) The plastid ndh genes code an NADH-specific dehydrogenase: isolation of a complex I analogue from pea thylakoid membranes. Proc Natl Acad Sci USA 95:1319-1324 (Pubitemid 28124956)
Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95:9705-9709 (Pubitemid 28506296)
Vallon O, Bulté L, Dainese P, Olive J, Bassi R, Wollman FA (1991) Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc Natl Acad Sci USA 88:8262-8266 (Pubitemid 21915337)
Willeford KO, Gombos Z, Gibbs M (1989) Evidence for chloroplastic succinate dehydrogenase participating in the chloroplastic respiratory and photosynthetic electron transport chains of Chlamydomonas reinhardtii. Plant Physiol 90:1084-1087
Wu DY, Wright DA, Wetzel C, Voytas DF, Rodermel S (1999) The immutans variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11:43-55
