The peculiar NPQ regulation in the stramenopile Phaeomonas sp. challenges the xanthophyll cycle dogma

[en] In changing light conditions, photosynthetic organisms develop different strategies to maintain a fine balance between light harvesting, photochemistry, and photoprotection. One of the most widespread photoprotective mechanisms consists in the dissipation of excess light energy in the form of heat in the photosystem II antenna, which participates to the Non Photochemical Quenching (NPQ) of chlorophyll fluorescence. It is tightly related to the reversible epoxidation of xanthophyll pigments, catalyzed by the two enzymes, the violaxanthin deepoxidase and the zeaxanthin epoxidase. In Phaeomonas sp. (Pinguiophyte, Stramenopiles), we show that the regulation of the heat dissipation process is different from that of the green lineage: the NPQ is strictly proportional to the amount of the xanthophyll pigment zeaxanthin and the xanthophyll cycle enzymes are differently regulated. The violaxanthin deepoxidase is already active in the dark, because of a low luminal pH, and the zeaxanthin epoxidase shows a maximal activity under moderate light conditions, being almost inactive in the dark and under high light. This light-dependency mirrors the one of NPQ: Phaeomonas sp. displays a large NPQ in the dark as well as under high light, which recovers under moderate light. Our results pinpoint zeaxanthin epoxidase activity as the prime regulator of NPQ in Phaeomonas sp. and therefore challenge the deepoxidase-regulated xanthophyll cycle dogma. © 2018 Elsevier B.V.

Disciplines :

Biochemistry, biophysics & molecular biology
Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Berne, Nicolas ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues

Fabryova, T.; Genetics and Physiology of microalgae, PhytoSYSTEMS/InBioS, Université de Liège, Liège, Belgium

Istaz, B.; Genetics and Physiology of microalgae, PhytoSYSTEMS/InBioS, Université de Liège, Liège, Belgium

Cardol, Pierre ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues

Bailleul, Benjamin ; Genetics and Physiology of microalgae, PhytoSYSTEMS/InBioS, Université de Liège, Liège, Belgium, UMR7141, Institut de Biologie Physico-Chimique (IBPC), Centre National de la Recherche Scientifique (CNRS), Université Pierre et Marie Curie, 13 rue Pierre et Marie Curie F-75005 Paris, France

Language :

English

Title :

The peculiar NPQ regulation in the stramenopile Phaeomonas sp. challenges the xanthophyll cycle dogma

Publication date :

2018

Journal title :

Biochimica et Biophysica Acta. Bioenergetics

ISSN :

0005-2728

eISSN :

1879-2650

Publisher :

Elsevier B.V.

Volume :

1859

Issue :

Pages :

491-500

Peer reviewed :

Peer Reviewed verified by ORBi

European Projects :

H2020 - 682580 - BEAL - Bioenergetics in microalgae : regulation modes of mitochondrial respiration, photosynthesis, and fermentative pathways, and their interactions in secondary algae

Name of the research project :

FNRS (CDR J.0032, CDR J.0079 and Incentive Grant for Scientific Research F.4520); EU grant agreement no 682580; EU grant agreement no 715579

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique
ERC - European Research Council
UE - Union Europ�enne
CE - Commission Europ�enne

Available on ORBi :

since 16 May 2018

Statistics

Number of views

102 (14 by ULiège)

Number of downloads

10 (9 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Holt, N.E., Fleming, G.R., Niyogi, K.K., Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43 (2004), 8281–8289, 10.1021/bi0494020.
Goss, R., Lepetit, B., Biodiversity of NPQ. J. Plant Physiol. 172 (2015), 13–32, 10.1016/j.jplph.2014.03.004.
Hagar, A., Stransky, H., The carotenoid pattern and occurrence of the light induced xanthophyll cycle in various classes of algae. V. A few members of the Cryptophyceae, Euglenophyceae, Bacillariophyceae, Chrysophyceae and Phaeophyceae. Arch. Mikrobiol. 73 (1970), 77–89 http://www.ncbi.nlm.nih.gov/pubmed/5484315 (accessed March 31, 2017).
Holt, N.E., Zigmantas, D., Valkunas, L., Li, X.-P., Niyogi, K.K., Fleming, G.R., Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307 (2005), 433–436 (New York, N.Y.) https://doi.org/10.1126/science.1105833.
Ruban, A.V., Berera, R., Ilioaia, C., van Stokkum, I.H.M., Kennis, J.T.M., Pascal, A.A., van Amerongen, H., Robert, B., Horton, P., van Grondelle, R., Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450 (2007), 575–578, 10.1038/nature06262.
Ahn, T.K., Avenson, T.J., Ballottari, M., Cheng, Y.-C., Niyogi, K.K., Bassi, R., Fleming, G.R., Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320 (2008), 794–797, 10.1126/science.1154800.
Horton, P., Johnson, M.P., Perez-Bueno, M.L., Kiss, A.Z., Ruban, A.V., Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states?. FEBS J. 275 (2008), 1069–1079, 10.1111/j.1742-4658.2008.06263.x.
Müller, M.G., Lambrev, P., Reus, M., Wientjes, E., Croce, R., Holzwarth, A.R., Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. ChemPhysChem 11 (2010), 1289–1296, 10.1002/cphc.200900852.
Chmeliov, J., Bricker, W.P., Lo, C., Jouin, E., Valkūnas, L., Ruban, A.V., Duffy, C.D.P.P., An “all pigment” model of excitation quenching in LHCII. Phys. Chem. Chem. Phys. 17 (2015), 15857–15867, 10.1039/C5CP01905B.
Olaizola, M., La Roche, J., Kolber, Z., Falkowski, P.G., Non-photochemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom. Photosynth. Res. 41 (1994), 357–370, 10.1007/BF00019413.
Pfundel, E.E., Renganathan, M., Gilmore, A.M., Yamamoto, H.Y., Dilley, R.A., Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin deepoxidation. Plant Physiol. 106 (1994), 1647–1658, 10.1104/pp.106.4.1647.
Goss, R., Garab, G., Non-photochemical chlorophyll fluorescence quenching and structural rearrangements induced by low pH in intact cells of Chlorella fusca (Chlorophyceae) and Mantoniella squamata (Prasinophyceae). Photosynth. Res. 67 (2001), 185–197, 10.1023/A:1010681511105.
Reinhold, C., Niczyporuk, S., Beran, K.C., Jahns, P., Short-term down-regulation of zeaxanthin epoxidation in Arabidopsis thaliana in response to photo-oxidative stress conditions. Biochim. Biophys. Acta Bioenerg. 1777 (2008), 462–469, 10.1016/j.bbabio.2008.03.002.
Li, X.-P., Björkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S., Niyogi, K.K., A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403 (2000), 391–395, 10.1038/35000131.
Tibiletti, T., Auroy, P., Peltier, G., Caffarri, S., Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light. Plant Physiol. 171 (2016), 2717–2730, 10.1104/pp.16.00572.
Peers, G., Truong, T.B., Ostendorf, E., Busch, A., Elrad, D., Grossman, A.R., Hippler, M., Niyogi, K.K., An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462 (2009), 518–521, 10.1038/nature08587.
Bailleul, B., Rogato, A., de Martino, A., Coesel, S., Cardol, P., Bowler, C., Falciatore, A., Finazzi, G., An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light. Proc. Natl. Acad. Sci. 107 (2010), 18214–18219, 10.1073/pnas.1007703107.
Ballottari, M., Truong, T.B., Re De, E., Erickson, E., Stella, G.R., Fleming, G.R., Bassi, R., Niyogi, K.K., Identification of pH-sensing sites in the light harvesting complex stress-related 3 protein essential for triggering non-photochemical quenching in Chlamydomonas reinhardtii. J. Biol. Chem. 291 (2016), 7334–7346, 10.1074/jbc.M115.704601.
Lavaud, J., Rousseau, B., van Gorkom, H.J., Etienne, A.-L., Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum 1. Plant Physiol. 129 (2002), 1398–1406, 10.1104/pp.002014.dissipation.
Honda, D., Inouye, I., Ultrastructure and taxonomy of a marine photosynthetic stramenopile Phaeomonas parva gen. et sp. nov. (Pinguiophyceae) with emphasis on the flagellar apparatus architecture. Phycol. Res. 50 (2002), 75–89, 10.1046/j.1440-1835.2002.00258.x.
Kawachi, M., Inouye, I., Honda, D., O'Kelly, C.J., Bailey, J.C., Bidigare, R.R., Andersen, R.A., The Pinguiophyceae classis nova, a new class of photosynthetic stramenopiles whose members produce large amounts of omega-3 fatty acids. Phycol. Res. 50 (2002), 31–47, 10.1046/j.1440-1835.2002.00260.x.
Guillard, R.R.L., Culture of phytoplankton for feeding marine invertebrates. In Smith, W.L., Chanley, M.H., (eds.) Culture of Marine Invertebrate Animals, 1975, Plenum Press, New York, USA, 29–60, 10.1007/978-1-4615-8714-9_3.
Bailleul, B., Berne, N., Murik, O., Petroutsos, D., Prihoda, J., Tanaka, A., Villanova, V., Bligny, R., Flori, S., Falconet, D., Krieger-Liszkay, A., Santabarbara, S., Rappaport, F., Joliot, P., Tirichine, L., Falkowski, P.G., Cardol, P., Bowler, C., Finazzi, G., Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524 (2015), 366–369, 10.1038/nature14599.
Johnson, X., Vandystadt, G., Bujaldon, S., Wollman, F.A., Dubois, R., Roussel, P., Alric, J., Béal, D., A new setup for in vivo fluorescence imaging of photosynthetic activity. Photosynth. Res. 102 (2009), 1–9, 10.1007/s11120-009-9487-2.
Genty, B., Briantais, J.M., Baker, N.R., The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta Gen. Subj. 990 (1989), 87–92, 10.1016/S0304-4165(89)80016-9.
Platt, T., Gallegos, C.L., Harrison, W.G., Photoinibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38 (1980), 687–701 (doi:citeulike-article-id:3354339, USA).
Kauny, J., Sétif, P., NADPH fluorescence in the cyanobacterium Synechocystis sp. PCC 6803: a versatile probe for in vivo measurements of rates, yields and pools. Biochim. Biophys. Acta Biomembr. Bioenergetics 1837 (2014), 792–801, 10.1016/J.BBABIO.2014.01.009.
Giovagnetti, V., Cataldo, M.L., Conversano, F., Brunet, C., Functional relation between growth, photosynthetic rate and regulation in the coastal picoeukaryote Phaeomonas sp. RCC 503 (Pinguiophyceae, Stramenopiles). J. Plankton Res. 32 (2010), 1501–1511, 10.1093/plankt/fbq074.
Jakob, T., Goss, R., Wilhelm, C., Unusual pH-dependence of diadinoxanthin de-epoxidase activation causes chlororespiratory induced accumulation of diatoxanthin in the diatom Phaeodactylum tricornutum. J. Plant Physiol. 158 (2001), 383–390, 10.1078/0176-1617-00288.
Cruz, J.A., Sacksteder, C.A., Kanazawa, A., Kramer, D.M., Contribution of electric field (Delta psi) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Delta psi and Delta pH by ionic strength. Biochemistry 40 (2001), 1226–1237, 10.1021/bi0018741.
Diner, B., Joliot, P., Effect of the transmembrane electric field on the photochemical and quenching properties of photosystem II in vivo. BBA-Bioenergetics 423 (1976), 479–498, 10.1016/0005-2728(76)90202-4.
Rappaport, F., Finazzi, G., Pierre, Y., Bennoun, P., A new electrochemical gradient generator in thylakoid membranes of green algae. Biochemistry 38 (1999), 2040–2047, 10.1021/bi982351k.
Witt, H.T., Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field. Biochim. Biophys. Acta Rev. Bioenergetics 505 (1979), 355–427, 10.1016/0304-4173(79)90008-9.
Harned, R.L., Hidy, P.H., Corum, C.J., Jones, K.L., Nigericin a new crystalline antibiotic from an unidentified Streptomyces. Antibiot. Chemother. 1 (1951), 594–596 (Northfield, Ill.) http://www.ncbi.nlm.nih.gov/pubmed/24541690. (Accessed 31 March 2017)
Graven, S.N., Estrada-O, S., Lardy, H.A., Alkali metal cation release and respiratory inhibition induced by nigericin in rat liver mitochondria. Proc. Natl. Acad. Sci. U. S. A. 56 (1966), 654–658, 10.1073/pnas.56.2.654.
Wollman, F.A., State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J. 20 (2001), 3623–3630, 10.1093/emboj/20.14.3623.
Briantais, J.M., Vernotte, C., Picaud, M., Krause, G.H., A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. BBA-Bioenergetics 548 (1979), 128–138, 10.1016/0005-2728(79)90193-2.
Demmig-Adams, B., Adams, W.W., The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci. 1 (1996), 21–26, 10.1016/S1360-1385(96)80019-7.
Maxwell, K., Johnson, G.N., Chlorophyll fluorescence—a practical guide. J. Exp. Bot. 51 (2000), 659–668, 10.1093/jxb/51.345.659.
Nilkens, M., Kress, E., Lambrev, P., Miloslavina, Y., Müller, M., Holzwarth, A.R., Jahns, P., Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim. Biophys. Acta Bioenerg. 1797 (2010), 466–475, 10.1016/j.bbabio.2010.01.001.
Demmig-Adams, B., Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. BBA-Bioenergetics 1020 (1990), 1–24, 10.1016/0005-2728(90)90088-L.
Barnett, A., Méléder, V., Blommaert, L., Lepetit, B., Gaudin, P., Vyverman, W., Sabbe, K., Dupuy, C., Lavaud, J., Growth form defines physiological photoprotective capacity in intertidal benthic diatoms. ISME J. 9 (2015), 32–45, 10.1038/ismej.2014.105.
Lepetit, B., Volke, D., Gilbert, M., Wilhelm, C., Goss, R., Evidence for the existence of one antenna-associated, lipid-dissolved and two protein-bound pools of diadinoxanthin cycle pigments in diatoms. Plant Physiol. 154 (2010), 1905–1920, 10.1104/pp.110.166454.
Goss, R., Lepetit, B., Wilhelm, C., Evidence for a rebinding of antheraxanthin to the light-harvesting complex during the epoxidation reaction of the violaxanthin cycle. J. Plant Physiol. 163 (2006), 585–590, 10.1016/j.jplph.2005.07.009.
Jakob, T., Goss, R., Wilhelm, C., Activation of diadinoxanthin de-epoxidase due to a chiororespiratory proton gradient in the dark in the diatom Phaeodactylum tricornutum. Plant Biol. 1 (1999), 76–82, 10.1111/j.1438-8677.1999.tb00711.x.
Grouneva, I., Jakob, T., Wilhelm, C., Goss, R., The regulation of xanthophyll cycle activity and of non-photochemical fluorescence quenching by two alternative electron flows in the diatoms Phaeodactylum tricornutum and Cyclotella meneghiniana. Biochim. Biophys. Acta 1787 (2009), 929–938, 10.1016/j.bbabio.2009.02.004.
Goss, R., Ann Pinto, E., Wilhelm, C., Richter, M., The importance of a highly active and DeltapH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J. Plant Physiol. 163 (2006), 1008–1021, 10.1016/j.jplph.2005.09.008.
Takahashi, H., Watanabe, A., Tanaka, A., Hashida, S.N., Kawai-Yamada, M., Sonoike, K., Uchimiya, H., Chloroplast NAD kinase is essential for energy transduction through the xanthophyll cycle in photosynthesis. Plant Cell Physiol. 47 (2006), 1678–1682, 10.1093/pcp/pcl029.
Da, Q., Wang, P., Wang, M., Sun, T., Jin, H., Liu, B., Wang, J., Grimm, B., Wang, H.-B., Thioredoxin and NADPH-dependent thioredoxin reductase C regulation of tetrapyrrole biosynthesis. Plant Physiol. 175 (2017), 652–666, 10.1104/pp.16.01500.
Eberhard, S., Finazzi, G., Wollman, F.-A., The dynamics of photosynthesis. Annu. Rev. Genet. 42 (2008), 463–515, 10.1146/annurev.genet.42.110807.091452.
Kalituho, L., Beran, K.C., Jahns, P., The Transiently Generated Nonphotochemical Quenching of Excitation Energy in Arabidopsis Leaves Is Modulated by Zeaxanthin. Plant Physiol. 143 (2007), 1861–1870, 10.1104/pp.106.095562.
Grouneva, I., Jakob, T., Wilhelm, C., Goss, R., A new multicomponent NPQ mechanism in the diatom Cyclotella meneghiniana. Plant Cell Physiol. 49 (2008), 1217–1225, 10.1093/pcp/pcn097.
Cardol, P., De Paepe, R., Franck, F., Forti, G., Finazzi, G., The onset of NPQ and ΔμH+ upon illumination of tobacco plants studied through the influence of mitochondrial electron transport. Biochim. Biophys. Acta Biomembr. Bioenergetics 1797 (2010), 177–188, 10.1016/j.bbabio.2009.10.002.