Abstract
Light is crucial for photosynthesis, but the amount of light that exceeds an organism’s assimilation efficacy can lead to photo-oxidative damage and even cell death. In Chlamydomonas (C). reinhardtii cyclic electron flow (CEF) is very important for the elicitation of non-photochemical quenching (NPQ) by controlling the acidification of thylakoid lumen. This process requires the cooperation of proton gradient regulation (PGR) proteins, PGRL1 and PGR5. Here, we compared the growth pattern and photosynthetic activity between wild type (137c, t222+) and mutants impaired in CEF (pgrl1 and pgr5) under photoautotrophic and photoheterotrophic conditions. We have observed the discriminative expression of NPQ in the mutants impaired in CEF of pgrl1 and pgr5. The results obtained from the mutants showed reduced cell growth and density, Chl a/b ratio, fluorescence, electron transport rate, and yield of photosystem (PS)II. These mutants have reduced capability to develop a strong NPQ indicating that the role of CEF is very crucial for photoprotection. Moreover, the CEF mutant exhibits increased photosensitivity compared with the wild type. Therefore, we suggest that besides NPQ, the fraction of non-regulated non-photochemical energy loss (NO) also plays a crucial role during high light acclimation despite a low growth rate. This low NPQ rate may be due to less influx of protons coming from the CEF in cases of pgrl1 and pgr5 mutants. These results are discussed in terms of the relative photoprotective benefit, related to the thermal dissipation of excess light in photoautotrophic and photoheterotrophic conditions.
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Allorent G, Tokutsu R, Roach T, Peers G, Cardol P, Girard-Bascou J, Seigneurin-Berny D, Petroutsos D, Kuntz M, Breyton C, Franck F, Wollman F-A, Krishna Niyogi K, Krieger-Liszkay A, Minagawa J, Finazzi G (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25:545–557
Alric J (2010) Cyclic electron flow around photosystem I in unicellular green algae. Photosynth Res 106(1):47–56
DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132(2):273–285
Dang K, Plet J, Tolleter D et al (2014) Combined increases in mitochondrial cooperation and oxygen photoreduction compensate for deficiency in cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 26:3036–3050
Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photo-protection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim Biophys Acta 1847:468–485
Erickson E, Wakao S, Niyogi KK (2015) Light stress and photoprotection in Chlamydomonas reinhardtii. Plant J 82:449–465
Fischer BB, Wiesendanger M, Eggen RIL (2006) Growth condition-dependent sensitivity, photodamage and stress response of Chlamydomonas reinhardtii exposed to high light conditions. Plant Cell Physiol 47(8):1135–1145
Heifetz PB, Förster B, Osmond CB, Giles LJ, Boynton JE (2000) Effects of acetate on facultative autotrophy in Chlamydomonas reinhardtii assessed by photosynthetic measurements and stable isotope analyses. Plant Physiol 122(4):1439–1445
Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M, Armbruster U, Leister D (2013) PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol Cell 49(3):511–523
Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophy Acta 1787:3–14
Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389
Johnson X, Steinbeck J, Dent RM, Takahashi H, Richaud P, Ozawa SI, Houille-Vernes L, Petroutsos D, Rappaport F, Grossman AR, Niyogi KK, Hippler M, Alric J (2014) Proton gradient regulation 5-mediated cyclic electron flow under ATP or redox-limited conditions: a study of ΔATPase pgr5and ΔrbcL pgr5; mutants in the green alga Chlamydomonas reinhardtii. Plant Physiol 165(1):438
Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, Goltsev V, Guidi L, Jajoo A, Li P, Losciale P, Mishra VK, Misra AN, Nebauer SG, Pancaldi S, Penella C, Pollastrini M, Suresh K, Tambussi E, Yanniccari M, Zivcak M, Cetner MD, Samborska IA, Stirbet A, Olsovska K, Kunderlikova K, Shelonzek H, Rusinowski S, Baba W (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res 132:13–66
Klughammer C, Schreiber U (1994) Saturation pulse method for assessment of energy conversion in PS I. Planta 192:261–268
Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Appl Notes 1:201–247
Kodru S, Malavath T, Devadasu E, Nellaepalli S, Stirbet A, Subramanyam R (2015) The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynth Res 125:219–231
Kramer DM, Avenson TJ, Edwards GE (2004a) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9(7):349–357
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004b) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218
Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346
Lichtenthaler HL (1987) Chlorophyll and carotenoids: pigments of photosynthetic bio membranes. Method Enzymol 148:350–382
Miyachi S, Iwasaki I, Shiraiwa Y (2003) Historical perspective on microalgal and cyanobacterial acclimation to low and extremely high CO2 conditions. Photosynth Res 77(2–3):139–153
Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110(3):361–371
Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429(6991):579–582
Nama S, Madireddi SK, Yadav RM, Subramanyam R (2019) Non-photochemical quenching dependent acclimation and thylakoid organization of Chlamydomonas reinhardtii to high light stress. Photosynth Res 139:387–400
Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis. Curr Opin Plant Biol 5(3):193–198
Papageorgiou G (1975) Chlorophyll fluorescence an intrinsic probe of photosynthesis. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, New York, pp 320–366
Peltier G, Tolleter D, Billon E, Cournac L (2010) Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth Res 106(1–2):19–31
Petroutsos D, Terauchi AM, Busch A, Hirschmann I, Merchant SS, Finazzi G, Hippler M (2009) PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J Biol Chem 284(47):32770–32781
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectrometry. Biochim Biophys Acta 975:384–439
Schreiber U (1986) Detection of rapid induction kinetics with a new type of high-frequency modulated chlorophyll fluorometer. Photosynth Res 9:261–271
Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotech 26:25–30
Stirbet A, Riznichenko G, Rubin AB (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry (Moscow) 79:291–323
Strasser RJ, Srivastava A (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42
Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism regulation and adaptation. Taylor and Francis, London, pp 443–480
Sueoka N (1960a) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 46:83–91
Sueoka N (1960b) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardi. Proc Natl Acad Sci USA 46:83–91
Terao T, Yamashita A, Katoh S (1985) Chlorophyll b-deficient mutants of rice. Absorption and fluorescence spectra and chlorophyll a/b ratios. Plant Cell Physiol 26:1361–1367
Terashima I, Hikosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant Cell Environ 18(10):1111–1128
Tolleter D, Ghysels B, Alric J, Petroutsos D, Tolstygina I, Krawietz D, Happe T, Auroy P, Adriano J-M, Beyly A, Cuiné S, Plet J, Reiter IM, Genty B, Cournac L, Hippler M, Peltier G (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23(7):2619–2630
Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193
Triantaphylides C, Havaux M (2009) Singlet oxygen in plants: production detoxification and signaling. Trends Plant Sci 14:219–228
Triantaphylides C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148:960–968
Zhao X, Chen T, Feng B, Zhang C, Peng S, Zhang X, Fu G, Tao L (2017) Non-photochemical quenching plays a key role in light acclimation of rice plants differing in leaf color. Front Plant Sci 7:1968
Zivcak M, Brestic M, Kalaji HM (2014) Photosynthetic responses of sun and shadegrown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light. Photosynth Res 119:339–354
Acknowledgements
R.S was supported by the Department of Biotechnology (Grant No. BT/PR14964/BPA/118/137/2015), Council of Scientific and Industrial Research (Grant No. 38 (1381)/14/EMR-II) and UGC-ISF Research Grant - File No. 6-8/2018 (IC), DST-FIST and UGC-SAP, Govt. of India, for financial support. We thank Gilles Peltier, CEA – CNRS - Aix Marseille Université, France, and Michael Hippler, Institute of Plant Biotechnology, University of Münster, Germany,
Biology, for proving the mutants of pgrl1 and pgr5.
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Yadav, R.M., Aslam, S.M., Madireddi, S.K. et al. Role of cyclic electron transport mutations pgrl1 and pgr5 in acclimation process to high light in Chlamydomonas reinhardtii. Photosynth Res 146, 247–258 (2020). https://doi.org/10.1007/s11120-020-00751-w
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DOI: https://doi.org/10.1007/s11120-020-00751-w