Abstract
It has previously been shown that the long-term treatment of Arabidopsis thaliana with the chloroplast inhibitor lincomycin leads to photosynthetic membranes enriched in antennas, strongly reduced in photosystem II reaction centers (PSII) and with enhanced nonphotochemical quenching (NPQ) (Belgio et al. Biophys J 102:2761–2771, 2012). Here, a similar physiological response was found in the microalga Chromera velia grown under high light (HL). In comparison to cells acclimated to low light, HL cells displayed a severe re-organization of the photosynthetic membrane characterized by (1) a reduction of PSII but similar antenna content; (2) partial uncoupling of antennas from PSII; (3) enhanced NPQ. The decrease in the number of PSII represents a rather unusual acclimation response compared to other phototrophs, where a smaller PSII antenna size is more commonly found under high light. Despite the diminished PSII content, no net damage could be detected on the basis of the Photosynthesis versus irradiance curve and electron transport rates pointing at the excess capacity of PSII. We therefore concluded that the photoinhibition is minimized under high light by a lower PSII content and that cells are protected by NPQ in the antennas.
Similar content being viewed by others
Abbreviations
- NPQ:
-
Nonphotochemical quenching
- PSII:
-
Photosystem II reaction centers
- HL:
-
High light
- LL:
-
Low light
- ΔpH:
-
Trans-thylakoid membrane proton gradient
- F m :
-
Variable fluorescence
- F m :
-
Maximum fluorescence
- P max :
-
Maximal photosynthetic rate or photosynthetic capacity
- TL:
-
Thermoluminescence
- FRRF:
-
Fast repetition rate fluorescence
- ETR:
-
Electron transport rates
- σPSII:
-
Effective antenna size of PSII
- I k :
-
Photosynthetic limiting light
- I sat :
-
Light intensity where photosynthetic saturation starts
- α-DM:
-
n-Dodecyl α-d-maltoside
- DES:
-
De-epoxidation state
References
Anderson J, Osmond B (2001) Sun-shade responses: compromises between acclimation and photoinhibition. Elsevier, Amsterdam
Anderson JM, Chow WS, Goodchild DJ (1988) Thylakoid membrane organization in sun/shade acclimation. Aust J Plant Physiol 15:11–26
Aro EM, McCaffery S, Anderson JM (1993) Photoinhibition and D1 protein—degradation in peas acclimated to different growth irradiances. Plant Physiol 103:835–843
Aro EM et al (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356. doi:10.1093/jxb/eri041
Bailey S, Horton P, Walters RG (2004) Acclimation of Arabidopsis thaliana to the light environment: the relationship between photosynthetic function and chloroplast composition. Planta 218:793–802. doi:10.1007/s00425-003-1158-5
Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958. doi:10.1074/jbc.M606417200
Barber J (1995) Photosynthesis—short-circuiting the Z-Scheme. Nature 376:388–389. doi:10.1038/376388a0
Beer A, Gundermann K, Beckmann J, Büchel C (2006) Subunit composition and pigmentation of fucoxanthin-chlorophyll proteins in diatoms: evidence for a subunit involved in diadinoxanthin and diatoxanthin binding. BioChemistry 45:13046–13053. doi:10.1021/bi061249h
Behrenfeld MJ, Lee H, Small LF (1994) Interactions between nutritional-status and long-term responses to ultraviolet-b radiation stress in a marine diatom. Mar Biol 118:523–530. doi:10.1007/bf00350309
Behrenfeld MJ, Prášil O, Kolber ZS, Babin M, Falkowski PG (1998) Compensatory changes in Photosystem II electron turnover rates protect photosynthesis from photoinhibition. Photosynth Res 58:259–268. doi:10.1023/a:1006138630573
Belgio E, Johnson MP, Juric S, Ruban AV (2012) Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited-state lifetime-both the maximum and the nonphotochemically quenched. Biophys J 102:2761–2771. doi:10.1016/j.bpj.2012.05.004
Belgio E, Ungerer P, Ruban AV (2015) Light-harvesting superstructures of green plant chloroplasts lacking photosystems. Plant Cell Environ 38:2035–2047. doi:10.1111/pce.12528
Belgio E et al (2017) High photochemical trapping efficiency in Photosystem I from the red clade algae Chromera velia and Phaeodactylum tricornutum. Biochim Biophysica Acta 1858:56–63. doi:10.1016/j.bbabio.2016.10.002
Boardman NK (1977) Comparative Photosynthesis of Sun and Shade Plants. Annu Rev Plant Physiol Plant Mol Biol 28:355–377 doi:10.1146/annurev.pp.28.060177.002035
Bonente G, Pippa S, Castellano S, Bassi R, Ballottari M (2012) Acclimation of Chlamydomonas reinhardtii to different growth irradiances. J Biol Chem 287:5833–5847. doi:10.1074/jbc.M111.304279
Bose S, Fork DC (1988) Mechanisms of light state transition in photosynthesis of green plants and red algae. Indian J Biochem Biophys 25:631–635
Büchel C (2003) Fucoxanthin-chlorophyll proteins in diatoms: 18 and 19 kDa subunits assemble into different oligomeric states. BioChemistry 42:13027–13034
Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28:3052–3063. doi:10.1038/emboj.2009.232
Cartaxana P, Domingues N, Cruz S, Jesus B, Laviale M, Serodio J, da Silva JM (2013) Photoinhibition in benthic diatom assemblages under light stress. Aquat Microb Ecol 70:87–92. doi:10.3354/ame01648
Chukhutsina VU, Büchel C, van Amerongen H (2013) Variations in the first steps of photosynthesis for the diatom Cyclotella meneghiniana grown under different light conditions. Biochim Biophys Acta 1827:10–18 doi:10.1016/j.bbabio.2012.09.015
Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophysica Acta 1020:1–24
Demmig-Adams B, Adams WW (1992) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell Environ 15:411–419. doi:10.1111/j.1365-3040.1992.tb00991.x
Dera J, Gordon H (1968) Light field fluctuations in the photic zone. Limnol Oceanogr 13:697–699
Dobáková M, Tichý M, Komenda J (2007) Role of the PsbI protein in photosystem II assembly and repair in the cyanobacterium Synechocystis sp PCC 6803. Plant Physiol 145:1681–1691. doi:10.1104/pp.107.107805
Eilers P, Peeters J (1988) A model for the relationship between light-intensity and the rate of photosynthesis in phytoplancton. Ecol Model 42:199–215
Falkowski PG, Owens TG (1980) Light-shade adaptation—2 strategies in marine-phytoplancton. Plant Physiol 66:592–595. doi:10.1104/pp.66.4.592
Falkowski PG, Raven JA (2007) Aquatic photosynthesis. 2nd edn. Princeton University Press, New Jersey
Falkowski P, Wirick C (1981) A simulation model of the effects of vertical mixing on primary productivity. Mar Biol 62:69–75
Finazzi G, Minagawa J (2014) High light acclimation in green microalgae. In: Demmig-Adams B, Adams WW, Garab G, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration—including bioenergy and related processes, vol 40. Springer Netherlands, Dordrecht
Gardian Z, Tichý J, Vácha F (2011) Structure of PSI, PSII and antennae complexes from yellow-green alga Xanthonema debile. Photosynth Res 108:25–32
Giovagnetti V, Ruban AV (2015) Discerning the effects of photoinhibition and photoprotection on the rate of oxygen evolution in Arabidopsis leaves. J Photochem Photobiol B 152(Part B):272–278 doi:10.1016/j.jphotobiol.2015.09.010
Goss R, Lepetit B, Wilhelm C (2006) Evidence for a rebinding of antheraxanthin to the light-harvesting complex during the epoxidation reaction of the violaxanthin cycle. J Plant Physiol 163:585–590. doi:10.1016/j.jplph.2005.07.009
Grouneva I, Jakob T, Wilhelm C, Goss R (2009) 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 1787:929–938 doi:10.1016/j.bbabio.2009.02.004
Grouneva I, Rokka A, Aro EM (2011) The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J Proteome Res 10:5338–5353. doi:10.1021/pr200600f
Hakala M, Tuominen I, Keranen M, Tyystjarvi T, Tyystjarvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. Biochim Biophys Acta 1706:68–80 doi:10.1016/j.bbabio.2004.09.001
Havelková-Doušová H, Prášil O, Behrenfeld M (2004) Photoacclimation of Dunaliella tertiolecta (Chlorophyceae) under fluctuating irradiance. Photosynthetica 42:273–281
Hogewoning SW, Wientjes E, Douwstra P, Trouwborst G, van Ieperen W, Croce R, Harbinson J (2012) Photosynthetic quantum yield dynamics: from photosystems to leaves. Plant Cell 24:1921–1935. doi:10.1105/tpc.112.097972
Johnson MP, Goral TK, Duffy CD, Brain AP, Mullineaux CW, Ruban AV (2011) Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23:1468–1479. doi:10.1105/tpc.110.081646
Kagawa T et al (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141
Kaňa R, Vass I (2008) Thermoimaging as a tool for studying light-induced heating of leaves Correlation of heat dissipation with the efficiency of photosystem II photochemistry and non-photochemical quenching. Environ Exp Bot 64:90–96. doi:10.1016/j.envexpbot.2008.02.006
Kaňa R, Lazár D, Prášil O, Naus J (2002) Experimental and theoretical studies on the excess capacity of Photosystem II. Photosynth Res 72:271–284. doi:10.1023/a:1019894720789
Kaňa R, Prášil O, Komárek O, Papageorgiou G, Govindjee (2009) Spectral characteristic of fluorescence induction in a model cyanobacterium, Synechococcus sp (PCC 7942). Biochim Biophysica Acta 1787:1170–1178
Kaňa R, Kotabová E, Kopečná J, Trsková E, Belgio E, Sobotka R, Ruban AV (2016) Violaxanthin inhibits nonphotochemical quenching in light-harvesting antennae of Chromera velia. FEBS Lett 590:1076–1085
Kendrick R, Kronenberg G (1994) Photomorphogenesis in plants. 2nd edn. Kluwer Academic Publishers, The Netherlands
Kirk JT (1994) Light and photosynthesis in aquatic ecosystems. 2nd edn. Cambridge Universtity press, Cambridge
Knoppová J, Jianfeng Y, Koník P, Nixon P, Komenda J (2016) CyanoP is involved in the early steps of Photosystem II assembly in the cyanobacterium Synechocystis sp PCC 6803. Plant Cell Physiol 57:1921–1931
Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21:234–244. doi:10.1016/0006-3002(56)90003-8
Kolber Z, Falkowski P (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665
Kolber Z, Prášil O, Falkowski P (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochimica et Biophysica Acta 1367:88–106
Komenda J, Reisinger V, Müller BC, Dobáková M, Granvogl B, Eichacker LA (2004) Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. J Biol Chem 279:48620–48629
Kotabová E, Kaňa R, Jarešová J, Prášil O (2011) Non-photochemical fluorescence quenching in Chromera velia is enabled by fast violaxanthin de-epoxidation. FEBS Lett 585:1941–1945 doi:10.1016/j.febslet.2011.05.015
Kotabová E, Jarešová J, Kaňa R, Sobotka R, Bína D, Prášil O (2014) Novel type of red-shifted chlorophyll alpha antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems. Biochim Biophys Acta 1837:734–743 doi:10.1016/j.bbabio.2014.01.012
Kouřil R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Acta 1817:2–12 doi:10.1016/j.bbabio.2011.05.024
Kouřil R, Wientjes E, Bultema JB, Croce R, Boekema EJ (2013) High-light vs. low-light: effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim Biophys Acta 1827:411–419 doi:10.1016/j.bbabio.2012.12.003
Küpper H, Setlik I, Spiller M, Küpper FC, Prasil O (2002) Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J Phycol 38:429–441. doi:10.1046/j.1529-8817.2002.t01-1-01148.x
Lavaud J, Strzepek RF, Kroth PG (2007) Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol Oceanogr 52:1188–1194
Leong TY, Anderson JM (1984) Adaptation of the thylakoid membranes of pea-chloroplasts to light intensities 0.1. study on the distribution of chlorophyll-protein complexes. Photosynth Res 5:105–115. doi:10.1007/bf00028524
Lepetit B, Volke D, Szabo M, Hoffmann R, Garab GZ, Wilhelm C, Goss R (2007) Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum. BioChemistry 46:9813–9822. doi:10.1021/bi7008344
Lepetit B, Volke D, Gilbert M, Wilhelm C, Goss R (2010) Evidence for the existence of one antenna-associated, lipid-dissolved and two protein-bound pools of diadinoxanthin cycle pigments in diatoms. Plant Physiol 154:1905–1920. doi:10.1104/pp.110.166454
Lichtenthaler HK, Burkard G, Kuhn G, Prenzel U (1981) Light-induced accumulation and stability of chlorophylls and chlorophyll-proteins during chloroplast development in radish seedlings. ZNaturforsch(C) 36:421–430
Mann M, Hoppenz P, Jakob T, Weisheit W, Mittag M, Wilhelm C, Goss R (2014) Unusual features of the high light acclimation of Chromera velia. Photosynth Res. doi:10.1007/s11120-014-0019-3
Moore RB et al (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–963. doi:10.1038/nature06635
Morosinotto T, Bassi R, Frigerio S, Finazzi G, Morris E, Barber J (2006) Biochemical and structural analyses of a higher plant photosystem II supercomplex of a photosystem I-less mutant of barley—consequences of a chronic over-reduction of the plastoquinone pool. Febs J 273:4616–4630. doi:10.1111/j.1742-4658.2006.05465.x
Nixon PJ, Michoux F, Yu JF, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16. doi:10.1093/aob/mcq059
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359 doi:10.1146/annurev.arplant.50.1.333
Oborník M, Vancová M, Lai DH, Janouškovec J, Keeling PJ, Lukeš J (2011) Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of apicomplexa, Chromera velia. Protist 162:115–130. doi:10.1016/j.protis.2010.02.004
Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505–512. doi:10.1046/j.1365-3040.2003.00981.x
Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. BioChemistry 44:8494–8499. doi:10.1021/bi047518q
Pesaresi P et al (2009) Mutants, overexpressors, and interactors of Arabidopsis plastocyanin isoforms: revised roles of plastocyanin in photosynthetic electron flow and thylakoid redox state. Mol Plant 2:236–248 doi:10.1093/mp/ssn041
Porra R, Thompson W, Kriedemann P (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 975:384–394
Powles SB (1984) Photoinhibition of Photosynthesis Induced by Visible-Light. Annu Rev Plant Physiol Plant Mol Biol 35:15–44 doi:10.1146/annurev.pp.35.060184.000311
Prášil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (ed) The Photosystems: structure, function and molecular biology, vol 11. Elsevier, Amsterdam, pp 293–348
Pyke K (2009) Plastid biology. Plastid biology. Cambridge University Press, Cambridge. doi:10.1017/cbo9780511626715
Quigg A et al (2012) Photosynthesis in Chromera velia represents a simple system with high efficiency. PloS ONE 7:e47036. doi:10.1371/journal.pone.0047036
Roach T, Krieger-Liszkay A (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr Protein Pept Sci 15:351–362
Roberty S, Bailleul B, Berne N, Franck F, Cardol P (2014) PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol 204:81–91. doi:10.1111/nph.12903
Ruban A (2013) The photosynthetic membrane. Molecular mechanisms and biophysics of light harvesting. Wiley, United Kingdom
Ruban AV, Murchie EH (2012) Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: A new approach. Biochim Biophys Acta 1817:977–982 doi:10.1016/j.bbabio.2012.03.026
Ruban A et al (2006) Plasticity in the composition of the light harvesting antenna of higher plants preserves structural integrity and biological function. J Biol Chem 281:14981–14990
Ruban AV, Johnson MP, Duffy CD (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181. doi:10.1016/j.bbabio.2011.04.007
Schöttler MA, Tóth SZ (2014) Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control. Front Plant Sci 5. doi:10.3389/fpls.2014.00188
Suggett DJ, Moore MC, Geider RJ (2010) Estimating aquatic productivity from active fluorescence measurement. In: Suggett DJ PO, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 103–127
Terashima I, Miyazawa SI, Hanba YT (2001) Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. J Plant Res 114:93–105. doi:10.1007/pl00013972
Tichý J et al (2013) Light harvesting complexes of Chromera velia, photosynthetic relative of apicomplexan parasites. Biochim Biophys Acta 1827:723–729. doi:10.1016/j.bbabio.2013.02.002
Tikkanen M et al (2006) State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779–793. doi:10.1007/s11103-006-9044-8
Tyystjarvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93:2213–2218. doi:10.1073/pnas.93.5.2213
van Kooten O, Snel J (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150
Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447. doi:10.1093/jxb/eri060
Ware MA, Belgio E, Ruban AV (2015) Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities. Photosynth Res 126:261–274. doi:10.1007/s11120-015-0102-4
Wientjes E, van Amerongen H, Croce R (2013) Quantum yield of charge separation in photosystem II: functional effect of changes in the antenna size upon light acclimation. J Phys Chem B 117:11200–11208. doi:10.1021/jp401663w
Acknowledgements
The authors thank Dr. Martina Bečková and Ms. Lenka Moravcová for excellent technical help with electrophoresis and Dr. E. Lawrenz for useful discussions. This research project was supported by the Institutional project Algatech Plus (MSMT LO1416) from the Czech Ministry of Education, Youth and Sport. The work of E.B. and E.T. was further supported by The Czech Science Foundation GAČR (Grantová agentura České republiky): 16-10088S granted to R.K and 17-02363Y granted to E.B; GAJU 014/2016/P was granted to E.T.
Author information
Authors and Affiliations
Corresponding author
Additional information
Erica Belgio and Eliška Trsková have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Belgio, E., Trsková, E., Kotabová, E. et al. High light acclimation of Chromera velia points to photoprotective NPQ. Photosynth Res 135, 263–274 (2018). https://doi.org/10.1007/s11120-017-0385-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-017-0385-8