Summary
All oxygenic photosynthetic organisms have mechanisms for regulation of light-harvesting efficiency in response to variable light intensity. Non-photochemical quenching of chlorophyll fluorescence (NPQ) is a marker for the rapid dissipation of excess excitation energy as heat, activated in order to prevent formation of reactive oxygen species. Although widespread among oxygenic photosynthetic organisms, NPQ is activated through distinct molecular effectors depending on taxa. In unicellular green algae as well as other algal groups (such as diatoms), NPQ activity depends on a light-harvesting complex (LHC)-like protein, called light-harvesting-complex stress-related (LHCSR). In land plants, such as Arabidopsis thaliana, NPQ instead relies on a different LHC-like protein: PsbS. This protein responds to low lumenal pH via protonation of two glutamate residues essential for activity. PsbS induces a reorganization of thylakoid membrane complexes upon lumen acidification, which is indispensable for the generation of the dissipative state. Upon reorganization, two distinct quenching components are generated: one is tightly connected to the photosystem II (PS II) reaction center and the other is located in a domain of the PS II antenna system, disconnected from the reaction center. Low lumenal pH also induces activation of the violaxanthin (V) de-epoxidase enzyme, leading to the synthesis of zeaxanthin (Z), which, in turn, up-regulates heat dissipation/NPQ upon binding to antenna proteins. PsbS-dependent NPQ is present in land plants and in the moss Physcomitrella patens. Although the PsbS gene sequence is conserved in all green algae whose genome has been sequenced thus far, the corresponding protein was not found to be accumulated in algal cells under any of many growth conditions explored, suggesting it may be a pseudogene. PsbS and LHCSR play a similar role in activating protective heat dissipation of excess light by responding to low lumenal pH. In contrast to PsbS, LHCSR exhibits a clear capacity for binding xanthophylls and chlorophylls. Thus LHCSR appears to combine the pH-responsive activity typical of PsbS with the capacity for binding pigments, chlorophylls and carotenoids, as a basis for engagement of energy dissipation reflected in NPQ. LHCSR appears to directly participate in energy dissipation possibly avoiding the need for reorganization of thylakoid complexes.
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Abbreviations
- C2S2:
-
Photosystem II supercomplex composed of 2 core complexes and 2 LHCII trimers
- Car:
-
Carotenoid
- C-B:
-
Calvin-Benson
- Chl:
-
Chlorophyll
- Fm :
-
(Fm′) maximal fluorescence in dark- (or light - respectively) adapted cells
- KO:
-
Knock-out
- Lhca (Lhcb):
-
Light harvesting complex of photosystem I (or II respectively)
- LhcbM:
-
Polypeptide of the major light-harvesting complex of photosystem II
- LHCI:
-
Light-harvesting complex protein of photosystem I
- LHCII:
-
Major light-harvesting complex of photosystem II
- LHCSR:
-
Stress-related light-harvesting complex
- NPQ:
-
Non-photochemical quenching of chlorophyll fluorescence
- OCP:
-
Orange carotenoid-binding protein
- Pi:
-
Inorganic phosphate
- PS I (II):
-
photosystem I (II)
- PsbS:
-
Photosystem II subunit S
- qE, qZ:
-
qI – energy-dependent quenching, zeaxanthin-related quenching, “photoinhibitory” quenching
- RC:
-
Reaction Center
- ROS:
-
Reactive oxygen species
- TP:
-
Triose phosphate
- V:
-
Violaxanthin
- WT:
-
Wild type
- Z:
-
Zeaxanthin
- ΔpH:
-
Proton gradient
References
Adams WW III, Muller O, Cohu CM, Demmig-Adams B (2013) May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Photosynth Res 117(1–3):31–44
Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797
Alboresi A, Caffarri S, Nogue F, Bassi R, Morosinotto T (2008) In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS One 3:e2033
Alboresi A, Gerotto C, Giacometti GM, Bassi R, Morosinotto T (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci USA 107:11128–11133
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 FA, Niyogi KK, Krieger-Liszkay A, Minagawa J, Finazzi G (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25:545–557
Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P, Jansson S (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness. Plant J 35:350–361
Arnoux P, Morosinotto T, Saga G, Bassi R, Pignol D (2009) A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 21:2036–2044
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Aspinall-O’Dea M, Wentworth M, Pascal A, Robert B, Ruban AV, Horton P (2002) In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proc Natl Acad Sci USA 99:16331–16335
Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, Bassi R, Fleming GR (2008) Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 283:3550–3558
Bailleul B, Rogato A, De Martino A, Coesel S, Cardol P, Bowler C, Falciatore A, Finazzi G (2010) An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light. Proc Natl Acad Sci USA 107:18214–18219
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
Ballottari M, Girardon J, Betterle N, Morosinotto T, Bassi R (2010) Identification of the chromophores involved in aggregation-dependent energy quenching of the monomeric photosystem II antenna protein Lhcb5. J Biol Chem 285:28309–28321
Barber J, Andersson B (1992) Too much of a good thing – light can be bad for photosynthesis. Trends Biochem Sci 17:61–66
Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103:999–1004
Betterle N, Ballottari M, Zorzan S, De Bianchi S, Cazzaniga S, Dall’Osto L, Morosinotto T, Bassi R (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 284:15255–15266
Bode S, Quentmeier CC, Liao PN, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci USA 106:12311–12316
Boekema EJ, van Roon H, Calkoen F, Bassi R, Dekker JP (1999) Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Biochemistry 38:2233–2239
Bonente G, Howes BD, Caffarri S, Smulevich G, Bassi R (2008a) Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J Biol Chem 283:8434–8445
Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia MC, Tripodi M, Bassi R, Caffarri S (2008b) The occurrence of the PsbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 84:1359–1370
Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2011) Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9:e1000577
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
Brugnoli E, Björkman O (1992) Chloroplast movements in leaves – influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynth Res 32:23–35
Dall’Osto L, Caffarri S, Bassi R (2005) A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 17:1217–1232
Dall’Osto L, Holt NE, Kaligotla S, Fuciman M, Cazzaniga S, Carbonera D, Frank HA, Alric J, Bassi R (2012) Zeaxanthin protects plant photosynthesis by modulating chlorophyll triplet yield in specific light-harvesting antenna subunits. J Biol Chem 287:41820–41834
De Bianchi S, Dall’Osto L, Tognon G, Morosinotto T, Bassi R (2008) Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell 20:1012–1028
De Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall’Osto L (2011) Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. Plant Cell 23:2659–2679
Demmig-Adams B, Adams WW III, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98:253–264
Dominici P, Caffarri S, Armenante F, Ceoldo S, Crimi M, Bassi R (2002) Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J Biol Chem 277:22750–22758
Elrad D, Niyogi KK, Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14:1801–1816
Engelken J, Brinkmann H, Adamska I (2010) Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily. BMC Evol Biol 10:233
Ferrante P, Ballottari M, Bonente G, Giuliano G, Bassi R (2012) LHCBM1 and LHCBM2/7 polypeptides, components of major LHCII complex, have distinct functional roles in photosynthetic antenna system of Chlamydomonas reinhardtii. J Biol Chem 287:16276–16288
Förster B, Pogson BJ, Osmond CB (2011) Lutein from deepoxidation of lutein epoxide replaces zeaxanthin to sustain an enhanced capacity for nonphotochemical chlorophyll fluorescence quenching in avocado shade leaves in the dark. Plant Physiol 156:393–403
Funk C, Schröder WP, Napiwotzki A, Tjus SE, Renger G, Andersson B (1995) The PSII-S protein of higher plants: a new type of pigment-binding protein. Biochemistry 34:11133–11141
Gagne G, Guertin M (1992) The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light dark cycles involves genes that represent direct responses to light and photosynthesis. Plant Mol Biol 18:429–445
Gerotto C, Morosinotto T (2013) Evolution of photoprotection mechanisms upon land colonization: evidence of PSBS-dependent NPQ in late Streptophyte algae. Physiol Plant 149(4):583–598
Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ 34:922–932
Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2012) Coexistence of plant and algal energy dissipation mechanisms in the moss Physcomitrella patens. New Phytol 196:763–773
Gilmore AM, Shinkarev VP, Hazlett TL, Govindjee G (1998) Quantitative analysis of the effects of intrathylakoid pH and xanathophyll cycle pigments on chlorophyll a fluorescence lifetime distributions and intensity in thylakoids. Biochemistry 37:13582–13593
Harrer R, Bassi R, Testi MG, Schäfer C (1998) Nearest-neighbor analysis of a photosystem II complex from Marchantia polymorpha L. (liverwort), which contains reaction center and antenna proteins. Eur J Biochem 255:196–205
Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767
Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520
Holt NE, Zigmantas D, Valkunas L, Li X-P, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436
Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett 292:1–4
Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193
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
Kasajima I, Ebana K, Yamamoto T, Takahara K, Yano M, Kawai-Yamada M, Uchimiya H (2011) Molecular distinction in genetic regulation of nonphotochemical quenching in rice. Proc Natl Acad Sci USA 108:13835–13840
Koziol AG, Borza T, Ishida K, Keeling P, Lee RW, Durnford DG (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143:1802–1816
Kruger TP, Wientjes E, Croce R, van Grondelle R (2011) Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc Natl Acad Sci USA 108:13516–13521
Kruger TP, Ilioaia C, Johnson MP, Ruban AV, Papagiannakis E, Horton P, van Grondelle R (2012) Controlled disorder in plant light-harvesting complex II explains its photoprotective role. Biophys J 102:2669–2676
Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93
Lambrev PH, Nilkens M, Miloslavina Y, Jahns P, Holzwarth AR (2010) Kinetic and spectral resolution of multiple nonphotochemical quenching components in Arabidopsis leaves. Plant Physiol 152:1611–1624
Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395
Li X-P, Phippard A, Pasari J, Niyogi KK (2002) Structure-function analysis of photosystem II subunit S (PsbS) in vivo. Funct Plant Biol 29:1131–1139
Li X-P, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874
Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, Bassi R, Fleming GR, Keasling JD, Niyogi KK (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21:1798–1812
Maurino VG, Peterhansel C (2010) Photorespiration: current status and approaches for metabolic engineering. Curr Opin Plant Biol 13:249–256
Miloslavina Y, Wehner A, Lambrev PH, Wientjes E, Reus M, Garab G, Croce R, Holzwarth AR (2008) Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett 582:3625–3631
Miloslavina Y, De Bianchi S, Dall’Osto L, Bassi R, Holzwarth AR (2011) Quenching in Arabidopsis thaliana mutants lacking monomeric antenna proteins of photosystem II. J Biol Chem 286:36830–36840
Morosinotto T, Baronio R, Bassi R (2002) Dynamics of chromophore binding to Lhc proteins in vivo and in vitro during operation of the xanthophyll cycle. J Biol Chem 277:36913–36920
Moya I, Silvestri M, Vallon O, Cinque G, Bassi R (2001) Time-resolved fluorescence analysis of the Photosystem II antenna proteins in detergent micelles and liposomes. Biochemistry 40:12552–12561
Nelson N, Ben Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5:971–982
Nichol CJ, Pieruschka R, Takayama K, Förster B, Kolber Z, Rascher U, Grace J, Robinson SA, Pogson B, Osmond B (2012) Canopy conundrums: building on the Biosphere 2 experience to scale measurements of inner and outer canopy photoprotection from the leaf to the landscape. Funct Plant Biol 39:1–24
Nilkens M, Kress E, Lambrev P, Miloslavina Y, Muller M, Holzwarth AR, Jahns P (2010) 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 1797:466–475
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359
Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460
Niyogi KK, Björkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 94:14162–14167
Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134
Niyogi KK, Shih C, Soon CW, Pogson BJ, DellaPenna D, Björkman O (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res 67:139–145
Pascal AA, Liu Z, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang W, Ruban A (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134–137
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
Pinnola A, Dall’Osto L, Gerotto C, Morosinotto T, Bassi R, Alboresi A (2013) Zeaxanthin binds to light-harvesting complex stress-related protein to enhance nonphotochemical quenching in Physcomitrella patens. Plant Cell 25(9):3519–3534
Reinhold C, Niczyporuk S, Beran KC, Jahns P (2008) Short-term down-regulation of zeaxanthin epoxidation in Arabidopsis thaliana in response to photo-oxidative stress conditions. Biochim Biophys Acta 1777:462–469
Remelli R, Varotto C, Sandona D, Croce R, Bassi R (1999) Chlorophyll binding to monomeric light-harvesting complex. A mutation analysis of chromophore-binding residues. J Biol Chem 274:33510–33521
Richard C, Ouellet H, Guertin M (2000) Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii. Plant Mol Biol 42:303–316
Ruban A, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne AL (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82:165–175
Ruban AV, Berera R, Ilioaia C, van Stokkum IH, Kennis JT, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578
Scott AC, Glasspool IJ (2006) The diversification of Paleozoic fire systems and fluctuations in atmospheric oxygen concentration. Proc Natl Acad Sci USA 103:10861–10865
Tokutsu R, Kato N, Bui KH, Ishikawa T, Minagawa J (2012) Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii. J Biol Chem 287:31574–31581
van Oort B, Alberts M, De Bianchi S, Dall’Osto L, Bassi R, Trinkunas G, Croce R, van Amerongen H (2010) Effect of antenna-depletion in Photosystem II on excitation energy transfer in Arabidopsis thaliana. Biophys J 98:922–931
Walters RG, Horton P (1991) Resolution of components of nonphotochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121–133
Waters ER (2003) Molecular adaptation and the origin of land plants. Mol Phylogenet Evol 29:456–463
Wilson A, Boulay C, Wilde A, Kerfeld CA, Kirilovsky D (2007) Light-induced energy dissipation in iron-starved cyanobacteria: roles of OCP and IsiA proteins. Plant Cell 19:656–672
Zhu SH, Green BR (2010) Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochim Biophys Acta 1797:1449–1457
Acknowledgments
RB thanks the EEC projects “Sunbiopaths”, “Harvest” and “Accliphot” for supporting research on regulation of photosynthesis in plants and algae. Luca Dall’Osto, Matteo Ballottari, Alberta Pinnola and Alessandro Alboresi are acknowledged for discussions and help. TM acknowledges financial support from “Cassa di Risparmio di Padova e Rovigo” (CaRiPaRo) Foundation and the University of Padova (grants CPDA089403 and CPDR104834).
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Morosinotto, T., Bassi, R. (2014). Molecular Mechanisms for Activation of Non-Photochemical Fluorescence Quenching: From Unicellular Algae to Mosses and Higher Plants. In: Demmig-Adams, B., Garab, G., Adams III, W., Govindjee, . (eds) Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration, vol 40. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9032-1_14
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