Skip to main content
Log in

Acclimation- and mutation-induced enhancement of PsbS levels affects the kinetics of non-photochemical quenching in Arabidopsis thaliana

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The efficiency of photosystem II antenna complexes (LHCs) in higher plants must be regulated to avoid potentially damaging overexcitation of the reaction centre in excess light. Regulation is achieved via a feedback mechanism known as non-photochemical quenching (NPQ), triggered the proton gradient (ΔpH) causing heat dissipation within the LHC antenna. ΔpH causes protonation of the LHCs, the PsbS protein and triggers the enzymatic de-epoxidation of the xanthophyll, violaxanthin, to zeaxanthin. A key step in understanding the mechanism is to decipher whether PsbS and zeaxanthin cooperate to promote NPQ. To obtain clues about their respective functions we studied the effects of PsbS and zeaxanthin on the rates of NPQ formation and relaxation in wild-type Arabidopsis leaves and those overexpressing PsbS (L17) or lacking zeaxanthin (npq1). Overexpression of PsbS was found to increase the rate of NPQ formation, as previously reported for zeaxanthin. However, PsbS overexpression also increased the rate of NPQ relaxation, unlike zeaxanthin, which is known decrease the rate. The enhancement of PsbS levels in plants lacking zeaxanthin (npq1) by either acclimation to high light or crossing with L17 plants showed that the effect of PsbS was independent of zeaxanthin. PsbS levels also affected the kinetics of the 535 nm absorption change (ΔA535), which monitors the formation of the conformational state of the LHC antenna associated with NPQ, in an identical way. The antagonistic action of PsbS and zeaxanthin with respect to NPQ and ΔA535 relaxation kinetics suggests that the two molecules have distinct regulatory functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

NPQ:

Non-photochemical quenching of chlorophyll fluorescence

VDE:

Violaxanthin de-epoxidase enzyme

PSII:

Photosystem II

LHC:

Light harvesting complexes of photosystem II

ΔpH:

Trans-thylakoid proton gradient

LL:

Low-light acclimated plants

HL:

High-light acclimated plants

WT:

Wild-type plants

SEM:

Standard error of the mean

References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Andersson J, Walters RG, Horton P, Jansson S (2001) Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13:1193–1204

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Avenson TJ, Ahn TK, Niyogi KK, Ballottari M, Bassi R, Fleming GR (2009) Lutein can act as a switchable charge transfer quencher in the CP26 light-harvesting complex. J Biol Chem 284:2830–2835

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ballottari M, Girardon J, Betterle N, Morosinotto T, Bassi R (2010) Identification of the chromophores involved in aggregation dependent energy quenching in the monomeric photosystem II antenna protein Lhcb5. J Biol Chem 285:28309–28321

    Article  PubMed  CAS  Google Scholar 

  • Bergantino E, Segalla A, Brunetta A, Teardo E, Rigoni F, Giacometti GM, Szabo I (2003) Light- and pH-dependent structural changes in the PsbS subunit of photosystem II. Proc Natl Acad Sci USA 100:15265–15270

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bilger W, Bjorkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbency changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosyn Res 25:173–185

    Article  CAS  Google Scholar 

  • Bonente G, Howes BD, Caffarri S, Smulevich G, Bassi R (2008) Interactions between the photosystem II subunit PsbS and xanthophylls as studied in vivo and in vitro. J Biol Chem 283:8434–8445

    Article  PubMed  CAS  Google Scholar 

  • Briantais JM, Vernotte C, Picaud M, Krause GH (1979) Quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138

    Article  PubMed  CAS  Google Scholar 

  • Bugos RC, Yamamoto HY (1996) Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc Natl Acad Sci USA 93:6320–6325

    Article  PubMed  CAS  Google Scholar 

  • Crouchman S, Ruban AV, Horton P (2006) PsbS enhances nonphotochemical fluorescence quenching in the absence of zeaxanthin. FEBS Lett 580:2053–2058

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gilmore AM, Hazlett TL, Govindjee TL (1995) Xanthophyll cycle-dependent quenching of photosystem-II chlorophyll-a fluorescence—formation of a quenching complex with a short fluorescence lifetime. Proc Natl Acad Sci USA 92:2273–2277

    Article  PubMed  CAS  Google Scholar 

  • Hartel H, Lokstein H, Grimm B, Rank B (1996) Kinetic studies on the xanthophyll cycle in barley leaves—influence of antenna size and relations to nonphotochemical chlorophyll fluorescence quenching. Plant Physiol 110:471–482

    PubMed  Google Scholar 

  • Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43:8281–8289

    Article  PubMed  CAS  Google Scholar 

  • Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P (2009) Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem Phys Lett 483:262–267

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Walters R, Ruban AV (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Wentworth M (2000) Allosteric regulation of the light-harvesting system of photosystem II. Philos Trans R Soc Lond B Biol Sci 355:1361–1370

    Article  PubMed  CAS  Google Scholar 

  • Ilioaia C, Johnson MP, Duffy CDP, Pascal A, van Grondelle R, Robert B, Ruban AV (2011) The origin of absorption changes associated with photoprotective energy dissipation in the absence of zeaxanthin. J Biol Chem 284:91–98

    Google Scholar 

  • Jahns P, Latowski D, Strzalka K (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim Biophys Acta 1787:3–14

    Article  PubMed  CAS  Google Scholar 

  • Johnson MP, Ruban AV (2010) Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J 61:283–289

    Article  PubMed  CAS  Google Scholar 

  • Johnson MP, Davison P, Ruban AV, Horton P (2008) The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett 582:262–266

    Article  PubMed  CAS  Google Scholar 

  • Johnson MP, Perez-Bueno ML, Zia A, Horton P, Ruban AV (2009) The zeaxanthin-independent and zeaxanthin-dependent qE components of nonphotochemical quenching involve common conformational changes within the photosystem II antenna in Arabidopsis. Plant Physiol 149:1061–1075

    Article  PubMed  CAS  Google Scholar 

  • Joliot PA, Finazzi G (2010) Proton equilibration in the chloroplast modulates the kinetics of non-photochemical quenching of fluorescence in plants. Proc Natl Acad Sci USA 107:12729–12733

    Article  Google Scholar 

  • Kereiche S, Kiss AZ, Kouril R, Boekema EJ, Horton P (2010) The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts. FEBS Lett 584:759–764

    Article  PubMed  CAS  Google Scholar 

  • Kiss AZ, Ruban AV, Horton P (2008) The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 283:3972–3978

    Article  PubMed  CAS  Google Scholar 

  • Kovacs L, Damkjær J, Kereïche S, Ilioaia C, Ruban AV, Boekema EJ, Jansson S, Horton P (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18:3106–3120

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Bjorkman 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

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Muller-Moule P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99:15222–15227

    Article  PubMed  CAS  Google Scholar 

  • Li XP, 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

    Article  PubMed  CAS  Google Scholar 

  • Muller MG, Lambrev P, Reus M, Wientjes E, Croce R, Holzwarth AR (2010) Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. Chem Phys Chem 11:1289–1296

    PubMed  Google Scholar 

  • Nield J, Funk C, Barber J (2000) Supermolecular structure of photosystem II and location of the PsbS protein. Phil Trans R Soc Lond B 355:1337–1344

    Article  CAS  Google Scholar 

  • Niyogi KK, Grossman AR, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK, Shih C, Chow WS, Pogson BJ, Dellapenna D, Björkman O (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res 67:139–145

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Rees D, Young AJ, Horton P (1991) The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence, and trans-thylakoid pH gradient in isolated chloroplasts. Biochim Biophys Acta 1057:320–330

    Article  CAS  Google Scholar 

  • Noctor G, Ruban AV, Horton P (1993) Modulation of ΔpH-dependent nonphotochemical quenching of chlorophyll fluorescence in spinach-chloroplasts. Biochim Biophys Acta 1183:339–344

    Article  CAS  Google Scholar 

  • 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 spectroscopy. Biochim Biophys Acta 975:384–394

    Google Scholar 

  • Ruban AV, Horton P (1999) The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light-harvesting complexes, intact chloroplasts, and leaves of spinach. Plant Physiol 119:531–542

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Young AJ, Horton P (1993) Induction of nonphotochemical energy-dissipation and absorbance changes in leaves—evidence for changes in the state of the light-harvesting system of photosystem-II in vivo. Plant Physiol 102:741–750

    PubMed  CAS  Google Scholar 

  • Ruban AV, Young AJ, Horton P (1996) Dynamic properties of the minor chlorophyll a/b binding proteins of photosystem II, an in vitro model for photoprotective energy dissipation in the photosynthetic membrane of green plants. Biochemistry 35:674–678

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Phillip D, Young AJ, Horton P (1997) Carotenoid-dependent oligomerization of the major chlorophyll a/b light harvesting complex of photosystem II of plants. Biochemistry 36:7855–7859

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Wentworth M, Horton P (2001) Kinetic analysis of non-photochemical quenching of chlorophyll fluorescence. 1. Isolated chloroplasts. Biochemistry 40:9896–9901

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Pascal AA, Robert B, Horton P (2002) Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting. J Biol Chem 277:7785–7789

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Solovieva S, Lee PJ, Ilioaia C, Wentworth M, Ganeteg U, Klimmek F, Chow WS, Anderson J, Jansson S, Horton P (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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Teardo E, Polverino de Laureto P, Bergantino E, Dalla Vecchia F, Rigoni F, Szabò I, Giacometti GM (2007) Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids. Biochim Biophys Acta 1767:703–711

    Article  PubMed  CAS  Google Scholar 

  • Walters RG, Ruban AV, Horton P (1994) Higher plant light-harvesting complexes LHCIIa and LHCIIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur J Biochem 226:1063–1069

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by research and equipment grants to A.V.R. from the Royal Society and UK Biotechnology and Biological Sciences Research Council. The authors would like to thank Peter Horton and Sophie Crouchman (Sheffield) for helpful discussions and thank Krishna Niyogi (Berkeley) for the kind gift of the seeds of L17 plants. A.Z. was a recipient of the Queen Mary University of London Postgraduate Studentship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander V. Ruban.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zia, A., Johnson, M.P. & Ruban, A.V. Acclimation- and mutation-induced enhancement of PsbS levels affects the kinetics of non-photochemical quenching in Arabidopsis thaliana . Planta 233, 1253–1264 (2011). https://doi.org/10.1007/s00425-011-1380-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1380-5

Keywords

Navigation