Skip to main content

Are Chlorophyll-Carotenoid Interactions Responsible for Rapidly Reversible Non-Photochemical Fluorescence Quenching?

  • Chapter
  • First Online:
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 40))

  • 3132 Accesses

Summary

Photoprotective thermal energy dissipation (as assessed via non-photochemical quenching of singlet-excited chlorophyll a, NPQ) in plants is driven by various mechanisms occurring over different time scales. The rapid and reversible part of NPQ, also called qE (for energy-dependent quenching), was demonstrated to correlate with the twisting of a neoxanthin molecule in the light-harvesting antenna as observed by resonance Raman spectroscopy (Nature 450: 575–578, 2007). Interestingly, the extent of fluorescence quenching correlates with the change in Raman signal in different situations: during NPQ in vivo, during fluorescence quenching upon aggregation of LHCII (the major light-harvesting complex in plants), and in crystals of LHCII. In the same study, it was proposed that the quenching is caused by excitation energy transfer from chlorophyll a to lutein in LHCII after a structural change that correlates with the twisting of the neoxanthin. However, this view has been challenged by others for different reasons. Here we discuss the arguments in favor and against this mechanism. A short overview is given of the spectroscopic data on chlorophyll-carotenoid interactions in plant light-harvesting systems, the changes in interactions upon aggregation or crystallization, and the possible relationship to the mechanism of NPQ.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

B4C:

Band 4 complex;

C2:

Dimeric core of PS II;

C2S2M2:

Supercomplex of PS II consisting of a dimeric core surrounded by the outer light-harvesting complexes (LHCs): 4 major (LHCII) and 6 minor ones (two each of CP24, CP26 and CP29);

Car:

Carotenoid;

Chl:

Chlorophyll;

Chl 610:

Chl A1;

Chl 612:

Chl A2;

CP24, CP26, CP29:

Minor light-harvesting complexes of photosystem II;

CT:

Charge-transfer;

DES:

De-epoxidation state;

EET:

Excitation energy transfer;

LHC:

Light-harvesting complex;

LHCII:

Light-harvesting complex II;

LHCII-M:

Moderately coupled LHCII trimer;

LHCII-S:

Strongly coupled LHCII trimer;

Lut1:

Lutein 1;

N:

Neoxanthin;

NPQ:

Non-photochemical quenching of chlorophyll fluorescence;

PS I:

Photosystem I;

PS II:

Photosystem II;

qE:

Energy-dependent quenching;

RC:

Reaction center;

ROS:

Reactive oxygen species;

V:

Violaxanthin;

Z:

Zeaxanthin

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  CAS  PubMed  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Barros T, Royant A, Standfuss J, Dreuw A, Kuhlbrandt W (2009) Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state. EMBO J 28:298–306

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barzda V, Peterman EJG, van Grondelle R, van Amerongen H (1998) The influence of aggregation on triplet formation in light-harvesting chlorophyll a/b pigment-protein complex II of green plants. Biochemistry 37:546–551

    Article  CAS  PubMed  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Bode S, Quentmeier CC, Liao PN, Haf 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28:3052–3063

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Caffarri S, Broess K, Croce R, van Amerongen H (2011) Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes. Biophys J 100:2094–2103

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Croce R, Muller MG, Bassi R, Holzwarth AR (2001) Carotenoid-to-chlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorption measurements. Biophys J 80:901–915

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39

    Article  CAS  PubMed  Google Scholar 

  • Demmig B, Winter K, Kruger A, Czygan FC (1987) Photoinhibition and zeaxanthin formation in intact leaves – a possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84:218–224

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  • Duffy CDP, Chmeliov J, Macernis M, Sulskus J, Valkunas L, Ruban AV (2013) Modeling of fluorescence quenching by lutein in the plant light-harvesting complex LHCII. J Phys Chem B. doi:10.1021/jp3110997I

    Google Scholar 

  • Frank HA, Bautista JA, Josue JS, Young AJ (2000) Mechanism of nonphotochemical quenching in green plants: energies of the lowest excited singlet states of violaxanthin and zeaxanthin. Biochemistry 39:2831–2837

    Article  CAS  PubMed  Google Scholar 

  • Gradinaru CC, van Stokkum IHM, Pascal AA, van Grondelle R, van Amerongen H (2000) Identifying the pathways of energy transfer between carotenoids and chlorophylls in LHCII and CP29. A multicolor, femtosecond pump-probe study. J Phys Chem B 104:9330–9342

    Article  CAS  Google Scholar 

  • Gradinaru CC, van Grondelle R, van Amerongen H (2003) Selective interaction between xanthophylls and chlorophylls in LHCII probed by femtosecond transient absorption spectroscopy. J Phys Chem B 107:3938–3943

    Article  CAS  Google Scholar 

  • Gruszecki WI, Zubik M, Luchowski R, Janik E, Grudzinksi W, Gospodarek M, Goc J, Fiedor L, Gryczynski Z, Gryczynski I (2010) Photoprotective role of the xanthophyll cycle studied by means of modeling of xanthophyll-LHCII interactions. Chem Phys 373:122–128

    Article  CAS  Google Scholar 

  • Haferkamp S, Haase W, Pascal AA, van Amerongen H, Kirchhoff H (2010) Efficient light harvesting by photosystem II requires an optimized protein packing density in grana thylakoids. J Biol Chem 285:17020–17028

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436

    Article  CAS  PubMed  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, Wentworth M, Ruban A (2005) Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett 579:4201–4206

    Article  CAS  PubMed  Google Scholar 

  • Ilioaia C, Johnson MP, Horton P, Ruban AV (2008) Induction of efficient energy dissipation in the isolated light-harvesting complex of photosystem II in the absence of protein aggregation. J Biol Chem 283:29505–29512

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ilioaia C, Johnson MP, Liao PN, Pascal AA, van Grondelle R, Walla PJ, Ruban AV, Robert B (2011) Photoprotection in plants involves a change in lutein 1 binding domain in the major light-harvesting complex of photosystem II. J Biol Chem 286:27247–27254

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kruger TPJ, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lampoura SS, Barzda V, Owen GM, Hoff AJ, van Amerongen H (2002) Aggregation of LHCII leads to a redistribution of the triplets over the central xanthophylls in LHCII. Biochemistry 41:9139–9144

    Article  CAS  PubMed  Google Scholar 

  • Liao PN, Bode S, Wilk L, Hafi N, Walla PJ (2010a) Correlation of electronic carotenoid-chlorophyll interactions and fluorescence quenching with the aggregation of native LHC II and chlorophyll deficient mutants. Chem Phys 373:50–55

    Article  CAS  Google Scholar 

  • Liao PN, Holleboom CP, Wilk L, Kuhlbrandt W, Walla PJ (2010b) Correlation of car S-1 - > Chl with Chl - > Car S-1 energy transfer supports the excitonic model in quenched light harvesting complex II. J Phys Chem B 114:15650–15655

    Article  CAS  PubMed  Google Scholar 

  • Liu ZF, Yan HC, Wang KB, Kuang TY, Zhang JP, Gui LL, An XM, Chang WR (2004) Crystal structure of spinach major light-harvesting complex at 2.72 angstrom resolution. Nature 428:287–292

    Article  CAS  PubMed  Google Scholar 

  • Macernis M, Sulskus J, Duffy CDP, Ruban AV, Valkunas L (2012) Electronic spectra of structurally deformed lutein. J Phys Chem A 116:9843–9853

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mozzo M, Passarini F, Bassi R, van Amerongen H, Croce R (2008) Photoprotection in higher plants: the putative quenching site is conserved in all outer light-harvesting complexes of photosystem II. Biochim Biophys Acta 1777:1263–1267

    Article  CAS  PubMed  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 

  • Naqvi KR, Melo TB, Raju BB, Javorfi T, Simidjiev I, Garab G (1997) Quenching of chlorophyll a singlets and triplets by carotenoids in light-harvesting complex of photosystem II: comparison of aggregates with trimers. Spectrochim Acta Part A 53:2659–2667

    Article  Google Scholar 

  • Naqvi KR, Javorfi T, Melo TB, Garab G (1999) More on the catalysis of internal conversion in chlorophyll a by an adjacent carotenoid in light-harvesting complex (Ch1a/b LHCII) of higher plants: time-resolved triplet-minus-singlet spectra of detergent-perturbed complexes. Spectrochim Acta Part A 55:193–204

    Article  Google Scholar 

  • Owens T (1994) Excitation energy transfer between chlorophylls and carotenoids. A proposed molecular mechanism for non-photochemical quenching. In: Baker RRB, Bowyer JR (eds) Photoinhibition in Photosynthesis: From Molecular Mehanisms to the Field. Bios Scientific Publishers, London, pp 95–107

    Google Scholar 

  • Palacios MA, Frese RN, Gradinaru CC, van Stokkum IHM, Premvardhan LL, Horton P (2003) Stark spectroscopy of the light-harvesting complex II in different oligomerisation states. Biochim Biophys Acta 1605:83–95

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Peterman EJG, Dukker FM, van Grondelle R, van Amerongen H (1995) Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys J 69:2670–2678

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peterman EJG, Monshouwer R, van Stokkum IHM, van Grondelle R, van Amerongen H (1997) Ultrafast singlet excitation transfer from carotenoids to chlorophylls via different pathways in light-harvesting complex II of higher plants. Chem Phys Lett 264:279–284

    Article  CAS  Google Scholar 

  • Pieper J, Irrgang KD, Ratsep M, Schrotter T, Voigt J, Small GJ, Renger G (1999) Effects of aggregation on trimeric light-harvesting complex II of green plants: a hole-burning study. J Phys Chem A 103:2422–2428

    Article  CAS  Google Scholar 

  • Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, 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  CAS  PubMed  Google Scholar 

  • Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M, Kuhlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24:919–928

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tikkanen M, Grieco M, Aro E-M (2011) Novel insights into plant light-harvesting complex II phosphorylation and ‘state transitions’. Trends Plant Sci 16:126–131

    Article  CAS  PubMed  Google Scholar 

  • van Amerongen H, van Grondelle R (2001) Understanding the energy transfer function of LHCII, the major light-harvesting complex of green plants. J Phys Chem B 105:604–617

    Article  Google Scholar 

  • Van der Vos R, Carbonera D, Hoff AJ (1991) Microwave and optical spectroscopy of carotenoid triplets in light-harvesting complex LHC II of spinach by absorbance-detected magnetic resonance. Appl Magn Res 2:179–202

    Article  Google Scholar 

  • Van Oort B, van Hoek A, Ruban AV, van Amerongen H (2007a) Aggregation of light-harvesting complex II leads to formation of efficient excitation energy traps in monomeric and trimeric complexes. FEBS Lett 581:3528–3532

    Article  PubMed  Google Scholar 

  • Van Oort B, van Hoek A, Ruban AV, van Amerongen H (2007b) Equilibrium between quenched and nonquenched conformations of the major plant light-harvesting complex studied with high-pressure time-resolved fluorescence. J Phys Chem B 111:7631–7637

    Article  PubMed  Google Scholar 

  • Van Oort B, Marechal A, Ruban AV, Robert B, Pascal AA, de Ruijter NCA, van Grondelle R, van Amerongen H (2011) Different crystal morphologies lead to slightly different conformations of light-harvesting complex II as monitored by variations of the intrinsic fluorescence lifetime. Phys Chem Chem Phys 13:12614–12622

    Article  PubMed  Google Scholar 

  • Wahadoszamen M, Berera R, Ara AM, Romero E, van Grondelle R (2012) Identification of two emitting sites in the dissipative state of the major light harvesting antenna. Phys Chem Chem Phys 14:759–766

    Article  CAS  PubMed  Google Scholar 

  • Wientjes E, Roest G, Croce R (2012) From red to blue to far-red in Lhca4: how does the protein modulate the spectral properties of the pigments? Biochim Biophys Acta 1817:711–717

    Article  CAS  PubMed  Google Scholar 

  • Wientjes E, Van Amerongen H, Croce R (2013) LHCII is an antenna of both photosystems after long-term acclimation. Biochim Biophys Acta 1827:420–426

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I would like to thank Dr. Roberta Croce for helpful discussions and for providing the figures. I am also obliged to Drs. B. Demmig-Adams, G. Garab, A.R. Holzwarth, and T. Polivka for helpful comments and suggestions. I would like to acknowledge support from the research programme of BioSolar Cells, cofinanced by the Dutch Ministry of Economic Affairs.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Herbert van Amerongen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

van Amerongen, H. (2014). Are Chlorophyll-Carotenoid Interactions Responsible for Rapidly Reversible Non-Photochemical Fluorescence Quenching?. 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_15

Download citation

Publish with us

Policies and ethics