Skip to main content

Can red-emitting state be responsible for fluorescence quenching in LHCII aggregates?

Abstract

Non-photochemical quenching (NPQ) is responsible for protecting the light-harvesting apparatus of plants from damage at high light conditions. Although it is agreed that the major part of NPQ, an energy-dependent quenching (qE), originates in the light-harvesting antenna, its exact mechanism is still debated. In our earlier work (Chmeliov et al. in Nat Plants 2:16045, 2016), we have analyzed the time-resolved fluorescence (TRF) from the trimers and aggregates of the major light-harvesting complexes of plants (LHCII) over a broad temperature range and came to a conclusion that three distinct states are required to describe the experimental data: two of them correspond to the emission bands centered at ~680 and ~700 nm, and the third state is responsible for the excitation quenching. This was opposite to earlier suggestions of a two-state model, where the red-shifted fluorescence and excitation quenching were assumed to be related. To examine such possibility, in the current work we repeat our analysis of the TRF data in terms of the two-state model. We find that even though it can reasonably describe the aggregate fluorescence, it fails to do so for the LHCII trimers. We conclude that the red-emitting state cannot be responsible for fluorescence quenching in the LHCII aggregates and reaffirm that the three-state model is the simplest possible description of the experimental data.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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(5877):794–797. doi:10.1126/science.1154800

    CAS  Article  PubMed  Google Scholar 

  • Ardia D, Mullen KM, Peterson BG, Ulrich J (2015) DEoptim: differential evolution in R. URL: http://CRAN.R-project.org/package=DEoptim, version 2.2-3

  • Balevičius V Jr, Gelzinis A, Abramavicius D, Valkunas L (2013) Excitation energy transfer and quenching in a heterodimer: applications to the carotenoid–phthalocyanine dyads. J Phys Chem B 117(38):11031–11041. doi:10.1021/jp3118083

    Article  PubMed  Google Scholar 

  • Barzda V, Gulbinas V, Kananavicius R, Cervinskas V, van Amerongen H, van Grondelle R, Valkunas L (2001) Singlet-singlet annihilation kinetics in aggregates and trimers of LHCII. Biophys J 80(5):2409–2421. doi:10.1016/S0006-3495(01)76210-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bennett DIG, Amarnath K, Fleming GR (2013) A structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes. J Am Chem Soc 135(24):9164–9173. doi:10.1021/ja403685a

    CAS  Article  PubMed  Google Scholar 

  • Blankenship RE (2014) Molecular mechanisms of photosynthesis, 2nd edn. Wiley, Chichester

    Google Scholar 

  • Broess K, Trinkunas G, van der Weij-de Wit CD, Dekker JP, van Hoek A, van Amerongen H (2006) Excitation energy transfer and charge separation in photosystem II membranes revisited. Biophys J 91(10):3776–3786. doi:10.1529/biophysj.106.085068

    CAS  Article  PubMed  PubMed Central  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(9):2094–2103. doi:10.1016/j.bpj.2011.03.049

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Chmeliov J, Trinkunas G, van Amerongen H, Valkunas L (2014) Light harvesting in a fluctuating antenna. J Am Chem Soc 136(25):8963–8972. doi:10.1021/ja5027858

    CAS  Article  PubMed  Google Scholar 

  • Chmeliov J, Bricker WP, Lo C, Jouin E, Valkunas L, Ruban AV, Duffy CDP (2015) An ‘all pigment’ model of excitation quenching in LHCII. Phys Chem Chem Phys 17(24):15857–15867. doi:10.1039/c5cp01905b

    CAS  Article  PubMed  Google Scholar 

  • Chmeliov J, Gelzinis A, Songaila E, Augulis R, Duffy CDP, Ruban AV, Valkunas L (2016) The nature of self-regulation in photosynthetic light-harvesting antenna. Nat Plants 2:16045. doi:10.1038/nplants.2016.45

    CAS  Article  PubMed  Google Scholar 

  • Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res 116(2–3):153–166. doi:10.1007/s11120-013-9838-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Croce R, van Amerongen H (2014) Natural strategies for photosynthetic light harvesting. Nat Chem Biol 10:492–501. doi:10.1038/nchembio.1555

    CAS  Article  PubMed  Google Scholar 

  • Demmig-Adams B, Garab G, Adams W III, Govindjee (eds) (2014) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria, advances in photosynthesis and respiration. Springer, Dordrecht. doi:10.1007/978-94-017-9032-1

    Google Scholar 

  • Duffy CDP, Chmeliov J, Macernis M, Sulskus J, Valkunas L, Ruban AV (2013a) Modeling of fluorescence quenching by lutein in the plant light-harvesting complex LHCII. J Phys Chem B 117(38):10974–10986. doi:10.1021/jp3110997

    CAS  Article  PubMed  Google Scholar 

  • Duffy CDP, Valkunas L, Ruban AV (2013b) Light-harvesting processes in the dynamic photosynthetic antenna. Phys Chem Chem Phys 15(43):18752–18770. doi:10.1039/c3cp51878g

    CAS  Article  PubMed  Google Scholar 

  • Gruber JM, Xu R, Chmeliov J, Krüger TPJ, Alexandre MTA, Valkunas L, Croce R, van Grondelle R (2016) Dynamic quenching in single photosystem II supercomplexes. Phys Chem Chem Phys 18(37):25852–25860. doi:10.1039/c6cp05493e

    CAS  Article  PubMed  Google Scholar 

  • Holt NE, Zigmantas D, Valkunas L, Li X, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436. doi:10.1126/science.1105833

    CAS  Article  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(4–6):262–267. doi:10.1016/j.cplett.2009.10.085

    CAS  Article  Google Scholar 

  • Horton P, Ruban AV, Rees D, Pascal A, Noctor G, Young A (1191) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett 292(1–2):1–4. doi:10.1016/0014-5793(91)80819-O

    Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684. doi:10.1146/annurev.arplant.47.1.655

    CAS  Article  PubMed  Google Scholar 

  • Kell A, Feng X, Lin C, Yang Y, Li J, Reus M, Holzwarth AR, Jankowiak R (2014) Charge-transfer character of the low-energy Chl a Q\(_\text{ y }\) absorption band in aggregated light harvesting complexes II. J Phys Chem B 118(23):6086–6091. doi:10.1021/jp501735p

    CAS  Article  PubMed  Google Scholar 

  • Krüger TPJ, Novoderezkhin VI, Ilioaia C, van Grondelle R (2010) Fluorescence spectral dynamics of single LHCII trimers. Biophys J 98(12):3093–3101. doi:10.1016/j.bpj.2010.03.028

    Article  PubMed  PubMed Central  Google Scholar 

  • Krüger TPJ, Ilioaia C, Valkunas L, van Grondelle R (2011a) Fluorescence intermittency from the main plant light-harvesting complex: sensitivity to the local environment. J Phys Chem B 115(18):5083–5095. doi:10.1021/jp109833x

    Article  PubMed  Google Scholar 

  • Krüger TPJ, Wientjes E, Croce R, van Grondelle R (2011b) Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc Natl Acad Sci USA 108(33):13516–13521. doi:10.1073/pnas.1105411108

    Article  PubMed  PubMed Central  Google Scholar 

  • Krüger TPJ, 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(11):2669–2676. doi:10.1016/j.bpj.2012.04.044

    Article  PubMed  PubMed Central  Google Scholar 

  • Krüger TPJ, Ilioaia C, Johnson MP, Ruban AV, van Grondelle R, van Grondelle R (2014) Disentangling the low-energy states of the major light-harvesting complex of plants and their role in photoprotection. Biochim Biophys Acta Bioenerg 1837(7):1027–1038. doi:10.1016/j.bbabio.2014.02.014

    Article  Google Scholar 

  • Lawton WH, Sylvestre EA (1971) Self modeling curve resolution. Technometrics 13(3):617–633. doi:10.2307/1267173

    Article  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(6768):391–395. doi:10.1038/35000131

    CAS  Article  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(25–26):3625–3631. doi:10.1016/j.febslet.2008.09.044

    CAS  Article  PubMed  Google Scholar 

  • Müh F, Madjet MEA, Renger T (2010) Structure-based identification of energy sinks in plant light-harvesting complex II. J Phys Chem B 114(42):13517–13535. doi:10.1021/jp106323e

    Article  PubMed  Google Scholar 

  • Müller 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. ChemPhysChem 11(6):1289–1296. doi:10.1002/cphc.200900852

    Article  PubMed  Google Scholar 

  • Novoderezhkin VI, Palacios MA, van Amerongen H (2005) Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Å crystal structure. J Phys Chem B 109(20):10493–10504. doi:10.1021/jp044082f

    CAS  Article  PubMed  Google Scholar 

  • Pascal AA, Liu ZF, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang WR, Ruban A (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436(7047):134–137. doi:10.1038/nature03795

    CAS  Article  PubMed  Google Scholar 

  • Price KV, Storn RM, Lampinen JA (2005) Natural computing series. Differential evolution. A practical approach to global optimization. Springer, Berlin

    Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL: http://www.R-project.org/

  • Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170(4):1903–1916. doi:10.1104/pp.15.01935

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ruban AV, Young A, Horton P (1994) Modulation of chlorophyll fluorescence quenching in isolated light harvesting complex of photosystem II. Biochim Biophys Acta Bioenerg 1186(1–2):123–127. doi:10.1016/0005-2728(94)90143-0

    CAS  Article  Google Scholar 

  • Ruban AV, Dekker JP, Horton P, van Grondelle R (1995) Temperature dependence of chlorophyll fluorescence from the light harvesting complex II of higher plants. Photochem Photobiol 61(2):216–221. doi:10.1111/j.1751-1097.1995.tb03964.x

    CAS  Article  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(7169):575–578. doi:10.1038/nature06262

    CAS  Article  PubMed  Google Scholar 

  • Ruban AV, Johnson MP (1817) Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta, Bioenerg 1:167–181. doi:10.1016/j.bbabio.2011.04.007

    Google Scholar 

  • Valkunas L, Trinkunas G, Chmeliov J, Ruban AV (2009) Modeling of exciton quenching in photosystem II. Phys Chem Chem Phys 11(35):7576–7584. doi:10.1039/B901848D

    CAS  Article  PubMed  Google Scholar 

  • Valkunas L, Chmeliov J, Krüger TPJ, Ilioaia C, van Grondelle R (2012) How photosynthetic proteins switch. J Phys Chem Lett 3(19):2779–2784. doi:10.1021/jz300983r

    CAS  Article  Google Scholar 

  • van Amerongen H, Croce R (2013) Light harvesting in photosystem II. Photosynth Res 116(2–3):251–263. doi:10.1007/s11120-013-9824-3

    Article  PubMed  PubMed Central  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(3):604–617. doi:10.1021/jp0028406

    Article  Google Scholar 

  • Walla PJ, Linden PA, Ohta K, Fleming GR (2002) Excited-state kinetics of the carotenoid S1 state in LHC II and two-photon excitation spectra of lutein and β-carotene in solution: Efficient Car S1→ Chl electronic energy transfer via hot S1 states? J Phys Chem A 106(10):1909–1916. doi:10.1021/jp011495x

    CAS  Article  Google Scholar 

Download references

Acknowledgements

AG and LV were supported by the Research Council of Lithuania (LMT Grant No. MIP-080/2015). JC was supported by the Young Scientist Scholarship from the Lithuanian Academy of Sciences. AVR would like to acknowledge The Royal Society for the Wolfson Research Merit Award. Computations were performed using the resources of the High Performance Computing Center “HPC Sauletekis” at Faculty of Physics, Vilnius University. The authors also thank Egidijus Songaila and Ramūnas Augulis for the experimental measurements.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leonas Valkunas.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (260 PDF)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gelzinis, A., Chmeliov, J., Ruban, A.V. et al. Can red-emitting state be responsible for fluorescence quenching in LHCII aggregates?. Photosynth Res 135, 275–284 (2018). https://doi.org/10.1007/s11120-017-0430-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-017-0430-7

Keywords

  • Light-harvesting complex
  • Fluorescence
  • Temperature
  • LHCII
  • NPQ