Carotenoid dark state to chlorophyll energy transfer in isolated light-harvesting complexes CP24 and CP29

Abstract

We present a comparison of the energy transfer between carotenoid dark states and chlorophylls for the minor complexes CP24 and CP29. To elucidate the potential involvement of certain carotenoid–chlorophyll coupling sites in fluorescence quenching of distinct complexes, varying carotenoid compositions and mutants lacking chlorophylls at specific binding sites were examined. Energy transfers between carotenoid dark states and chlorophylls were compared using the coupling parameter, \(\varPhi_{\text{Coupling}}^{{{\text{Car S}}_{ 1} {-}{\text{Chl}}}}\), which is calculated from the chlorophyll fluorescence observed after preferential carotenoid two-photon excitation. In CP24, artificial reconstitution with zeaxanthin leads to a significant reduction in the chlorophyll fluorescence quantum yield, \(\varPhi_{\text{F1}}\), and a considerable increase in \(\varPhi_{\text{Coupling}}^{{{\text{Car S}}_{ 1} {-}{\text{Chl}}}}\). Similar effects of zeaxanthin were also observed in certain samples of CP29. In CP29, also the replacement of violaxanthin by the sole presence of lutein results in a significant quenching and increased \(\varPhi_{\text{Coupling}}^{{{\text{Car S}}_{ 1} {-}{\text{Chl}}}}\). In contrast, the replacement of violaxanthin by lutein in CP24 is not significantly increasing \(\varPhi_{\text{Coupling}}^{{{\text{Car S}}_{ 1} {-}{\text{Chl}}}}\). In general, these findings provide evidence that modification of the electronic coupling between carotenoid dark states and chlorophylls by changing carotenoids at distinct sites can significantly influence the quenching of these minor proteins, particularly when zeaxanthin or lutein is used. The absence of Chl612 in CP24 and of Chl612 or Chl603 in CP29 has a considerably smaller effect on \(\varPhi_{{{\text{F}}1}}\) and \(\varPhi_{\text{Coupling}}^{{{\text{Car S}}_{ 1} {-}{\text{Chl}}}}\) than the influence of some carotenoids reported above. However, in CP29 our results indicate slightly dequenching and decreased \(\varPhi_{\text{Coupling}}^{{{\text{Car S}}_{ 1} {-}{\text{Chl}}}}\) when these chlorophylls are absent. This might indicate that both, Chl612 and Chl603 are involved in carotenoid-dependent quenching in isolated CP29.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Bassi R, Croce R, Cugini D, Sandona D (1999) Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites. Proc Natl Acad Sci USA 96:10056–10061. https://doi.org/10.1073/pnas.96.18.10056

    CAS  Article  PubMed  Google Scholar 

  2. 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. https://doi.org/10.1074/jbc.M808625200

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Betterle N, Ballottari M, Hienerwadel R, Dall’Osto L, Bassi R (2010) Dynamics of zeaxanthin binding to the photosystem II monomeric antenna protein Lhcb6 (CP24) and modulation of its photoprotection properties. Arch Biochem Biophys 504:67–77. https://doi.org/10.1016/j.abb.2010.05.016

    CAS  Article  PubMed  Google Scholar 

  4. Bode S, Quentmeier CC, Liao P-N, 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. https://doi.org/10.1073/pnas.0903536106

    Article  PubMed  Google Scholar 

  5. Caffarri S, Passarini F, Bassi R, Croce R (2007) A Specific binding site for neoxanthin in the monomeric antenna proteins CP26 and CP29 of photosystem II. FEBS Lett 581:4704–4710. https://doi.org/10.1016/j.febslet.2007.08.066

    CAS  Article  PubMed  Google Scholar 

  6. Caffarri S, Kouril R, Kereïche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28:3052–3063. https://doi.org/10.1038/emboj.2009.232

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Cheng Y-C, Ahn TK, Avenson TJ, Zigmantas D, Niyogi KK, Ballottari M, Bassi R, Fleming GR (2008) Kinetic modeling of charge-transfer quenching in the CP29 minor complex. J Phys Chem. B 112:13418–13423. https://doi.org/10.1021/jp802730c

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  9. Croce R, Weiss S, Bassi R (1999) Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J Biol Chem 274:29613–29623. https://doi.org/10.1074/jbc.274.42.29613

    CAS  Article  PubMed  Google Scholar 

  10. Croce R, Müller MG, Caffarri S, Bassi R, Holzwarth AR (2003) Energy transfer pathways in the minor antenna complex CP29 of photosystem II. A femtosecond study of carotenoid to chlorophyll transfer on mutant and WT complexes. Biophys J 84:2517–2532. https://doi.org/10.1016/S0006-3495(03)75057-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Dall’Osto L, Cazzaniga S, Bressan M, Paleček D, Židek K, Niyogi KK, Fleming GR, Zigmantas D, Bassi R (2017) Two mechanisms for dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nat Plants 3:17033. https://doi.org/10.1038/nplants.2017.33

    CAS  Article  PubMed  Google Scholar 

  12. Dall’Osto L, Cazzaniga S, Zappone D, Bassi R (2019) Monomeric light harvesting complexes enhance excitation energy transfer from LHCII to PSII and control their lateral spacing in thylakoids. Biochim Biophys Acta Bioenergy. https://doi.org/10.1016/j.bbabio.2019.06.007

    Article  Google Scholar 

  13. 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. https://doi.org/10.1105/tpc.111.087320

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26. https://doi.org/10.1016/S1360-1385(96)80019-7

    Article  Google Scholar 

  15. Demmig-Adams B, Adams WW (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153. https://doi.org/10.1126/science.1078002

    CAS  Article  PubMed  Google Scholar 

  16. 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 117:10974–10986. https://doi.org/10.1021/jp3110997

    CAS  Article  PubMed  Google Scholar 

  17. Fox KF, Ünlü C, Balevičius V, Ramdour BN, Kern C, Pan X, Li M, van Amerongen H, Duffy CDP (2018) A possible molecular basis for photoprotection in the minor antenna proteins of plants. Biochim Biophys Acta Bioenergy 1859:471–481. https://doi.org/10.1016/j.bbabio.2018.03.015

    CAS  Article  Google Scholar 

  18. Gacek DA, Moore AL, Moore TA, Walla PJ (2017) Two-photon spectra of chlorophylls and carotenoid-tetrapyrrole dyads. J Phys Chem B 121:10055–10063. https://doi.org/10.1021/acs.jpcb.7b08502

    CAS  Article  PubMed  Google Scholar 

  19. Gacek DA, Holleboom CP, Tietz S, Kirchhoff H, Walla PJ (2019) PsbS-dependent and -independent mechanisms regulate carotenoid-chlorophyll energy coupling in grana thylakoids. FEBS Lett. (in press)

  20. Gargouri M, Bates PD, Park J-J, Kirchhoff H, Gang DR (2017) Functional photosystem I maintains proper energy balance during nitrogen depletion in Chlamydomonas Reinhardtii, promoting triacylglycerol accumulation. Biotechnol Biofuels 10:89. https://doi.org/10.1186/s13068-017-0774-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Gastaldelli M, Canino G, Croce R, Bassi R (2003) Xanthophyll binding sites of the CP29 (Lhcb4) subunit of higher plant photosystem II investigated by domain swapping and mutation analysis. J Biol Chem 278:19190–19198. https://doi.org/10.1074/jbc.M212125200

    CAS  Article  PubMed  Google Scholar 

  22. Goral TK, Johnson MP, Duffy CDP, Brain APR, Ruban AV, Mullineaux CW (2012) Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. Plant J 69:289–301. https://doi.org/10.1111/j.1365-313X.2011.04790.x

    CAS  Article  PubMed  Google Scholar 

  23. Höhner R, Marques JV, Ito T, Amakura Y, Budgeon AD, Weitz K, Hixson KK, Davin LB, Kirchhoff H, Lewis NG (2018) Reduced arogenate dehydratase expression. ramifications for photosynthesis and metabolism. Plant Physiol 177:115–131. https://doi.org/10.1104/pp.17.01766

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Holleboom C-P, Walla PJ (2014) The back and forth of energy transfer between carotenoids and chlorophylls and its role in the regulation of light harvesting. Photosynth Res 119:215–221. https://doi.org/10.1007/s11120-013-9815-4

    CAS  Article  PubMed  Google Scholar 

  25. Holleboom C-P, Gacek DA, Liao P-N, Negretti M, Croce R, Walla PJ (2015) Carotenoid-chlorophyll coupling and fluorescence quenching in aggregated minor PSII proteins CP24 and CP29. Photosynth Res 124:171–180. https://doi.org/10.1007/s11120-015-0113-1

    CAS  Article  PubMed  Google Scholar 

  26. Humphrey W, Dalke A, Schulten K (1996) VMD visual molecular dynamics. J Mol Graph 14:33–38. https://doi.org/10.1016/0263-7855(96)00018-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Ilioaia C, Johnson MP, Liao P-N, 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. https://doi.org/10.1074/jbc.M111.234617

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 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. https://doi.org/10.1016/j.bbabio.2011.04.012

    CAS  Article  PubMed  Google Scholar 

  29. Johnson MP, Goral TK, Duffy CDP, Brain APR, 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. https://doi.org/10.1105/tpc.110.081646

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Kereïche 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. https://doi.org/10.1016/j.febslet.2009.12.031

    CAS  Article  PubMed  Google Scholar 

  31. 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. https://doi.org/10.1074/jbc.M707410200

    CAS  Article  PubMed  Google Scholar 

  32. Kovács L, Damkjaer 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. https://doi.org/10.1105/tpc.106.045641

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Kühlbrandt W, Thaler T, Wehrli E (1983) The structure of membrane crystals of the light-harvesting chlorophyll a/b protein complex. J Cell Biol 96:1414–1424. https://doi.org/10.1083/jcb.96.5.1414

    Article  PubMed  Google Scholar 

  34. Leuenberger M, Morris JM, Chan AM, Leonelli L, Niyogi KK, Fleming GR (2017) Dissecting and modeling Zeaxanthin- and lutein-dependent nonphotochemical quenching in Arabidopsis thaliana. Proc Natl Acad Sci USA 114:E7009–E7017. https://doi.org/10.1073/pnas.1704502114

    CAS  Article  PubMed  Google Scholar 

  35. 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. https://doi.org/10.1038/35000131

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Li X-P, 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. https://doi.org/10.1073/pnas.232447699

    CAS  Article  PubMed  Google Scholar 

  37. 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. https://doi.org/10.1074/jbc.M402461200

    CAS  Article  PubMed  Google Scholar 

  38. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260. https://doi.org/10.1146/annurev.arplant.58.032806.103844

    CAS  Article  PubMed  Google Scholar 

  39. Liao P-N, Holleboom C-P, Wilk L, Kühlbrandt W, Walla PJ (2010) 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. https://doi.org/10.1021/jp1034163

    CAS  Article  PubMed  Google Scholar 

  40. Liao P-N, Pillai S, Kloz M, Gust D, Moore AL, Moore TA, Kennis JTM, van Grondelle R, Walla PJ (2012) On the role of excitonic interactions in carotenoid-phthalocyanine dyads and implications for photosynthetic regulation. Photosynth Res 111:237–243. https://doi.org/10.1007/s11120-011-9690-9

    CAS  Article  PubMed  Google Scholar 

  41. Liguori N, Xu P, van Stokkum IHM, van Oort B, Lu Y, Karcher D, Bock R, Croce R (2017) Different carotenoid conformations have distinct functions in light-harvesting regulation in plants. Nat Commun 8:1994. https://doi.org/10.1038/s41467-017-02239-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Mascoli V, Liguori N, Xu P, Roy LM, van Stokkum IHM, Croce R (2019) Capturing the quenching mechanism of light-harvesting complexes of plants by zooming in on the ensemble. Chem. https://doi.org/10.1016/j.chempr.2019.08.002

    Article  Google Scholar 

  43. 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. https://doi.org/10.1016/j.febslet.2008.09.044

    CAS  Article  PubMed  Google Scholar 

  44. Mirkovic T, Ostroumov EE, Anna JM, van Grondelle R, Govindjee Scholes GD (2017) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117:249–293. https://doi.org/10.1021/acs.chemrev.6b00002

    CAS  Article  PubMed  Google Scholar 

  45. Mozzo M, Dall’Osto L, Hienerwadel R, Bassi R, Croce R (2008a) Photoprotection in the antenna complexes of photosystem II: role of individual xanthophylls in chlorophyll triplet quenching. J Biol Chem 283:6184–6192. https://doi.org/10.1074/jbc.M708961200

    CAS  Article  PubMed  Google Scholar 

  46. Mozzo M, Passarini F, Bassi R, van Amerongen H, Croce R (2008b) 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. https://doi.org/10.1016/j.bbabio.2008.04.036

    CAS  Article  PubMed  Google Scholar 

  47. Müh F, Lindorfer D, Am Schmidt Busch M, Renger T (2014) Towards a structure-based exciton Hamiltonian for the CP29 antenna of photosystem II. Phys Chem Chem Phys 16:11848–11863. https://doi.org/10.1039/c3cp55166k

    CAS  Article  PubMed  Google Scholar 

  48. Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:307–314. https://doi.org/10.1016/j.pbi.2013.03.011

    CAS  Article  PubMed  Google Scholar 

  49. Pan X, Li M, Wan T, Wang L, Jia C, Hou Z, Zhao X, Zhang J, Chang W (2011) Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat Struct Mol Biol 18:309–315. https://doi.org/10.1038/nsmb.2008

    CAS  Article  PubMed  Google Scholar 

  50. Pan X, Liu Z, Li M, Chang W (2013) Architecture and function of plant light-harvesting complexes II. Curr Opin Struct Biol 23:515–525. https://doi.org/10.1016/j.sbi.2013.04.004

    CAS  Article  PubMed  Google Scholar 

  51. Papageorgiou GC (2014) The non-photochemical quenching of the electronically excited state of chlorophyll a in plants: definitions, timelines, viewpoints, open questions. In: Demmig-Adams B, Garab G, Adams W III, Govindjee U (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Dordrecht

    Google Scholar 

  52. Park S, Fischer AL, Steen CJ, Iwai M, Morris JM, Walla PJ, Niyogi KK, Fleming GR (2018) Chlorophyll-carotenoid excitation energy transfer in high-light-exposed thylakoid membranes investigated by snapshot transient absorption spectroscopy. J Am Chem Soc 140:11965–11973. https://doi.org/10.1021/jacs.8b04844

    CAS  Article  PubMed  Google Scholar 

  53. Park S, Steen CJ, Lyska D, Fischer AL, Endelman B, Iwai M, Niyogi KK, Fleming GR (2019) Chlorophyll-carotenoid excitation energy transfer and charge transfer in nannochloropsis oceanica for the regulation of photosynthesis. Proc Natl Acad Sci USA 116:3385–3390. https://doi.org/10.1073/pnas.1819011116

    CAS  Article  PubMed  Google Scholar 

  54. Passarini F, Wientjes E, Hienerwadel R, Croce R (2009) Molecular basis of light harvesting and photoprotection in CP24: unique features of the most recent antenna complex. J Biol Chem 284:29536–29546. https://doi.org/10.1074/jbc.M109.036376

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Phillip D, Hobe S, Paulsen H, Molnar P, Hashimoto H, Young AJ (2002) The binding of xanthophylls to the bulk light-harvesting complex of photosystem II of higher plants. A specific requirement for carotenoids with a 3-hydroxy-beta-end group. J Biol Chem 277:25160–25169. https://doi.org/10.1074/jbc.M202002200

    CAS  Article  PubMed  Google Scholar 

  56. Rochaix J-D (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65:287–309. https://doi.org/10.1146/annurev-arplant-050213-040226

    CAS  Article  PubMed  Google Scholar 

  57. 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. https://doi.org/10.1038/nature06262

    CAS  Article  PubMed  Google Scholar 

  58. Shima S, Ilagan RP, Gillespie N, Sommer BJ, Hiller RG, Sharples FP, Frank HA, Birge RR (2003) Two-photon and fluorescence spectroscopy and the effect of environment on the photochemical properties of peridinin in solution and in the peridinin-chlorophyll-protein from Amphidinium carterae. J Phys Chem A 107:8052–8066. https://doi.org/10.1021/jp022648z

    CAS  Article  Google Scholar 

  59. Son M, Pinnola A, Bassi R, Schlau-Cohen GS (2019) The electronic structure of lutein 2 is optimized for light harvesting in plants. Chem 5:575–584. https://doi.org/10.1016/j.chempr.2018.12.016

    CAS  Article  Google Scholar 

  60. Staleva H, Komenda J, Shukla MK, Šlouf V, Kaňa R, Polívka T, Sobotka R (2015) Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat Chem Biol 11:287–291. https://doi.org/10.1038/nchembio.1755

    CAS  Article  PubMed  Google Scholar 

  61. Su X, Ma J, Wei X, Cao P, Zhu D, Chang W, Liu Z, Zhang X, Li M (2017) Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. Science 357:815–820. https://doi.org/10.1126/science.aan0327

    CAS  Article  PubMed  Google Scholar 

  62. Tietz S, Puthiyaveetil S, Enlow HM, Yarbrough R, Wood M, Semchonok DA, Lowry T, Li Z, Jahns P, Boekema EJ, Lenhert S, Niyogi KK, Kirchhoff H (2015) Functional implications of photosystem II crystal formation in photosynthetic membranes. J Biol Chem 290:14091–14106. https://doi.org/10.1074/jbc.M114.619841

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Tutkus M, Chmeliov J, Rutkauskas D, Ruban AV, Valkunas L (2017) Influence of the carotenoid composition on the conformational dynamics of photosynthetic light-harvesting complexes. J Phys Chem Lett 8:5898–5906. https://doi.org/10.1021/acs.jpclett.7b02634

    CAS  Article  PubMed  Google Scholar 

  64. 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. https://doi.org/10.1021/jp0028406

    CAS  Article  Google Scholar 

  65. 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. https://doi.org/10.1016/j.bpj.2009.11.012

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. van Oort B, van Grondelle R, van Stokkum Ivo H M (2015) A hidden state in light-harvesting complex II revealed by multipulse spectroscopy. J Phys Chem B 119:5184–5193. https://doi.org/10.1021/acs.jpcb.5b01335

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. Walla PJ, Linden PA, Hsu CP, Scholes GD, Fleming GR (2000a) Femtosecond dynamics of the forbidden carotenoid s1 state in light-harvesting complexes of purple bacteria observed after two-photon excitation. Proc Natl Acad Sci USA 97:10808–10813. https://doi.org/10.1073/pnas.190230097

    CAS  Article  PubMed  Google Scholar 

  68. Walla PJ, Yom J, Krueger BP, Fleming GR (2000b) Two-photon excitation spectrum of light-harvesting complex II and fluorescence upconversion after one- and two-photon excitation of the carotenoids. J Phys Chem B 104:4799–4806. https://doi.org/10.1021/jp9943023

    CAS  Article  Google Scholar 

  69. Walla PJ, Linden PA, Fleming GR (2001) Fs-transient absorption and fluorescence upconversion after two-photon excitation of carotenoids in solution and in LHC II. In: Schäfer FP, Toennies JP, Zinth W, Elsaesser T, Mukamel S, Murnane MM, Scherer NF (eds) Ultrafast phenomena XII. Springer, Berlin

    Google Scholar 

  70. Walla PJ, Linden PA, Ohta K, Fleming GR (2002) Excited-state kinetics of the carotenoid S 1 state in LHC II and two-photon excitation spectra of lutein and β-carotene in solution: efficient car S 1 - > Chl electronic energy transfer via hot S 1 states? J Phys Chem A 106:1909–1916. https://doi.org/10.1021/jp011495x

    CAS  Article  Google Scholar 

  71. Ware MA, Dall’Osto L, Ruban AV (2016) An in vivo quantitative comparison of photoprotection in Arabidopsis xanthophyll mutants. Front Plant Sci 7:841. https://doi.org/10.3389/fpls.2016.00841

    Article  PubMed  PubMed Central  Google Scholar 

  72. Wei X, Su X, Cao P, Liu X, Chang W, Li M, Zhang X, Liu Z (2016) Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution. Nature 534:69–74. https://doi.org/10.1038/nature18020

    CAS  Article  PubMed  Google Scholar 

  73. Xu P, Tian L, Kloz M, Croce R (2015) Molecular insights into zeaxanthin-dependent quenching in higher plants. Sci. Rep. 5:13679. https://doi.org/10.1038/srep13679

    Article  PubMed  PubMed Central  Google Scholar 

  74. Xu P, Roy LM, Croce R (2017) Functional organization of photosystem II antenna complexes. CP29 under the spotlight. Biochim Biophys Acta 1858:815–822. https://doi.org/10.1016/j.bbabio.2017.07.003

    CAS  Article  Google Scholar 

Download references

Funding

This work was supported by the German science foundation (DFG) under the Project Number 31763058.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Peter Jomo Walla.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 53 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gacek, D.A., Holleboom, CP., Liao, PN. et al. Carotenoid dark state to chlorophyll energy transfer in isolated light-harvesting complexes CP24 and CP29. Photosynth Res 143, 19–30 (2020). https://doi.org/10.1007/s11120-019-00676-z

Download citation

Keywords

  • CP24
  • CP29
  • Electronic coupling
  • Carotenoids
  • Chlorophylls
  • Photosynthetic regulation