Natural strategies for light harvesting in oxygenic photosynthesis: from excess light to shade
Mascoli, V.
2021
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Mascoli, V. (2021). Natural strategies for light harvesting in oxygenic photosynthesis: from excess light to shade.
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References
1. Kromdijk, J., Glowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K., and Long, S.P. (2016). Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857–861.
2. Gan, F., Zhang, S., Rockwell, N.C., Martin, S.S., Lagarias, J.C., and Bryant, D.A. (2014). Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345, 1312–1317.
3. Ruban, A. V. (2017). Crops on the fast track for light. Nature 541, 36–37. 4. Gan, F., and Bryant, D.A. (2015). Adaptive and acclimative responses of
cyanobacteria to far-red light. Environ. Microbiol. 17, 3450–3465.
5. Staehelin, L.A. (2003). Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth. Res. 76, 185–196. 6. Kirchhoff, H., Mukherjee, U., and Galla, H.J. (2002). Molecular architecture of the
thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41, 4872–4882.
7. Margulis, L. (1993). Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons (San Francisco: W.H. Freeman).
8. Blankenship, R.E. (2014). Molecular mechanisms of photosynthesis (Wiley-Blackwell).
9. Emerson, R., and Arnold, W. (1932). A separation of the reactions in
photosynthesis by means of intermittent light. J. Gen. Physiol. 15, 391–420. 10. Duysens, L.N.M. (1952). Transfer of excitation energy in photosynthesis. Dr.
Thesis.
11. Jansson, S. (1999). A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4, 236–240.
12. Glazer, A.N. (1984). Phycobilisome. A macromolecular complex optimized for light energy transfer. Biochim. Biophys. Acta 768, 29–51.
13. Murphy, D.J. (1986). The molecular organisation of the photosynthetic membranes of higher plants. Biochim. Biophys. Acta 864, 33–94.
14. Andersson, B., and Anderson, J.M. (1980). Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach
chloroplasts. Biochim. Biophys. Acta 593, 427–440.
15. Trissl, H.W., and Wilhelm, C. (1993). Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem. Sci. 18, 415–419.
16. Strašková, A., Steinbach, G., Konert, G., Kotabová, E., Komenda, J., Tichý, M., and Kaňa, R. (2019). Pigment-protein complexes are organized into stable microdomains in cyanobacterial thylakoids. Biochim. Biophys. Acta - Bioenerg.
1860, 148053.
17. Gouterman, M., Wagnière, G.H., and Snyder, L.C. (1963). Spectra of porphyrins. Part II. Four orbital model. J. Mol. Spectrosc. 11, 108–127.
18. Niedzwiedzki, D.M., Sullivan, J.O., Polívka, T., Birge, R.R., and Frank, H.A. (2006). Femtosecond time-resolved transient absorption spectroscopy of xanthophylls. J. Phys. Chem. B 110, 22872–22885.
276
19. Liguori, N., Xu, P., van Stokkum, I.H.M., van Oort, B., Lu, Y., Karcher, D., Bock, R., and Croce, R. (2017). Different carotenoid conformations have distinct
functions in light-harvesting regulation in plants. Nat. Commun. 8, 1994.
20. Gradinaru, C.C., Kennis, J.T.M., Papagiannakis, E., van Stokkum, I.H.M., Cogdell, R.J., Fleming, G.R., Niederman, R.A., and van Grondelle, R. (2001). An unusual pathway of excitation energy deactivation in carotenoids: singlet-to-triplet
conversion on an ultrafast timescale in a photosynthetic antenna. Proc. Natl. Acad. Sci. U. S. A. 98, 2364–2369.
21. Papagiannakis, E., Kennis, J.T.M., van Stokkum, I.H.M., Cogdell, R.J., and van Grondelle, R. (2002). An alternative carotenoid-to-bacteriochlorophyll energy transfer pathway in photosynthetic light harvesting. Proc. Natl. Acad. Sci. U. S. A.
99, 6017–6022.
22. Cohen-Bazire, G., Béguin, S., Rimon, S., Glazer, A.N., and Brown, D.M. (1977). Physico-chemical and immunological properties of allophycocyanins. Arch. Microbiol. 111, 225–238.
23. Miyashita, H., Ikemoto, H., Kurano, N., Adachi, K., Chihara, M., and Miyachi, S. (1996). Chlorophyll d as a major pigment. Nature 383, 402.
24. Chen, M., Schliep, M., Willows, R.D., Cai, Z.-L., Neilan, B.A., and Scheer, H. (2010). A red-shifted chlorophyll. Science 329, 1318–1319.
25. Chen, M. (2014). Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Annu. Rev. Biochem. 83, 317–340.
26. Zucchelli, G., Brogioli, D., Casazza, A.P., Garlaschi, F.M., and Jennings, R.C. (2007). Chlorophyll ring deformation modulates Qy electronic energy in
chlorophyll-protein complexes and generates spectral forms. Biophys. J. 93, 2240– 2254.
27. Krawczyk, S. (1989). The effects of hydrogen bonding and coordination interaction in visible absorption and vibrational spectra of chlorophyll a. Biochim. Biophys. Acta - Bioenerg. 976, 140–149.
28. Segatta, F., Cupellini, L., Garavelli, M., and Mennucci, B. (2019). Quantum chemical modeling of the photoinduced activity of multichromophoric biosystems. Chem. Rev. 119, 9361–9380.
29. van Amerongen, H., Valkunas, L., and van Grondelle, R. (2000). Photosynthetic excitons (Singapore: World Scientific Publishing).
30. Jabłoński, A. (1935). Über den mechanismus der photolumineszenz von farbstoffphosphoren. Zeitschrift für Phys. 94, 38–46.
31. Kasha, M. (1950). Characterization of electronic transitions in complex molecules. Discuss. Faraday Soc. 9, 14–19.
32. Shi, Y., Liu, J.Y., and Han, K.L. (2005). Investigation of the internal conversion time of the chlorophyll a from S3, S2 to S1. Chem. Phys. Lett. 410, 260–263. 33. Niedzwiedzki, D.M., and Blankenship, R.E. (2010). Singlet and triplet excited-state
properties of natural chlorophylls and bacteriochlorophylls. Photosynth. Res. 106, 227–238.
34. Niedzwiedzki, D.M., Liu, H., Chen, M., and Blankenship, R.E. (2014). Excited-state properties of chlorophyll f in organic solvents at ambient and cryogenic
277 temperatures. Photosynth. Res. 121, 25–34.
35. Björn, L.O., Papageorgiou, G.C., Blankenship, R.E., and Govindjee (2009). A viewpoint: why chlorophyll a? Photosynth. Res. 99, 85–98.
36. Ledermann, B., Aras, M., and Frankenberg-Dinkel, N. (2017). Biosynthesis of cyanobacterial light-harvesting pigments and their assembly into phycobiliproteins. In Modern Topics in the Phototrophic Prokaryotes, P. Hallenbeck, ed. (Springer, Cham), pp. 305–340.
37. Qin, X., Suga, M., Kuang, T., and Shen, J.R. (2015). Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348, 989–995. 38. Su, X., Ma, J., Wei, X., Cao, P., Zhu, D., Chang, W., Liu, Z., Zhang, X., and Li, M.
(2017). Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. Science 357, 815–820.
39. Polívka, T., and Sundström, V. (2004). Ultrafast dynamics of carotenoid excited states−from solution to natural and artificial systems. Chem. Rev. 104, 2021–2071. 40. Tavan, P., and Schulten, K. (1987). Electronic excitations in finite and infinite
polyenes. Phys. Rev. B 36, 4337–4358.
41. Ritz, T., Damjanović, A., and Schulten, K. (2002). The quantum physics of photosynthesis. ChemPhysChem 3, 243–248.
42. Frank, H.A., Cua, A., Chynwat, V., Young, A., Gosztola, D., and Wasielewski, M.R. (1994). Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis. Photosynth. Res. 41, 389–395.
43. Frank, H.A., Desamero, R.Z.B., Chynwat, V., Gebhard, R., van der Hoef, I., Jansen, F.J., Lugtenburg, J., Gosztola, D., and Wasielewski, M.R. (1997). Spectroscopic properties of spheroidene analogs having different extents of π-electron
conjugation. J. Phys. Chem. A 101, 149–157.
44. Andersson, P.O., Gillbro, T., Ferguson, L., and Cogdell, R.J. (1991). Absorption spectral shifts of carotenoids related to medium polarizability. Photochem. Photobiol. 54, 353–360.
45. Rätsep, M., Linnanto, J., and Freiberg, A. (2009). Mirror symmetry and vibrational structure in optical spectra of chlorophyll a. J. Chem. Phys. 130, 194501.
46. Polívka, T., Herek, J.L., Zigmantas, D., Åkerlund, H.E., and Sundström, V. (1999). Direct observation of the (forbidden) S1 state in carotenoids. Proc. Natl. Acad. Sci. U. S. A. 96, 4914–4917.
47. Polívka, T., and Sundström, V. (2009). Dark excited states of carotenoids : consensus and controversy. Chem. Phys. Lett. 477, 1–11.
48. Larsen, D.S., Papagiannakis, E., van Stokkum, I.H.M., Vengris, M., Kennis, J.T.M., and van Grondelle, R. (2003). Excited-state dynamics of β-carotene explored with dispersed multi-pulse transient absorption. Chem. Phys. Lett. 381, 733–742. 49. Niedzwiedzki, D., Koscielecki, J.F., Cong, H., Sullivan, J.O., Gibson, G.N., Birge,
R.R., and Frank, H.A. (2007). Ultrafast dynamics and excited state spectra of open-chain carotenoids at room and low temperatures. J. Phys. Chem. B 111, 5984–5998. 50. Cong, H., Niedzwiedzki, D.M., Gibson, G.N., and Frank, H.A. (2008). Ultrafast
time-resolved spectroscopy of xanthophylls at low temperature. J. Phys. Chem. B
278
51. Andersson, P.O., and Gillbro, T. (1995). Photophysics and dynamics of the lowest excited singlet state in long substituted polyenes with implications to the very long-chain limit. J. Chem. Phys. 103, 2509–2519.
52. Balevičius, V., Wei, T., Di Tommaso, D., Abramavicius, D., Hauer, J., Polívka, T., and Duffy, C.D.P. (2019). The full dynamics of energy relaxation in large organic molecules: from photo-excitation to solvent heating. Chem. Sci. 10, 4792–4804. 53. Kloz, M., Weissenborn, J., Polívka, T., Frank, H.A., and Kennis, J.T.M. (2016).
Spectral watermarking in femtosecond stimulated Raman spectroscopy: resolving the nature of the carotenoid S* state. Phys. Chem. Chem. Phys. 18, 14619–14628. 54. Siefermann-Harms, D. (1987). The light-harvesting and protective functions of
carotenoids in photosynthetic membranes. Physiol. Plant. 69, 561–568.
55. May, V., and Kühn, O. (2008). Charge and energy transfer dynamics in molecular systems (John Wiley & Sons).
56. Gilmore, A.M., Hazlett, T.L., and Govindjee (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. U. S. A. 92, 2273–2277.
57. Belgio, E., Johnson, M.P., Jurić, S., and Ruban, A. V. (2012). Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited-state lifetime - both the maximum and the nonphotochemically quenched. Biophys. J. 102, 2761–2771.
58. Tian, L., Dinc, E., and Croce, R. (2015). LHCII populations in different quenching states are present in the thylakoid membranes in a ratio that depends on the light conditions. J. Phys. Chem. Lett. 6, 2339–2344.
59. Redfield, A.G. (1957). On the theory of relaxation processes. IBM J. Res. Dev. 1, 19–31.
60. Yang, M., and Fleming, G.R. (2002). Influence of phonons on exciton transfer dynamics: comparison of the Redfield, Förster, and modified Redfield equations. Chem. Phys. 282, 163–180.
61. Ishizaki, A., and Tanimura, Y. (2005). Quantum dynamics of system strongly coupled to low-temperature colored noise bath: reduced hierarchy equations approach. J. Phys. Soc. Japan 74, 3131–3134.
62. Moix, J.M., Ma, J., and Cao, J. (2015). Förster resonance energy transfer,
absorption and emission spectra in multichromophoric systems. III. Exact stochastic path integral evaluation. J. Chem. Phys. 142, 94108.
63. Malý, P., and van Grondelle, R. (2018). Interplay of disorder and delocalization in photosynthetic light harvesting. Curr. Opin. Chem. Biol. 47, 1–6.
64. Novoderezhkin, V.I., and van Grondelle, R. (2017). Modeling of excitation dynamics in photosynthetic light-harvesting complexes: exact versus perturbative approaches. J. Phys. B At. Mol. Opt. Phys. 50, 124003.
65. Marcus, R.A., and Sutin, N. (1985). Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811, 265–322.
66. Moser, C.C., Keske, J.M., Warncke, K., Farid, R.S., and Dutton, P.L. (1992). Nature of biological electron transfer. Nature 355, 796–802.
279 67. Hoff, A.J., and Deisenhofer, J. (1997). Photophysics of photosynthesis. Structure
and spectroscopy of reaction centers of purple bacteria. Phys. Rep. 287, 1–247. 68. Croce, R., and van Amerongen, H. (2013). Light-harvesting in photosystem I.
Photosynth. Res. 116, 153–166.
69. van Amerongen, H., and Croce, R. (2013). Light harvesting in photosystem II. Photosynth. Res. 116, 251–263.
70. Renger, T. (2004). Theory of optical spectra involving charge transfer states: dynamic localization predicts a temperature dependent optical band shift. Phys. Rev. Lett. 93, 188101.
71. Mančal, T., Valkunas, L., and Fleming, G.R. (2006). Theory of exciton-charge transfer state coupled systems. Chem. Phys. Lett. 432, 301–305.
72. Miloslavina, Y., Wehner, A., Lambrev, P.H., Wientjes, E., Reus, M., Garab, G., Croce, R., and Holzwarth, A.R. (2008). Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett.
582, 3625–3631.
73. Romero, E., Mozzo, M., van Stokkum, I.H.M., Dekker, J.P., van Grondelle, R., and Croce, R. (2009). The origin of the low-energy form of photosystem I
light-harvesting complex Lhca4: mixing of the lowest exciton with a charge-transfer state. Biophys. J. 96, L35–L37.
74. Wahadoszamen, M., Berera, R., Ara, A.M., Romero, E., and 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.
75. Umena, Y., Kawakami, K., Shen, J.R., and Kamiya, N. (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55–60. 76. Shen, L., Huang, Z., Chang, S., Wang, W., Wang, J., Kuang, T., Han, G., Shen,
J.R., and Zhang, X. (2019). Structure of a C2S2M2N2-type PSII–LHCII
supercomplex from the green alga Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U. S. A. 116, 21246–21255.
77. Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W., and Krauß, N. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411, 909–917.
78. Shkuropatov, A.Y., Khatypov, R.A., Volshchukova, T.S., Shkuropatova, V.A., Owens, T.G., and Shuvalov, V.A. (1997). Spectral and photochemical properties of borohydride-treated D1-D2-cytochrome b-559 complex of photosystem II. FEBS Lett. 420, 171–174.
79. Shkuropatov, A.Y., Khatypov, R.A., Shkuropatova, V.A., Zvereva, M.G., Owens, T.G., and Shuvalov, V.A. (1999). Reaction centers of photosystem II with a chemically-modified pigment composition: exchange of pheophytins with 131-deoxo-131-hydroxy-pheophytin a. FEBS Lett. 450, 163–167.
80. Diner, B.A., and Rappaport, F. (2002). Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu. Rev. Plant Biol. 53, 551–580.
81. Cardona, T., Sedoud, A., Cox, N., and Rutherford, A.W. (2012). Charge separation in photosystem II: a comparative and evolutionary overview. Biochim. Biophys.
280
Acta - Bioenerg. 1817, 26–43.
82. Romero, E., Diner, B.A., Nixon, P.J., Coleman, W.J., Dekker, J.P., and van
Grondelle, R. (2012). Mixed exciton-charge-transfer states in photosystem II: Stark spectroscopy on site-directed mutants. Biophys. J. 103, 185–194.
83. Müh, F., Glöckner, C., Hellmich, J., and Zouni, A. (2012). Light-induced quinone reduction in photosystem II. Biochim. Biophys. Acta - Bioenerg. 1817, 44–65. 84. Styring, S., Sjöholm, J., and Mamedov, F. (2012). Two tyrosines that changed the
world: interfacing the oxidizing power of photochemistry to water splitting in photosystem II. Biochim. Biophys. Acta - Bioenerg. 1817, 76–87.
85. Müh, F., Madjet, M.E.A., and Renger, T. (2012). Structure-based simulation of linear optical spectra of the CP43 core antenna of photosystem II. Photosynth. Res.
111, 87–101.
86. Hall, J., Renger, T., Müh, F., Picorel, R., and Krausz, E. (2016). The lowest-energy chlorophyll of photosystem II is adjacent to the peripheral antenna: emitting states of CP47 assigned via circularly polarized luminescence. Biochim. Biophys. Acta - Bioenerg. 1857, 1580–1593.
87. Raszewski, G., and Renger, T. (2008). Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode? J. Am. Chem. Soc. 130, 4431–4446.
88. Schatz, G., Brock, H., and Holzwarth, A.R. (1988). Kinetic and energetic model for the primary processes in photosystem II. Biophys. J. 54, 397–405.
89. Vassiliev, S., Lee, C.I., Brudvig, G.W., and Bruce, D. (2002). Structure-based kinetic modeling of excited-state transfer and trapping in histidine-tagged photosystem II core complexes from Synechocystis. Biochemistry 41, 12236– 12243.
90. Miloslavina, Y., Szczepaniak, M., Müller, M.G., Sander, J., Nowaczyk, M., Rögner, M., and Holzwarth, A.R. (2006). Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study. Biochemistry 45, 2436–2442.
91. Tumino, G., Casazza, A.P., Engelmann, E., Garlaschi, F.M., Zucchelli, G., and Jennings, R.C. (2008). Fluorescence lifetime spectrum of the plant photosystem II core complex: photochemistry does not induce specific reaction center quenching. Biochemistry 47, 10449–10457.
92. Mazor, Y., Borovikova, A., Caspy, I., and Nelson, N. (2017). Structure of the plant photosystem I supercomplex at 2.6 Å resolution. Nat. Plants 3, 17014.
93. Suga, M., Ozawa, S.I., Yoshida-Motomura, K., Akita, F., Miyazaki, N., and
Takahashi, Y. (2019). Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I. Nat. Plants 5, 626–636.
94. Amunts, A., and Nelson, N. (2009). Plant photosystem I design in the light of evolution. Structure 17, 637–650.
95. Watanabe, M., Kubota, H., Wada, H., Narikawa, R., and Ikeuchi, M. (2011). Novel supercomplex organization of photosystem I in Anabaena and Cyanophora
paradoxa. Plant Cell Physiol. 52, 162–168.
281 Structure of the maize photosystem I supercomplex with light-harvesting
complexes I and II. Science 360, 1109–1113.
97. Guergova-Kuras, M., Boudreaux, B., Joliot, A., Joliot, P., and Redding, K. (2001). Evidence for two active branches for electron transfer in photosystem I. Proc. Natl. Acad. Sci. U. S. A. 98, 4437–4442.
98. Müller, M.G., Slavov, C., Luthra, R., Redding, K.E., and Holzwarth, A.R. (2010). Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center. Proc. Natl. Acad. Sci. U. S. A. 107, 4123–4128. 99. Golbeck, J.H. (2006). Photosystem I. The light driven plastocyanin-ferredoxin
oxidoreductase. In Advances in Photosynthesis and Respiration (Springer). 100. Cherepanov, D.A., Shelaev, I. V., Gostev, F.E., Mamedov, M.D., Petrova, A.A.,
Aybush, A. V., Shuvalov, V.A., Semenov, A.Y., and Nadtochenko, V.A. (2017). Mechanism of adiabatic primary electron transfer in photosystem I: femtosecond spectroscopy upon excitation of reaction center in the far-red edge of the Qy band. Biochim. Biophys. Acta - Bioenerg. 1858, 895–905.
101. Karapetyan, N. V., Holzwarth, A.R., and Rögner, M. (1999). The photosystem I trimer of cyanobacteria: molecular organization, excitation dynamics and
physiological significance. FEBS Lett. 460, 395–400.
102. Gobets, B., and van Grondelle, R. (2001). Energy transfer and trapping in photosystem I. Biochim. Biophys. Acta - Bioenerg. 1507, 80–99.
103. Trissl, H.W. (1993). Long-wavelength absorbing antenna pigments and
heterogeneous absorption bands concentrate excitons and increase absorption cross section. Photosynth. Res. 35, 247–263.
104. Rivadossi, A., Zucchelli, G., Garlaschi, F.M., and Jennings, R.C. (1999). The importance of PS I chlorophyll red forms in light-harvesting by leaves. Photosynth. Res. 60, 209–215.
105. Carbonera, D., Agostini, G., Morosinotto, T., and Bassi, R. (2005). Quenching of chlorophyll triplet states by carotenoids in reconstituted Lhca4 subunit of peripheral light-harvesting complex of photosystem I. Biochemistry 44, 8337–8346.
106. van Stokkum, I.H.M., Desquilbet, T.E., van der Weij-de Wit, C.D., Snellenburg, J.J., van Grondelle, R., Thomas, J.C., Dekker, J.P., and Robert, B. (2013). Energy transfer and trapping in red-chlorophyll-free photosystem I from Synechococcus WH 7803. J. Phys. Chem. B 117, 11176–11183.
107. Karapetyan, N. V., Dorra, D., Schweitzer, G., Bezsmertnaya, I.N., and Holzwarth, A.R. (1997). Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from the cyanobacterium Spirulina platensis. Biochemistry 36, 13830–13837.
108. Gobets, B., van Stokkum, I.H.M., Rögner, M., Kruip, J., Schlodder, E., Karapetyan, N. V., Dekker, J.P., and van Grondelle, R. (2001). Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model. Biophys. J. 81, 407–424.
109. Nelson, N. (2009). Plant photosystem I – the most efficient nano-photochemical machine. J. Nanosci. Nanotechnol. 9, 1709–1713.
282
In Light Harvesting in Photosynthesis (CRC Press), pp. 59–76.
111. Adamska, I. (1997). ELIPs - light-induced stress proteins. Physiol. Plant. 100, 794– 805.
112. Montané, M.H., and Kloppstech, K. (2000). The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene 258, 1–8.
113. Li, X.-P., Björkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S., and Niyogi, K.K. (2000). A pigment-binding protein essential for regulation of
photosynthetic light harvesting. Nature 403, 391–395.
114. Peers, G., Truong, T.B., Ostendorf, E., Busch, A., Elrad, D., Grossman, A.R., Hippler, M., and Niyogi, K.K. (2009). An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462, 518–521.
115. Wientjes, E., and Croce, R. (2011). The light-harvesting complexes of higher-plant Photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers. Biochem. J. 433, 477–485.
116. Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J., Gui, L., An, X., and Chang, W. (2004). Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428, 287–292.
117. Caffarri, S., Kouřil, R., Kereïche, S., Boekema, E.J., and Croce, R. (2009).
Functional architecture of higher plant photosystem II supercomplexes. EMBO J.
28, 3052–3063.
118. van Bezouwen, L.S., Caffarri, S., Kale, R.S., Kouřil, R., Thunnissen, A.-M.W.H., Oostergetel, G.T., and Boekema, E.J. (2017). Subunit and chlorophyll organization of the plant photosystem II supercomplex. Nat. Plants 3, 17080.
119. Elrad, D., and Grossman, A.R. (2004). A genome’s eye view of the light-harvesting polypeptides of Chlamydomonas reinhardtii. Curr. Genet. 45, 61–75.
120. Kouřil, R., Nosek, L., Bartoš, J., Boekema, E.J., and Ilík, P. (2016). Evolutionary loss of light-harvesting proteins Lhcb6 and Lhcb3 in major land plant groups - break-up of current dogma. New Phytol. 210, 808–814.
121. Caffarri, S., Broess, K., Croce, R., and van Amerongen, H. (2011). Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes. Biophys. J. 100, 2094–2103.
122. Vasil’ev, S., and Bruce, D. (1998). Nonphotochemical quenching of excitation energy in photosystem II. A picosecond time-resolved study of the low yield of chlorophyll a fluorescence induced by single-turnover flash in isolated spinach thylakoids. Biochemistry 37, 11046–11054.
123. van Oort, B., Alberts, M., De Bianchi, S., Dall’Osto, L., Bassi, R., Trinkunas, G., Croce, R., and van Amerongen, H. (2010). Effect of antenna-depletion in
photosystem II on excitation energy transfer in Arabidopsis thaliana. Biophys. J. 98, 922–931.
124. Wientjes, E., van Amerongen, H., and Croce, R. (2013). Quantum yield of charge separation in photosystem II: functional effect of changes in the antenna size upon light acclimation. J. Phys. Chem. B 117, 11200–11208.
283 The role of Lhca complexes in the supramolecular organization of higher plant photosystem I. J. Biol. Chem. 284, 7803–7810.
126. Ballottari, M., Dall’Osto, L., Morosinotto, T., and Bassi, R. (2007). Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J. Biol. Chem. 282, 8947–8958.
127. Wientjes, E., van Stokkum, I.H.M., van Amerongen, H., and Croce, R. (2011). The role of the individual Lhcas in photosystem I excitation energy trapping. Biophys. J.
101, 745–754.
128. Galka, P., Santabarbara, S., Khuong, T.T.H., Degand, H., Morsomme, P., Jennings, R.C., Boekema, E.J., and Caffarri, S. (2012). Functional analyses of the plant photosystem I-harvesting complex II supercomplex reveal that
light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24, 2963–2978.
129. Chukhutsina, V.U., Liu, X., Xu, P., and Croce, R. (2020). Light-harvesting complex II is an antenna of photosystem I in dark-adapted plants. Nat. Plants 6, 860–868. 130. Lemeille, S., and Rochaix, J.-D. (2010). State transitions at the crossroad of
thylakoid signalling pathways. Photosynth. Res. 106, 33–46.
131. Pan, X., Li, M., Wan, T., Wang, L., Jia, C., Hou, Z., Zhao, X., Zhang, J., and Chang, W. (2011). Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nat. Struct. Mol. Biol. 18, 309–315.
132. Dockter, C., Müller, A.H., Dietz, C., Volkov, A., Polyhach, Y., Jeschke, G., and Paulsen, H. (2012). Rigid core and flexible terminus. Structure of solubilized light-harvesting chlorophyll a/b complex (LHCII) measured by EPR. J. Biol. Chem. 287, 2915–2925.
133. Sunku, K., de Groot, H.J.M., and Pandit, A. (2013). Insights into the
photoprotective switch of the major light-harvesting complex II (LHCII). J. Biol. Chem. 288, 19796–19804.
134. Shabestari, M.H., Wolfs, C.J.A.M., Spruijt, R.B., van Amerongen, H., and Huber, M. (2014). Exploring the structure of the 100 amino-acid residue long N-terminus of the plant antenna protein CP29. Biophys. J. 106, 1349–1358.
135. Liguori, N., Periole, X., Marrink, S.J., and Croce, R. (2015). From light-harvesting to photoprotection: structural basis of the dynamic switch of the major antenna complex of plants (LHCII). Sci. Rep. 5, 15661.
136. Fristedt, R., Granath, P., and Vener, A. V. (2010). A protein phosphorylation threshold for functional stacking of plant photosynthetic membranes. PLoS One 5, e10963.
137. Hobe, S., Förster, R., Klingler, J., and Paulsen, H. (1995). N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the
trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34, 10224– 10228.
138. Albanese, P., Tamara, S., Saracco, G., Scheltema, R.A., and Pagliano, C. (2020). How paired PSII–LHCII supercomplexes mediate the stacking of plant thylakoid membranes unveiled by structural mass-spectrometry. Nat. Commun. 11, 1361. 139. Remelli, R., Varotto, C., Sandonà, D., Croce, R., and Bassi, R. (1999). Chlorophyll
284
binding to monomeric light-harvesting complex. J. Biol. Chem. 274, 33510–33521. 140. Bassi, R., Croce, R., Cugini, D., and Sandonà, D. (1999). Mutational analysis of a
higher plant antenna protein provides identification of chromophores bound into multiple sites. Proc. Natl. Acad. Sci. U. S. A. 96, 10056–10061.
141. Mozzo, M., Morosinotto, T., Bassi, R., and Croce, R. (2006). Probing the structure of Lhca3 by mutation analysis. Biochim. Biophys. Acta - Bioenerg. 1757, 1607– 1613.
142. Mozzo, M., Passarini, F., Bassi, R., van Amerongen, H., and 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 - Bioenerg. 1777, 1263–1267.
143. Ballottari, M., Mozzo, M., Croce, R., Morosinotto, T., and Bassi, R. (2009).
Occupancy and functional architecture of the pigment binding sites of photosystem II antenna complex Lhcb5. J. Biol. Chem. 284, 8103–8113.
144. Caffarri, S., Croce, R., Breton, J., and Bassi, R. (2001). The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. J. Biol. Chem. 276, 35924–35933.
145. Demmig-Adams, B., and Adams, W.W. (1996). The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci. 1, 21–26. 146. Xu, P., Tian, L., Kloz, M., and Croce, R. (2015). Molecular insights into
zeaxanthin-dependent quenching in higher plants. Sci. Rep. 5, 13679.
147. Croce, R., Weiss, S., and Bassi, R. (1999). Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J. Biol. Chem. 274, 29613–29623. 148. Son, M., Pinnola, A., and Schlau-Cohen, G.S. (2020). Zeaxanthin independence of
photophysics in light-harvesting complex II in a membrane environment. Biochim. Biophys. Acta - Bioenerg. 1861, 148115.
149. Caffarri, S., Passarini, F., Bassi, R., and 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.
150. Mozzo, M., Dall’Osto, L., Hienerwadel, R., Bassi, R., and Croce, R. (2008). Photoprotection in the antenna complexes of photosystem II. Role of individual xanthophylls in chlorophyll triplet quenching. J. Biol. Chem. 283, 6184–6192. 151. Ruban, A. V., Berera, R., Ilioaia, C., van Stokkum, I.H.M., Kennis, J.T.M., Pascal,
A.A., van Amerongen, H., Robert, B., Horton, P., and van Grondelle, R. (2007). Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450, 575–578.
152. Ahn, T.K., Avenson, T.J., Ballottari, M., Cheng, Y.-C., Niyogi, K.K., Bassi, R., and Fleming, G.R. (2008). Architecture of a charge-transfer state regulating light
harvesting in a plant antenna protein. Science 320, 794–797.
153. Mascoli, V., Liguori, N., Xu, P., Roy, L.M., van Stokkum, I.H.M., and Croce, R. (2019). Capturing the quenching mechanism of light-harvesting complexes of plants by zooming in on the ensemble. Chem 5, 1–13.
154. Croce, R., Morosinotto, T., Castelletti, S., Breton, J., and Bassi, R. (2002). The Lhca antenna complexes of higher plants photosystem I. Biochim. Biophys. Acta -
285 Bioenerg. 1556, 29–40.
155. Castelletti, S., Morosinotto, T., Robert, B., Caffarri, S., Bassi, R., and Croce, R. (2003). Recombinant Lhca2 and Lhca3 subunits of the photosystem I antenna system. Biochemistry 42, 4226–4234.
156. Jennings, R.C., Bassi, R., Garlaschi, F.M., Dainese, P., and Zucchelli, G. (1993). Distribution of the chlorophyll spectral forms in the chlorophyll-protein complexes of photosystem II antenna. Biochemistry 32, 3203–3210.
157. Nussberger, S., Dekker, J.P., Kühlbrandt, W., van Bolhuis, B., van Grondelle, R., and van Amerongen, H. (1994). Spectroscopic characterization of three different monomeric forms of the main chlorophyll a/b binding protein from chloroplast membranes. Biochemistry 33, 14775–14783.
158. Zhang, H., Goodman, H.M., and Jansson, S. (1997). Antisense inhibition of the photosystem I antenna protein Lhca4 in Arabidopsis thaliana. Plant Physiol. 115, 1525–1531.
159. Schmid, V.H.R., Cammarata, K. V., Bruns, B.U., and Schmidt, G.W. (1997). In vitro reconstitution of the photosystem I light-harvesting complex LHCI-730: heterodimerization is required for antenna pigment organization. Proc. Natl. Acad. Sci. U. S. A. 94, 7667–7672.
160. Morosinotto, T., Castelletti, S., Breton, J., Bassi, R., and Croce, R. (2002). Mutation analysis of Lhca1 antenna complex: low energy absorption forms originate from pigment-pigment interactions. J. Biol. Chem. 277, 36253–36261.
161. Croce, R., Morosinotto, T., Ihalainen, J.A., Chojnicka, A., Breton, J., Dekker, J.P., van Grondelle, R., and Bassi, R. (2004). Origin of the 701-nm fluorescence
emission of the Lhca2 subunit of higher plant photosystem I. J. Biol. Chem. 279, 48543–48549.
162. Morosinotto, T., Mozzo, M., Bassi, R., and Croce, R. (2005). Pigment-pigment interactions in Lhca4 antenna complex of higher plants photosystem I. J. Biol. Chem. 280, 20612–20619.
163. Krüger, T.P.J., Wientjes, E., Croce, R., and van Grondelle, R. (2011).
Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc. Natl. Acad. Sci. U. S. A. 108, 13516–13521. 164. Watanabe, M., and Ikeuchi, M. (2013). Phycobilisome: architecture of a
light-harvesting supercomplex. Photosynth. Res. 116, 265–276.
165. Bryant, D.A., and Canniffe, D.P. (2018). How nature designs light-harvesting antenna systems: design principles and functional realization in chlorophototrophic prokaryotes. J. Phys. B At. Mol. Opt. Phys. 51, 33001.
166. Sidler, W.A. (1994). Phycobilisome and phycobiliprotein structures. In The molecular biology of cyanobacteria (Dordrecht: Springer), pp. 139–216.
167. Glazer, A.N. (1989). Directional energy transfer in a photosynthetic antenna. J. Biol. Chem. 264, 1–4.
168. Dong, C., Tang, A., Zhao, J., Mullineaux, C.W., Shen, G., and Bryant, D.A. (2009). ApcD is necessary for efficient energy transfer from phycobilisomes to
photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002. Biochim. Biophys. Acta - Bioenerg. 1787, 1122–
286
1128.
169. Liu, H., Zhang, H., Niedzwiedzki, D.M., Prado, M., He, G., Gross, M.L., and Blankenship, R.E. (2013). Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342, 1104–1107.
170. Chukhutsina, V., Bersanini, L., Aro, E.M., and van Amerongen, H. (2015). Cyanobacterial light-harvesting phycobilisomes uncouple from photosystem I during dark-to-light transitions. Sci. Rep. 5, 14193.
171. Zhang, J., Ma, J., Liu, D., Qin, S., Sun, S., Zhao, J., and Sui, S.F. (2017). Structure of phycobilisome from the red alga Griffithsia pacifica. Nature 551, 57–63.
172. Ma, J., You, X., Sun, S., Wang, X., Qin, S., and Sui, S.F. (2020). Structural basis of energy transfer in Porphyridium purpureum phycobilisome. Nature 579, 146–151. 173. Krogmann, D.W., Pérez-Gómez, B., Gutiérrez-Cirlos, E.B., Chagolla-López, A.,
González de la Vara, L., and Gómez-Lojero, C. (2007). The presence of
multidomain linkers determines the bundle-shape structure of the phycobilisome of the cyanobacterium Gloeobacter violaceus PCC 7421. Photosynth. Res. 93, 27–43. 174. Rippka, R., Waterbury, J., and Cohen-Bazire, G. (1974). A cyanobacterium which
lacks thylakoids. Arch. Microbiol. 100, 419–436.
175. Watanabe, M., Semchonok, D.A., Webber-Birungi, M.T., Ehira, S., Kondo, K., Narikawa, R., Ohmori, M., Boekema, E.J., and Ikeuchi, M. (2014). Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria. Proc. Natl. Acad. Sci. U. S. A. 111, 2512–2517.
176. Marquardt, J., Senger, H., Miyashita, H., Miyachi, S., and Mörschel, E. (1997). Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett. 410, 428–432.
177. Arteni, A.A., Ajlani, G., and Boekema, E.J. (2009). Structural organisation of phycobilisomes from Synechocystis sp. strain PCC6803 and their interaction with the membrane. Biochim. Biophys. Acta - Bioenerg. 1787, 272–279.
178. Chang, L., Liu, X., Li, Y., Liu, C.C., Yang, F., Zhao, J., and Sui, S.F. (2015). Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res. 25, 726–737.
179. van Grondelle, R., Dekker, J.P., Gillbro, T., and Sundström, V. (1994). Energy transfer and trapping in photosynthesis. Biochim. Biophys. Acta 1187, 1–65.
180. Schirmer, T., Bode, W., and Huber, R. (1987). Refined three-dimensional structures of two cyanobacterial C-phycocyanins at 2.1 and 2.5 Å resolution. A common principle of phycobilin-protein interaction. J. Mol. Biol. 196, 677–695.
181. Anderson, L.K., and Toole, C.M. (1998). A model for early events in the assembly pathway of cyanobacterial phycobilisomes. Mol. Microbiol. 30, 467–474.
182. Reuter, W., Wiegand, G., Huber, R., and Than, M.E. (1999). Structural analysis at 2.2 Å of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, AP·LC7.8, from phycobilisomes of Mastigocladus laminosus. Proc. Natl. Acad. Sci. U. S. A. 96, 1363–1368.
183. Schirmer, T., Huber, R., Schneider, M., Bode, W., Miller, M., and Hackert, M.L. (1986). Crystal structure analysis and refinement at 2.5 Å of hexameric
C-287 phycocyanin from the cyanobacterium Agmenellum quadruplicatum. The molecular model and its implications for light-harvesting. J. Mol. Biol. 188, 651–676.
184. Gindt, Y.M., Zhou, J., Bryant, D.A., and Sauer, K. (1992). Core mutations of
Synechococcus sp. PCC 7002 phycobilisomes: a spectroscopic study. J. Photochem. Photobiol. B Biol. 15, 75–89.
185. Gindt, Y.M., Zhou, J., Bryant, D.A., and Sauer, K. (1994). Spectroscopic studies of phycobilisome subcore preparations lacking key core chromophores: assignment of excited-state energies to the Lcm, β18 and αAP-B chromophores. Biochim.
Biophys. Acta 1186, 153–162.
186. Zhao, J., Zhou, J., and Bryant, D.A. (1992). Energy transfer processes in
phycobilisomes as deduced from analyses of mutants of Synechococcus sp. PCC 7002. In Research in Photosynthesis, vol. 1, N. Murata, ed. (Dordrecht: Kluwer Academic Publisher), pp. 25–32.
187. Zlenko, D. V., Krasilnikov, P.M., and Stadnichuk, I.N. (2016). Structural modeling of the phycobilisome core and its association with the photosystems. Photosynth. Res. 130, 347–356.
188. van Stokkum, I.H.M., Gwizdala, M., Tian, L., Snellenburg, J.J., van Grondelle, R., van Amerongen, H., and Berera, R. (2018). A functional compartmental model of the Synechocystis PCC 6803 phycobilisome. Photosynth. Res. 135, 87–102. 189. Croce, R., and van Amerongen, H. (2014). Natural strategies for photosynthetic
light harvesting. Nat. Chem. Biol. 10, 492–501.
190. Long, S.P., Humphries, S., and Falkowski, P.G. (1994). Photoinhibition of
photosynthesis in nature. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 633–662. 191. Niyogi, K.K. (1999). Photoprotection revisited: genetic and molecular approaches.
Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333–359.
192. Mullineaux, C.W., Ruban, A. V., and Horton, P. (1994). Prompt heat release associated with ΔpH-dependent quenching in spinach thylakoid membranes. Biochim. Biophys. Acta 1185, 119–123.
193. Wraight, C.A., and Crofts, A.R. (1970). Energy-dependent quenching of
chlorophyll a fluorescence in isolated chloroplasts. Eur. J. Biochem. 17, 319–327. 194. Briantais, J.M., Vernotte, C., Picaud, M., and Krause, G.H. (1979). A quantitative
study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim. Biophys. Acta 548, 128–138.
195. Holzwarth, A.R., Miloslavina, Y., Nilkens, M., and 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.
196. Powles, S.B. (1984). Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol. 35, 15–44.
197. Greenberg, B.M., Gaba, V., Mattoo, A.K., and Edelman, M. (1987). Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kd protein of photosystem II. EMBO J. 6, 2865–2869.
198. Aro, E.M., Virgin, I., and Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113–134. 199. Ruban, A. V., Johnson, M.P., and Duffy, C.D.P. (2012). The photoprotective
288
molecular switch in the photosystem II antenna. Biochim. Biophys. Acta - Bioenerg. 1817, 167–181.
200. Müller, P., Li, X.P., and Niyogi, K.K. (2001). Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125, 1558–1566.
201. Horton, P., Ruban, A. V., Rees, D., Pascal, A.A., Noctor, G., and Young, A.J. (1991). Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett. 292, 1–4. 202. Briantais, J.M. (1994). Light-harvesting chlorophyll a-b complex requirement for
regulation of photosystem II photochemistry by non-photochemical quenching. Photosynth. Res. 40, 287–294.
203. Johnson, M.P., Goral, T.K., Duffy, C.D.P., Brain, A.P.R., Mullineaux, C.W., and Ruban, A. V. (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.
204. Dall’Osto, L., Cazzaniga, S., Bressan, M., Paleček, D., Židek, K., Niyogi, K.K., Fleming, G.R., Zigmantas, D., and Bassi, R. (2017). Two mechanisms for
dissipation of excess light in monomeric and trimeric light-harvesting complexes. Nat. Plants 3, 17033.
205. Havaux, M., Dall’Osto, L., and 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.
206. Nicol, L., Nawrocki, W.J., and Croce, R. (2019). Disentangling the sites of non-photochemical quenching in vascular plants. Nat. Plants 5, 1177–1183.
207. Avenson, T.J., Ahn, T.K., Zigmantas, D., Niyogi, K.K., Li, Z., Ballottari, M., Bassi, R., and Fleming, G.R. (2008). Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J. Biol. Chem. 283, 3550–3558. 208. de Bianchi, S., Betterle, N., Kouřil, R., Cazzaniga, S., Boekema, E., Bassi, R., and
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.
209. Li, X.P., Gilmore, A.M., Caffarri, S., Bassi, R., Golan, T., Kramer, D., and Niyogi, K.K. (2004). Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J. Biol. Chem. 279, 22866–22874.
210. Liguori, N., Campos, S.R.R., Baptista, A.M., and Croce, R. (2019). Molecular anatomy of plant photoprotective switches: the sensitivity of PsbS to the environment, residue by residue. J. Phys. Chem. Lett. 10, 1737–1742.
211. Dominici, P., Caffarri, S., Armenante, F., Ceoldo, S., Crimi, M., and Bassi, R. (2002). Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J. Biol. Chem. 277, 22750–22758.
212. Fan, M., Li, M., Liu, Z., Cao, P., Pan, X., Zhang, H., Zhao, X., Zhang, J., and Chang, W. (2015). Crystal structures of the PsbS protein essential for
photoprotection in plants. Nat. Struct. Mol. Biol. 22, 729–735.
289 and 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 - Bioenerg.
1797, 466–475.
214. Holt, N.E., Zigmantas, D., Valkunas, L., Li, X.-P., Niyogi, K.K., and Fleming, G.R. (2005). Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307, 433–436.
215. Kirilovsky, D., and Kerfeld, C.A. (2016). Cyanobacterial photoprotection by the orange carotenoid protein. Nat. Plants 2, 16180.
216. Calzadilla, P.I., and Kirilovsky, D. (2020). Revisiting cyanobacterial state transitions. Photochem. Photobiol. Sci. 19, 585–603.
217. Pascal, A.A., Liu, Z., Broess, K., van Oort, B., van Amerongen, H., Wang, C., Horton, P., Robert, B., Chang, W., and Ruban, A. (2005). Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436, 134– 137.
218. Valkunas, L., Chmeliov, J., Krüger, T.P.J., Ilioaia, C., and van Grondelle, R. (2012). How photosynthetic proteins switch. J. Phys. Chem. Lett. 3, 2779–2784. 219. Chmeliov, J., Trinkunas, G., van Amerongen, H., and Valkunas, L. (2014). Light
harvesting in a fluctuating antenna. J. Am. Chem. Soc. 136, 8963–8972. 220. Krüger, T.P.J., Ilioaia, C., Johnson, M.P., Ruban, A. V., and 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, 1027–1038.
221. Jurinovich, S., Viani, L., Prandi, I.G., Renger, T., and Mennucci, B. (2015).
Towards an ab initio description of the optical spectra of light-harvesting antennae: application to the CP29 complex of photosystem II. Phys. Chem. Chem. Phys. 17, 14405–14416.
222. Liguori, N., Roy, L.M., Opacic, M., Durand, G., and Croce, R. (2013). Regulation of light harvesting in the green alga Chlamydomonas reinhardtii: The C-terminus of LHCSR is the knob of a dimmer switch. J. Am. Chem. Soc. 135, 18339–18342. 223. Li, H., Wang, Y., Ye, M., Li, S., Li, D., Ren, H., Wang, M., Du, L., Li, H., Veglia,
G., et al. (2020). Dynamical and allosteric regulation of photoprotection in light harvesting complex II. Sci. China Chem. 63, 1121–1133.
224. Moya, I., Silvestri, M., Vallon, O., Cinque, G., and Bassi, R. (2001). Time-resolved fluorescence analysis of the photosystem II antenna proteins in detergent micelles and liposomes. Biochemistry 40, 12552–12561.
225. van Oort, B., van Hoek, A., Ruban, A. V., and van Amerongen, H. (2007).
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.
226. Natali, A., Gruber, J.M., Dietzel, L., Stuart, M.C.A., van Grondelle, R., and Croce, R. (2016). Light-harvesting complexes (LHCs) cluster spontaneously in membrane environment leading to shortening of their excited-state lifetimes. J. Biol. Chem.
290
227. Son, M., Pinnola, A., Gordon, S.C., Bassi, R., and Schlau-cohen, G.S. (2020). Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs. Nat. Commun. 11, 1295. 228. Krüger, T.P.J., Novoderezhkin, V.I., Ilioaia, C., and van Grondelle, R. (2010).
Fluorescence spectral dynamics of single LHCII trimers. Biophys. J. 98, 3093– 3101.
229. Schlau-Cohen, G.S., Yang, H.Y., Krüger, T.P.J., Xu, P., Gwizdala, M., van
Grondelle, R., Croce, R., and Moerner, W.E. (2015). Single-molecule identification of quenched and unquenched states of LHCII. J. Phys. Chem. Lett. 6, 860–867. 230. Cupellini, L., Bondanza, M., Nottoli, M., and Mennucci, B. (2020). Successes &
challenges in the atomistic modeling of light-harvesting and its photoregulation. Biochim. Biophys. Acta - Bioenerg. 1861, 148049.
231. Liguori, N., Croce, R., Marrink, S.J., and Thallmair, S. (2020). Molecular dynamics simulations in photosynthesis. Photosynth. Res. 144, 273–295.
232. Müller, M.G., Lambrev, P., Reus, M., Wientjes, E., Croce, R., and Holzwarth, A.R. (2010). Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids. ChemPhysChem 11, 1289–1296. 233. Passarini, F., Wientjes, E., van Amerongen, H., and Croce, R. (2010). Photosystem
I light-harvesting complex Lhca4 adopts multiple conformations: red forms and excited-state quenching are mutually exclusive. Biochim. Biophys. Acta - Bioenerg.
1797, 501–508.
234. Wientjes, E., Roest, G., and 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 - Bioenerg. 1817, 711–717.
235. van Oort, B., Roy, L.M., Xu, P., Lu, Y., Karcher, D., Bock, R., and Croce, R.
(2018). Revisiting the role of xanthophylls in nonphotochemical quenching. J. Phys. Chem. Lett. 9, 346–352.
236. de la Cruz Valbuena, G., Camargo, F.V.A., Borrego-Varillas, R., Perozeni, F., D’Andrea, C., Ballottari, M., and Cerullo, G. (2019). Molecular mechanisms of nonphotochemical quenching in the LHCSR3 protein of Chlamydomonas reinhardtii. J. Phys. Chem. Lett. 10, 2500–2505.
237. Cupellini, L., Calvani, D., Jacquemin, D., and Mennucci, B. (2020). Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants. Nat. Commun. 11, 662.
238. Staleva, H., Komenda, J., Shukla, M.K., Šlouf, V., Kaňa, R., Polívka, T., and
Sobotka, R. (2015). Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat. Chem. Biol. 11, 287–291.
239. Balevičius, V., Fox, K.F., Bricker, W.P., Jurinovich, S., Prandi, I.G., Mennucci, B., and Duffy, C.D.P. (2017). Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants. Sci. Rep. 7, 13956. 240. Fox, K.F., Ünlü, C., Balevičius, V., Ramdour, B.N., Kern, C., Pan, X., Li, M., van
Amerongen, H., and Duffy, C.D.P. (2018). A possible molecular basis for
photoprotection in the minor antenna proteins of plants. Biochim. Biophys. Acta - Bioenerg. 1859, 471–481.
291 241. Bode, S., Quentmeier, C.C., Liao, P.-N., Hafi, N., Barros, T., Wilk, L., Bittner, F.,
and Walla, P.J. (2009). On the regulation of photosynthesis by excitonic
interactions between carotenoids and chlorophylls. Proc. Natl. Acad. Sci. U. S. A.
106, 12311–12316.
242. Mullineaux, C.W., Pascal, A.A., Horton, P., and Holzwarth, A.R. (1993). Excitation-energy quenching in aggregates of the LHC II chlorophyll-protein complex: a time-resolved fluorescence study. Biochim. Biophys. Acta - Bioenerg.
1141, 23–28.
243. Vasil’ev, S., Irrgang, K.D., Schrötter, T., Bergmann, A., Eichler, H.J., and Renger, G. (1997). Quenching of chlorophyll a fluorescence in the aggregates of LHCII: steady state fluorescence and picosecond relaxation kinetics. Biochemistry 36, 7503–7512.
244. Ruban, A. V., Rees, D., Pascal, A.A., and Horton, P. (1992). Mechanism of ΔpH-dependent dissipation of absorbed excitation energy by photosynthetic membranes. II. The relationship between LHCII aggregation in vitro and qE in isolated
thylakoids. Biochim. Biophys. Acta 1102, 39–44.
245. Chmeliov, J., Gelzinis, A., Franckevičius, M., Tutkus, M., Saccon, F., Ruban, A. V., and Valkunas, L. (2019). Aggregation-related nonphotochemical quenching in the photosynthetic membrane. J. Phys. Chem. Lett. 10, 7340–7346.
246. Gaidukov, N. (1902). Uber den Einfluss farbigen Lichts auf die Färbung lebender Oscillarien. Königl. Akad. der Wissenschaften.
247. Kehoe, D.M., and Gutu, A. (2006). Responding to color: the regulation of complementary chromatic adaptation. Annu. Rev. Plant Biol. 57, 127–150. 248. Ho, M.-Y., Shen, G., Canniffe, D.P., Zhao, C., and Bryant, D.A. (2016).
Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353, aaf9178.
249. Trinugroho, J.P., Bečková, M., Shao, S., Yu, J., Zhao, Z., Murray, J.W., Sobotka, R., Komenda, J., and Nixon, P.J. (2020). Chlorophyll f synthesis by a super-rogue photosystem II complex. Nat. Plants 6, 238–244.
250. Bryant, D.A., Shen, G., Turner, G.M., Soulier, N., Laremore, T.N., and Ho, M.-Y. (2020). Far-red light allophycocyanin subunits play a role in chlorophyll d
accumulation in far-red light. Photosynth. Res. 143, 81–95.
251. Chen, M., Li, Y., Birch, D., and Willows, R.D. (2012). A cyanobacterium that contains chlorophyll f - a red-absorbing photopigment. FEBS Lett. 586, 3249–3254. 252. Ho, M.-Y., Soulier, N.T., Canniffe, D.P., Shen, G., and Bryant, D.A. (2017). Light
regulation of pigment and photosystem biosynthesis in cyanobacteria. Curr. Opin. Plant Biol. 37, 24–33.
253. Nürnberg, D.J., Morton, J., Santabarbara, S., Telfer, A., Joliot, P., Antonaru, L.A., Ruban, A. V., Cardona, T., Krausz, E., Boussac, A., et al. (2018). Photochemistry beyond the red limit in chlorophyll f-containing photosystems. Science 360, 1210– 1213.
254. Li, Y., Vella, N., and Chen, M. (2018). Characterization of isolated photosystem I from Halomicronema hongdechloris, a chlorophyll f-producing cyanobacterium. Photosynthetica 56, 306–315.
292
255. Kurashov, V., Ho, M.-Y., Shen, G., Piedl, K., Laremore, T.N., Bryant, D.A., and Golbeck, J.H. (2019). Energy transfer from chlorophyll f to the trapping center in naturally occurring and engineered photosystem I complexes. Photosynth. Res. 141, 151–163.
256. Kato, K., Shinoda, T., Nagao, R., Akimoto, S., Suzuki, T., Dohmae, N., Chen, M., Allakhverdiev, S.I., Shen, J.R., Akita, F., et al. (2020). Structural basis for the adaptation and function of chlorophyll f in photosystem I. Nat. Commun. 11, 238. 257. Gisriel, C., Shen, G., Kurashov, V., Ho, M.-Y., Zhang, S., Williams, D., Golbeck,
J.H., Fromme, P., and Bryant, D.A. (2020). The structure of photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis. Sci. Adv. 6, eaay6415.
258. Ho, M.-Y., Niedzwiedzki, D.M., MacGregor-Chatwin, C., Gerstenecker, G.,
Hunter, C.N., Blankenship, R.E., and Bryant, D.A. (2020). Extensive remodeling of the photosynthetic apparatus alters energy transfer among photosynthetic
complexes when cyanobacteria acclimate to far-red light. Biochim. Biophys. Acta - Bioenerg. 1861, 148064.
259. Li, Y., Lin, Y., Garvey, C.J., Birch, D., Corkery, R.W., Loughlin, P.C., Scheer, H., Willows, R.D., and Chen, M. (2016). Characterization of red-shifted
phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. Biochim. Biophys. Acta - Bioenerg. 1857, 107– 114.
260. Ho, M.-Y., Gan, F., Shen, G., and Bryant, D.A. (2017). Far-red light
photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335. II. Characterization of phycobiliproteins produced during acclimation to far-red light. Photosynth. Res.
131, 187–202.
261. Miao, D., Ding, W.L., Zhao, B.Q., Lu, L., Xu, Q.Z., Scheer, H., and Zhao, K.H. (2016). Adapting photosynthesis to the near-infrared: non-covalent binding of phycocyanobilin provides an extreme spectral red-shift to phycobilisome core-membrane linker from Synechococcus sp. PCC7335. Biochim. Biophys. Acta - Bioenerg. 1857, 688–694.
262. Soulier, N., Laremore, T.N., and Bryant, D.A. (2020). Characterization of cyanobacterial allophycocyanins absorbing far-red light. Photosynth. Res.
263. Mascoli, V., Bersanini, L., and Croce, R. (2020). Far-red absorption and light-use efficiency trade-offs in chlorophyll f photosynthesis. Nat. Plants 6, 1044–1053. 264. Wilhelm, C., and Jakob, T. (2006). Uphill energy transfer from long-wavelength
absorbing chlorophylls to PS II in Ostreobium sp. is functional in carbon assimilation. Photosynth. Res. 87, 323–329.
265. Kotabová, E., Jarešová, J., Kaňa, R., Sobotka, R., Bína, D., and Prášil, O. (2014). Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems. Biochim. Biophys. Acta - Bioenerg. 1837, 734–743.
266. Wolf, B.M., Niedzwiedzki, D.M., Magdaong, N.C.M., Roth, R., Goodenough, U., and Blankenship, R.E. (2018). Characterization of a newly isolated freshwater Eustigmatophyte alga capable of utilizing far-red light as its sole light source. Photosynth. Res. 135, 177–189.
293 267. Kosugi, M., Ozawa, S.I., Takahashi, Y., Kamei, Y., Itoh, S., Kudoh, S., Kashino,
Y., and Koike, H. (2020). Red-shifted chlorophyll a bands allow uphill energy transfer to photosystem II reaction centers in an aerial green alga, Prasiola crispa, harvested in Antarctica. Biochim. Biophys. Acta - Bioenerg. 1861, 148139. 268. Miyashita, H., Adachi, K., Kurano, N., Ikemoto, H., Chihara, M., and Miyachi, S.
(1997). Pigment composition of a novel oxygenic photosynthetic prokaryote
containing chlorophyll d as the major chlorophyll. Plant Cell Physiol. 38, 274–281. 269. Tomo, T., Kato, Y., Suzuki, T., Akimoto, S., Okubo, T., Noguchi, T., Hasegawa,
K., Tsuchiya, T., Tanaka, K., Fukuya, M., et al. (2008). Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated
cyanobacterium Acaryochloris marina MBIC 11017. J. Biol. Chem. 283, 18198– 18209.
270. Renger, T., and Schlodder, E. (2008). The primary electron donor of photosystem II of the cyanobacterium Acaryochloris marina is a chlorophyll d and the water
oxidation is driven by a chlorophyll a/chlorophyll d heterodimer. J. Phys. Chem. B
112, 7351–7354.
271. Rochaix, J.-D. (2014). Regulation and dynamics of the light-harvesting system. Annu. Rev. Plant Biol. 65, 287–309.
272. Ballottari, M., Girardon, J., Dall’Osto, L., and Bassi, R. (2012). Evolution and functional properties of photosystem II light harvesting complexes in eukaryotes. Biochim. Biophys. Acta - Bioenerg. 1817, 143–157.
273. Hobe, S., Niemeier, H., Bender, A., and Paulsen, H. (2000). Carotenoid binding sites in LHCIIb. Relative affinities towards major xanthophylls of higher plants. Eur. J. Biochem. 267, 616–624.
274. Hobe, S., Fey, H., Rogl, H., and Paulsen, H. (2003). Determination of relative chlorophyll binding affinities in the major light-harvesting chlorophyll a/b complex. J. Biol. Chem. 278, 5912–5919.
275. Novoderezhkin, V.I., Palacios, M.A., van Amerongen, H., and van Grondelle, R. (2005). Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Å crystal structure. J. Phys. Chem. B 109, 10493–10504. 276. Müh, F., Lindorfer, D., Schmidt am Busch, M., and Renger, T. (2014). Towards a
structure-based exciton Hamiltonian for the CP29 antenna of photosystem II. Phys. Chem. Chem. Phys. 16, 11848–11863.
277. Chmeliov, J., Gelzinis, A., Songaila, E., Augulis, R., Duffy, C.D.P., Ruban, A. V., and Valkunas, L. (2016). The nature of self-regulation in photosynthetic light-harvesting antenna. Nat. Plants 2, 16045.
278. Wei, X., Su, X., Cao, P., Liu, X., Chang, W., Li, M., Zhang, X., and Liu, Z. (2016). Structure of spinach photosystem II – LHCII supercomplex at 3.2 Å resolution. Nature 534, 69–74.
279. Croce, R., Müller, M.G., Bassi, R., and Holzwarth, A.R. (2003). Chlorophyll b to chlorophyll a energy transfer kinetics in the CP29 antenna complex: a comparative femtosecond absorption study between native and reconstituted proteins. Biophys. J. 84, 2508–2516.
280. Salverda, J.M., Vengris, M., Krueger, B.P., Scholes, G.D., Czarnoleski, A.R., Novoderezhkin, V., van Amerongen, H., and van Grondelle, R. (2003). Energy
294
transfer in light-harvesting complexes LHCII and CP29 of spinach studied with three pulse echo peak shift and transient grating. Biophys. J. 84, 450–465. 281. Feng, X., Pan, X., Li, M., Pieper, J., Chang, W., and Jankowiak, R. (2013).
Spectroscopic study of the light-harvesting CP29 antenna complex of photosystem II-Part I. J. Phys. Chem. B 117, 6585–6592.
282. Gradinaru, C.C., van Stokkum, I.H.M., Pascal, A.A., van Grondelle, R., and 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.
283. Novoderezhkin, V., Marin, A., and van Grondelle, R. (2011). Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield-Förster picture. Phys. Chem. Chem. Phys. 13, 17093–17103.
284. Feng, X., Kell, A., Pieper, J., and Jankowiak, R. (2013). Modeling of optical spectra of the light-harvesting CP29 antenna complex of photosystem II-Part II. J. Phys. Chem. B 117, 6593–6602.
285. Georgakopoulou, S., van der Zwan, G., Bassi, R., van Grondelle, R., van
Amerongen, H., and Croce, R. (2007). Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization. Biochemistry 46, 4745–4754.
286. Müh, F., and Renger, T. (2012). Refined structure-based simulation of plant light-harvesting complex II: linear optical spectra of trimers and aggregates. Biochim. Biophys. Acta - Bioenerg. 1817, 1446–1460.
287. Schlau-Cohen, G.S., Calhoun, T.R., Ginsberg, N.S., Ballottari, M., Bassi, R., and Fleming, G.R. (2010). Spectroscopic elucidation of uncoupled transition energies in the major photosynthetic light-harvesting complex, LHCII. Proc. Natl. Acad. Sci. U. S. A. 107, 13276–13281.
288. Xu, P., Roy, L.M., and Croce, R. (2017). Functional organization of photosystem II antenna complexes: CP29 under the spotlight. Biochim. Biophys. Acta - Bioenerg.
1858, 815–822.
289. Miloslavina, Y., de Bianchi, S., Dall’Osto, L., Bassi, R., and Holzwarth, A.R. (2011). Quenching in Arabidopsis thaliana mutants lacking monomeric antenna proteins of photosystem II. J. Biol. Chem. 286, 36830–36840.
290. Sandonà, D., Croce, R., Pagano, A., Crimi, M., and Bassi, R. (1998). Higher plants light harvesting proteins. Structure and function as revealed by mutation analysis of either protein or chromophore moieties. Biochim. Biophys. Acta - Bioenerg. 1365, 207–214.
291. Breton, J., Michel-Villaz, M., and Paillotin, G. (1973). Orientation of pigments and structural proteins in the photosynthetic membrane of spinach chloroplasts: a linear dichroism study. Biochim. Biophys. Acta 314, 42–56.
292. Haworth, P., Tapie, P., Arntzen, C.J., and Breton, J. (1982). Orientation of pigments in the thylakoid membrane and in isolated chlorophyll-protein complexes of higher plants. Biochim. Biophys. Acta 682, 152–159.
293. van Stokkum, I.H.M., Larsen, D.S., and van Grondelle, R. (2004). Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta - Bioenerg. 1657, 82– 104.
295 294. Novoderezhkin, V.I., Croce, R., Wahadoszamen, M., Polukhina, I., Romero, E., and
van Grondelle, R. (2016). Mixing of exciton and charge-transfer states in light-harvesting complex Lhca4. Phys. Chem. Chem. Phys. 18, 19368–19377.
295. Novoderezhkin, V.I., Palacios, M.A., van Amerongen, H., and van Grondelle, R. (2004). Energy-transfer dynamics in the LHCII complex of higher plants: modified Redfield approach. J. Phys. Chem. B 108, 10363–10375.
296. Ramanan, C., Gruber, J.M., Malý, P., Negretti, M., Novoderezhkin, V., Krüger, T.P.J., Mančal, T., Croce, R., and van Grondelle, R. (2015). The role of exciton delocalization in the major photosynthetic light-harvesting antenna of plants. Biophys. J. 108, 1047–1056.
297. Liguori, N., Novoderezhkin, V., Roy, L.M., van Grondelle, R., and Croce, R.
(2016). Excitation dynamics and structural implication of the stress-related complex LHCSR3 from the green alga Chlamydomonas reinhardtii. Biochim. Biophys. Acta - Bioenerg. 1857, 1514–1523.
298. Raszewski, G., Saenger, W., and Renger, T. (2005). Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor. Biophys. J. 88, 986–998.
299. Marin, A., Passarini, F., Croce, R., and van Grondelle, R. (2010). Energy transfer pathways in the CP24 and CP26 antenna complexes of higher plant photosystem II: a comparative study. Biophys. J. 99, 4056–4065.
300. Kreisbeck, C., and Aspuru-Guzik, A. (2016). Efficiency of energy funneling in the photosystem II supercomplex of higher plants. Chem. Sci. 7, 4174–4183.
301. Broess, K., Trinkunas, G., van Hoek, A., Croce, R., and van Amerongen, H. (2008). Determination of the excitation migration time in photosystem II. Biochim.
Biophys. Acta - Bioenerg. 1777, 404–409.
302. Bennett, D.I.G., Amarnath, K., and Fleming, G.R. (2013). A structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes. J. Am. Chem. Soc. 135, 9164–9173.
303. Tian, L., van Stokkum, I.H.M., Koehorst, R.B.M., Jongerius, A., Kirilovsky, D., and van Amerongen, H. (2011). Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J. Am. Chem. Soc. 133, 18304–18311.
304. Jennings, R.C., Garlaschi, F.M., Bassi, R., Zucchelli, G., Vianelli, A., and Dainese, P. (1993). A study of photosystem II fluorescence emission in terms of the antenna chlorophyll-protein complexes. Biochim. Biophys. Acta - Bioenerg. 1183, 194–200. 305. Li, X.-P., Müller-Moulé, P., Gilmore, A.M., and Niyogi, K.K. (2002).
PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl. Acad. Sci. U. S. A. 99, 15222–15227.
306. Barzda, V., Gulbinas, V., Kananavicius, R., Cervinskas, V., van Amerongen, H., van Grondelle, R., and Valkunas, L. (2001). Singlet-singlet annihilation kinetics in aggregates and trimers of LHCII. Biophys. J. 80, 2409–2421.
307. van Oort, B., van Hoek, A., Ruban, A. V., and van Amerongen, H. (2007).
Aggregation of light-harvesting complex II leads to formation of efficient excitation energy traps in monomeric and trimeric complexes. FEBS Lett. 581, 3528–3532. 308. Ruban, A. V., and Horton, P. (1992). Mechanism of ΔpH-dependent dissipation of
296
absorbed excitation energy by photosynthetic membranes. I. Spectroscopic analysis of isolated light-harvesting complexes. Biochim. Biophys. Acta 1102, 30–38. 309. Horton, P., Wentworth, M., and Ruban, A. V. (2005). Control of the light
harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett. 579, 4201–4206.
310. Ilioaia, C., Johnson, M.P., Horton, P., and Ruban, A. V. (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.
311. Dolganov, N.A., Bhaya, D., and Grossman, A.R. (1995). Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc. Natl. Acad. Sci. U. S. A. 92, 636–640.
312. van Oort, B., Amunts, A., Borst, J.W., van Hoek, A., Nelson, N., van Amerongen, H., and Croce, R. (2008). Picosecond fluorescence of intact and dissolved PSI-LHCI crystals. Biophys. J. 95, 5851–5861.
313. Farooq, S., Chmeliov, J., Wientjes, E., Koehorst, R., Bader, A., Valkunas, L., Trinkunas, G., and van Amerongen, H. (2018). Dynamic feedback of the
photosystem II reaction centre on photoprotection in plants. Nat. Plants 4, 225–231. 314. Kondo, T., Pinnola, A., Chen, W.J., Dall’Osto, L., Bassi, R., and Schlau-Cohen,
G.S. (2017). Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection. Nat. Chem. 9, 772–778.
315. Gruber, J.M., Xu, P., Chmeliov, J., Krüger, T.P.J., Alexandre, M.T.A., Valkunas, L., Croce, R., and van Grondelle, R. (2016). Dynamic quenching in single
photosystem II supercomplexes. Phys. Chem. Chem. Phys. 18, 25852–25860. 316. Akhtar, P., Görföl, F., Garab, G., and Lambrev, P.H. (2019). Dependence of
chlorophyll fluorescence quenching on the lipid-to-protein ratio in reconstituted light-harvesting complex II membranes containing lipid labels. Chem. Phys. 522, 242–248.
317. Gruber, J.M., Scheidelaar, S., van Roon, H., Dekker, J.P., Killian, J.A., and van Grondelle, R. (2016). Photophysics in single light-harvesting complexes II: from micelle to native nanodisks. Proc. Single Mol. Spectrosc. Superresolution Imaging IX 9714.
318. Berera, R., van Grondelle, R., and Kennis, J.T.M. (2009). Ultrafast transient absorption spectroscopy: principles and application to photosynthetic systems. Photosynth. Res. 101, 105–118.
319. Croce, R., Müller, M.G., Caffarri, S., Bassi, R., and Holzwarth, A.R. (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, 2517–32.
320. Papagiannakis, E., Das, S.K., Gall, A., van Stokkum, I.H.M., Robert, B., van Grondelle, R., Frank, H.A., and Kennis, J.T.M. (2003). Light harvesting by
carotenoids incorporated into the B850 light-harvesting complex from Rhodobacter sphaeroides R-26.1: excited-state relaxation, ultrafast triplet formation, and energy transfer to bacteriochlorophyll. J. Phys. Chem. B 107, 5642–5649.
