Abstract
Major light-harvesting complex of photosystem II (LHCII) plays a dual role in light-harvesting and excited energy dissipation to protect photodamage from excess energy. The regulatory switch is induced by increased acidity, temperature or both. However, the molecular origin of the protein dynamics at the atomic level is still unknown. We carried out temperature-jump time-resolved infrared spectroscopy and molecular dynamics simulations to determine the energy quenching dynamics and conformational changes of LHCII trimers. We found that the spontaneous formation of a pair of local α-helices from the 310-helix E/loop and the C-terminal coil of the neighboring monomer, in response to the increased environmental temperature and/or acidity, induces a scissoring motion of transmembrane helices A and B, shifting the conformational equilibrium to a more open state, with an increased angle between the associated carotenoids. The dynamical and allosteric conformation change leads to close contacts between carotenoid lutein 1 and chlorophyll pigment 612, facilitating the fluorescence quenching. Based on these results, we suggest a unified mechanism by which the LHCII trimer controls the dissipation of excess excited energy in response to increased temperature and acidity, as an intrinsic result of intense sun light in plant photosynthesis.
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Demmig-Adams B, Garab G, Adams W III, Govindjee. Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. In: Govindjee, Sharkey TD, Eds. Advances in Photosynthesis and Respiration Including Bioenergy and Related Processes. Vol 40. The Netherlands: Springer Science & Business Media, 2014
Rochaix JD. Annu Rev Plant Biol, 2014, 65: 287–309
Ruban AV. FEBS Lett, 2018, 592: 3030–3039
Müller P, Li XP, Niyogi KK. Plant Physiol, 2001, 125: 1558–1566
Nicol L, Nawrocki WJ, Croce R. Nat Plants, 2019, 5: 1177–1183
Croce R, van Amerongen H. Nat Chem Biol, 2014, 10: 492–501
Külheim C, Agren J, Jansson S. Science, 2002, 297: 91–93
Tian L, Nawrocki WJ, Liu X, Polukhina I, van Stokkum IHM, Croce R. Proc Natl Acad Sci USA, 2019, 116: 8320–8325
Miloslavina Y, Wehner A, Lambrev PH, Wientjes E, Reus M, Garab G, Croce R, Holzwarth AR. FEBS Lett, 2008, 582: 3625–3631
Correa-Galvis V, Poschmann G, Melzer M, Stühler K, Jahns P. Nat Plants, 2016, 2: 15225
Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P. Chem Phys Lett, 2009, 483: 262–267
Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP. Science, 2016, 354: 857–861
Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R, Croce R, Hanson MR, Hibberd JM, Long SP, Moore TA, Moroney J, Niyogi KK, Parry MAJ, Peralta-Yahya PP, Prince RC, Redding KE, Spalding MH, van Wijk KJ, Vermaas WFJ, von Caemmerer S, Weber APM, Yeates TO, Yuan JS, Zhu XG. Proc Natl Acad Sci USA, 2015, 112: 8529–8536
Engel GS, Calhoun TR, Read EL, Ahn TK, Mancal T, Cheng YC, Blankenship RE, Fleming GR. Nature, 2007, 446: 782–786
Arsenault EA, Yoneda Y, Iwai M, Niyogi KK, Fleming GR. Nat Commun, 2020, 11: 1460
Pinnola A, Bassi R. Biochem Soc Trans, 2018, 46: 467–482
Ruban AV, Johnson MP, Duffy CDP. Biochim Biophysica Acta (BBA), 2012, 1817: 167–181
Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W. Nature, 2004, 428: 287–292
Kühlbrandt W, Wang DN, Fujiyoshi Y. Nature, 1994, 367: 614–621
Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M, Kühlbrandt W. EMBO J, 2005, 24: 919–928
Caffarri S, Kouril R, Kereïche S, Boekema EJ, Croce R. EMBO J, 2009, 28: 3052–3063
Wei X, Su X, Cao P, Liu X, Chang W, Li M, Zhang X, Liu Z. Nature, 2016, 534: 69–74
Sunku K, de Groot HJM, Pandit A. J Biol Chem, 2013, 288: 19796–19804
Yang C, Lambrev P, Chen Z, Jávorfi T, Kiss AZ, Paulsen H, Garab G. Biochim Biophysica Acta (BBA), 2008, 1777: 1463–1470
Pascal AA, Liu Z, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang W, Ruban A. Nature, 2005, 436: 134–137
Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R. Nature, 2007, 450: 575–578
Bode S, Quentmeier CC, Liao PN, Barros T, Walla PJ. Chem Phys Lett, 2008, 450: 379–385
Liao PN, Bode S, Wilk L, Hafi N, Walla PJ. Chem Phys, 2010, 373: 50–55
Liao PN, Pillai S, Gust D, Moore TA, Moore AL, Walla PJ. J Phys Chem A, 2011, 115: 4082–4091
Holleboom CP, Walla PJ. Photosynth Res, 2014, 119: 215–221
Bode S, Quentmeier CC, Liao PN, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ. Proc Natl Acad Sci USA, 2009, 106: 12311–12316
Valkunas L, Chmeliov J, Krüger TPJ, Ilioaia C, van Grondelle R. J Phys Chem Lett, 2012, 3: 2779–2784
Daskalakis V, Maity S, Hart CL, Stergiannakos T, Duffy CDP, Kleinekathöfer U. J Phys Chem B, 2019, 123: 9609–9615
Ilioaia C, Johnson MP, Horton P, Ruban AV. J Biol Chem, 2008, 283: 29505–29512
Schlau-Cohen GS, Yang HY, Krüger TPJ, Xu P, Gwizdala M, van Grondelle R, Croce R, Moerner WE. J Phys Chem Lett, 2015, 6: 860–867
Tang Y, Wen X, Lu Q, Yang Z, Cheng Z, Lu C. Plant Physiol, 2007, 143: 629–638
Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR. Science, 2005, 307: 433–436
Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR. Science, 2008, 320: 794–797
Amarie S, Wilk L, Barros T, Kühlbrandt W, Dreuw A, Wachtveitl J. Biochim Biophysica Acta (BBA), 2009, 1787: 747–752
Park S, Steen CJ, Fischer AL, Fleming GR. Photosynth Res, 2019, 141: 367–376
Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, Bassi R, Fleming GR. J Biol Chem, 2008, 283: 3550–3558
Miloslavina Y, de Bianchi S, Dall’Osto L, Bassi R, Holzwarth AR. J Biol Chem, 2011, 286: 36830–36840
Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwarth AR, Jahns P. Biochim Biophysica Acta (BBA), 2010, 1797: 466–475
Ansari AQ, Loomis WE. Am J Bot, 1959, 46: 713–717
Pereira AB, Villa Nova NA, Galvani E. Biosyst Eng, 2003, 86: 27–34
Ruban AV, Pesaresi P, Wacker U, Irrgang KDJ, Bassi R, Horton P. Biochemistry, 1998, 37: 11586–11591
Zhou R, Chen W, Jiang X, Wang S, Gong Q. Appl Phys Lett, 2010, 96: 133309
Li D, Li Y, Li H, Wu X, Yu Q, Weng Y. Rev Sci Instrum, 2015, 86: 053105
Wu EL, Cheng X, Jo S, Rui H, Song KC, Dávila-Contreras EM, Qi Y, Lee J, Monje-Galvan V, Venable RM, Klauda JB, Im W. J Comput Chem, 2014, 35: 1997–2004
Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. J Chem Phys, 1983, 79: 926–935
Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang J, Kollman P. J Comput Chem, 2003, 24: 1999–2012
Zhang L, Silva DA, Yan YJ, Huang X. J Comput Chem, 2012, 33: 1969–1980
Wang J, Wang W, Kollman PA, Case DA. J Mol Graph, 2006, 25: 247–260
Hess B, Kutzner C, van der Spoel D, Lindahl E. J Chem Theor Comput, 2008, 4: 435–447
Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. J Comput Chem, 1997, 18: 1463–1472
Darden T, York D, Pedersen L. J Chem Phys, 1993, 98: 10089–10092
Parrinello M, Rahman A. Phys Rev Lett, 1980, 45: 1196–1199
Bowman GR, Ensign DL, Pande VS. J Chem Theor Comput, 2010, 6: 787–794
Wentworth M, Ruban AV, Horton P. J Biol Chem, 2003, 278: 21845–21850
van Oort B, van Hoek A, Ruban AV, van Amerongen H. J Phys Chem B, 2007, 111: 7631–7637
Santabarbara S, Horton P, Ruban AV. Biophys J, 2009, 97: 1188–1197
Krause GH. Photosynthetica, 1992, 27: 249–252
Ren H, Provorse MR, Bao P, Qu Z, Gao J. J Phys Chem Lett, 2016, 7: 2286–2293
Gao J, Grofe A, Ren H, Bao P. J Phys Chem Lett, 2016, 7: 5143–5149
Dockter C, Müller AH, Dietz C, Volkov A, Polyhach Y, Jeschke G, Paulsen H. J Biol Chem, 2012, 287: 2915–2925
Zhang Y, Li B, Xu Y, Li H, Li S, Zhang D, Mao Z, Guo S, Yang C, Weng Y, Chong K. Plant Cell, 2013, 25: 2504–2521
Li S, Wang R, Li D, Ma J, Li H, He X, Chang Z, Weng Y. Sci Rep, 2014, 4: 4834
Liu C, Rao Y, Zhang L, Yang C. J Biochem, 2014, 156: 203–210
Kuttkat A, Hartmann A, Hobe S, Paulsen H. Eur J Biochem, 1996, 242: 288–292
Belgio E, Duffy CDP, Ruban AV. Phys Chem Chem Phys, 2013, 15: 12253–12261
Yan H, Zhang P, Wang C, Liu Z, Chang W. Biochem Biophys Res Commun, 2007, 355: 457–463
Jas GS, Kuczera K. Biophys J, 2004, 87: 3786–3798
Seelig J, Schönfeld HJ. Quart Rev Biophys, 2016, 49: e9
Marqusee S, Robbins VH, Baldwin RL. Proc Natl Acad Sci USA, 1989, 86: 5286–5290
Polívka T, Zigmantas D, Sundström V, Formaggio E, Cinque G, Bassi R. Biochemistry, 2002, 41: 439–450
Mascoli V, Liguori N, Xu P, Roy LM, van Stokkum IHM, Croce R. Chem, 2019, 5: 2900–2912
Wehling A, Walla PJ. Photosynth Res, 2006, 90: 101–110
Papadatos S, Charalambous AC, Daskalakis V. Sci Rep, 2017, 7: 2523
Johnson MP, Brain APR, Ruban AV. Plant Signal Behav, 2011, 6: 1386–1390
Tardy F, Havaux M. Biochim Biophysica Acta (BBA), 1997, 1330: 179–193
Janik E, Bednarska J, Zubik M, Puzio M, Luchowski R, Grudzinski W, Mazur R, Garstka M, Maksymiec W, Kulik A, Dietler G, Gruszecki WI. Plant Cell, 2013, 25: 2155–2170
Seiwert D, Witt H, Janshoff A, Paulsen H. Sci Rep, 2017, 7: 5158
Tietz S, Leuenberger M, Höhner R, Olson AH, Fleming GR, Kirchhoff H. J Biol Chem, 2020, 295: 1857–1866
Murakami S, Packer L. J Cell Biol, 1970, 47: 332–351
Duffy CDP, Pandit A, Ruban AV. Phys Chem Chem Phys, 2014, 16: 5571–5580
Balevičius V Jr., Fox KF, Bricker WP, Jurinovich S, Prandi IG, Mennucci B, Duffy CDP. Sci Rep, 2017, 7: 13956
Mullineaux CW, Ruban AV, Horton P. Biochim Biophysica Acta (BBA), 1994, 1185: 119–123
Clark AH, Saunderson DHP, Suggett A. Int J Peptide Protein Res, 1981, 17: 353–364
Neuweiler H, Johnson CM, Fersht AR. Proc Natl Acad Sci USA, 2009, 106: 18569–18574
Dall’Osto L, Cazzaniga S, Bressan M, Paleček D, Židek K, Niyogi KK, Fleming GR, Zigmantas D, Bassi R. Nat Plants, 2017, 3: 17033
Acknowledgements
This work was supported by the National Natural Science Foundation of China (21433014, 11721404, 21533003), the Ministry of Science and Technology (2017YFB0203400), Chinese Academy of Sciences Innovation Program (KJCX2-YW-W25) and the National Institutes of Health (GM46736, GM64742). Y.W. thanks Prof. Tingyun Kuang for encouragement, Prof. Xinguang Zhu for in-depth discussion, Prof. Chunhong Yang for the single-site mutant S123G sample, and Miss Ju Wang and Prof. Shufeng Wang from Peking University for the help in streak camera measurement.
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Li, H., Wang, Y., Ye, M. et al. Dynamical and allosteric regulation of photoprotection in light harvesting complex II. Sci. China Chem. 63, 1121–1133 (2020). https://doi.org/10.1007/s11426-020-9771-2
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DOI: https://doi.org/10.1007/s11426-020-9771-2