Photosynthetic light-harvesting complexes have a remarkable capacity to perform robust photo-physics at ambient temperatures and in fluctuating environments. Protein conformational dynamics and membrane mobility are processes that contribute to the light-harvesting efficiencies and control photoprotective responses. This short review describes the application of magic angle spinning nuclear magnetic resonance (NMR) spectroscopy for characterizing the structural dynamics of pigment, protein, and thylakoid membrane components related to light harvesting and photoprotection. I will discuss the use of dynamics-based spectral editing solid-state NMR for distinguishing rigid and mobile components and assessing protein, pigment, and lipid dynamics on sub-nanosecond to millisecond timescales. Dynamic spectral editing NMR has been applied to investigate light-harvesting complex II protein conformational dynamics inside lipid bilayers and in native membranes. Furthermore, we used the NMR approach to assess thylakoid membrane dynamics. Finally, it is shown that dynamics-based spectral editing NMR for reducing spectral complexity by filtering motion-dependent signals enabled us to follow processes in live photosynthetic cells.
REFERENCES
1.
R. E.
Blankenship
, “The basic principles of photosynthetic energy storage
,” in Molecular Mechanisms of Photosynthesis
(Wiley
, 2002
), pp. 1
–10
.2.
M.
Pribil
, M.
Labs
, and D.
Leister
, “Structure and dynamics of thylakoids in land plants
,” J. Exp. Bot.
65
(8
), 1955
–1972
(2014
).3.
M. P.
Johnson
and E.
Wientjes
, “The relevance of dynamic thylakoid organisation to photosynthetic regulation
,” Biochim. Biophys. Acta, Bioenerg.
1861
(4
), 148039
(2020
).4.
R.
Moya
, A. C.
Norris
, T.
Kondo
, and G. S.
Schlau-Cohen
, “Observation of robust energy transfer in the photosynthetic protein allophycocyanin using single-molecule pump–probe spectroscopy
,” Nat. Chem.
14
(2
), 153
–159
(2022
).5.
Y.-C.
Cheng
and G. R.
Fleming
, “Dynamics of light harvesting in photosynthesis
,” Annu. Rev. Phys. Chem.
60
(1
), 241
–262
(2009
).6.
G. S.
Schlau-Cohen
, H.-Y.
Yang
, T. P. J.
Krüger
, P.
Xu
, M.
Gwizdala
, R.
van Grondelle
, R.
Croce
, and W. E.
Moerner
, “Single-molecule identification of quenched and unquenched states of LHCII
,” J. Phys. Chem. Lett.
6
(5
), 860
–867
(2015
).7.
H.
Kirchhoff
, S.
Haferkamp
, J. F.
Allen
, D. B. A.
Epstein
, and C. W.
Mullineaux
, “Protein diffusion and macromolecular crowding in thylakoid membranes
,” Plant Physiol.
146
(4
), 1571
–1578
(2008
).8.
E. A.
Arsenault
, Y.
Yoneda
, M.
Iwai
, K. K.
Niyogi
, and G. R.
Fleming
, “Vibronic mixing enables ultrafast energy flow in light-harvesting complex II
,” Nat. Commun.
11
(1
), 1460
(2020
).9.
M.
Baldus
, A. T.
Petkova
, J.
Herzfeld
, and R. G.
Griffin
, “Cross polarization in the tilted frame: Assignment and spectral simplification in heteronuclear spin systems
,” Mol. Phys.
95
(6
), 1197
–1207
(1998
).10.
V.
Ladizhansky
, “Applications of solid-state NMR to membrane proteins
,” Biochim. Biophys. Acta, Proteins Proteomics
1865
(11, Part B
), 1577
–1586
(2017
).11.
B. J.
Wylie
, H. Q.
Do
, C. G.
Borcik
, and E. P.
Hardy
, “Advances in solid-state NMR of membrane proteins
,” Mol. Phys.
114
(24
), 3598
–3609
(2016
).12.
M.
Bonaccorsi
, T.
Le Marchand
, and G.
Pintacuda
, “Protein structural dynamics by Magic-Angle Spinning NMR
,” Curr. Opin. Struct. Biol.
70
, 34
–43
(2021
).13.
M. J.
Duer
, “The basics of solid-state NMR
,” in Solid‐State NMR Spectroscopy Principles and Applications
(Wiley
, 2001
), pp. 1
–72
.14.
J.
Boisbouvier
and L. E.
Kay
, “Advanced isotopic labeling for the NMR investigation of challenging proteins and nucleic acids
,” J. Biomol. NMR
71
(3
), 115
–117
(2018
).15.
I.
Matlahov
and P. C. A.
van der Wel
, “Hidden motions and motion-induced invisibility: Dynamics-based spectral editing in solid-state NMR
,” Methods
148
, 123
–135
(2018
).16.
M.
Baldus
and B. H.
Meier
, “Total correlation spectroscopy in the solid state. The use of scalar couplings to determine the through-bond connectivity
,” J. Magn. Reson., Ser. A
121
(1
), 65
–69
(1996
).17.
B.
Elena
, A.
Lesage
, S.
Steuernagel
, A.
Böckmann
, and L.
Emsley
, “Proton to carbon-13 INEPT in solid-state NMR spectroscopy
,” J. Am. Chem. Soc.
127
(49
), 17296
–17302
(2005
).18.
A.
Nowacka
, N. A.
Bongartz
, O. H. S.
Ollila
, T.
Nylander
, and D.
Topgaard
, “Signal intensities in 1H–13C CP and INEPT MAS NMR of liquid crystals
,” J. Magn. Reson.
230
, 165
–175
(2013
).19.
J. C.
Boatz
, T.
Piretra
, A.
Lasorsa
, I.
Matlahov
, J. F.
Conway
, and P. C. A.
van der Wel
, “Protofilament structure and supramolecular polymorphism of aggregated mutant huntingtin exon 1
,” J. Mol. Biol.
432
(16
), 4722
–4744
(2020
).20.
H.-K.
Lin
, J. C.
Boatz
, I. E.
Krabbendam
, R.
Kodali
, Z.
Hou
, R.
Wetzel
, A. M.
Dolga
, M. A.
Poirier
, and P. C. A.
van der Wel
, “Fibril polymorphism affects immobilized non-amyloid flanking domains of huntingtin exon 1 rather than its polyglutamine core
,” Nat. Commun.
8
(1
), 15462
(2017
).21.
M.
Li
, A.
Mandal
, V. A.
Tyurin
, M.
DeLucia
, J.
Ahn
, V. E.
Kagan
, and P. C. A.
van der Wel
, “Surface-binding to cardiolipin nanodomains triggers cytochrome c pro-apoptotic peroxidase activity via localized dynamics
,” Structure
27
(5
), 806
–815.e4
(2019
).22.
M.
El Hariri El Nokab
, A.
Lasorsa
, K. O.
Sebakhy
, F.
Picchioni
, and P. C. A.
van der Wel
, “Solid-state NMR spectroscopy insights for resolving different water pools in alginate hydrogels
,” Food Hydrocolloids
127
, 107500
(2022
).23.
A.
Nowacka
, P. C.
Mohr
, J.
Norrman
, R. W.
Martin
, and D.
Topgaard
, “Polarization transfer solid-state NMR for studying surfactant phase behavior
,” Langmuir
26
(22
), 16848
–16856
(2010
).24.
C.
Galvagnion
, D.
Topgaard
, K.
Makasewicz
, A. K.
Buell
, S.
Linse
, E.
Sparr
, and C. M.
Dobson
, “Lipid dynamics and phase transition within α-synuclein amyloid fibrils
,” J. Phys. Chem. Lett.
10
(24
), 7872
–7877
(2019
).25.
D.
Courtier-Murias
, H.
Farooq
, H.
Masoom
, A.
Botana
, R.
Soong
, J. G.
Longstaffe
, M. J.
Simpson
, W. E.
Maas
, M.
Fey
, B.
Andrew
, J.
Struppe
, H.
Hutchins
, S.
Krishnamurthy
, R.
Kumar
, M.
Monette
, H. J.
Stronks
, A.
Hume
, and A. J.
Simpson
, “Comprehensive multiphase NMR spectroscopy: Basic experimental approaches to differentiate phases in heterogeneous samples
,” J. Magn. Reson.
217
, 61
–76
(2012
).26.
Y. L.
Mobarhan
, B.
Fortier-McGill
, R.
Soong
, W. E.
Maas
, M.
Fey
, M.
Monette
, H. J.
Stronks
, S.
Schmidt
, H.
Heumann
, W.
Norwood
, and A. J.
Simpson
, “Comprehensive multiphase NMR applied to a living organism
,” Chem. Sci.
7
(8
), 4856
–4866
(2016
).27.
L.
Shen
, Z.
Huang
, S.
Chang
, W.
Wang
, J.
Wang
, T.
Kuang
, G.
Han
, J.-R.
Shen
, and X.
Zhang
, “Structure of a C2S2M2N2-type PSII–LHCII supercomplex from the green alga Chlamydomonas reinhardtii
,” Proc. Natl. Acad. Sci. U. S. A.
116
(42
), 21246
–21255
(2019
).28.
X.
Sheng
, Z.
Liu
, E.
Kim
, and J.
Minagawa
, “Plant and algal PSII–LHCII supercomplexes: Structure, evolution and energy transfer
,” Plant Cell Physiol.
62
(7
), 1108
–1120
(2021
).29.
M.
Fan
, M.
Li
, Z.
Liu
, P.
Cao
, X.
Pan
, H.
Zhang
, X.
Zhao
, J.
Zhang
, and W.
Chang
, “Crystal structures of the PsbS protein essential for photoprotection in plants
,” Nat. Struct. Mol. Biol.
22
(9
), 729
–735
(2015
).30.
Z.
Liu
, H.
Yan
, K.
Wang
, T.
Kuang
, J.
Zhang
, L.
Gui
, X.
An
, and W.
Chang
, “Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution
,” Nature
428
(6980
), 287
–292
(2004
).31.
T. A.
Egorova-Zachernyuk
, J.
Hollander
, N.
Fraser
, P.
Gast
, A. J.
Hoff
, R.
Cogdell
, H. J. M.
de Groot
, and M.
Baldus
, “MAS NMR on a uniformly [13C, 15N] labeled LH2 light-harvesting complex from Rhodopseudomonas Acidophila 10050 at ultra-high magnetic fields
,” in Perspectives on Solid State NMR in Biology
, edited by S. R.
Kiihne
and H. J. M.
de Groot
(Springer Netherlands
, Dordrecht
, 2001
), pp. 171
–183
.32.
A.
Pandit
, F.
Buda
, A. J.
van Gammeren
, S.
Ganapathy
, and H. J. M.
de Groot
, “Selective chemical shift assignment of bacteriochlorophyll a in uniformly [13C–15N]-labeled light-harvesting 1 complexes by solid-state NMR in ultrahigh magnetic field
,” J. Phys. Chem. B
114
(18
), 6207
–6215
(2010
).33.
S.
Ganapathy
, A. J.
van Gammeren
, F. B.
Hulsbergen
, and H. J. M.
de Groot
, “Probing secondary, tertiary, and quaternary structure along with protein–cofactor interactions for a helical transmembrane protein complex through 1H spin diffusion with MAS NMR spectroscopy
,” J. Am. Chem. Soc.
129
(6
), 1504
–1505
(2007
).34.
Alia
, J.
Matysik
, C.
Soede-Huijbregts
, M.
Baldus
, J.
Raap
, J.
Lugtenburg
, P.
Gast
, H. J.
van Gorkom
, A. J.
Hoff
, and H. J. M.
de Groot
, “Ultrahigh field MAS NMR dipolar correlation spectroscopy of the histidine residues in light-harvesting complex II from photosynthetic bacteria reveals partial internal charge transfer in the B850/His complex
,” J. Am. Chem. Soc.
123
(20
), 4803
–4809
(2001
).35.
Alia
, J.
Matysik
, I.
de Boer
, P.
Gast
, H. J.
van Gorkom
, and H. J.
de Groot
, “Heteronuclear 2D (1H-13C) MAS NMR resolves the electronic structure of coordinated histidines in light-harvesting complex II: Assessment of charge transfer and electronic delocalization effect
,” J. Biomol. NMR
28
(2
), 157
–164
(2004
).36.
A.
Diller
, E.
Roy
, P.
Gast
, H. J.
van Gorkom
, H. J. M.
de Groot
, C.
Glaubitz
, G.
Jeschke
, J.
Matysik
, and A.
Alia
, “15N photochemically induced dynamic nuclear polarization magic-angle spinning NMR analysis of the electron donor of photosystem II
,” Proc. Natl. Acad. Sci. U. S. A.
104
(31
), 12767
–12771
(2007
).37.
J. C.
Zill
, M.
Kansy
, R.
Goss
, A.
Alia
, C.
Wilhelm
, and J.
Matysik
, “15N photo-CIDNP MAS NMR on both photosystems and magnetic field-dependent 13C photo-CIDNP MAS NMR in photosystem II of the diatom Phaeodactylum tricornutum
,” Photosynth. Res.
140
(2
), 151
–171
(2019
).38.
G. J.
Janssen
, E.
Daviso
, M.
van Son
, H. J.
de Groot
, A.
Alia
, and J.
Matysik
, “Observation of the solid-state photo-CIDNP effect in entire cells of cyanobacteria Synechocystis
,” Photosynth. Res.
104
(2
), 275
–282
(2010
).39.
S.
Ganapathy
, G. T.
Oostergetel
, P. K.
Wawrzyniak
, M.
Reus
, A.
Gomez Maqueo Chew
, F.
Buda
, E. J.
Boekema
, D. A.
Bryant
, A. R.
Holzwarth
, and H. J. M.
de Groot
, “Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes
,” Proc. Natl. Acad. Sci. U. S. A.
106
(21
), 8525
–8530
(2009
).40.
S.
Ganapathy
, S.
Sengupta
, P. K.
Wawrzyniak
, V.
Huber
, F.
Buda
, U.
Baumeister
, F.
Würthner
, and H. J. M.
de Groot
, “Zinc chlorins for artificial light-harvesting self-assemble into antiparallel stacks forming a microcrystalline solid-state material
,” Proc. Natl. Acad. Sci. U. S. A.
106
(28
), 11472
–11477
(2009
).41.
A.
Pandit
, K.
Ocakoglu
, F.
Buda
, T.
van Marle
, A. R.
Holzwarth
, and H. J. M.
de Groot
, “Structure determination of a bio-inspired self-assembled light-harvesting antenna by solid-state NMR and molecular modeling
,” J. Phys. Chem. B
117
(38
), 11292
–11298
(2013
).42.
X.
Li
, F.
Buda
, H. J. M.
de Groot
, and G. J. A.
Sevink
, “Contrasting modes of self-assembly and hydrogen-bonding heterogeneity in chlorosomes of Chlorobaculum tepidum
,” J. Phys. Chem. C
122
(26
), 14877
–14888
(2018
).43.
X.
Li
, F.
Buda
, H. J. M.
de Groot
, and G. J. A.
Sevink
, “Molecular insight in the optical response of tubular chlorosomal assemblies
,” J. Phys. Chem. C
123
(26
), 16462
–16478
(2019
).44.
T. P. J.
Krüger
, C.
Ilioaia
, M. P.
Johnson
, A. V.
Ruban
, E.
Papagiannakis
, P.
Horton
, and R.
van Grondelle
, “Controlled disorder in plant light-harvesting complex II explains its photoprotective role
,” Biophys. J.
102
(11
), 2669
–2676
(2012
).45.
A. V.
Ruban
, “Light harvesting control in plants
,” FEBS Lett.
592
(18
), 3030
–3039
(2018
).46.
J.
Standfuss
, A. C.
Terwisscha van Scheltinga
, M.
Lamborghini
, and W.
Kühlbrandt
, “Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution
,” EMBO J.
24
(5
), 919
–928
(2005
).47.
X.
Pan
, M.
Li
, T.
Wan
, L.
Wang
, C.
Jia
, Z.
Hou
, X.
Zhao
, J.
Zhang
, and W.
Chang
, “Structural insights into energy regulation of light-harvesting complex CP29 from spinach
,” Nat. Struct. Mol. Biol.
18
(3
), 309
–315
(2011
).48.
N.
Liguori
, R.
Croce
, S. J.
Marrink
, and S.
Thallmair
, “Molecular dynamics simulations in photosynthesis
,” Photosynth. Res.
144
(2
), 273
–295
(2020
).49.
N.
Liguori
, X.
Periole
, S. J.
Marrink
, and R.
Croce
, “From light-harvesting to photoprotection: Structural basis of the dynamic switch of the major antenna complex of plants (LHCII)
,” Sci. Rep.
5
(1
), 15661
(2015
).50.
S.
Thallmair
, P. A.
Vainikka
, and S. J.
Marrink
, “Lipid fingerprints and cofactor dynamics of light-harvesting complex II in different membranes
,” Biophys. J.
116
(8
), 1446
–1455
(2019
).51.
F. J.
van Eerden
, D. H.
de Jong
, A. H.
de Vries
, T. A.
Wassenaar
, and S. J.
Marrink
, “Characterization of thylakoid lipid membranes from cyanobacteria and higher plants by molecular dynamics simulations
,” Biochim. Biophys. Acta, Biomembr.
1848
(6
), 1319
–1330
(2015
).52.
V.
Daskalakis
, S.
Papadatos
, and U.
Kleinekathöfer
, “Fine tuning of the photosystem II major antenna mobility within the thylakoid membrane of higher plants
,” Biochim. Biophys. Acta, Biomembr.
1861
(12
), 183059
(2019
).53.
V.
Daskalakis
, S.
Papadatos
, and T.
Stergiannakos
, “The conformational phase space of the photoprotective switch in the major light harvesting complex II
,” Chem. Commun.
56
(76
), 11215
–11218
(2020
).54.
N.
Liguori
, S. R. R.
Campos
, A. M.
Baptista
, and R.
Croce
, “Molecular anatomy of plant photoprotective switches: The sensitivity of PsbS to the environment, residue by residue
,” J. Phys. Chem. Lett.
10
(8
), 1737
–1742
(2019
).55.
C.
Dockter
, A. H.
Müller
, C.
Dietz
, A.
Volkov
, Y.
Polyhach
, G.
Jeschke
, and H.
Paulsen
, “Rigid core and flexible terminus: Structure of solubilized light-harvesting chlorophyll a/b complex (LHCII) measured by EPR
,” J. Biol. Chem.
287
(4
), 2915
–2925
(2012
).56.
M.
Golub
, L.
Rusevich
, K.-D.
Irrgang
, and J.
Pieper
, “Rigid versus flexible protein matrix: Light-harvesting complex II exhibits a temperature-dependent phonon spectral density
,” J. Phys. Chem. B
122
(28
), 7111
–7121
(2018
).57.
K.
Vrandecic
, M.
Rätsep
, L.
Wilk
, L.
Rusevich
, M.
Golub
, M.
Reppert
, K.-D.
Irrgang
, W.
Kühlbrandt
, and J.
Pieper
, “Protein dynamics tunes excited state positions in light-harvesting complex II
,” J. Phys. Chem. B
119
(10
), 3920
–3930
(2015
).58.
M.
Golub
, H.
Lokstein
, D.
Soloviov
, A.
Kuklin
, D. C. F.
Wieland
, and J.
Pieper
, “Light-harvesting complex II adopts different quaternary structures in solution as observed using small-angle scattering
,” J. Phys. Chem. Lett.
13
(5
), 1258
–1265
(2022
).59.
F.
Azadi-Chegeni
, M. E.
Ward
, G.
Perin
, D.
Simionato
, T.
Morosinotto
, M.
Baldus
, and A.
Pandit
, “Conformational dynamics of light-harvesting complex II in a native membrane environment
,” Biophys. J.
120
(2
), 270
–283
(2021
).60.
T.
Gopinath
and G.
Veglia
, “Probing membrane protein ground and conformationally excited states using dipolar- and J-coupling mediated MAS solid state NMR experiments
,” Methods
148
, 115
–122
(2018
).61.
M. E.
Ward
, E.
Ritz
, M. A. M.
Ahmed
, V. V.
Bamm
, G.
Harauz
, L. S.
Brown
, and V.
Ladizhansky
, “Proton detection for signal enhancement in solid-state NMR experiments on mobile species in membrane proteins
,” J. Biomol. NMR
63
(4
), 375
–388
(2015
).62.
Y.
Luo
, S.
Xiang
, P. J.
Hooikaas
, L.
van Bezouwen
, A. S.
Jijumon
, C.
Janke
, F.
Förster
, A.
Akhmanova
, and M.
Baldus
, “Direct observation of dynamic protein interactions involving human microtubules using solid-state NMR spectroscopy
,” Nat. Commun.
11
(1
), 18
(2020
).63.
P. C. A.
van der Wel
, “New applications of solid-state NMR in structural biology
,” Emerging Top. Life Sci.
2
(1
), 57
–67
(2018
).64.
F.
Azadi-Chegeni
, S.
Thallmair
, M. E.
Ward
, G.
Perin
, S. J.
Marrink
, M.
Baldus
, T.
Morosinotto
, and A.
Pandit
, “Protein dynamics and lipid affinity of monomeric, zeaxanthin-binding LHCII in thylakoid membranes
,” Biophys. J.
121
(3
), 396
–409
(2022
).65.
T.
Kondo
, A.
Pinnola
, W. J.
Chen
, L.
Dall’Osto
, R.
Bassi
, and G. S.
Schlau-Cohen
, “Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection
,” Nat. Chem.
9
(8
), 772
–778
(2017
).66.
E.
Cignoni
, M.
Lapillo
, L.
Cupellini
, S.
Acosta-Gutiérrez
, F. L.
Gervasio
, and B.
Mennucci
, “A different perspective for nonphotochemical quenching in plant antenna complexes
,” Nat. Commun.
12
(1
), 7152
(2021
).67.
L.
Cupellini
, D.
Calvani
, D.
Jacquemin
, and B.
Mennucci
, “Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants
,” Nat. Commun.
11
(1
), 662
(2020
).68.
C.
Gray
, T.
Wei
, T.
Polívka
, V.
Daskalakis
, and C. D. P.
Duffy
, “Trivial excitation energy transfer to carotenoids is an unlikely mechanism for non-photochemical quenching in LHCII
,” Front. Plant Sci.
12
, 797373
(2022
).69.
K.
Sunku
, H. J. M.
de Groot
, and A.
Pandit
, “Insights into the photoprotective switch of the major light-harvesting complex II (LHCII): A preserved core of arginine-glutamate interlocked helices complemented by adjustable loops
,” J. Biol. Chem.
288
(27
), 19796
–19804
(2013
).70.
A.
Pandit
, M.
Reus
, T.
Morosinotto
, R.
Bassi
, A. R.
Holzwarth
, and H. J. M.
de Groot
, “An NMR comparison of the light-harvesting complex II (LHCII) in active and photoprotective states reveals subtle changes in the chlorophyll a ground-state electronic structures
,” Biochim. Biophys. Acta, Bioenerg.
1827
(6
), 738
–744
(2013
).71.
X.
Sheng
, X.
Liu
, P.
Cao
, M.
Li
, and Z.
Liu
, “Structural roles of lipid molecules in the assembly of plant PSII–LHCII supercomplex
,” Biophys. Rep.
4
(4
), 189
–203
(2018
).72.
E.
Kim
, A.
Watanabe
, C. D. P.
Duffy
, A. V.
Ruban
, and J.
Minagawa
, “Multimeric and monomeric photosystem II supercomplexes represent structural adaptations to low- and high-light conditions
,” J. Biol. Chem.
295
(43
), 14537
–14545
(2020
).73.
Z.
Huang
, L.
Shen
, W.
Wang
, Z.
Mao
, X.
Yi
, T.
Kuang
, J.-R.
Shen
, X.
Zhang
, and G.
Han
, “Structure of photosystem I-LHCI-LHCII from the green alga Chlamydomonas reinhardtii in state 2
,” Nat. Commun.
12
(1
), 1100
(2021
).74.
P.
Albanese
, S.
Tamara
, G.
Saracco
, R. A.
Scheltema
, and C.
Pagliano
, “How paired PSII–LHCII supercomplexes mediate the stacking of plant thylakoid membranes unveiled by structural mass-spectrometry
,” Nat. Commun.
11
(1
), 1361
(2020
).75.
S. B.
Krumova
, C.
Dijkema
, P.
de Waard
, H.
Van As
, G.
Garab
, and H.
van Amerongen
, “Phase behavior of phosphatidylglycerol in spinach thylakoid membranes as revealed by 31P-NMR
,” Biochim. Biophys. Acta
1778
(4
), 997
–1003
(2008
).76.
G.
Garab
, B.
Ughy
, P. d.
Waard
, P.
Akhtar
, U.
Javornik
, C.
Kotakis
, P.
Šket
, V.
Karlický
, Z.
Materová
, V.
Špunda
, J.
Plavec
, H.
van Amerongen
, L.
Vígh
, H. V.
As
, and P. H.
Lambrev
, “Lipid polymorphism in chloroplast thylakoid membranes—As revealed by 31P-NMR and time-resolved merocyanine fluorescence spectroscopy
,” Sci. Rep.
7
(1
), 13343
(2017
).77.
H.
Kirchhoff
, “Architectural switches in plant thylakoid membranes
,” Photosynth. Res.
116
(2–3
), 481
–487
(2013
).78.
E.
Janik
, W.
Maksymiec
, W.
Grudziński
, and W. I.
Gruszecki
, “Strong light-induced reorganization of pigment–protein complexes of thylakoid membranes in rye (spectroscopic study)
,” J. Plant Physiol.
169
(1
), 65
–71
(2012
).79.
G.
Nagy
, R.
Ünnep
, O.
Zsiros
, R.
Tokutsu
, K.
Takizawa
, L.
Porcar
, L.
Moyet
, D.
Petroutsos
, G.
Garab
, G.
Finazzi
, and J.
Minagawa
, “Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo
,” Proc. Natl. Acad. Sci. U. S. A.
111
(13
), 5042
–5047
(2014
).80.
H.
Kirchhoff
, C.
Hall
, M.
Wood
, M.
Herbstová
, O.
Tsabari
, R.
Nevo
, D.
Charuvi
, E.
Shimoni
, and Z.
Reich
, “Dynamic control of protein diffusion within the granal thylakoid lumen
,” Proc. Natl. Acad. Sci. U. S. A.
108
(50
), 20248
–20253
(2011
).81.
H.
Kirchhoff
, “Diffusion of molecules and macromolecules in thylakoid membranes
,” Biochim. Biophys. Acta, Bioenerg.
1837
(4
), 495
–502
(2014
).82.
L.-R.
Stingaciu
, H.
O’Neill
, M.
Liberton
, V. S.
Urban
, H. B.
Pakrasi
, and M.
Ohl
, “Revealing the dynamics of thylakoid membranes in living cyanobacterial cells
,” Sci. Rep.
6
(1
), 19627
(2016
).83.
R.
Ünnep
, G.
Nagy
, M.
Markó
, and G.
Garab
, “Monitoring thylakoid ultrastructural changes in vivo using small-angle neutron scattering
,” Plant Physiol. Biochem.
81
, 197
–207
(2014
).84.
T. M.
Ferreira
, O. H. S.
Ollila
, R.
Pigliapochi
, A. P.
Dabkowska
, and D.
Topgaard
, “Model-free estimation of the effective correlation time for C–H bond reorientation in amphiphilic bilayers: 1H–13C solid-state NMR and MD simulations
,” J. Chem. Phys.
142
(4
), 044905
(2015
).85.
F.
Azadi Chegeni
, G.
Perin
, K. B.
Sai Sankar Gupta
, D.
Simionato
, T.
Morosinotto
, and A.
Pandit
, “Protein and lipid dynamics in photosynthetic thylakoid membranes investigated by in-situ solid-state NMR
,” Biochim. Biophys. Acta
1857
(12
), 1849
–1859
(2016
).86.
F.
Azadi-Chegeni
, C.
Schiphorst
, and A.
Pandit
, “In vivo NMR as a tool for probing molecular structure and dynamics in intact Chlamydomonas reinhardtii cells
,” Photosynth. Res.
135
(1–3
), 227
–237
(2018
).87.
F.
Nami
, L.
Tian
, M.
Huber
, R.
Croce
, and A.
Pandit
, “Lipid and protein dynamics of stacked and cation-depletion induced unstacked thylakoid membranes
,” BBA Adv.
1
, 100015
(2021
).88.
R. N.
Purusottam
, L.
Sénicourt
, J.-J.
Lacapère
, and P.
Tekely
, “Probing the gel to liquid-crystalline phase transition and relevant conformation changes in liposomes by 13C magic-angle spinning NMR spectroscopy
,” Biochim. Biophys. Acta, Biomembr.
1848
(12
), 3134
–3139
(2015
).89.
M.
Havaux
, “Carotenoids as membrane stabilizers in chloroplasts
,” Trends Plant Sci.
3
(4
), 147
–151
(1998
).90.
S.
Tuzi
, A.
Naito
, and H.
Saitô
, “Local protein structure and dynamics at kinked transmembrane α-helices of [1-13C]Pro-labeled bacteriorhodopsin as revealed by site-directed solid-state 13C NMR
,” J. Mol. Struct.
654
(1–3
), 205
–214
(2003
).91.
L. M.
Wlodarczyk
, E.
Dinc
, R.
Croce
, and J. P.
Dekker
, “Excitation energy transfer in Chlamydomonas reinhardtii deficient in the PSI core or the PSII core under conditions mimicking state transitions
,” Biochim. Biophys. Acta, Bioenerg.
1857
(6
), 625
–633
(2016
).92.
E.
Luchinat
and L.
Banci
, “In-cell NMR: A topical review
,” IUCrJ
4
(Pt. 2
), 108
–118
(2017
).93.
F.
Nami
, M. J.
Ferraz
, T.
Bakkum
, J. M. F. G.
Aerts
, and A.
Pandit
, “Real-time NMR recording of fermentation and lipid metabolism processes in live microalgae cells
,” Angew. Chem., Int. Ed.
61
(14
), e202117521
(2022
).94.
D. R.
Janero
and R.
Barrnett
, “Cellular and thylakoid-membrane glycolipids of Chlamydomonas reinhardtii 137+
,” J. Lipid Res.
22
(7
), 1119
–1125
(1981
).© 2022 Author(s). Published under an exclusive license by AIP Publishing.
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