Impact of ion fluxes across thylakoid membranes on photosynthetic electron transport and photoprotection.
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
29
04
2020
accepted:
18
05
2021
pubmed:
19
6
2021
medline:
24
9
2021
entrez:
18
6
2021
Statut:
ppublish
Résumé
In photosynthetic thylakoid membranes the proton motive force (pmf) not only drives ATP synthesis, in addition it is central to controlling and regulating energy conversion. As a consequence, dynamic fine-tuning of the two pmf components, electrical (Δψ) and chemical (ΔpH), is an essential element for adjusting photosynthetic light reactions to changing environmental conditions. Good evidence exists that the Δψ/ΔpH partitioning is controlled by thylakoid potassium and chloride ion transporters and channels. However, a detailed mechanistic understanding of how these thylakoid ion transporter/channels control pmf partitioning is lacking. Here, we combined functional measurements on potassium and chloride ion transporter and channel loss-of-function mutants with extended mathematical simulations of photosynthetic light reactions in thylakoid membranes to obtain detailed kinetic insights into the complex interrelationship between membrane energization and ion fluxes across thylakoid membranes. The data reveal that potassium and chloride fluxes in the thylakoid lumen determined by the K
Identifiants
pubmed: 34140667
doi: 10.1038/s41477-021-00947-5
pii: 10.1038/s41477-021-00947-5
doi:
Types de publication
Comparative Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
979-988Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Mitchell, P. Coupling of photophosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191, 144–148 (1961).
pubmed: 13771349
doi: 10.1038/191144a0
Williams, R. J. P. Possible functions of chains of catalysts. J. Theor. Biol. 1, 1–13 (1961).
pubmed: 13785509
doi: 10.1016/0022-5193(61)90023-6
Williams, R. J. P. Possible functions of chains of catalysts II. J. Theor. Biol. 3, 209–220 (1962).
doi: 10.1016/S0022-5193(62)80015-0
Witt, H. T. Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods: the central role of the electric field. Biochim. Biophys. Acta 505, 355–427 (1979).
pubmed: 35227
doi: 10.1016/0304-4173(79)90008-9
Bulychev, A. A. & Vredenberg, W. J. Light-triggered electrical events in the thylakoid membrane of plant chloroplasts. Physiol. Plant. 105, 577–584 (1999).
doi: 10.1034/j.1399-3054.1999.105325.x
Kramer, D. M., Cruz, J. A. & Kanazawa, A. Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci. 8, 27–32 (2003).
pubmed: 12523997
doi: 10.1016/S1360-1385(02)00010-9
Allorent, G. et al. Global spectroscopic analysis to study the regulation of the photosynthetic proton motive force: a critical reappraisal. Biochim. Biophys. Acta Bioenerg. 1859, 676–683 (2018).
pubmed: 29981721
doi: 10.1016/j.bbabio.2018.07.001
Klughammer, C., Siebke, K. & Scheiber, U. Continuous ECS-indicated recording of the proton-motive charge flux in leaves. Photosynth. Res. 117, 471–487 (2013).
pubmed: 23860827
pmcid: 3825596
doi: 10.1007/s11120-013-9884-4
Davis, G. A., Rutherford, A. W. & Kramer, D. M. Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δψ and ΔpH. Philos. Trans. Roy. Soc. B 372, 20160381 (2017).
doi: 10.1098/rstb.2016.0381
Avenson, T., Cruz, J. A. & Kramer, D. Modulation of energy dependent quenching of excitons (qE) in antenna of higher plants. Proc. Natl Acad. Sci. USA 101, 5530–5535 (2004).
pubmed: 15064404
pmcid: 397417
doi: 10.1073/pnas.0401269101
Rumberg, B. & Siggel, U. pH changes in the inner phase of the thylakoids during photosynthesis. Z. Naturwiss 56, 130–132 (1969).
doi: 10.1007/BF00601025
Kobayashi, Y., Inoue, Y., Shibata, K. & Heber, U. Control of electron flow in intact chloroplasts by intathylakoid pH, not by the phosphorylation potential. Planta 146, 481–486 (1979).
pubmed: 24318257
doi: 10.1007/BF00380864
Ruban, A. V. Light harvesting control in plants. FEBS Lett. 592, 3030–3039 (2018).
pubmed: 29797317
doi: 10.1002/1873-3468.13111
Li, Z., Wakao, S., Fischer, B. B. & Niyogi, K. K. Sensing and responding to excess light. Annu. Rev. Plant Biol. 60, 239–260 (2009).
pubmed: 19575582
doi: 10.1146/annurev.arplant.58.032806.103844
Pinnola, A. & Bassi, R. Molecular mechanisms involved in plant photoprotection. Biochem. Soc. Trans. 46, 467–482 (2018).
pubmed: 29666217
doi: 10.1042/BST20170307
Armbruster, U., Correa Galvis, V., Kunz, H. H. & Strand, D. D. The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light. Curr. Opin. Plant Biol. 37, 56–62 (2017).
pubmed: 28426975
doi: 10.1016/j.pbi.2017.03.012
Demmig, B. & Gimmler, H. Properties of the isolated intact chloroplast at cytoplasmic K
pubmed: 16663169
pmcid: 1066428
doi: 10.1104/pp.73.1.169
Robinson, S. P. & Downtown, W. J. Potassium, sodium, and chloride content of isolated intact chloroplasts in relation to ionic compartmentation in leaves. Arch. Biochem. Biophys. 228, 197–206 (1984).
pubmed: 6696431
doi: 10.1016/0003-9861(84)90061-4
Schonknecht, G., Hederich, R., Junge, W. & Raschke, K. A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant. Nature 336, 589–592 (1988).
doi: 10.1038/336589a0
Enz, C., Steinkamp, T. & Wagner, R. Ion channels in the thylakoid membrane (a patch-clamp study). Biochim. Biophys. Acta 1143, 67–76 (1993).
doi: 10.1016/0005-2728(93)90217-4
Finazzi, G. et al. Ion channels/trasnporters and chloroplast regulation. Cell Calcium 58, 86–97 (2015).
pubmed: 25454594
doi: 10.1016/j.ceca.2014.10.002
Spetea, C. et al. An update on the regulation of photosynthesis by thylakoid ion channels and transporters in Arabidopsis. Physiol. Plant. 161, 16–27 (2017).
pubmed: 28332210
doi: 10.1111/ppl.12568
Kunz, H. H. et al. Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 7480–7485 (2014).
pubmed: 24794527
pmcid: 4034250
doi: 10.1073/pnas.1323899111
Duan, Z. et al. A bestrophin-like protein modulates the proton motive force across the thylakoid membrane in Arabidopsis. J. Integr. Plant Biol. 58, 848–858 (2016).
pubmed: 26947269
pmcid: 5074266
doi: 10.1111/jipb.12475
Herdean, A. et al. A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat. Commun. 7, 11654 (2016).
pubmed: 27216227
pmcid: 4890181
doi: 10.1038/ncomms11654
Herdean, A. et al. The Arabidopsis thylakoid chloride channel AtCLCe functions in chloride homeostasis and regulation of photosynthetic electron transport. Front. Plant Sci. 7, 115 (2016).
pubmed: 26904077
pmcid: 4746265
doi: 10.3389/fpls.2016.00115
Marmagne, A. et al. Two members of the Arabidopsis CLC (chloride channel) family, ATCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively. J. Exp. Bot. 58, 3358–3393 (2007).
doi: 10.1093/jxb/erm187
Carraretto, L. et al. A thylakoid-located two-pore K
pubmed: 24009357
doi: 10.1126/science.1242113
Höhner, R. et al. Photosynthesis in Arabidopsis is unaffected by the function of the vacuolar K
pubmed: 31053658
pmcid: 6752931
doi: 10.1104/pp.19.00255
Jaslan, D. et al. Voltage-dependent gating of SV channel TPC1 confers vacuole excitability. Nat. Commun. 10, 2659 (2019).
pubmed: 31201323
pmcid: 6572840
doi: 10.1038/s41467-019-10599-x
Tang, R.-J. et al. A calcium signalling network activates vacuolar K
pubmed: 32231253
doi: 10.1038/s41477-020-0621-7
Dukic, E. et al. K
pubmed: 31201341
pmcid: 6570773
doi: 10.1038/s41598-019-44972-z
Armbruster, U. et al. Ion antiport accelerates photosynthetic acclimation in fluctuating light environments. Nat. Commun. 5, 5439 (2014).
pubmed: 25451040
doi: 10.1038/ncomms6439
Wang, C. & Shikanai, T. Modification of activity of the thylakoid H
pubmed: 31427465
pmcid: 6776848
doi: 10.1104/pp.19.00766
Tian, L. et al. pH dependence, kinetics and light-harvesting regulation of nonphotochemical quenching in Chlamydomonas. Proc. Natl Acad. Sci. USA 116, 8320–8325 (2019).
pubmed: 30962362
pmcid: 6486713
doi: 10.1073/pnas.1817796116
Takizawa, K., Cruz, J. A. & Kramer, D. M. Depletion of stromal inorganic phosphate induces high ‘energy-dependent’ antenna exciton quenching (qE) by decreasing proton conductivity at CFO-CF1 ATP synthase. Plant Cell Environ. 31, 235–243 (2008).
pubmed: 17996016
doi: 10.1111/j.1365-3040.2007.01753.x
Cruz, J. A., Sacksteder, C. A., Kanazawa, A. & Kramer, D. M. Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Δψ and ΔpH by ionic strength. Biochemistry 40, 1226–1237 (2001).
pubmed: 11170448
doi: 10.1021/bi0018741
Bailleul, B., Cardol, P., Breyton, C. & Finazzi, G. Electrochromism: a useful tool to study algal photosynthesis. Photosynth. Res. 106, 179–189 (2010).
pubmed: 20632109
doi: 10.1007/s11120-010-9579-z
Schuldiner, S., Rottenberg, H. & Avron, M. Determination of ΔpH in chloroplasts. 2. Fluorescent amines as a probe for the determination of ΔpH in chloroplasts. Eur. J. Biochem. 25, 64–70 (1972).
pubmed: 5023581
doi: 10.1111/j.1432-1033.1972.tb01667.x
Johnson, M. P., Zia, A. & Ruban, A. V. Elevated ΔpH restores rapidly reversible photoprotective energy dissipation in Arabidopsis chloroplasts deficient in lutein and xanthophyll cycle activity. Planta 235, 193–204 (2011).
pubmed: 21866345
doi: 10.1007/s00425-011-1502-0
Jahns, P. & Holzwarth, A. R. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim. Biophys. Acta 1817, 182–193 (2012).
pubmed: 21565154
doi: 10.1016/j.bbabio.2011.04.012
Nielkens, M. et al. Idnetification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim. Biophys. Acta 1797, 466–475 (2010).
doi: 10.1016/j.bbabio.2010.01.001
Correa Galivs, V. et al. H
doi: 10.1104/pp.19.01561
Wang, C. et al. Fine-tuned regulation of the K
pubmed: 27783435
doi: 10.1111/tpj.13405
Armbruster, U. et al. Regulation and levels of the thylakoid K
pubmed: 27335350
pmcid: 4937787
Roosild, T. P. et al. KTN (RCK) domains regulate K
pubmed: 19523906
pmcid: 2920069
doi: 10.1016/j.str.2009.03.018
Uflewski, M. et al. Functional characterization of proton antiport regulation in the thylakoid membrane. Plant Physiol. https://doi.org/10.1093/plphys/kiab135 (2021).
Gräber, P., Junesch, U. & Schatz, G. H. Kinetics of proton-transport coupled ATP synthesis in chloroplasts. Activation of the ATPase by an artificially generated ΔpH and Δψ. Ber. Bunsenges. 88, 599–608 (1984).
doi: 10.1002/bbpc.19840880706
Schneider, D. et al. Fluctuating light experiments and semi-automated plant phenotyping enabled by self-built growth racks and simple upgrades to the IMAGING-PAM. Plant Methods 15, 156 (2019).
pubmed: 31889980
pmcid: 6927185
doi: 10.1186/s13007-019-0546-1
Koochak, H., Puthiyaveetil, S., Mullendore, D. L., Li, M. & Kirchhoff, H. The structural and functional domains of plant thylakoid membranes. Plant J. 97, 412–429 (2019).
pubmed: 30312499
doi: 10.1111/tpj.14127
Van, T. V., Heinze, T & Rumberg, B . in Progress in Photosynthesis Research Vol. III (ed. Biggens J) (Martinus Nijhoff, 1987).
Tietz, S. et al. Functional implications of photosystem II crystal formation in photosynthetic membranes. J. Biol. Chem. 290, 14091–14106 (2015).
pubmed: 25897076
pmcid: 4447980
doi: 10.1074/jbc.M114.619841
Kramer, D. M., Johnson, G., Kiirats, O. & Edwards, G. E. New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth. Res 79, 209–218 (2004).
pubmed: 16228395
doi: 10.1023/B:PRES.0000015391.99477.0d
Puthiyaveetil, S. et al. Compartmentalization of the protein repair machinery in photosynthetic membranes. Proc. Natl Acad. Sci. USA 111, 15839–15844 (2014).
pubmed: 25331882
pmcid: 4226077
doi: 10.1073/pnas.1413739111