DOI: 10.1073/pnas.1214265109. Architectural switch in plant photosynthetic membranes induced by light stress

Architectural switch in plant photosynthetic membranes induced by light stress

10.1073/pnas.1214265109

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

Unavoidable side reactions of photosynthetic energy conversion can damage the water-splitting photosystem II (PSII) holocomplex embedded in the thylakoid membrane system inside chloroplasts. Plant survival is crucially dependent on an efficient molecular repair of damaged PSII realized by a multistep repair cycle. The PSII repair cycle requires a brisk lateral protein traffic between stacked grana thylakoids and unstacked stroma lamellae that is challenged by the tight stacking and low protein mobility in grana. We demonstrated that high light stress induced two main structural changes that work synergistically to improve the accessibility between damaged PSII in grana and its repair machinery in stroma lamellae: lateral shrinkage of grana diameter and increased protein mobility in grana thylakoids. It follows that high light stress triggers an architectural switch of the thylakoid network that is advantageous for swift protein repair. Studies of the thylakoid kinase mutant stn8 and the double mutant stn7/8 demonstrate the central role of protein phosphorylation for the structural alterations. These findings are based on the elaboration of mathematical tools for analyzing confocal laser-scanning microscopic images to study changes in the sophisticated thylakoid architecture in intact protoplasts.

Bibliography

HerbstovÃ¡, M., Tietz, S., Kinzel, C., Turkina, M. V., & Kirchhoff, H. (2012). Architectural switch in plant photosynthetic membranes induced by light stress. Proceedings of the National Academy of Sciences, 109(49), 20130â20135.

Authors 5

Miroslava Herbstová (first)
Stefanie Tietz (additional)
Christopher Kinzel (additional)
Maria V. Turkina (additional)
Helmut Kirchhoff (additional)

References 54 Referenced 129

10.1083/jcb.99.2.481
10.1042/BJ20042098
10.1038/emboj.2009.232
10.1016/j.bbabio.2011.05.024
10.1016/S1360-1385(99)01387-4
10.1073/pnas.81.13.4070
10.1007/s11120-008-9320-3
10.1016/j.bbabio.2011.05.005
10.1016/j.bbabio.2010.08.002
10.1093/jb/mvp073
10.1104/pp.110.170647
10.1093/jxb/err034
R Nevo, SG Chuartzman, O Tsabari, Z Reich, Architecture of thylakoid membrane networks. Lipids in Photosynthesis: Essential and Regulatory Functions, eds H Wada, N Murata (Springer, Dordrecht, The Netherlands), pp. 295–328 (2009). (10.1007/978-90-481-2863-1_14) / Lipids in Photosynthesis: Essential and Regulatory Functions by Nevo R (2009)
10.1016/0006-291X(81)90269-2
LA Staehelin, GWM van der Staay, Structure, composition, functional organization and dynamic properties of thylakoid membranes. Oxygenic Photosynthesis: The Light Reactions, eds DA Ort, CF Yocum (Kluwer, Dordrecht, The Netherlands), pp. 11–30 (1996). (10.1007/0-306-48127-8_2) / Oxygenic Photosynthesis: The Light Reactions by Staehelin LA (1996)
10.1016/S1360-1385(01)02021-0
10.1016/j.tplants.2008.03.001
10.1104/pp.107.115170
TK Goral, et al., Visualizing the mobility and distribution of chlorophyll proteins in higher plant thylakoid membranes: Effects of photoinhibition and protein phosphorylation. Plant J 62, 948–959 (2010). / Plant J / Visualizing the mobility and distribution of chlorophyll proteins in higher plant thylakoid membranes: Effects of photoinhibition and protein phosphorylation by Goral TK (2010)
10.1021/bi0494626
10.1038/nature04016
10.1074/jbc.M505729200
10.1371/journal.pone.0024565
10.1016/j.bbabio.2008.08.004
10.1016/j.bbabio.2003.09.004
10.1073/pnas.1104141109
10.1105/tpc.107.055830
JM Anderson, Thylakoid membrane organization in sun/shade acclimation. Aust J Plant Physiol 15, 11–26 (1988). / Aust J Plant Physiol / Thylakoid membrane organization in sun/shade acclimation by Anderson JM (1988)
10.1074/jbc.M109.007740
10.1105/tpc.109.069435
10.1073/pnas.93.5.2213
10.1016/j.bbabio.2009.05.002
10.1371/journal.pone.0010963
10.1016/j.bbabio.2010.11.010
R Kettunen, E Tyystjärvi, EM Aro, Do grana margins of thylakoid membranes form a functional domain during repair cycle of photosystem II? Photosynthesis: From Light to Biosphere, ed P Mathis (Kluwer, Dordrecht, The Netherlands) Vol IV, 331–334 (1995). / Photosynthesis: From Light to Biosphere by Kettunen R (1995)
10.1073/pnas.0908808107
10.1073/pnas.180054297
10.1016/j.febslet.2007.04.038
10.1007/s004250050550
10.1093/aob/mcq059
10.1016/j.molcel.2006.04.020
10.1105/tpc.109.071431
10.1074/jbc.M110.117432
10.1016/j.jphotobiol.2011.01.016
10.1038/sj.embor.7400464
10.1016/j.febslet.2009.10.057
10.1016/0304-4157(86)90015-8
10.1007/s00294-010-0329-8
10.1083/jcb.71.1.136
10.1021/bi048473w
10.1016/S0005-2728(89)80347-0
10.1021/bi011650y
10.1038/227680a0
10.1073/pnas.76.9.4350

Dates

Type	When
Created	12 years, 9 months ago (Nov. 20, 2012, 1:01 a.m.)
Deposited	3 years, 4 months ago (April 12, 2022, 10:15 p.m.)
Indexed	1 day, 6 hours ago (Aug. 23, 2025, 9:10 p.m.)
Issued	12 years, 9 months ago (Nov. 19, 2012)
Published	12 years, 9 months ago (Nov. 19, 2012)
Published Online	12 years, 9 months ago (Nov. 19, 2012)
Published Print	12 years, 8 months ago (Dec. 4, 2012)

Funders 0

None

BibTeX

@article{Herbstov__2012, title={Architectural switch in plant photosynthetic membranes induced by light stress}, volume={109}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1214265109}, DOI={10.1073/pnas.1214265109}, number={49}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Herbstová, Miroslava and Tietz, Stefanie and Kinzel, Christopher and Turkina, Maria V. and Kirchhoff, Helmut}, year={2012}, month=nov, pages={20130–20135} }

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