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Title: Atomic Force Microscopy of Photosystem II and Its Unit Cell Clustering Quantitatively Delineate the Mesoscale Variability in Arabidopsis Thylakoids

Abstract

Photoautotrophic organisms efficiently regulate absorption of light energy to sustain photochemistry while promoting photoprotection. Photoprotection is achieved in part by triggering a series of dissipative processes termed non-photochemical quenching (NPQ), which depend on the re-organization of photosystem (PS) II supercomplexes in thylakoid membranes. Using atomic force microscopy, we characterized the structural attributes of grana thylakoids from Arabidopsis thaliana to correlate differences in PSII organization with the role of SOQ1, a recently discovered thylakoid protein that prevents formation of a slowly reversible NPQ state. We developed a statistical image analysis suite to discriminate disordered from crystalline particles and classify crystalline arrays according to their unit cell properties. Through detailed analysis of the local organization of PSII supercomplexes in ordered and disordered phases, we found evidence that interactions among light-harvesting antenna complexes are weakened in the absence of SOQ1, inducing protein rearrangements that favor larger separations between PSII complexes in the majority (disordered) phase and reshaping the PSII crystallization landscape. The features we observe are distinct from known protein rearrangements associated with NPQ, providing further support for a role of SOQ1 in a novel NPQ pathway. The particle clustering and unit cell methodology developed here is generalizable to multiple types of microscopymore » and will enable unbiased analysis and comparison of large data sets.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [3];  [7]
+ Show Author Affiliations
  1. Univ. of California, Berkeley, CA (United States). California Inst. for Quantitative Biosciences
  2. Univ. of California, Berkeley, CA (United States). Biophysics Graduate Group
  3. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology. Howard Hughes Medical Inst.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division
  4. Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.
  5. Univ. of California, Berkeley, CA (United States). California Inst. for Quantitative Biosciences. Howard Hughes Medical Inst. Dept. of Molecular and Cell Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
  6. Univ. of California, Berkeley, CA (United States). California Inst. for Quantitative Biosciences. Biophysics Graduate Group. Dept. of Chemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division
  7. Univ. of California, Berkeley, CA (United States). California Inst. for Quantitative Biosciences. Howard Hughes Medical Inst. Dept. of Molecular and Cell Biology. Dept. of Physics; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division. Kavli Energy NanoSciences Inst.
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); Gordon and Betty Moore Foundation (United States)
OSTI Identifier:
1407241
Grant/Contract Number:  
AC02-05CH11231; MCB-1158555; CHE-7178966; GBMF3070
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 9; Journal Issue: 7; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; crystals; Arabidopsis thaliana; antennas; crystal lattices; crystal structure; membrane protein crystallization; photons; protein-protein interactions

Citation Formats

Onoa, Bibiana, Schneider, Anna R., Brooks, Matthew D., Grob, Patricia, Nogales, Eva, Geissler, Phillip L., Niyogi, Krishna K., and Bustamante, Carlos. Atomic Force Microscopy of Photosystem II and Its Unit Cell Clustering Quantitatively Delineate the Mesoscale Variability in Arabidopsis Thylakoids. United States: N. p., 2014. Web. doi:10.1371/journal.pone.0101470.
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Onoa, Bibiana, Schneider, Anna R., Brooks, Matthew D., Grob, Patricia, Nogales, Eva, Geissler, Phillip L., Niyogi, Krishna K., & Bustamante, Carlos. Atomic Force Microscopy of Photosystem II and Its Unit Cell Clustering Quantitatively Delineate the Mesoscale Variability in Arabidopsis Thylakoids. United States. https://doi.org/10.1371/journal.pone.0101470
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Onoa, Bibiana, Schneider, Anna R., Brooks, Matthew D., Grob, Patricia, Nogales, Eva, Geissler, Phillip L., Niyogi, Krishna K., and Bustamante, Carlos. Wed . "Atomic Force Microscopy of Photosystem II and Its Unit Cell Clustering Quantitatively Delineate the Mesoscale Variability in Arabidopsis Thylakoids". United States. https://doi.org/10.1371/journal.pone.0101470. https://www.osti.gov/servlets/purl/1407241.
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@article{osti_1407241,
title = {Atomic Force Microscopy of Photosystem II and Its Unit Cell Clustering Quantitatively Delineate the Mesoscale Variability in Arabidopsis Thylakoids},
author = {Onoa, Bibiana and Schneider, Anna R. and Brooks, Matthew D. and Grob, Patricia and Nogales, Eva and Geissler, Phillip L. and Niyogi, Krishna K. and Bustamante, Carlos},
abstractNote = {Photoautotrophic organisms efficiently regulate absorption of light energy to sustain photochemistry while promoting photoprotection. Photoprotection is achieved in part by triggering a series of dissipative processes termed non-photochemical quenching (NPQ), which depend on the re-organization of photosystem (PS) II supercomplexes in thylakoid membranes. Using atomic force microscopy, we characterized the structural attributes of grana thylakoids from Arabidopsis thaliana to correlate differences in PSII organization with the role of SOQ1, a recently discovered thylakoid protein that prevents formation of a slowly reversible NPQ state. We developed a statistical image analysis suite to discriminate disordered from crystalline particles and classify crystalline arrays according to their unit cell properties. Through detailed analysis of the local organization of PSII supercomplexes in ordered and disordered phases, we found evidence that interactions among light-harvesting antenna complexes are weakened in the absence of SOQ1, inducing protein rearrangements that favor larger separations between PSII complexes in the majority (disordered) phase and reshaping the PSII crystallization landscape. The features we observe are distinct from known protein rearrangements associated with NPQ, providing further support for a role of SOQ1 in a novel NPQ pathway. The particle clustering and unit cell methodology developed here is generalizable to multiple types of microscopy and will enable unbiased analysis and comparison of large data sets.},
doi = {10.1371/journal.pone.0101470},
journal = {PLoS ONE},
number = 7,
volume = 9,
place = {United States},
year = {Wed Jul 09 00:00:00 EDT 2014},
month = {Wed Jul 09 00:00:00 EDT 2014}
}
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https://doi.org/10.1371/journal.pone.0101470
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Cited by: 19 works
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Works referenced in this record:

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Supramolecular organization of thylakoid membrane proteins in green plants
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Fine structure of granal thylakoid membrane organization using cryo electron tomography
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Supramolecular organization of photosystem II in green plants
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  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
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Refined structure-based simulation of plant light-harvesting complex II: Linear optical spectra of trimers and aggregates
journal, August 2012

High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana
journal, March 2013

  • Kouřil, Roman; Wientjes, Emilie; Bultema, Jelle B.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 3
  • DOI: 10.1016/j.bbabio.2012.12.003

The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts
journal, December 2009

Growing a multi-class classifier with a reject option
journal, July 2008

The Structure of Photosystem II in Arabidopsis: Localization of the CP26 and CP29 Antenna Complexes †
journal, January 2003

  • Yakushevska, Alevtyna E.; Keegstra, Wilko; Boekema, Egbert J.
  • Biochemistry, Vol. 42, Issue 3
  • DOI: 10.1021/bi027109z

Supramolecular Photosystem II Organization in Grana Thylakoid Membranes:  Evidence for a Structured Arrangement †
journal, July 2004

  • Kirchhoff, Helmut; Tremmel, Ira; Haase, Winfried
  • Biochemistry, Vol. 43, Issue 28
  • DOI: 10.1021/bi0494626

Probing the Organization of Photosystem II in Photosynthetic Membranes by Atomic Force Microscopy †
journal, January 2008

  • Kirchhoff, Helmut; Lenhert, Steven; Büchel, Claudia
  • Biochemistry, Vol. 47, Issue 1
  • DOI: 10.1021/bi7017877

Plants lacking the main light-harvesting complex retain photosystem II macro-organization
journal, February 2003

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  • DOI: 10.1038/nature01344

Different crystal morphologies lead to slightly different conformations of light-harvesting complex II as monitored by variations of the intrinsic fluorescence lifetime
journal, January 2011

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  • DOI: 10.1039/c1cp20331b

A thioredoxin-like/ -propeller protein maintains the efficiency of light harvesting in Arabidopsis
journal, July 2013

  • Brooks, M. D.; Sylak-Glassman, E. J.; Fleming, G. R.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 29
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Lack of the Light-Harvesting Complex CP24 Affects the Structure and Function of the Grana Membranes of Higher Plant Chloroplasts
journal, November 2006

  • Kovács, László; Damkjær, Jakob; Kereïche, Sami
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  • DOI: 10.1105/tpc.106.045641

Arrangement of Photosystem II and ATP Synthase in Chloroplast Membranes of Spinach and Pea
journal, April 2010

  • Daum, Bertram; Nicastro, Daniela; Austin, Jotham
  • The Plant Cell, Vol. 22, Issue 4
  • DOI: 10.1105/tpc.109.071431

Photoprotective Energy Dissipation Involves the Reorganization of Photosystem II Light-Harvesting Complexes in the Grana Membranes of Spinach Chloroplasts
journal, April 2011

  • Johnson, Matthew P.; Goral, Tomasz K.; Duffy, Christopher D. P.
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Characterizing Complex Particle Morphologies Through Shape Matching: Descriptors, Applications, and Algorithms
text, January 2010

Coexistence between fluid and crystalline phases of proteins in photosynthetic membranes
text, January 2013

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    journal, January 2016

    • Amarnath, Kapil; Bennett, Doran I. G.; Schneider, Anna R.
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    Models and mechanisms of the rapidly reversible regulation of photosynthetic light harvesting
    journal, April 2019

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    • Biophysical Journal, Vol. 108, Issue 4
    • DOI: 10.1016/j.bpj.2014.12.042

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    journal, July 2016

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    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep29940

    Models and mechanisms of the rapidly reversible regulation of photosynthetic light harvesting
    journal, April 2019

    • Bennett, Doran I. G.; Amarnath, Kapil; Park, Soomin
    • Open Biology, Vol. 9, Issue 4
    • DOI: 10.1098/rsob.190043

    Structural analysis of human NHLRC2, mutations of which are associated with FINCA disease
    journal, August 2018

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