Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids.

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 p...

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Main Authors: Bibiana Onoa, Anna R Schneider, Matthew D Brooks, Patricia Grob, Eva Nogales, Phillip L Geissler, Krishna K Niyogi, Carlos Bustamante
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4090009?pdf=render
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spelling doaj-38174b01a8ab471dadaae3b2fe7c6d252020-11-25T00:48:00ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0197e10147010.1371/journal.pone.0101470Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids.Bibiana OnoaAnna R SchneiderMatthew D BrooksPatricia GrobEva NogalesPhillip L GeisslerKrishna K NiyogiCarlos BustamantePhotoautotrophic 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.http://europepmc.org/articles/PMC4090009?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Bibiana Onoa
Anna R Schneider
Matthew D Brooks
Patricia Grob
Eva Nogales
Phillip L Geissler
Krishna K Niyogi
Carlos Bustamante
spellingShingle Bibiana Onoa
Anna R Schneider
Matthew D Brooks
Patricia Grob
Eva Nogales
Phillip L Geissler
Krishna K Niyogi
Carlos Bustamante
Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids.
PLoS ONE
author_facet Bibiana Onoa
Anna R Schneider
Matthew D Brooks
Patricia Grob
Eva Nogales
Phillip L Geissler
Krishna K Niyogi
Carlos Bustamante
author_sort Bibiana Onoa
title Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids.
title_short Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids.
title_full Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids.
title_fullStr Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids.
title_full_unstemmed Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids.
title_sort atomic force microscopy of photosystem ii and its unit cell clustering quantitatively delineate the mesoscale variability in arabidopsis thylakoids.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2014-01-01
description 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.
url http://europepmc.org/articles/PMC4090009?pdf=render
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