Recovery of the cortical chloroplast layer in the green alga Chara after local irradiation

The cytoplasm of characean internodal cells is characterized by a stationary layer of cortical chloroplast files and a mobile endoplasm moving along subcortical actin bundles. Occasionally, chloroplasts detach from the cortex and are passively carried along with the endoplasmic flow. Previous studie...

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Main Authors: Marion C. Hoepflinger, Margit Höftberger, Aniela Sommer, Florian Hohenberger, Michael Schagerl, Ilse Foissner
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1544999/full
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author Marion C. Hoepflinger
Margit Höftberger
Aniela Sommer
Florian Hohenberger
Michael Schagerl
Ilse Foissner
author_facet Marion C. Hoepflinger
Margit Höftberger
Aniela Sommer
Florian Hohenberger
Michael Schagerl
Ilse Foissner
author_sort Marion C. Hoepflinger
collection DOAJ
description The cytoplasm of characean internodal cells is characterized by a stationary layer of cortical chloroplast files and a mobile endoplasm moving along subcortical actin bundles. Occasionally, chloroplasts detach from the cortex and are passively carried along with the endoplasmic flow. Previous studies revealed that local irradiation with intense light causes chloroplast bleaching followed by a release into the endoplasm (“window formation”). We found that endoplasmic chloroplasts of Chara australis resettle at the window and align parallel to the streaming direction. The process takes several weeks with neither chloroplast division nor growth of proplastids being involved. Both release and re-attachment are actin-dependent. Resettled chloroplasts showed slightly, but significantly lower maximum quantum efficiency (Fv/Fm) values as compared with control regions. Extremely low Fv/Fm values were measured in chloroplasts at the border of the window even after three months indicating longevity, although with serious damage. In higher plants, a protein complex is responsible for the motility and anchorage of chloroplasts, with CHUP1 (CHLOROPLAST UNUSUAL POSITIONING 1) being an essential part. We discovered a homologous form CaCHUP1, encoding a polypeptide of 1201 amino acids with a calculated molecular mass of about 130 kDa. When transiently expressed in epidermal cells of Nicotiana benthamiana leaves, fluorescently tagged CaCHUP1 localizes to chloroplasts. We assume that CaCHUP1 is involved in the anchorage of chloroplasts and in the polymerization of actin filaments, but not in active movement. Our study revealed that endoplasmic chloroplasts can re-anchor at the cell cortex thereby refilling chloroplast-free regions, which we interpret as a repair mechanism after various kinds of damage. It confirms that chloroplasts use different strategies for repositioning, either via polymerization of cp-actin or via cytoplasmic streaming.
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spelling doaj-art-7bf6c4d71c4c4645bcdcd3ef896f81f52025-08-20T03:10:56ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-05-011610.3389/fpls.2025.15449991544999Recovery of the cortical chloroplast layer in the green alga Chara after local irradiationMarion C. Hoepflinger0Margit Höftberger1Aniela Sommer2Florian Hohenberger3Michael Schagerl4Ilse Foissner5Department of Environment and Biodiversity, University of Salzburg, Salzburg, AustriaDepartment of Environment and Biodiversity, University of Salzburg, Salzburg, AustriaDepartment of Environment and Biodiversity, University of Salzburg, Salzburg, AustriaDepartment of Environment and Biodiversity, University of Salzburg, Salzburg, AustriaDepartment of Functional and Evolutionary Ecology, Faculty of Life Sciences, University of Vienna, Vienna, AustriaDepartment of Environment and Biodiversity, University of Salzburg, Salzburg, AustriaThe cytoplasm of characean internodal cells is characterized by a stationary layer of cortical chloroplast files and a mobile endoplasm moving along subcortical actin bundles. Occasionally, chloroplasts detach from the cortex and are passively carried along with the endoplasmic flow. Previous studies revealed that local irradiation with intense light causes chloroplast bleaching followed by a release into the endoplasm (“window formation”). We found that endoplasmic chloroplasts of Chara australis resettle at the window and align parallel to the streaming direction. The process takes several weeks with neither chloroplast division nor growth of proplastids being involved. Both release and re-attachment are actin-dependent. Resettled chloroplasts showed slightly, but significantly lower maximum quantum efficiency (Fv/Fm) values as compared with control regions. Extremely low Fv/Fm values were measured in chloroplasts at the border of the window even after three months indicating longevity, although with serious damage. In higher plants, a protein complex is responsible for the motility and anchorage of chloroplasts, with CHUP1 (CHLOROPLAST UNUSUAL POSITIONING 1) being an essential part. We discovered a homologous form CaCHUP1, encoding a polypeptide of 1201 amino acids with a calculated molecular mass of about 130 kDa. When transiently expressed in epidermal cells of Nicotiana benthamiana leaves, fluorescently tagged CaCHUP1 localizes to chloroplasts. We assume that CaCHUP1 is involved in the anchorage of chloroplasts and in the polymerization of actin filaments, but not in active movement. Our study revealed that endoplasmic chloroplasts can re-anchor at the cell cortex thereby refilling chloroplast-free regions, which we interpret as a repair mechanism after various kinds of damage. It confirms that chloroplasts use different strategies for repositioning, either via polymerization of cp-actin or via cytoplasmic streaming.https://www.frontiersin.org/articles/10.3389/fpls.2025.1544999/fullactin cytoskeletoncharacean internodal cellschloroplast anchorageCaCHUP1 (Chara australis chloroplast unusual positioning 1)confocal laser scanning microscopycortex regeneration
spellingShingle Marion C. Hoepflinger
Margit Höftberger
Aniela Sommer
Florian Hohenberger
Michael Schagerl
Ilse Foissner
Recovery of the cortical chloroplast layer in the green alga Chara after local irradiation
Frontiers in Plant Science
actin cytoskeleton
characean internodal cells
chloroplast anchorage
CaCHUP1 (Chara australis chloroplast unusual positioning 1)
confocal laser scanning microscopy
cortex regeneration
title Recovery of the cortical chloroplast layer in the green alga Chara after local irradiation
title_full Recovery of the cortical chloroplast layer in the green alga Chara after local irradiation
title_fullStr Recovery of the cortical chloroplast layer in the green alga Chara after local irradiation
title_full_unstemmed Recovery of the cortical chloroplast layer in the green alga Chara after local irradiation
title_short Recovery of the cortical chloroplast layer in the green alga Chara after local irradiation
title_sort recovery of the cortical chloroplast layer in the green alga chara after local irradiation
topic actin cytoskeleton
characean internodal cells
chloroplast anchorage
CaCHUP1 (Chara australis chloroplast unusual positioning 1)
confocal laser scanning microscopy
cortex regeneration
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1544999/full
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AT anielasommer recoveryofthecorticalchloroplastlayerinthegreenalgacharaafterlocalirradiation
AT florianhohenberger recoveryofthecorticalchloroplastlayerinthegreenalgacharaafterlocalirradiation
AT michaelschagerl recoveryofthecorticalchloroplastlayerinthegreenalgacharaafterlocalirradiation
AT ilsefoissner recoveryofthecorticalchloroplastlayerinthegreenalgacharaafterlocalirradiation