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Protein-Induced Modulation of Chloroplast Membrane Morphology

Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is well established that lipids affect protein functioning and vice versa, it has been only recently suggested that elevated membrane protein concentrations may affect the shape and organization of membran...

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Autores principales: Machettira, Anu B., Groß, Lucia E., Tillmann, Bodo, Weis, Benjamin L., Englich, Gisela, Sommer, Maik S., Königer, Martina, Schleiff, Enrico
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Research Foundation 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3355639/
https://www.ncbi.nlm.nih.gov/pubmed/22639631
http://dx.doi.org/10.3389/fpls.2011.00118
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author Machettira, Anu B.
Groß, Lucia E.
Tillmann, Bodo
Weis, Benjamin L.
Englich, Gisela
Sommer, Maik S.
Königer, Martina
Schleiff, Enrico
author_facet Machettira, Anu B.
Groß, Lucia E.
Tillmann, Bodo
Weis, Benjamin L.
Englich, Gisela
Sommer, Maik S.
Königer, Martina
Schleiff, Enrico
author_sort Machettira, Anu B.
collection PubMed
description Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is well established that lipids affect protein functioning and vice versa, it has been only recently suggested that elevated membrane protein concentrations may affect the shape and organization of membranes. We therefore analyzed the effects of high chloroplast envelope protein concentrations on membrane structures using an in vivo approach with protoplasts. Transient expression of outer envelope proteins or protein domains such as CHUP1-TM–GFP, outer envelope protein of 7 kDa–GFP, or outer envelope protein of 24 kDa–GFP at high levels led to the formation of punctate, circular, and tubular membrane protrusions. Expression of inner membrane proteins such as translocase of inner chloroplast membrane 20, isoform II (Tic20-II)–GFP led to membrane protrusions including invaginations. Using increasing amounts of DNA for transfection, we could show that the frequency, size, and intensity of these protrusions increased with protein concentration. The membrane deformations were absent after cycloheximide treatment. Co-expression of CHUP1-TM–Cherry and Tic20-II–GFP led to membrane protrusions of various shapes and sizes including some stromule-like structures, for which several functions have been proposed. Interestingly, some structures seemed to contain both proteins, while others seem to contain one protein exclusively, indicating that outer and inner envelope dynamics might be regulated independently. While it was more difficult to investigate the effects of high expression levels of membrane proteins on mitochondrial membrane shapes using confocal imaging, it was striking that the expression of the outer membrane protein Tom20 led to more elongate mitochondria. We discuss that the effect of protein concentrations on membrane structure is possibly caused by an imbalance in the lipid to protein ratio and may be involved in a signaling pathway regulating membrane biogenesis. Finally, the observed phenomenon provides a valuable experimental approach to investigate the relationship between lipid synthesis and membrane protein expression in future studies.
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spelling pubmed-33556392012-05-25 Protein-Induced Modulation of Chloroplast Membrane Morphology Machettira, Anu B. Groß, Lucia E. Tillmann, Bodo Weis, Benjamin L. Englich, Gisela Sommer, Maik S. Königer, Martina Schleiff, Enrico Front Plant Sci Plant Science Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is well established that lipids affect protein functioning and vice versa, it has been only recently suggested that elevated membrane protein concentrations may affect the shape and organization of membranes. We therefore analyzed the effects of high chloroplast envelope protein concentrations on membrane structures using an in vivo approach with protoplasts. Transient expression of outer envelope proteins or protein domains such as CHUP1-TM–GFP, outer envelope protein of 7 kDa–GFP, or outer envelope protein of 24 kDa–GFP at high levels led to the formation of punctate, circular, and tubular membrane protrusions. Expression of inner membrane proteins such as translocase of inner chloroplast membrane 20, isoform II (Tic20-II)–GFP led to membrane protrusions including invaginations. Using increasing amounts of DNA for transfection, we could show that the frequency, size, and intensity of these protrusions increased with protein concentration. The membrane deformations were absent after cycloheximide treatment. Co-expression of CHUP1-TM–Cherry and Tic20-II–GFP led to membrane protrusions of various shapes and sizes including some stromule-like structures, for which several functions have been proposed. Interestingly, some structures seemed to contain both proteins, while others seem to contain one protein exclusively, indicating that outer and inner envelope dynamics might be regulated independently. While it was more difficult to investigate the effects of high expression levels of membrane proteins on mitochondrial membrane shapes using confocal imaging, it was striking that the expression of the outer membrane protein Tom20 led to more elongate mitochondria. We discuss that the effect of protein concentrations on membrane structure is possibly caused by an imbalance in the lipid to protein ratio and may be involved in a signaling pathway regulating membrane biogenesis. Finally, the observed phenomenon provides a valuable experimental approach to investigate the relationship between lipid synthesis and membrane protein expression in future studies. Frontiers Research Foundation 2012-01-16 /pmc/articles/PMC3355639/ /pubmed/22639631 http://dx.doi.org/10.3389/fpls.2011.00118 Text en Copyright © 2012 Machettira, Groß, Tillmann, Weis, Englich, Sommer, Königer and Schleiff. http://www.frontiersin.org/licenseagreement This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.
spellingShingle Plant Science
Machettira, Anu B.
Groß, Lucia E.
Tillmann, Bodo
Weis, Benjamin L.
Englich, Gisela
Sommer, Maik S.
Königer, Martina
Schleiff, Enrico
Protein-Induced Modulation of Chloroplast Membrane Morphology
title Protein-Induced Modulation of Chloroplast Membrane Morphology
title_full Protein-Induced Modulation of Chloroplast Membrane Morphology
title_fullStr Protein-Induced Modulation of Chloroplast Membrane Morphology
title_full_unstemmed Protein-Induced Modulation of Chloroplast Membrane Morphology
title_short Protein-Induced Modulation of Chloroplast Membrane Morphology
title_sort protein-induced modulation of chloroplast membrane morphology
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3355639/
https://www.ncbi.nlm.nih.gov/pubmed/22639631
http://dx.doi.org/10.3389/fpls.2011.00118
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