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SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes

Bicontinuous membranes in cell organelles epitomize nature’s ability to create complex functional nanostructures. Like their synthetic counterparts, these membranes are characterized by continuous membrane sheets draped onto topologically complex saddle-shaped surfaces with a periodic network-like s...

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Autores principales: Hain, Tobias M, Bykowski, Michał, Saba, Matthias, Evans, Myfanwy E, Schröder-Turk, Gerd E, Kowalewska, Łucja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8774748/
https://www.ncbi.nlm.nih.gov/pubmed/34662407
http://dx.doi.org/10.1093/plphys/kiab476
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author Hain, Tobias M
Bykowski, Michał
Saba, Matthias
Evans, Myfanwy E
Schröder-Turk, Gerd E
Kowalewska, Łucja
author_facet Hain, Tobias M
Bykowski, Michał
Saba, Matthias
Evans, Myfanwy E
Schröder-Turk, Gerd E
Kowalewska, Łucja
author_sort Hain, Tobias M
collection PubMed
description Bicontinuous membranes in cell organelles epitomize nature’s ability to create complex functional nanostructures. Like their synthetic counterparts, these membranes are characterized by continuous membrane sheets draped onto topologically complex saddle-shaped surfaces with a periodic network-like structure. Their structure sizes, (around 50–500 nm), and fluid nature make transmission electron microscopy (TEM) the analysis method of choice to decipher their nanostructural features. Here we present a tool, Surface Projection Image Recognition Environment (SPIRE), to identify bicontinuous structures from TEM sections through interactive identification by comparison to mathematical “nodal surface” models. The prolamellar body (PLB) of plant etioplasts is a bicontinuous membrane structure with a key physiological role in chloroplast biogenesis. However, the determination of its spatial structural features has been held back by the lack of tools enabling the identification and quantitative analysis of symmetric membrane conformations. Using our SPIRE tool, we achieved a robust identification of the bicontinuous diamond surface as the dominant PLB geometry in angiosperm etioplasts in contrast to earlier long-standing assertions in the literature. Our data also provide insights into membrane storage capacities of PLBs with different volume proportions and hint at the limited role of a plastid ribosome localization directly inside the PLB grid for its proper functioning. This represents an important step in understanding their as yet elusive structure–function relationship.
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spelling pubmed-87747482022-01-21 SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes Hain, Tobias M Bykowski, Michał Saba, Matthias Evans, Myfanwy E Schröder-Turk, Gerd E Kowalewska, Łucja Plant Physiol Breakthrough Technologies, Tools, and Resources Bicontinuous membranes in cell organelles epitomize nature’s ability to create complex functional nanostructures. Like their synthetic counterparts, these membranes are characterized by continuous membrane sheets draped onto topologically complex saddle-shaped surfaces with a periodic network-like structure. Their structure sizes, (around 50–500 nm), and fluid nature make transmission electron microscopy (TEM) the analysis method of choice to decipher their nanostructural features. Here we present a tool, Surface Projection Image Recognition Environment (SPIRE), to identify bicontinuous structures from TEM sections through interactive identification by comparison to mathematical “nodal surface” models. The prolamellar body (PLB) of plant etioplasts is a bicontinuous membrane structure with a key physiological role in chloroplast biogenesis. However, the determination of its spatial structural features has been held back by the lack of tools enabling the identification and quantitative analysis of symmetric membrane conformations. Using our SPIRE tool, we achieved a robust identification of the bicontinuous diamond surface as the dominant PLB geometry in angiosperm etioplasts in contrast to earlier long-standing assertions in the literature. Our data also provide insights into membrane storage capacities of PLBs with different volume proportions and hint at the limited role of a plastid ribosome localization directly inside the PLB grid for its proper functioning. This represents an important step in understanding their as yet elusive structure–function relationship. Oxford University Press 2021-10-18 /pmc/articles/PMC8774748/ /pubmed/34662407 http://dx.doi.org/10.1093/plphys/kiab476 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Breakthrough Technologies, Tools, and Resources
Hain, Tobias M
Bykowski, Michał
Saba, Matthias
Evans, Myfanwy E
Schröder-Turk, Gerd E
Kowalewska, Łucja
SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes
title SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes
title_full SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes
title_fullStr SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes
title_full_unstemmed SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes
title_short SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes
title_sort spire—a software tool for bicontinuous phase recognition: application for plastid cubic membranes
topic Breakthrough Technologies, Tools, and Resources
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8774748/
https://www.ncbi.nlm.nih.gov/pubmed/34662407
http://dx.doi.org/10.1093/plphys/kiab476
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