Cargando…
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...
Autores principales: | , , , , , |
---|---|
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 |
_version_ | 1784636421059903488 |
---|---|
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. |
format | Online Article Text |
id | pubmed-8774748 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT haintobiasm spireasoftwaretoolforbicontinuousphaserecognitionapplicationforplastidcubicmembranes AT bykowskimichał spireasoftwaretoolforbicontinuousphaserecognitionapplicationforplastidcubicmembranes AT sabamatthias spireasoftwaretoolforbicontinuousphaserecognitionapplicationforplastidcubicmembranes AT evansmyfanwye spireasoftwaretoolforbicontinuousphaserecognitionapplicationforplastidcubicmembranes AT schroderturkgerde spireasoftwaretoolforbicontinuousphaserecognitionapplicationforplastidcubicmembranes AT kowalewskałucja spireasoftwaretoolforbicontinuousphaserecognitionapplicationforplastidcubicmembranes |