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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. and Kowalewska, Łucja (2022) In Plant Physiology 188(1). p.81-96
Abstract

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... (More)

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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author
; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
subject
in
Plant Physiology
volume
188
issue
1
pages
16 pages
publisher
American Society of Plant Biologists
external identifiers
  • scopus:85123731306
  • pmid:34662407
ISSN
0032-0889
DOI
10.1093/plphys/kiab476
language
English
LU publication?
no
id
b9c6d47d-d39b-45e5-afa2-2cd7ee36d23d
date added to LUP
2022-02-18 15:22:52
date last changed
2024-04-23 01:50:50
@article{b9c6d47d-d39b-45e5-afa2-2cd7ee36d23d,
  abstract     = {{<p>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.</p>}},
  author       = {{Hain, Tobias M. and Bykowski, Michał and Saba, Matthias and Evans, Myfanwy E. and Schröder-Turk, Gerd E. and Kowalewska, Łucja}},
  issn         = {{0032-0889}},
  language     = {{eng}},
  month        = {{01}},
  number       = {{1}},
  pages        = {{81--96}},
  publisher    = {{American Society of Plant Biologists}},
  series       = {{Plant Physiology}},
  title        = {{SPIRE—a software tool for bicontinuous phase recognition : application for plastid cubic membranes}},
  url          = {{http://dx.doi.org/10.1093/plphys/kiab476}},
  doi          = {{10.1093/plphys/kiab476}},
  volume       = {{188}},
  year         = {{2022}},
}