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SPIRE—a software tool for bicontinuous phase recognition: application for plastid cubic membranes
Plant Physiology ( IF 7.4 ) Pub Date : 2021-10-13 , DOI: 10.1093/plphys/kiab476
Tobias M Hain 1, 2, 3 , Michał Bykowski 4 , Matthias Saba 5 , Myfanwy E Evans 1 , Gerd E Schröder-Turk 2, 6 , Łucja Kowalewska 4
Affiliation  

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.

中文翻译:

SPIRE——双连续相识别软件工具:质体立方膜的应用

细胞器中的双连续膜体现了​​大自然创造复杂功能纳米结构的能力。与合成膜一样,这些膜的特点是连续的膜片覆盖在拓扑复杂的鞍形表面上,具有周期性的网络状结构。它们的结构尺寸(约 50-500 nm)和流体性质使透射电子显微镜 (TEM) 成为解读其纳米结构特征的首选分析方法。在这里,我们提出了一种工具,即表面投影图像识别环境 (SPIRE),通过与数学“节点表面”模型进行比较,通过交互式识别来识别 TEM 切片中的双连续结构。植物黄质体的原板层体(PLB)是一种双连续膜结构,在叶绿体生物发生中具有关键的生理作用。然而,由于缺乏能够识别和定量分析对称膜构象的工具,其空间结构特征的确定受到阻碍。使用我们的 SPIRE 工具,我们对双连续金刚石表面作为被子植物原生质体中主要的 PLB 几何形状进行了可靠的识别,这与文献中早期的长期主张形成鲜明对比。我们的数据还提供了对不同体积比例的 PLB 的膜存储容量的见解,并暗示直接位于 PLB 网格内部的质体核糖体对其正常功能的作用有限。这代表着理解它们迄今为止难以捉摸的结构-功能关系的重要一步。
更新日期:2021-10-13
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