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Statistical analysis of organelle movement using state-space models

BACKGROUND: Organelle motility is essential for the correct cellular function of various eukaryotic cells. In plant cells, chloroplasts move towards the intracellular area irradiated by a weak light to maximise photosynthesis. To initiate this process, an unknown signal is transferred from the irrad...

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Autores principales: Nishio, Haruki, Hirano, Satoyuki, Kodama, Yutaka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10321007/
https://www.ncbi.nlm.nih.gov/pubmed/37407985
http://dx.doi.org/10.1186/s13007-023-01038-6
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author Nishio, Haruki
Hirano, Satoyuki
Kodama, Yutaka
author_facet Nishio, Haruki
Hirano, Satoyuki
Kodama, Yutaka
author_sort Nishio, Haruki
collection PubMed
description BACKGROUND: Organelle motility is essential for the correct cellular function of various eukaryotic cells. In plant cells, chloroplasts move towards the intracellular area irradiated by a weak light to maximise photosynthesis. To initiate this process, an unknown signal is transferred from the irradiated area to distant chloroplasts. Quantification of this chloroplast movement has been performed using visual estimations that are analyst-dependent and labour-intensive. Therefore, an objective and faster method is required. RESULTS: In this study, we developed the cellssm package of R (https://github.com/hnishio/cellssm.git), which is a user-friendly tool for state-space modelling to statistically analyse the directional movement of cells or organelles. Our method showed a high accuracy in estimating the start time of chloroplast movement in the liverwort Marchantia polymorpha over a short period. The tool indicated that chloroplast movement accelerates during transport to the irradiated area and that signal transfer speed is uneven within a cell. We also developed a method to estimate the common dynamics among multiple chloroplasts in each cell, which clarified different characteristics among cells. CONCLUSIONS: We demonstrated that state-space modelling is a powerful method to understand organelle movement in eukaryotic cells. The cellssm package can be applied to various directional movements (both accumulation and avoidance) at cellular and subcellular levels to estimate the true transition of states behind the time-series data. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13007-023-01038-6.
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spelling pubmed-103210072023-07-06 Statistical analysis of organelle movement using state-space models Nishio, Haruki Hirano, Satoyuki Kodama, Yutaka Plant Methods Research BACKGROUND: Organelle motility is essential for the correct cellular function of various eukaryotic cells. In plant cells, chloroplasts move towards the intracellular area irradiated by a weak light to maximise photosynthesis. To initiate this process, an unknown signal is transferred from the irradiated area to distant chloroplasts. Quantification of this chloroplast movement has been performed using visual estimations that are analyst-dependent and labour-intensive. Therefore, an objective and faster method is required. RESULTS: In this study, we developed the cellssm package of R (https://github.com/hnishio/cellssm.git), which is a user-friendly tool for state-space modelling to statistically analyse the directional movement of cells or organelles. Our method showed a high accuracy in estimating the start time of chloroplast movement in the liverwort Marchantia polymorpha over a short period. The tool indicated that chloroplast movement accelerates during transport to the irradiated area and that signal transfer speed is uneven within a cell. We also developed a method to estimate the common dynamics among multiple chloroplasts in each cell, which clarified different characteristics among cells. CONCLUSIONS: We demonstrated that state-space modelling is a powerful method to understand organelle movement in eukaryotic cells. The cellssm package can be applied to various directional movements (both accumulation and avoidance) at cellular and subcellular levels to estimate the true transition of states behind the time-series data. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13007-023-01038-6. BioMed Central 2023-07-05 /pmc/articles/PMC10321007/ /pubmed/37407985 http://dx.doi.org/10.1186/s13007-023-01038-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Nishio, Haruki
Hirano, Satoyuki
Kodama, Yutaka
Statistical analysis of organelle movement using state-space models
title Statistical analysis of organelle movement using state-space models
title_full Statistical analysis of organelle movement using state-space models
title_fullStr Statistical analysis of organelle movement using state-space models
title_full_unstemmed Statistical analysis of organelle movement using state-space models
title_short Statistical analysis of organelle movement using state-space models
title_sort statistical analysis of organelle movement using state-space models
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10321007/
https://www.ncbi.nlm.nih.gov/pubmed/37407985
http://dx.doi.org/10.1186/s13007-023-01038-6
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