Cargando…

Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions

Maintaining energy production efficiency is of vital importance to plants growing under changing environments. Cardiolipin localized in the inner mitochondrial membrane plays various important roles in mitochondrial function and its activity, although the regulation of mitochondrial morphology to va...

Descripción completa

Detalles Bibliográficos
Autores principales: Nakata, Keisuke, Hatakeyama, Yuto, Erra-Balsells, Rosa, Nonami, Hiroshi, Wada, Hiroshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9249792/
https://www.ncbi.nlm.nih.gov/pubmed/35778427
http://dx.doi.org/10.1038/s41598-022-14164-3
_version_ 1784739666152390656
author Nakata, Keisuke
Hatakeyama, Yuto
Erra-Balsells, Rosa
Nonami, Hiroshi
Wada, Hiroshi
author_facet Nakata, Keisuke
Hatakeyama, Yuto
Erra-Balsells, Rosa
Nonami, Hiroshi
Wada, Hiroshi
author_sort Nakata, Keisuke
collection PubMed
description Maintaining energy production efficiency is of vital importance to plants growing under changing environments. Cardiolipin localized in the inner mitochondrial membrane plays various important roles in mitochondrial function and its activity, although the regulation of mitochondrial morphology to various stress conditions remains obscure, particularly in the context of changes in cellular water relations and metabolisms. By combining single-cell metabolomics with transmission electron microscopy, we have investigated the adaptation mechanism in tomato trichome stalk cells at moderate salt stress to determine the kinetics of cellular parameters and metabolisms. We have found that turgor loss occurred just after the stress conditions, followed by the contrasting volumetric changes in mitochondria and cells, the accumulation of TCA cycle-related metabolites at osmotic adjustment, and a temporal increase in cardiolipin concentration, resulting in a reversible topological modification in the tubulo-vesicular cristae. Because all of these cellular events were dynamically observed in the same single-cells without causing any disturbance for redox states and cytoplasmic streaming, we conclude that turgor pressure might play a regulatory role in the mitochondrial morphological switch throughout the temporal activation of cardiolipin biosynthesis, which sustains mitochondrial respiration and energy conversion even under the salt stress conditions.
format Online
Article
Text
id pubmed-9249792
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-92497922022-07-03 Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions Nakata, Keisuke Hatakeyama, Yuto Erra-Balsells, Rosa Nonami, Hiroshi Wada, Hiroshi Sci Rep Article Maintaining energy production efficiency is of vital importance to plants growing under changing environments. Cardiolipin localized in the inner mitochondrial membrane plays various important roles in mitochondrial function and its activity, although the regulation of mitochondrial morphology to various stress conditions remains obscure, particularly in the context of changes in cellular water relations and metabolisms. By combining single-cell metabolomics with transmission electron microscopy, we have investigated the adaptation mechanism in tomato trichome stalk cells at moderate salt stress to determine the kinetics of cellular parameters and metabolisms. We have found that turgor loss occurred just after the stress conditions, followed by the contrasting volumetric changes in mitochondria and cells, the accumulation of TCA cycle-related metabolites at osmotic adjustment, and a temporal increase in cardiolipin concentration, resulting in a reversible topological modification in the tubulo-vesicular cristae. Because all of these cellular events were dynamically observed in the same single-cells without causing any disturbance for redox states and cytoplasmic streaming, we conclude that turgor pressure might play a regulatory role in the mitochondrial morphological switch throughout the temporal activation of cardiolipin biosynthesis, which sustains mitochondrial respiration and energy conversion even under the salt stress conditions. Nature Publishing Group UK 2022-07-01 /pmc/articles/PMC9249792/ /pubmed/35778427 http://dx.doi.org/10.1038/s41598-022-14164-3 Text en © The Author(s) 2022 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/) .
spellingShingle Article
Nakata, Keisuke
Hatakeyama, Yuto
Erra-Balsells, Rosa
Nonami, Hiroshi
Wada, Hiroshi
Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
title Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
title_full Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
title_fullStr Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
title_full_unstemmed Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
title_short Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
title_sort dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9249792/
https://www.ncbi.nlm.nih.gov/pubmed/35778427
http://dx.doi.org/10.1038/s41598-022-14164-3
work_keys_str_mv AT nakatakeisuke dynamicsandstabilizationmechanismofmitochondrialcristaemorphofunctionassociatedwithturgordrivencardiolipinbiosynthesisundersaltstressconditions
AT hatakeyamayuto dynamicsandstabilizationmechanismofmitochondrialcristaemorphofunctionassociatedwithturgordrivencardiolipinbiosynthesisundersaltstressconditions
AT errabalsellsrosa dynamicsandstabilizationmechanismofmitochondrialcristaemorphofunctionassociatedwithturgordrivencardiolipinbiosynthesisundersaltstressconditions
AT nonamihiroshi dynamicsandstabilizationmechanismofmitochondrialcristaemorphofunctionassociatedwithturgordrivencardiolipinbiosynthesisundersaltstressconditions
AT wadahiroshi dynamicsandstabilizationmechanismofmitochondrialcristaemorphofunctionassociatedwithturgordrivencardiolipinbiosynthesisundersaltstressconditions