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

Autores
Nakata, Keisuke; Hatakeyama, Yuto; Erra Balsells, Rosa; Nonami, Hiroshi; Wada, Hiroshi
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: Nakata, Keisuke. Ehime University; Japón
Fil: Hatakeyama, Yuto. Ehime University; Japón
Fil: Erra Balsells, Rosa. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Centro de Investigaciones en Hidratos de Carbono. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Centro de Investigaciones en Hidratos de Carbono; Argentina
Fil: Nonami, Hiroshi. Ehime University; Japón
Fil: Wada, Hiroshi. Ehime University; Japón
Materia
Metabolomic
picoPPESI-MS
Cardiolipins
Plant Phisiology
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/212867
Acceder
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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditionsNakata, KeisukeHatakeyama, YutoErra Balsells, RosaNonami, HiroshiWada, HiroshiMetabolomicpicoPPESI-MSCardiolipinsPlant Phisiologyhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Maintaining 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.Fil: Nakata, Keisuke. Ehime University; JapónFil: Hatakeyama, Yuto. Ehime University; JapónFil: Erra Balsells, Rosa. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Centro de Investigaciones en Hidratos de Carbono. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Centro de Investigaciones en Hidratos de Carbono; ArgentinaFil: Nonami, Hiroshi. Ehime University; JapónFil: Wada, Hiroshi. Ehime University; JapónNature2022-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/212867Nakata, 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; Nature; Scientific Reports; 12; 1; 12-2022; 1-162045-2322CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-022-14164-3info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:10:30Zoai:ri.conicet.gov.ar:11336/212867instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:10:30.99CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv 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
spellingShingle Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
Nakata, Keisuke
Metabolomic
picoPPESI-MS
Cardiolipins
Plant Phisiology
title_short 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_sort Dynamics and stabilization mechanism of mitochondrial cristae morphofunction associated with turgor-driven cardiolipin biosynthesis under salt stress conditions
dc.creator.none.fl_str_mv Nakata, Keisuke
Hatakeyama, Yuto
Erra Balsells, Rosa
Nonami, Hiroshi
Wada, Hiroshi
author Nakata, Keisuke
author_facet Nakata, Keisuke
Hatakeyama, Yuto
Erra Balsells, Rosa
Nonami, Hiroshi
Wada, Hiroshi
author_role author
author2 Hatakeyama, Yuto
Erra Balsells, Rosa
Nonami, Hiroshi
Wada, Hiroshi
author2_role author
author
author
author
dc.subject.none.fl_str_mv Metabolomic
picoPPESI-MS
Cardiolipins
Plant Phisiology
topic Metabolomic
picoPPESI-MS
Cardiolipins
Plant Phisiology
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv 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.
Fil: Nakata, Keisuke. Ehime University; Japón
Fil: Hatakeyama, Yuto. Ehime University; Japón
Fil: Erra Balsells, Rosa. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Centro de Investigaciones en Hidratos de Carbono. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Centro de Investigaciones en Hidratos de Carbono; Argentina
Fil: Nonami, Hiroshi. Ehime University; Japón
Fil: Wada, Hiroshi. Ehime University; Japón
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.
publishDate 2022
dc.date.none.fl_str_mv 2022-12
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/212867
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; Nature; Scientific Reports; 12; 1; 12-2022; 1-16
2045-2322
CONICET Digital
CONICET
url http://hdl.handle.net/11336/212867
identifier_str_mv 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; Nature; Scientific Reports; 12; 1; 12-2022; 1-16
2045-2322
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-022-14164-3
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature
publisher.none.fl_str_mv Nature
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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