Longitudinal growth of the Saccharina kelp embryo depends on actin filaments that control the formation of a corset-like structure composed of alginate

Abstract The initiation of embryogenesis in the kelp Saccharina latissima is accompanied by significant anisotropy in cell shape. Using monoclonal antibodies, we show that this anisotropy coincides with a spatio-temporal pattern of accumulation of alginates in the cell wall of the zygote and embryo....

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Main Authors: Samuel Boscq, Ioannis Theodorou, Roman Milstein, Aude Le Bail, Sabine Chenivesse, Bernard Billoud, Bénédicte Charrier
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-024-83814-5
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author Samuel Boscq
Ioannis Theodorou
Roman Milstein
Aude Le Bail
Sabine Chenivesse
Bernard Billoud
Bénédicte Charrier
author_facet Samuel Boscq
Ioannis Theodorou
Roman Milstein
Aude Le Bail
Sabine Chenivesse
Bernard Billoud
Bénédicte Charrier
author_sort Samuel Boscq
collection DOAJ
description Abstract The initiation of embryogenesis in the kelp Saccharina latissima is accompanied by significant anisotropy in cell shape. Using monoclonal antibodies, we show that this anisotropy coincides with a spatio-temporal pattern of accumulation of alginates in the cell wall of the zygote and embryo. Alginates rich in guluronates as well as sulphated fucans show a homogeneous distribution in the embryo throughout Phase I of embryogenesis, but mannuronate alginates accumulate mainly on the sides of the zygote and embryo, disappearing as the embryo enlarges at the start of Phase II. This pattern depends on the presence of cortical actin filaments. In contrast, within the embryo lamina, the alginate composition of the walls newly formed by cytokinesis is not affected by the depolymerisation of actin filaments. Thus, in addition to revealing the existence of a mannuronate-rich alginate corset-like structure that may restrict the enlargement of the zygote and the embryo, thereby promoting the formation of the apico-basal growth axis, we demonstrate stage- and cytoskeleton-dependent differences in cell wall deposition in Saccharina embryos.
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institution Kabale University
issn 2045-2322
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publishDate 2025-01-01
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series Scientific Reports
spelling doaj-art-6b48e9f5375d422185582aa7f9dda6192025-01-12T12:23:22ZengNature PortfolioScientific Reports2045-23222025-01-0115111510.1038/s41598-024-83814-5Longitudinal growth of the Saccharina kelp embryo depends on actin filaments that control the formation of a corset-like structure composed of alginateSamuel Boscq0Ioannis Theodorou1Roman Milstein2Aude Le Bail3Sabine Chenivesse4Bernard Billoud5Bénédicte Charrier6Morphogenesis of Macro Algae, UMR8227, CNRS - Sorbonne UniversityMorphogenesis of Macro Algae, UMR8227, CNRS - Sorbonne UniversityMorphogenesis of Macro Algae, UMR8227, CNRS - Sorbonne UniversityMorphogenesis of Macro Algae, UMR8227, CNRS - Sorbonne UniversityMorphogenesis of Macro Algae, UMR8227, CNRS - Sorbonne UniversityMorphogenesis of Macro Algae, UMR8227, CNRS - Sorbonne UniversityMorphogenesis of Macro Algae, UMR8227, CNRS - Sorbonne UniversityAbstract The initiation of embryogenesis in the kelp Saccharina latissima is accompanied by significant anisotropy in cell shape. Using monoclonal antibodies, we show that this anisotropy coincides with a spatio-temporal pattern of accumulation of alginates in the cell wall of the zygote and embryo. Alginates rich in guluronates as well as sulphated fucans show a homogeneous distribution in the embryo throughout Phase I of embryogenesis, but mannuronate alginates accumulate mainly on the sides of the zygote and embryo, disappearing as the embryo enlarges at the start of Phase II. This pattern depends on the presence of cortical actin filaments. In contrast, within the embryo lamina, the alginate composition of the walls newly formed by cytokinesis is not affected by the depolymerisation of actin filaments. Thus, in addition to revealing the existence of a mannuronate-rich alginate corset-like structure that may restrict the enlargement of the zygote and the embryo, thereby promoting the formation of the apico-basal growth axis, we demonstrate stage- and cytoskeleton-dependent differences in cell wall deposition in Saccharina embryos.https://doi.org/10.1038/s41598-024-83814-5
spellingShingle Samuel Boscq
Ioannis Theodorou
Roman Milstein
Aude Le Bail
Sabine Chenivesse
Bernard Billoud
Bénédicte Charrier
Longitudinal growth of the Saccharina kelp embryo depends on actin filaments that control the formation of a corset-like structure composed of alginate
Scientific Reports
title Longitudinal growth of the Saccharina kelp embryo depends on actin filaments that control the formation of a corset-like structure composed of alginate
title_full Longitudinal growth of the Saccharina kelp embryo depends on actin filaments that control the formation of a corset-like structure composed of alginate
title_fullStr Longitudinal growth of the Saccharina kelp embryo depends on actin filaments that control the formation of a corset-like structure composed of alginate
title_full_unstemmed Longitudinal growth of the Saccharina kelp embryo depends on actin filaments that control the formation of a corset-like structure composed of alginate
title_short Longitudinal growth of the Saccharina kelp embryo depends on actin filaments that control the formation of a corset-like structure composed of alginate
title_sort longitudinal growth of the saccharina kelp embryo depends on actin filaments that control the formation of a corset like structure composed of alginate
url https://doi.org/10.1038/s41598-024-83814-5
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