Normal oil body formation in Marchantia polymorpha requires functional coat protein complex I proteins

Eukaryotic cells possess endomembrane organelles equipped with specific sets of proteins, lipids, and polysaccharides that are fundamental for realizing each organelle’s specific function and shape. A tightly regulated membrane trafficking system mediates the transportation and localization of these...

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Main Authors: Takehiko Kanazawa, Ryuichi Nishihama, Takashi Ueda
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.979066/full
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author Takehiko Kanazawa
Takehiko Kanazawa
Ryuichi Nishihama
Takashi Ueda
Takashi Ueda
author_facet Takehiko Kanazawa
Takehiko Kanazawa
Ryuichi Nishihama
Takashi Ueda
Takashi Ueda
author_sort Takehiko Kanazawa
collection DOAJ
description Eukaryotic cells possess endomembrane organelles equipped with specific sets of proteins, lipids, and polysaccharides that are fundamental for realizing each organelle’s specific function and shape. A tightly regulated membrane trafficking system mediates the transportation and localization of these substances. Generally, the secretory/exocytic pathway is responsible for transporting cargo to the plasma membrane and/or the extracellular space. However, in the case of oil body cells in the liverwort Marchantia polymorpha, the oil body, a liverwort-unique organelle, is thought to be formed by secretory vesicle fusion through redirection of the secretory pathway inside the cell. Although their formation mechanism remains largely unclear, oil bodies exhibit a complex and bumpy surface structure. In this study, we isolated a mutant with spherical oil bodies through visual screening of mutants with abnormally shaped oil bodies. This mutant harbored a mutation in a coat protein complex I (COPI) subunit MpSEC28, and a similar effect on oil body morphology was also detected in knockdown mutants of other COPI subunits. Fluorescently tagged MpSEC28 was localized to the periphery of the Golgi apparatus together with other subunits, suggesting that it is involved in retrograde transport from and/or in the Golgi apparatus as a component of the COPI coat. The Mpsec28 mutants also exhibited weakened stiffness of the thalli, suggesting impaired cell–cell adhesion and cell wall integrity. These findings suggest that the mechanism of cell wall biosynthesis is also involved in shaping the oil body in M. polymorpha, supporting the redirection of the secretory pathway inward the cell during oil body formation.
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spelling doaj.art-f8863113fe2a4dbe8e4fb28adfadb7942022-12-22T02:45:46ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-08-011310.3389/fpls.2022.979066979066Normal oil body formation in Marchantia polymorpha requires functional coat protein complex I proteinsTakehiko Kanazawa0Takehiko Kanazawa1Ryuichi Nishihama2Takashi Ueda3Takashi Ueda4Division of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Aichi, JapanThe Department of Basic Biology, SOKENDAI (The Graduate University for Advanced Studies), Okazaki, Aichi, JapanDepartment of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, Noda, JapanDivision of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Aichi, JapanThe Department of Basic Biology, SOKENDAI (The Graduate University for Advanced Studies), Okazaki, Aichi, JapanEukaryotic cells possess endomembrane organelles equipped with specific sets of proteins, lipids, and polysaccharides that are fundamental for realizing each organelle’s specific function and shape. A tightly regulated membrane trafficking system mediates the transportation and localization of these substances. Generally, the secretory/exocytic pathway is responsible for transporting cargo to the plasma membrane and/or the extracellular space. However, in the case of oil body cells in the liverwort Marchantia polymorpha, the oil body, a liverwort-unique organelle, is thought to be formed by secretory vesicle fusion through redirection of the secretory pathway inside the cell. Although their formation mechanism remains largely unclear, oil bodies exhibit a complex and bumpy surface structure. In this study, we isolated a mutant with spherical oil bodies through visual screening of mutants with abnormally shaped oil bodies. This mutant harbored a mutation in a coat protein complex I (COPI) subunit MpSEC28, and a similar effect on oil body morphology was also detected in knockdown mutants of other COPI subunits. Fluorescently tagged MpSEC28 was localized to the periphery of the Golgi apparatus together with other subunits, suggesting that it is involved in retrograde transport from and/or in the Golgi apparatus as a component of the COPI coat. The Mpsec28 mutants also exhibited weakened stiffness of the thalli, suggesting impaired cell–cell adhesion and cell wall integrity. These findings suggest that the mechanism of cell wall biosynthesis is also involved in shaping the oil body in M. polymorpha, supporting the redirection of the secretory pathway inward the cell during oil body formation.https://www.frontiersin.org/articles/10.3389/fpls.2022.979066/fullMarchantia polymorphaoil bodymembrane trafficGolgi apparatussecretory pathwayCOPI coat
spellingShingle Takehiko Kanazawa
Takehiko Kanazawa
Ryuichi Nishihama
Takashi Ueda
Takashi Ueda
Normal oil body formation in Marchantia polymorpha requires functional coat protein complex I proteins
Frontiers in Plant Science
Marchantia polymorpha
oil body
membrane traffic
Golgi apparatus
secretory pathway
COPI coat
title Normal oil body formation in Marchantia polymorpha requires functional coat protein complex I proteins
title_full Normal oil body formation in Marchantia polymorpha requires functional coat protein complex I proteins
title_fullStr Normal oil body formation in Marchantia polymorpha requires functional coat protein complex I proteins
title_full_unstemmed Normal oil body formation in Marchantia polymorpha requires functional coat protein complex I proteins
title_short Normal oil body formation in Marchantia polymorpha requires functional coat protein complex I proteins
title_sort normal oil body formation in marchantia polymorpha requires functional coat protein complex i proteins
topic Marchantia polymorpha
oil body
membrane traffic
Golgi apparatus
secretory pathway
COPI coat
url https://www.frontiersin.org/articles/10.3389/fpls.2022.979066/full
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AT ryuichinishihama normaloilbodyformationinmarchantiapolymorpharequiresfunctionalcoatproteincomplexiproteins
AT takashiueda normaloilbodyformationinmarchantiapolymorpharequiresfunctionalcoatproteincomplexiproteins
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