Dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort Marchantia polymorpha

Summary: Mitochondria change their morphology in response to developmental and environmental cues. During sexual reproduction, bryophytes produce spermatozoids with two mitochondria in the cell body. Although intensive morphological analyses have been conducted, how this fixed number of mitochondria...

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Main Authors: Takuya Norizuki, Naoki Minamino, Miyuki Sato, Hirokazu Tsukaya, Takashi Ueda
Format: Article
Language:English
Published: Elsevier 2022-06-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124722007616
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author Takuya Norizuki
Naoki Minamino
Miyuki Sato
Hirokazu Tsukaya
Takashi Ueda
author_facet Takuya Norizuki
Naoki Minamino
Miyuki Sato
Hirokazu Tsukaya
Takashi Ueda
author_sort Takuya Norizuki
collection DOAJ
description Summary: Mitochondria change their morphology in response to developmental and environmental cues. During sexual reproduction, bryophytes produce spermatozoids with two mitochondria in the cell body. Although intensive morphological analyses have been conducted, how this fixed number of mitochondria is realized remains poorly understood. Here, we investigate how mitochondria are reorganized during spermiogenesis in Marchantia polymorpha. We find that the mitochondrial number is reduced to one through fission followed by autophagic degradation during early spermiogenesis, and then the posterior mitochondrion arises by fission of the anterior mitochondrion. Autophagy is also responsible for the removal of other organelles, including peroxisomes, but these other organelles are removed at distinct developmental stages from mitochondrial degradation. We also find that spermiogenesis involves nonautophagic organelle degradation. Our findings highlight the dynamic reorganization of mitochondria, which is regulated distinctly from that of other organelles, and multiple degradation mechanisms operate in organelle remodeling during spermiogenesis in M. polymorpha.
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spelling doaj.art-ec58b6e199754dc99af19c92bf80421d2022-12-22T00:29:28ZengElsevierCell Reports2211-12472022-06-013911110975Dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort Marchantia polymorphaTakuya Norizuki0Naoki Minamino1Miyuki Sato2Hirokazu Tsukaya3Takashi Ueda4Division of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan; Laboratory of Molecular Membrane Biology, Institute for Molecular and Cellular Regulation, Gunma University, Maebashi, Gunma 371-8512, JapanDivision of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Aichi 444-8585, JapanLaboratory of Molecular Membrane Biology, Institute for Molecular and Cellular Regulation, Gunma University, Maebashi, Gunma 371-8512, JapanDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, JapanDivision of Cellular Dynamics, National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan; Department of Basic Biology, SOKENDAI (The Graduate University for Advanced Studies), Okazaki, Aichi 444-8585, Japan; Corresponding authorSummary: Mitochondria change their morphology in response to developmental and environmental cues. During sexual reproduction, bryophytes produce spermatozoids with two mitochondria in the cell body. Although intensive morphological analyses have been conducted, how this fixed number of mitochondria is realized remains poorly understood. Here, we investigate how mitochondria are reorganized during spermiogenesis in Marchantia polymorpha. We find that the mitochondrial number is reduced to one through fission followed by autophagic degradation during early spermiogenesis, and then the posterior mitochondrion arises by fission of the anterior mitochondrion. Autophagy is also responsible for the removal of other organelles, including peroxisomes, but these other organelles are removed at distinct developmental stages from mitochondrial degradation. We also find that spermiogenesis involves nonautophagic organelle degradation. Our findings highlight the dynamic reorganization of mitochondria, which is regulated distinctly from that of other organelles, and multiple degradation mechanisms operate in organelle remodeling during spermiogenesis in M. polymorpha.http://www.sciencedirect.com/science/article/pii/S2211124722007616CP: Plants
spellingShingle Takuya Norizuki
Naoki Minamino
Miyuki Sato
Hirokazu Tsukaya
Takashi Ueda
Dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort Marchantia polymorpha
Cell Reports
CP: Plants
title Dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort Marchantia polymorpha
title_full Dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort Marchantia polymorpha
title_fullStr Dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort Marchantia polymorpha
title_full_unstemmed Dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort Marchantia polymorpha
title_short Dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort Marchantia polymorpha
title_sort dynamic rearrangement and autophagic degradation of mitochondria during spermiogenesis in the liverwort marchantia polymorpha
topic CP: Plants
url http://www.sciencedirect.com/science/article/pii/S2211124722007616
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