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

Norizuki, Takuya; Minamino, Naoki; Sato, Miyuki; Tsukaya, Hirokazu; Ueda, Takashi

doi:10.1016/j.celrep.2022.110975

Cited by 14 publications

(19 citation statements)

References 55 publications

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“…MpSEC28-mCherry was also observed as ring-like structures without any detectable localization to the oil-body membrane in oil body cells ( Supplementary Figure 6A ). We compared its localization with that of other fluorescent markers [MpSEC21-mCitrine (COPI-coated vesicles), MpRET1-mCitrine (COPI-coated vesicles), mCitrine-MpGOS11 (Golgi apparatus), MpERD2-mCitrine (Golgi apparatus), mCitrine-MpSYP4 [ trans -Golgi network (TGN)], mCitrine-MpRAB5 [multivesicular body (MVB)], and MpIDH1-mCitrine (mitochondria)] to help identify the MpSEC28-mCherry-positive structure ( Kanazawa et al, 2016 , 2020 ; Minamino et al, 2017 ; Norizuki et al, 2022 ). The data obtained using the lambda scan unit were analyzed for colocalization and indicated that MpSEC28-mCherry was highly colocalized with the COPI markers MpSEC21-mCitrine and MpRET1-mCitrine ( Figures 4A , C ; Supplementary Figure 7A ).…”

Section: Resultsmentioning

confidence: 99%

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

2022

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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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Section: Resultsmentioning

confidence: 99%

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

2022

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“…The degradation of mitochondria appears to occur before that of other organelles, indicating that the autophagic degradation of each organelle may be regulated differently . degradation of the plastid must also be distinctly regulated from that of other organelles; unlike endomembrane organelles such as the endoplasmic reticulum and Golgi apparatus, which are fully removed from spermatids during spermiogenesis, the plastid is retained in the mature spermatozoid (Figure 1A; Minamino et al, 2022;Norizuki et al, 2022). Further studies will be required to fully understand the molecular mechanisms underlying the degradation of each organelle.…”

Section: Discussionmentioning

confidence: 99%

“…We previously demonstrated that multiple organelles including mitochondria are degraded in the vacuole through autophagy during spermiogenesis in M. polymorpha (Norizuki et al, 2022).…”

Section: The Plastid Is Degraded By Autophagy During Spermiogenesismentioning

confidence: 99%

“…Recently, autophagy has been shown to be required for organelle reorganization during spermiogenesis in bryophytes, including the moss Physcomitrium patens and the liverwort Marchantia polymorpha ( Sanchez-Vera et al., 2017 ; Norizuki et al., 2022 ). In P. patens , impairment of autophagy results in an increased number of plastids without a change in the total area of the plastid ( Sanchez-Vera et al., 2017 ), implying that autophagy suppresses plastid division through an unknown mechanism.…”

Section: Introductionmentioning

confidence: 99%

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Autophagy regulates plastid reorganization during spermatogenesis in the liverwort Marchantia polymorpha

Norizuki

Minamino²,

Sato³

et al. 2023

Front. Plant Sci.

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Autophagy is a highly conserved system that delivers cytoplasmic components to lysosomes/vacuoles. Plastids are also degraded through autophagy for nutrient recycling and quality control; however, the involvement of autophagic degradation of plastids in plant cellular differentiation remains unclear. Here, we investigated whether spermiogenesis, the differentiation of spermatids into spermatozoids, in the liverwort Marchantia polymorpha involves autophagic degradation of plastids. Spermatozoids of M. polymorpha possess one cylindrical plastid at the posterior end of the cell body. By fluorescently labeling and visualizing plastids, we detected dynamic morphological changes during spermiogenesis. We found that a portion of the plastid was degraded in the vacuole in an autophagy-dependent manner during spermiogenesis, and impaired autophagy resulted in defective morphological transformation and starch accumulation in the plastid. Furthermore, we found that autophagy was dispensable for the reduction in plastid number and plastid DNA elimination. These results demonstrate a critical but selective role of autophagy in plastid reorganization during spermiogenesis in M. polymorpha.

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“…polymorpha spermiogenesis ( Minamino et al, 2017 ; Minamino et al, 2022 ). Multimodal autophagic degradation of cytoplasmic components is also potentiated during spermiogenesis ( Norizuki et al, 2022 ). Thus, spermiogenesis in M. polymorpha involves multiple distinct degradation pathways and occurs in a cell-autonomous manner, differing from spermiogenesis in mammalian cells, which requires phagocytic elimination of excess cytoplasm by neighboring Sertoli cells ( O'Donnell et al, 2011 ).…”

Section: Geneticsmentioning

confidence: 99%

The renaissance and enlightenment ofMarchantiaas a model system

et al. 2022

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The liverwort Marchantia polymorpha has been utilized as a model for biological studies since the 18th century. In the past few decades there has been a Renaissance in its utilization in genomic and genetic approaches to investigating physiological, developmental, and evolutionary aspects of land plant biology. The reasons for its adoption are similar to those of other genetic models, e.g. simple cultivation, ready access via its worldwide distribution, ease of crossing, facile genetics, and more recently, efficient transformation, genome editing, and genomic resources. The haploid gametophyte dominant life cycle of M. polymorpha is conducive to forward genetic approaches. The lack of ancient whole-genome duplications within liverworts facilitates reverse genetic approaches, and possibly related to this genomic stability, liverworts possess sex chromosomes that evolved in the ancestral liverwort. As a representative of one of the three bryophyte lineages, its phylogenetic position allows comparative approaches to provide insights into ancestral land plants. Given the karyotype and genome stability within liverworts, the resources developed for M. polymorpha have facilitated the development of related species as models for biological processes lacking in M. polymorpha.

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

Cited by 14 publications

References 55 publications

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

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

Autophagy regulates plastid reorganization during spermatogenesis in the liverwort Marchantia polymorpha

The renaissance and enlightenment ofMarchantiaas a model system

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